Review ArticleReverse Methanogenesis and Respiration inMethanotrophic Archaea

Peer H A Timmers123 Cornelia U Welte34 Jasper J Koehorst5 Caroline M Plugge12

Mike S M Jetten346 and Alfons J M Stams137

1Laboratory of Microbiology Wageningen University Stippeneng 4 6708 WEWageningen Netherlands2Wetsus European Centre of Excellence for Sustainable Water Technology Oostergoweg 9 8911 MA Leeuwarden Netherlands3Soehngen Institute of Anaerobic Microbiology Heyendaalseweg 135 6525 AJ Nijmegen Netherlands4Department of Microbiology Radboud University Heyendaalseweg 135 6525 AJ Nijmegen Netherlands5Laboratory of Systems and Synthetic Biology Wageningen University Stippeneng 4 6708 WEWageningen Netherlands6TU Delft Biotechnology Julianalaan 67 2628 BC Delft Netherlands7Centre of Biological Engineering University of Minho Campus de Gualtar 4710-057 Braga Portugal

Correspondence should be addressed to Peer H A Timmers peertimmerswurnl

Received 3 August 2016 Revised 11 October 2016 Accepted 31 October 2016 Published 5 January 2017

Academic Editor Michael W Friedrich

Copyright copy 2017 Peer H A Timmers et al This is an open access article distributed under the Creative Commons AttributionLicense which permits unrestricted use distribution and reproduction in any medium provided the original work is properlycited

Anaerobic oxidation of methane (AOM) is catalyzed by anaerobic methane-oxidizing archaea (ANME) via a reverse and modifiedmethanogenesis pathway Methanogens can also reverse the methanogenesis pathway to oxidize methane but only during netmethane production (ie ldquotrace methane oxidationrdquo) In turn ANME can produce methane but only during net methaneoxidation (ie enzymatic back flux) Net AOM is exergonic when coupled to an external electron acceptor such as sulfate (ANME-1 ANME-2abc and ANME-3) nitrate (ANME-2d) or metal (oxides) In this review the reversibility of the methanogenesispathway and essential differences between ANME and methanogens are described by combining published information withdomain based (meta)genome comparison of archaeal methanotrophs and selected archaea These differences include abundancesand special structure of methyl coenzyme M reductase and of multiheme cytochromes and the presence of menaquinones ormethanophenazines ANME-2a and ANME-2d can use electron acceptors other than sulfate or nitrate for AOM respectivelyEnvironmental studies suggest that ANME-2d are also involved in sulfate-dependent AOM ANME-1 seem to use a differentmechanism for disposal of electrons and possibly are less versatile in electron acceptors use than ANME-2 Future research willshed light on the molecular basis of reversal of the methanogenic pathway and electron transfer in different ANME types

1 Introduction

11 Anaerobic Methane-Oxidizing Archaea (ANME) Anaer-obic methane-oxidizing archaea (ANME) perform anaerobicoxidation of methane (AOM) via reversal of the metha-nogenic pathway ANME were first discovered in marinesediments where AOM was coupled to sulfate reduction(SR) (Table 1 reaction (1)) Here ANME formed metaboli-cally interdependent consortia with sulfate-reducing bacteria(SRB) that belong to the Deltaproteobacteria [1ndash3] Threedistinct methanotrophic groups were identified ANME-1(subclusters a and b) ANME-2 (subclusters a b and c)

and ANME-3 The ANME-1 cluster is related to Metha-nomicrobiales and Methanosarcinales but forms a separatecluster [2] ANME-2 are related to cultivated members ofthe Methanosarcinales [4] and ANME-3 are more relatedto Methanococcoides spp [5] (Figure 1) The ANME cladesare not monophyletic with each other and the phylogeneticdistance between the subgroups is large with 16S rRNA genesequence similarity of only 75ndash92 [6] Subclusters ANME-2a and ANME-2b form a coherent clade that is distinguishedfrom ANME-2c [7] and are therefore often grouped togetheras ANME-2ab (Figure 1)Thewide phylogenetic distributionis reflected in the ecological niche adaptation of the different

HindawiArchaeaVolume 2017 Article ID 1654237 22 pageshttpsdoiorg10115520171654237

2 Archaea

Methanosaeta

Methanomicrobiales

ANME-1

Archaeoglobales

Methanococcales

Methanosarcina

Methanococcoides

MethanohalophilusMethanolobus

10

AAAGoM-Arc IANME-2d

ANME-2cANME-2ab

ANME-3

Figure 1 Phylogenetic tree of full length archaeal 16S rRNA sequences showing all methanotrophic clades so far described (grey) and otherarchaeal clades used in our domain based (meta)genome comparison (black) The tree was constructed with the ARB software package(version arb-601rev12565) [49] using 2800 sequences from the SILVA SSURef NR 99 database (release 1191) [50] Trees were calculatedby maximum likelihood analysis (RAxML PHYML) and the ARB neighbor-joining method with terminal filtering and the Jukes-Cantorcorrection Resulting trees were compared manually and a consensus tree was constructed Sulfolobales as outgroup was removed after treecalculations The scale bar represents the percentage of changes per nucleotide position

Table 1 Gibbs free energy changes under standard conditions (Δ1198660) for anaerobic methane oxidation coupled to different electron acceptors(possibly) performed by ANME

Reaction Gibbs free energy (Δ1198660 kJmolminus1)(1) CH

4+ SO4

2minus rarr HCO3

minus + HSminus+ H2O minus163

(2) CH4+ 4 NO

3

minus rarr HCO3

minus + 4 NO2

minus + H2O + H+ minus5172

(3) CH4+ 8 Fe(OH)

3+ 16 H+ rarr CO

2+ 8 Fe2+ + 22 H

2O minus5712

(4) CH4+ 4 MnO

2+ 8 H+ rarr CO

2+ 4 Mn2+ + 6 H

2O minus7632

(5) CH4+ 43 Cr

2O7

2minus + 323 H+ rarr 83 Cr3+ + CO2+ 223 H

2O minus8414

ANME clades ANME clades involved in sulfate-dependentAOM (S-AOM) co-occur in many different marine envi-ronments except for ANME-3 that was mainly found inmud volcanoes and in some seep sediments [6 8 9] Inmarine sediments a distinct zonation occurs where ANME-2ab dominate upper layers and ANME-2c andor ANME-1 abundance increases in deeper zones indicating ecologicalniche separation [10ndash15] ANME also form a versatile part-nership with non-SRB such as beta-proteobacteria [16] andVerrucomicrobia [17] ANME and especially ANME-1 havealso been observed without a (closely associated) bacterialpartner [5 12 13 18ndash22] It was therefore suggested thatANME could perform AOM alone using electron acceptorssuch as metal oxides or perform other processes such asmethanogenesis [23 24] Indications exist that AOM can

be coupled to the reduction of different metal (oxides)(Table 1 reactions (3)ndash(5)) but limited experimental evidenceexists to date that ANME are responsible for this reaction(discussed in Section 33) Besides marine environmentsANME involved in S-AOMcan be found in terrestrial [25 26]and freshwater ecosystems [27]

A member of a fourth subcluster ldquoCandidatus (Ca)Methanoperedens nitroreducensrdquo was recently discovered toperform nitrate-dependent AOM (N-AOM) [28] (Table 1reaction (2)) This cluster was named ldquoANME-2drdquo [29] butlater renamed to ldquoGOM Arc Irdquo [30] and ldquoAOM-associatedarchaea (AAA)rdquo [6] Phylogenetic analysis shows that theANME-2d cluster is monophyletic with ldquoCa M nitrore-ducensrdquo and other AAAGoM Arc I sequences but distinctfrom other ANME-2 subclusters (Figure 1) ANME-2d were

Archaea 3

initially enriched in bioreactors inoculated with freshwatersamples [28 31ndash33] As ANME-2d archaea were only recentlyrecognized their environmental preferences remain insuffi-ciently studied So far they have been found in freshwatercanals [31] soils and rice paddy fields [34ndash36] lakes andrivers [35] andwastewater treatment plants [33] In situAOMactivity of ANME-2d was determined recently for the firsttime [36] More ANME phylotypes in different environmentsand possibly new archaeal clades involved in AOM may yethave to be discovered For example methyl coenzyme Mreductase A genes (mcrA) from Bathyarchaeota (formerlyknown as Miscellaneous Crenarchaeota Group) and fromthe new archaeal phylum Verstraetearchaeota were recentlyfound indicating their involvement in methane metabolism[37 38]

This review focusses on archaea performing AOMthrough the reversal of the methanogenesis pathway Wedescribe the reversibility of the central methanogenic path-way including the key enzyme in methanogenesis and anaer-obic methanotrophy (ie methyl coenzyme M reductaseMcr) The possibility of methanogens to perform methaneoxidation and of ANME to perform methanogenesis is alsoaddressed Lastly the physiological adaptations of ANME toperform respiration using different electron acceptors duringAOM are discussed

12 ANME versus Methanogens Domain Based (Meta)Ge-nome Comparison In order to find additional differencesbetween archaeal methanotrophs and related methanogensthat could validate and complement findings in the lit-erature we performed domain based (meta)genome com-parison between selected metagenomes of ANME andgenomes of methanogens as done previously for bacterialgenomes [39] For archaeal methanotrophs we used themetagenomes of ANME-1 [40 41] ANME-2a [42] andANME-2d [28 43] For methanogens we used genomes ofclosely and distantly related species able to perform acetoclas-tic methanogenesis (A Methanosaeta concilii GP6) methy-lotrophic methanogenesis (M-1 Methanococcoides burtoniiDSM6242 M-2 Methanolobus tindarius DSM2278 and M-3 Methanohalophilus mahii DSM5219) hydrogenotrophicmethanogenesis (H-1 Methanospirillum hungatei JF-1 H-2Methanobacterium formicicum DSM3637 H-3 Methanococ-cus maripaludis C5 and H-4 Methanoregula formicicaSMSP) and both acetoclastic and methylotrophic methano-genesis (AMMethanosarcina acetivorans C2A) The genomeof a sulfate-reducing archaeon that contained most enzymesfor methanogenesis except forMcr (SArchaeoglobus fulgidusDSM 4304) was also included in the comparison For eachdataset the protein domains were obtained through Inter-ProScan 517-560 using the TIGRFAM ProDom SMARTPROSITE PfamA PRINTS SUPERFAMILY COILS andGene3D domain databases Results of the analysis are givenin Table 2 and Table S1 of the Supplementary Material avail-able online at httpsdoiorg10115520171654237 Since theANME-1 metagenome assembled by Stokke et al 2012 [40]contained many bacterial genes we did not refer to this datafor the domain based (meta)genome comparison but onlyused the ANME-1 metagenome described by Meyerdierks

et al 2010 [41] We included both ANME-1 metagenomesto analyze the organization of genes for the formaldehyde-activating enzyme (Table S2) and the iron-only hydrogenase(Table S3)

2 Reversal of the Methanogenesis Pathway

21 The Central Methanogenesis Pathway ANME are de-scribed to perform ldquoreverse methanogenesisrdquo [44] whichimplies the complete reversal ofmethanogenesis fromH

2and

CO2 that is hydrogenotrophic methanogenesis (for kinetic

and thermodynamic considerations the reader is referredto [45]) During ldquoforwardrdquo hydrogenotrophic methano-genesis CO

2is reduced to CH

4with reducing equiva-

lents derived from H2(Figure 2) During methylotrophic

methanogenesis this pathway is already partly reversedMethylotrophicmethanogens utilize one-carbon compoundssuch as methylamines methanol or methylated sulfur com-pounds (methanethiol dimethyl sulfide) that are activatedto methyl coenzyme M About 75 of the methyl coen-zyme M (CH

3-CoM) is reduced to produce CH

4and about

25 of CH3-CoM is oxidized to CO

2using the methano-

genesis pathway in reverse during methylotrophic growthThe oxidative part provides reducing equivalents that areneeded for the generation of the proton motive force in themethanogenic respiratory chain and the reduction of CH

3-

CoMbymethyl coenzymeM reductase (Mcr) [46] (Figure 3)In all methanogens the Mcr reaction operates in the forwardreaction and yields methane and the heterodisulfide ofcoenzyme B and coenzyme M (CoB-S-S-CoM)

CH3-CoM + CoB-SH 997888rarr CH

4+ CoB-S-S-CoM

Δ1198660= minus30 kJmolminus1 [52]

(1)

The heterodisulfide is a central intermediate and actsas terminal electron acceptor in all methanogens Inhydrogenotrophic methanogens without cytochromes it isthe electron acceptor of the cytoplasmic electron-bifurcatingCoB-S-S-CoM reductase (HdrABC) and F

420-nonreducing

hydrogenase (MvhADG) complex [47 48] that is needed toprovide reduced ferredoxin for the first step in methano-genesis the reduction of CO

2to a formyl group Within

the methanogens with cytochromes only a few membersof the genus Methanosarcina are able to grow on H

2CO2

They use a ferredoxin-dependent hydrogenase (Ech) forferredoxin reduction and an additional membrane boundmethanophenazine-dependent hydrogenase (Vho) for H

2

oxidation coupled to the reduction of the heterodisulfideby the membrane bound CoB-S-S-CoM reductase (HdrDE)F420

cycling can be accomplished using the F420

-dependenthydrogenase (Frh) and F

420H2 phenazine oxidoreductase

(Fpo) complex [48] (Figure 2) For methanogens it is ofcrucial importance that Mcr operates in the forward reactionto yield methane and the heterodisulfide If all reactionsof the methanogenic pathway are reversed such as duringAOM the pathway requires the input of energy and produceselectron donors (Figures 4ndash6) Therefore during AOMan external electron acceptor is needed which makes the

Archaea 3

initially enriched in bioreactors inoculated with freshwatersamples [28 31ndash33] As ANME-2d archaea were only recentlyrecognized their environmental preferences remain insuffi-ciently studied So far they have been found in freshwatercanals [31] soils and rice paddy fields [34ndash36] lakes andrivers [35] andwastewater treatment plants [33] In situAOMactivity of ANME-2d was determined recently for the firsttime [36] More ANME phylotypes in different environmentsand possibly new archaeal clades involved in AOM may yethave to be discovered For example methyl coenzyme Mreductase A genes (mcrA) from Bathyarchaeota (formerlyknown as Miscellaneous Crenarchaeota Group) and fromthe new archaeal phylum Verstraetearchaeota were recentlyfound indicating their involvement in methane metabolism[37 38]

This review focusses on archaea performing AOMthrough the reversal of the methanogenesis pathway Wedescribe the reversibility of the central methanogenic path-way including the key enzyme in methanogenesis and anaer-obic methanotrophy (ie methyl coenzyme M reductaseMcr) The possibility of methanogens to perform methaneoxidation and of ANME to perform methanogenesis is alsoaddressed Lastly the physiological adaptations of ANME toperform respiration using different electron acceptors duringAOM are discussed

12 ANME versus Methanogens Domain Based (Meta)Ge-nome Comparison In order to find additional differencesbetween archaeal methanotrophs and related methanogensthat could validate and complement findings in the lit-erature we performed domain based (meta)genome com-parison between selected metagenomes of ANME andgenomes of methanogens as done previously for bacterialgenomes [39] For archaeal methanotrophs we used themetagenomes of ANME-1 [40 41] ANME-2a [42] andANME-2d [28 43] For methanogens we used genomes ofclosely and distantly related species able to perform acetoclas-tic methanogenesis (A Methanosaeta concilii GP6) methy-lotrophic methanogenesis (M-1 Methanococcoides burtoniiDSM6242 M-2 Methanolobus tindarius DSM2278 and M-3 Methanohalophilus mahii DSM5219) hydrogenotrophicmethanogenesis (H-1 Methanospirillum hungatei JF-1 H-2Methanobacterium formicicum DSM3637 H-3 Methanococ-cus maripaludis C5 and H-4 Methanoregula formicicaSMSP) and both acetoclastic and methylotrophic methano-genesis (AMMethanosarcina acetivorans C2A) The genomeof a sulfate-reducing archaeon that contained most enzymesfor methanogenesis except forMcr (SArchaeoglobus fulgidusDSM 4304) was also included in the comparison For eachdataset the protein domains were obtained through Inter-ProScan 517-560 using the TIGRFAM ProDom SMARTPROSITE PfamA PRINTS SUPERFAMILY COILS andGene3D domain databases Results of the analysis are givenin Table 2 and Table S1 of the Supplementary Material avail-able online at httpsdoiorg10115520171654237 Since theANME-1 metagenome assembled by Stokke et al 2012 [40]contained many bacterial genes we did not refer to this datafor the domain based (meta)genome comparison but onlyused the ANME-1 metagenome described by Meyerdierks

et al 2010 [41] We included both ANME-1 metagenomesto analyze the organization of genes for the formaldehyde-activating enzyme (Table S2) and the iron-only hydrogenase(Table S3)

2 Reversal of the Methanogenesis Pathway

21 The Central Methanogenesis Pathway ANME are de-scribed to perform ldquoreverse methanogenesisrdquo [44] whichimplies the complete reversal ofmethanogenesis fromH

2and

CO2 that is hydrogenotrophic methanogenesis (for kinetic

and thermodynamic considerations the reader is referredto [45]) During ldquoforwardrdquo hydrogenotrophic methano-genesis CO

2is reduced to CH

4with reducing equiva-

lents derived from H2(Figure 2) During methylotrophic

methanogenesis this pathway is already partly reversedMethylotrophicmethanogens utilize one-carbon compoundssuch as methylamines methanol or methylated sulfur com-pounds (methanethiol dimethyl sulfide) that are activatedto methyl coenzyme M About 75 of the methyl coen-zyme M (CH

3-CoM) is reduced to produce CH

4and about

25 of CH3-CoM is oxidized to CO

2using the methano-

genesis pathway in reverse during methylotrophic growthThe oxidative part provides reducing equivalents that areneeded for the generation of the proton motive force in themethanogenic respiratory chain and the reduction of CH

3-

CoMbymethyl coenzymeM reductase (Mcr) [46] (Figure 3)In all methanogens the Mcr reaction operates in the forwardreaction and yields methane and the heterodisulfide ofcoenzyme B and coenzyme M (CoB-S-S-CoM)

CH3-CoM + CoB-SH 997888rarr CH

4+ CoB-S-S-CoM

Δ1198660= minus30 kJmolminus1 [52]

(1)

The heterodisulfide is a central intermediate and actsas terminal electron acceptor in all methanogens Inhydrogenotrophic methanogens without cytochromes it isthe electron acceptor of the cytoplasmic electron-bifurcatingCoB-S-S-CoM reductase (HdrABC) and F

420-nonreducing

hydrogenase (MvhADG) complex [47 48] that is needed toprovide reduced ferredoxin for the first step in methano-genesis the reduction of CO

2to a formyl group Within

the methanogens with cytochromes only a few membersof the genus Methanosarcina are able to grow on H

2CO2

They use a ferredoxin-dependent hydrogenase (Ech) forferredoxin reduction and an additional membrane boundmethanophenazine-dependent hydrogenase (Vho) for H

2

oxidation coupled to the reduction of the heterodisulfideby the membrane bound CoB-S-S-CoM reductase (HdrDE)F420

cycling can be accomplished using the F420

-dependenthydrogenase (Frh) and F

420H2 phenazine oxidoreductase

(Fpo) complex [48] (Figure 2) For methanogens it is ofcrucial importance that Mcr operates in the forward reactionto yield methane and the heterodisulfide If all reactionsof the methanogenic pathway are reversed such as duringAOM the pathway requires the input of energy and produceselectron donors (Figures 4ndash6) Therefore during AOMan external electron acceptor is needed which makes the

4 Archaea

Table2

Dom

ainbased(m

eta)geno

mecomparis

onof

selected

metagenom

esof

methano

troph

sandselected

geno

mes

ofotherarchaea

Dom

ainabun

dancein

every(m

eta)geno

meis

indicatedby

numbersS-AOM

perfo

rmingANMEinclu

deANME-1-s

[40]A

NME-1-m

[41]and

ANME-2a

[42]N

-AOM

perfo

rmingANMEinclu

deANME-2d-h

[28]

andANME-2d-

a[43]Th

eacetoclastic

(A)a

ndmethylotro

phic

(M)m

ethano

gens

inclu

deMethanosarcinaacetivoran

sC2A

(AM)MethanosaetaconciliiG

P6(A

)Methanococcoidesb

urtoniiD

SM6242

(M-1)Methanolobu

stin

dariu

sDSM

2278

(M-2)andMethanohalophilu

smahiiDSM

5219

(M-3)Hydrogeno

troph

icmethano

gens

(H)inclu

deMethanospirillum

hungatei

JF-1

(H-1)

Methanobacteriumform

icicumDSM

3637

(H-2)Methanococcus

maripalud

isC5

(H-3)andMethanoregulaform

icica

SMSP

(H-4)Th

esulfate-reducinga

rchaeon(S)isA

rchaeoglo

busfulgidu

sDSM

4304

InterPro

IDANME-1S

ANME-1M

ANME-2a

ANME-2d

HANME-2d

AAM

AM-1

M-2

M-3

H-1

H-2

H-3

H-4

SCe

ntralpathw

ayMcralpha

subu

nitN-te

rminal

IPR0

03183

42

11

11

11

11

12

12

0Mcralpha

subu

nitN-te

rminal

subd

omain1

IPR0

15811

23

11

11

11

11

12

12

0

Mcralpha

subu

nitN-te

rminal

subd

omain2

IPR0

15823

22

22

22

22

22

24

24

0

Mcralpha

subu

nitC-

term

inal

IPR0

09047

32

11

11

11

11

12

12

0Mcralphabetas

ubun

itC-

term

inal

IPR0

08924

64

22

22

22

22

24

24

0Mcralphabetas

ubun

itdo

main2

C-term

inal

IPR0

22681

96

33

33

33

33

36

36

0

Mcrbetas

ubun

itIPR0

03179

12

11

11

11

11

12

12

0Mcrbetas

ubun

itC-

term

inal

IPR0

22679

32

11

11

11

11

12

12

0Mcrbetas

ubun

itN-te

rminal

IPR0

22680

42

11

11

11

11

12

12

0Mcrgam

mas

ubun

itIPR0

03178

148

44

44

44

44

48

48

0Mcrprotein

CIPR0

07687

21

11

11

11

11

11

11

0Mcrprotein

C-lik

eIPR0

26327

52

22

22

21

22

22

21

0Mcrprotein

DIPR0

03901

00

36

63

33

33

39

36

0Mcrferredo

xin-lik

efold

IPR0

09024

126

33

33

33

33

36

36

0510-

methylenetetrahydromethano

pterin

redu

ctase

IPR0

19946

00

21

11

11

11

11

11

1

Acetoclasticm

ethanogenesis

COdehydrogenaseacetyl-C

oAsynthase

complex

alph

asub

unit

IPR0

0446

00

11

11

31

11

11

11

12

COdehydrogenaseacetyl-C

oAsynthase

complex

betasubu

nit

IPR0

04461

134

22

24

42

22

22

24

2

COdehydrogenaseacetyl-C

oAsynthase

delta

subu

nit

IPR0

04486

51

11

12

11

11

11

11

1

COdehydrogenaseacetyl-C

oAsynthase

delta

subu

nitTIM

barrel

IPR0

16041

112

53

24

22

33

32

25

2

COdehydrogenaseb

subu

nita

cetyl-C

oAsynthase

epsilon

subu

nit

IPR0

03704

32

22

24

22

22

22

22

4

Archaea 5

Table2Con

tinued

InterPro

IDANME-1S

ANME-1M

ANME-2a

ANME-2d

HANME-2d

AAM

AM-1

M-2

M-3

H-1

H-2

H-3

H-4

SMethylotro

phicmethanogenesis

Methyltransfe

rase

MtaACmuA

IPR0

06360

00

00

07

04

56

00

10

0Methano

l-cob

alam

inmethyltransfe

raseB

subu

nit

IPR0

21079

00

00

03

02

22

00

00

0

Mon

omethylamine

methyltransfe

rase

Mtm

BIPR0

08031

30

00

012

012

2115

00

00

0

Trim

ethylaminem

ethyltransfe

rase

IPR0

10426

110

00

04

05

22

00

00

0Dim

ethylaminem

ethyltransfe

rase

MtbB

IPR0

12653

00

00

09

06

66

00

00

0

Trim

ethylaminem

ethyltransfe

rase

Methanosarcina

IPR0

12740

00

00

02

01

11

00

00

0

Methylaminem

ethyltransfe

rase

corrinoidproteinredu

ctivea

ctivase

IPR0

26339

00

00

04

02

22

00

00

0

C-type

cytochromes

Di-h

aem

cytochrome

transm

embranenitrater

eductio

nIPR0

16174

20

43

74

00

40

11

00

1

Dou

bled

CXXC

Hmotif

IPR0

10177

330

32

30

00

00

00

00

0Cy

tochromec

-like

domain

IPR0

09056

20

60

1715

04

86

00

00

4ClassIIIcytochromeC

(tetrahem

ecytochrome)

IPR0

20942

20

03

30

00

00

00

00

0

Tetrahem

ecytochrom

edom

ain

flavocytochromec

3(Shewa

nella)

IPR0

12286

40

45

42

00

10

10

00

2

Octahem

ec-ty

pecytochrome

IPR0

24673

10

20

00

00

22

00

00

1Methano

genesis

multih

emec

-type

cytochrome

IPR0

27594

00

10

01

01

11

00

00

0

Multih

emec

ytochrom

eIPR0

11031

7815

5280

733

06

814

00

01

7S-layerd

omains

S-layerfam

ilydu

plicationdo

main

IPR0

06457

130

2916

2634

1916

4417

00

00

0Sarcinarrayfamily

protein

IPR0

26476

00

60

41

00

21

00

00

0S-layerh

omolog

ydo

main

IPR0

01119

10

20

00

00

00

00

00

0Ce

llexportandcelladhesio

nHYR

domain

IPR0

03410

15

20

00

00

00

00

00

0CA

RDBdo

main

IPR0

11635

6414

156

630

41

40

90

03

8Collagen-bind

ingsurfa

ceprotein

Cna-lik

eB-type

domain

IPR0

08454

41

21

80

60

22

00

00

0

vonWillebrand

factortypeA

IPR0

02035

5528

1732

1437

2317

429

288

027

7VWAN-te

rminal

IPR0

13608

12

00

00

00

00

00

00

0Ad

hesio

nlip

oprotein

IPR0

06128

84

45

00

53

04

45

00

0Ad

hesin

BIPR0

06129

03

45

00

30

04

03

00

0

6 Archaea

Table2Con

tinued

InterPro

IDANME-1S

ANME-1M

ANME-2a

ANME-2d

HANME-2d

AAM

AM-1

M-2

M-3

H-1

H-2

H-3

H-4

SInvasin

intim

incell-adhesio

nfragments

IPR0

0896

417

03

26

70

27

01

20

22

Putativ

ecellw

allbinding

repeat2

IPR0

07253

22

00

00

00

00

00

00

0ArchaeosortaseA

IPR0

14522

20

12

21

11

11

10

02

1ArchaeosortaseB

IPR0

26430

00

00

00

00

01

00

00

0ArchaeosortaseC

IPR0

22504

00

12

10

01

10

00

00

0Ex

osortasearchaeosortased

omain

IPR0

26392

50

25

31

12

22

10

12

1Ex

osortaseE

psH

IPR0

13426

10

01

00

00

00

00

00

0Ex

osortase

EpsH

-related

IPR0

19127

42

23

21

12

11

10

12

1Archaeosortasefam

ilyproteinArtE

IPR0

26485

00

00

00

00

00

00

10

0Cellw

allhydrolaseautolysin

catalytic

IPR0

02508

22

10

00

00

00

00

01

0

PEF-CT

ERM

proteinsorting

domain

IPR0

17474

00

34

10

010

190

00

00

0

PGF-pre-PG

Fdo

main

IPR0

26453

11

189

824

07

2111

00

01

1PG

F-CT

ERM

archaeal

protein-sortingsig

nal

IPR0

26371

94

62

12

02

12

10

01

3

LPXT

Gcellwallancho

rdom

ain

IPR0

19931

30

10

00

11

00

00

00

0VPX

XXP

-CTE

RMproteinsorting

domain

IPR0

26428

00

00

00

00

05

00

00

0

Cellu

losome-relatedDockerin

Cellulosomea

ncho

ringprotein

cohesin

domain

IPR0

02102

8077

524

122

04

153

11

00

4

Dockerin

domain

IPR0

16134

149

112

444

65

172

40

90

00

2Dockerin

type

Irepeat

IPR0

02105

10

50

00

00

00

00

00

1Ca

rbohydrate-binding

domains

Carboh

ydrate-binding

domain

IPR0

08965

5042

392

62

03

132

30

10

2Ca

rboh

ydrate-binding

-like

fold

IPR0

13784

145

310

190

00

01

30

06

1Ca

rboh

ydrate-binding

CenC-

like

IPR0

03305

10

70

170

00

00

00

00

0Ca

rboh

ydrate-binding

sugar

hydrolysisdo

main

IPR0

06633

2722

52

227

37

88

05

21

8

Carboh

ydrate-binding

domain

family

9IPR0

10502

10

00

20

00

00

00

00

0

Bacteroidetes-associated

carboh

ydrate-binding

often

N-te

rminal

IPR0

24361

00

10

00

00

00

00

00

0

Carboh

ydratebind

ingmod

ule

xylan-bind

ingdo

main

IPR0

31768

00

00

10

00

00

00

00

0

Galactose-binding

domain-lik

eIPR0

08979

121

176

394

42

13

00

00

0

Archaea 7

Table2Con

tinued

InterPro

IDANME-1S

ANME-1M

ANME-2a

ANME-2d

HANME-2d

AAM

AM-1

M-2

M-3

H-1

H-2

H-3

H-4

SMenaquinones

3-Dem

ethylubiqu

inon

e-9

3-methyltransfe

rase

IPR0

28973

00

03

30

00

00

01

00

0

Succinated

ehydrogenasefu

marate

redu

ctaseflavoproteinsubu

nit

IPR0

1400

60

01

21

00

00

10

00

01

UbiECO

Q5methyltransfe

rase

IPR0

04033

30

02

21

01

00

00

00

0UbiECO

Q5methyltransfe

rase

conservedsite

IPR0

23576

30

02

20

00

10

00

00

0

NrfD

family

IPR0

05614

30

04

30

00

00

00

00

3Fu

talosin

ehydrolase

IPR0

19963

00

01

10

00

00

00

00

0Cy

clicd

ehypoxanthinefutalosine

synthase

IPR0

22431

11

01

10

00

00

00

00

1

Aminod

eoxyfutalosin

esynthase

IPR0

22432

00

01

10

00

00

00

00

0Menaquino

nesynthesis

(cho

rismate

dehydrataseamp

naph

thoatesynthase)

IPR0

03773

86

02

20

00

00

00

00

2

FOsynthasesub

unit2

IPR0

20050

33

13

32

12

12

22

22

3Ph

enazines

Phenazineb

iosynthesis

PhzF

protein

IPR0

03719

11

40

02

00

00

00

02

0

8 Archaea

Frh

Mch

Mer

Mtd

Ftr

Fmd

Mcr

MPh

Vho

Ech

Mtr

CoM-SH

CoB-S-S-CoM

CoB-SHHdrDE2H+

H2

H2

H2

MPhH2

H+

CH4

CH3-CoM

CH3-H4MPTF420H2

F420

F420H2

F420

CH2=H4MPT

CHequivH4MPT

CHO-H4MPT

CHO-MFR

CO2

Fdred

Fdox

H2O

2Na+

H2

Figure 2 Hydrogenotrophic methanogenesis in cytochrome containing Methanosarcina barkeri Black lines represent presence ofconversions See Table 3 for nomenclature

reaction thermodynamically favourable (Table 1)The reversereaction of Mcr is therefore an essential step in AOM andis discussed in Section 22 The respiratory chain that isneeded for using different terminal electron acceptors will bediscussed in Section 3

Evidence that ANME use the reverse methanogenesispathway during AOM is derived from metagenomic andmetatranscriptomic analyses This showed that all genesfor the (reverse) methanogenic pathway were present andexpressed in ANME-2a [42] (Figure 4) and ANME-2d[28] (Figure 5) ANME-1 were consistently lacking thegene encoding N5N10-methylene- tetrahydromethanopterin(H4MPT) reductase (Mer) which is an enzyme needed to

oxidize methyl-H4MPT during methane oxidation [40 41

44 51] (Figure 6 Table 2) Possible explanations could be that(1) the mer gene is present but not yet detected (2) ANME-1 used a bypass of this step and (3) Mer was replaced bya structural analogue The first possibility is highly unlikelyAlthough no closed genome of ANME-1 is publicly availableto date all ANME-1 metagenomes consistently only lackMerand no other methanogenic genes The second possibilitywas proposed previously where ANME-1 uses a bypass of

Mer via the formation of methanol or methylamine [41] aswas detected in deletion mutants ofMethanosarcina [52 53]Here CH

3-CoM was presumably converted to methanol by

a methyltransferase and subsequently to formaldehyde by amethanol dehydrogenase (Mdh) Then formaldehyde wouldbe converted to N5N10 methylene-H

4MPT using a fusion

protein of the formaldehyde-activating enzyme (Fae) and ahexulose-6-phosphate synthase (Hps) [53] (Figure 6) BothFae and Hps were found in the ANME-1 metagenome [41]and metaproteome [40 51] However no genes coding forenzymes involved in methanol metabolism were detectedin these ANME-1 datasets [40 41 51] (Table 2) indicatingthat this alternative pathway probably does not occur Thepresence of the FaeHps fusion protein in ANME-1 duringAOM could also be explained by its involvement in ribosephosphate synthesis and not in AOM [54] Indeed the Faegene domains of ANME-1 were located in between ribulose-phosphate binding barrel and ribosomal protein S5 domains(Table S2) The third possibility of a structural analogue ismost likely since an analogue of N5N10-methylene tetrahy-drofolate (H

4HF) reductase (MetF) was expressed byANME-

1 during AOM which could replace Mer [40] (Figure 6)

Archaea 9

Table 3 Nomenclature

Central methanogenic pathwayFmd Formylmethanofuran (CHO-MFR) dehydrogenaseFtr Formylmethanofuran-tetrahydromethanopterin (H

4MPT) formyltransferase

Mch N5N10-methenyl-H4MPT cyclohydrolase

Mtd F420

H2-dependent methylene -H

4MPT dehydrogenase

Mer N5N10-methylene-H4MPT reductase

Mtr N5-methyl-H4MPTcoenzyme M (CoM) methyltransferase

Mcr Methyl coenzyme M (CH3-CoM) reductase

Mdh Methanol dehydrogenaseFaeHps Fusion protein of formaldehyde activating enzyme hexulose-6-phosphate synthaseMetF N5N10-methylene tetrahydrofolate (H

4HF) reductase analogue

Electron transportMvh F

420-nonreducing hydrogenase

Vho Methanophenazine-dependent hydrogenaseFpo F

420H2phenazine oxidoreductase

Fqo F420

H2quinone oxidoreductase

Hdr Coenzyme B-coenzyme M heterodisulfide (CoB-S-S-CoM) reductaseFrh F

420-dependent hydrogenase

Ech Ferredoxin-dependent hydrogenaseMePhMePhH

2Methanophenazine

MQMQH2

MenaquinoneCyt b Cytochrome bCyt c Cytochrome cMHC Multiheme c-type cytochromeRieske Rieske cytochrome b complexOrf7 Pseudoperiplasmic b-type cytochromeNar Nitrate reductaseNap Periplasmic nitrate reductaseNrf Nitrite reductase

22 Methyl Coenzyme M Reductase (Mcr) The enzymaticreaction of a purified Mcr from ANME has not been mea-sured to date The key question is whether a methanogenicMcr can explain the observed in situ AOM rates or if theMcr of ANME is structurally altered There are three mainfactors to be considered the kinetic limitations as definedby enzyme properties (ie half-maximal activity at a specific119870119872value) the thermodynamic constraints of the enzymatic

reaction and the maximal or ambient rate of the enzymaticreaction For the Mcr from Methanothermobacter marbur-gensis kinetic parameters have been determined to illustratethe reversibility of reaction (1) In themethanogenic reactionthe purified Mcr isoform I [55] catalyzes the production ofmethane with a 119881max of 30Umgminus1 and a 119870

119872of 5mM for

CH3-CoM The same (methanogenic) enzyme was able to

oxidize methane to CH3-CoM with a rate of 00114Umgminus1

and a 119870119872for methane of sim10 mM [56]

To answer if the observed AOM rates are in accordancewith the measured methane oxidation rate for the purifiedMcr enzyme from M marburgensis the Mcr activity duringAOM is needed Estimates for AOM rates in terms of activity(per cell dry mass) range between lt1 and 20mmol dayminus1 andg cell dry massminus1 [56ndash66] This equals an activity of 07 to

sim14 nmol min and mg cell dry massminus1 About half of the celldry mass is protein so the activity for the ANME archaeawould approximate 14 to 28 nmol min and mg proteinminus1 Toestimate the activity per mg of Mcr the proportion of Mcrto cellular protein is needed It was reported that 7 of theprotein of ANMEmicrobial mats from the Black Sea [67 68]and 104 of peptides fromHydrate Ridge mesocosms is Mcr[51] As these were no pure cultures the actual percentagesof Mcr in ANME cells may be higher Transcriptome data forANME-2d [43] showed that about 19 of the total transcriptswere derived from the mcr genes indicating (though notdemonstrating) a highMcr content in ANME-2d Estimatingthat 10 of the cellular protein would be Mcr the specificactivity of the enzymewould be between 14 and 280 nmolminand mg Mcr proteinminus1 which is up to 25 times higher thanthe measured reverse reaction rate of the M marburgensisenzyme (sim12 nmol min and mg Mcrminus1 [56]) However thereverse reaction rate of the M marburgensis Mcr was deter-mined under nonsaturating substrate conditions and wastherefore not possibly representing the true maximum rateNevertheless both reverse reaction rates are in the same orderof magnitude other than the forward reaction of 30000ndash100000 nmol min and mgMcrminus1 Thus it seems that the

10 Archaea

H2

CoM-SH

Mch

Mer

Mtd

Ftr

Fmd

Mcr

MPh

MPhH2

MPh

MPh

MPhH2

MtrVho

CoM-SH

CoB-S-S-CoM

CoB-SHHdrDE

Fpo

Fpo

Ech

CH3-CoM

2H+

H2

2H+

2H+

H+

MPhH2

CH4

CH3-H4MPTF420H2

F420

F420H2

F420

CH2=H4MPT

CHequivH4MPT

CHO-H4MPT

CHO-MFR

CO2

Fdred

Fdox

H2O

2Na+

CH3-OH

Figure 3 Methylotrophic methanogenesis in cytochrome containingMethanosarcina barkeri Black lines represent presence of conversionsand red lines indicate reversal of the hydrogenotrophic methanogenic pathway See Table 3 for nomenclature

Mcr in ANME may have similar catalytic properties as themethanogenic enzyme and that the high amount of Mcr permg total cell biomass in ANME may in part compensates forthe apparently relatively slow catalysis

Considering the thermodynamic constraints the Gibbsfree energy change of the Mcr forward reaction under stan-dard conditions is around minus30 kJmolminus1 [56] Therefore thereverse reaction is endergonic under standard conditions andwill not proceed However highmethane concentrations (105according to reaction (1) [69 70]) may lead to a favourablechange in the Gibbs free energy in the direction of AOMHigh methane partial pressure prevails at many habitatswhere AOM has been detected The solubility of methaneat atmospheric pressure is only 13mM [71] Consequentlyincreased AOM rates were reported upon pressurizing sam-ples of different geographical origin [59 60 72 73] The 119870

119872

of Mcr of M marburgensis for methane was determined ator above 10mM and reported 119870

119872values of S-AOM varied

from (at least) 11mM [74] a few mM [57] to even 37mM(equivalent to 3MPa CH

4) [58] Thus high pressure and

therefore high concentrations of methane in the natural habi-tat accelerate the oxidation rate of methane by Mcr Futureresearch to accurately determine119870

119872values and rates forMcr

at differentmethane partial pressures is however neededThismay seem difficult but microbial activity measurements at insitu methane partial pressure were shown to be successful inthe laboratory [75]

It was suggested that the Mcr reaction is the rate limitingstep in reverse methanogenesis [56] which is in line withthe above described challenges Supporting these findingsthere does not seem to be a major change in the aminoacid structure that determines whether the backwards or theforward reaction of Mcr is favoured Amino acid alignments[67] and the crystal structure of ANME-1 Mcr [76] indicatedhigh overall similarity of the methanogenic and methan-otrophic enzyme and unambiguously demonstrated that

Archaea 11

MHC

MHCS-layer

2H+

minuse

cyt b

Mch

Mer

Mtd

Ftr

Fmd

Mcr

MPh

HdrABC

MPh

MHC

MHC

MPh

CoB-S-S-CoM

CoB-SH

CoM-SH

HdrDE

Mtr

Fpo

Fpo

Rnf

MPhH2

MPhH2

MPhH2

MPhH2

CH4

CH3-CoM

CH3-H4MPT

F420H2

F420

F420H2

F420

CH2=H4MPT

CHequivH4MPT

CHO-H4MPT

CHO-MFR

CO2

Fdred

Fdox

H2O

2Na+

MPh

minuse

S-layer

MHC

SRB 2H+

2H+

2Na+

minuse

minuse

minuse

Figure 4 Methanotrophic pathway during S-AOM by ANME-2a [42] Red lines indicate reversal of the hydrogenotrophic methanogenicpathway See Table 3 for nomenclature

CoM-SH and CoB-SH are substrates of the methanotrophicenzyme However several posttranslational modifications ofamino acids were different betweenmethanogens andANMEarchaea and the cofactor F

430(the prosthetic group of Mcr)

is modified in ANME-1 but not in ANME-2 or ANME-3archaea [51 63 67 68 76 77] Furthermore ANME-1 seemsto lack the noncatalytic proteinDdomain of themcr gene thatis present in all other methanogens and methanotrophs butof which the function is unknown (IPR003901 Table 2) [51]A metabolically engineered Methanosarcina acetivorans wasable to convert methane and CO

2to acetate with a plasmid

containingMcr derived from ANME-1 [78] It is thus unclearif only thermodynamic constraints and the abundance ofMcrensureAOMactivity or if also specificmodifications canhavean effect on the reverse activity of Mcr

23 Methane Oxidation by Methanogens Pure cultures ofmethanogens were not able to oxidize methane under highmethane and low hydrogen concentrations (reviewed in[79 80]) Methanogens are only able to oxidize methaneduring net methane production [81] Labeled methane addi-tion (13C or 14C) to pure cultures of methanogens showedproduction of labeled CO

2during net methane production

This characteristic was confirmed with several pure culturesof methanogens [82ndash84] The process was called ldquotracemethane oxidationrdquo (TMO) since the CO

2was formed in

trace amounts relative to the methane produced [83] It isnot clear if TMO is due to the reported reversibility ofindividual enzymes [66] or if it is an active microbial processfrom which energy can be conserved TMO was speculatedto be an active metabolic process for three reasons (1)the amount of methane oxidized varied between differentspecies of methanogens grown on the same methanogenicsubstrate (2) the amount ofmethane oxidized varied betweendifferent methanogenic substrates and (3) TMO productsvaried between different methanogenic substrates [83 84]For instance when grown on acetate Methanosarcina ace-tivorans produced labeled acetate from labeled methaneWhen grown on carbon monoxide it produced both labeledacetate and methyl sulfides from labeled methane [84] Dur-ing hydrogenotrophic and methylotrophic methanogenesisTMO mainly produced CO

2from labeled methane [83]

However in contrast with AOM TMO rates never exceededmethanogenesis rates even during long-term incubationwith methane and sulfate [85] It seems that methanogensare not able to conserve energy from TMO even under

12 Archaea

Mch

Mer

Mtd

Ftr

Fmd

Mcr

MQ

MQ

EchHdrFrh

3MQ

HdrABC

MQ

cyt b Mtr

NrfH

cyt c

NrfA

CoB-S-S-CoM

CoB-SH

CoM-SH

HdrDE

HCOIIHCOIINapHOrf7

NarGH

S-layer

Fqo

Fqo

3H+

3H+

4H+

CH4

CH3-CoM

CH3-H4MPT

F420

F420H2

F420

F420H2

CH2=H4MPT

CHequivH4MPT

CHO-H4MPT

CHO-MFR

CO2

Fdred

Fdox

H2O

2Na+

NH4+

NO2minus

NO2minus

NO3minus

3MQH2

MQH2

MQH2

MQH2eminus

eminus

Rieske

Figure 5 Methanotrophic pathway during N-AOM by ldquoCaM nitroreducensrdquo MPEBLZ (ANME-2d) [43] Red lines indicate reversal of thehydrogenotrophic methanogenic pathway See Table 3 for nomenclature

thermodynamically favourable conditions TMOoccurs bothin absence and presence of an external electron acceptor andonly during net methanogenesis It is therefore most likelycaused by the reported back flux of individual enzymes of themethanogenic pathway [66]

TMO also occurred in granular sludge and in freshwaterand terrestrial samples These mixed communities showedhigher TMO rates than pure cultures reaching up to 90of the methane produced [27 85ndash87] TMO should thereforebe carefully considered in the experimental setup and inter-pretation of results when studying AOM in environmentalsamples especially since TMO rates were like AOM stim-ulated by a high methane partial pressure [72 86 88] Sulfatereduction was also stimulated by higher methane partialpressures [85]Thus a highmethane partial pressure can havea stimulating effect on methane oxidation (either throughAOM or TMO) and SR which could be unrelated to S-AOMMoreover addition of iron sulfate (FeSO

4) or manganese

oxide (MnO2) also increased TMO rates [86] Therefore

methane-dependent SR and sulfate- or metal-dependentmethane oxidation are not necessarily indications for AOMin mixed cultures In conclusion when studying complexldquoblack-boxrdquo communities only net methane oxidation isproof for AOM activity

24 Methane Production by ANME The process of S-AOMis at the energetic limit for sustaining life with estimates

of Gibbs free energy yields between minus18 and minus35 kJmolminus1[45 79 89ndash91] and doubling times between 11 and 75months [65 72 73 92 93] Since S-AOM operates close toits thermodynamic equilibrium the reversibility of individualenzymes leads to measurable back flux producing methane(3ndash7 of AOM) and sulfate (55ndash13 of SR) during S-AOM [66] This ldquotrace methane productionrdquo was observedin situ [11] and in sediment slurries with methanogenesisaround 10 [62 94] or even as high as 50 of AOM [34]When sulfate becomes depleted Gibbs free energy yieldsbecome even lower (less negative) and the enzymatic backflux becomes even more apparent up to 78 of net AOM[95] Previous measurements of 13C depletion below thesulfate-methane transition zone (SMTZ) ofmarine sedimentsthat were thought to be indicative for methanogenesis couldtherefore instead be attributed to the back flux of AOM [95]The occurrence of ANME-1 without a bacterial partner insediment layers where sulfate was depleted was previouslyinterpreted as evidence that ANME-1 perform methanogen-esis [24] but in light of the above it could also indicate AOMThere are indeed reports of AOM activity below the SMTZin the methanogenic zone [96ndash99] In contrast AOM withother electron acceptors than sulfate operates far from thethermodynamic equilibrium with Gibbs free energy changesbetween minus5172 and minus8414 kJmolmethaneminus1 (Table 1) Herethe reported anaerobic back flux [66] is expected to be lessapparent

Archaea 13

MetFMer

Mdh

FaeHps

SRB

MHC

Mch

Mtd

Ftr

Fmd

McrMQ

Hdr1

MQ

MHC

Hdr2

CoB-S-S-CoMCoB-SHCoM-SH

Mtr

Fqo

CH4

CH3-CoMCH3-OH

CH2O CH3-H4MPT

F420F420H2

CHO-H4MPT

CHO-MFR

CO2

FdredFdox

H2O

eminus

eminus

CHequivH4MPT

CH2=H4MPT

xH+

H2

MQH2

MQH2

+xNa

Figure 6 Methanotrophic pathway during S-AOM by ANME-1 [40 41] Red lines indicate reversal of the hydrogenotrophic methanogenicpathway grey lines represent absence of conversions and blue lines indicate a bypass of the hydrogenotrophic methanogenic pathway SeeTable 3 for nomenclature

In laboratory incubations researchers were not ableto stimulate net methanogenesis through addition ofmethanogenic substrates to AOM performing sediments[62 94] In two cases researchers were successful [23 100]In one of these cases sediment-free long-term AOM enrich-ments that were dominated by ANMESRB were incubatedwith methanogenic substrates The resulting methanogenicactivity most likely came from the enrichment of a minorpopulation of methanogens (up to 7permil of total archaealgene tag sequences) that was present in the inoculum[100] In the second study methanogenic substrates wereadded to ANME-1 and ANME-2 dominated microbialmat samples and methanogenesis also occurred [23]However no information was provided for the total archaealcommunity composition which makes it impossible toexclude methanogens as the responsible organisms

Genomic information of ANME also gives indication onpotential methanogenic routes Considering methylotrophicmethanogenesis no gene homologues catalyzing methyltransfer from methylated substrates to coenzyme M weredetected in ANME (Table 2) [40ndash43] Acetoclastic methano-genesis needs either the AMP- and ADP-forming acetyl-coenzyme A synthetase (Acs and Acd resp) or proceedsvia acetate kinase and phosphotransacetylase In ANME-1only the alpha subunit of a homologue of Acd was expressed

during AOM [41] but in an ANME-1 proteome of activeAOM biomass no Acd was detected [40] The Acd gene wasdetected in the single-aggregate genome and transcriptomeof ANME-2a [42] and in ANME-2d [43] However genedomains for Acd are also present in methanogens unableto use acetate as substrate (Table 2) and are probably usedfor lipid metabolism In hydrogenotrophic methanogenesishydrogenases are used to replenish reduced coenzyme B andto recycle oxidized F

420(discussed in Section 21) Both the

cytoplasmic Mvh complex and the membrane bound Vhowere not present in ANME-2d [43] and not expressed inANME-2a (which also lackedEch andF

420-dependent hydro-

genase (Frh)) [42] making hydrogenotrophic methanogen-esis unlikely In ANME-1 both the cytoplasmic HdrABCand MvhD are present as well as homologues of Frh andEch but these were lacking catalytic subunits [40 41] Aniron hydrogenase was found in both ANME-1 metagenomesbut not in any other methanotroph or methanogen [41](Table 2) This iron hydrogenase domain is part of a genethat is 70 identical to a [FeFe]-hydrogenase of Dehalococ-coides mccartyi [FeFe]-hydrogenases catalyze reversible H

2

production and uptake but these were presumed to have nokey function in AOM [41] However the gene is part of a genecluster of three genes containing a 51 kDaNADH ubiquinoneoxidoreductase subunit (Table S3) which could potentially

14 Archaea

form a complex that generates a proton motive force duringhydrogen oxidation Therefore hydrogenotrophic methano-genesis by ANME-1 cannot be excluded yet

3 Respiration during AnaerobicOxidation of Methane

For netAOMtooccur an external electron acceptor is neededwhich results in a favourable Gibbs free energy change(Table 1) A variety of terminal electron acceptors have beendiscovered for AOM which will be discussed in Sections 31ndash33

31 Sulfate-Dependent AOM During sulfate-dependentAOM electrons are transferred from ANME to the sulfate-reducing bacterial partner Previous work tried to uncoverhow electrons were transferred and most compoundsthat could act as interspecies electron carrier (IEC) wereexcluded to be involved in AOM such as methanolhydrogen methanethiol acetate and carbon monoxide[57 61 62 94 101] Indications that polysulfide could actas IEC were found and ANME-2a archaea were thoughtto perform both AOM and sulfate reduction (SR) [102]However in marine seeps hydrothermal vents and othernondiffusion based sediments AOM rates are high andANME form close associations with SRB in dense aggregates[1 5 103 104] In these aggregates the high AOM ratescould not be explained by diffusion of an IEC whichmade direct interspecies electron transfer (DIET) a moreplausible mechanism [89 105 106] Cellular activities wereindependent of aggregate type and distance between thesyntrophic partners within the aggregate which is bestexplained by DIET [107] DIET is normally achieved usingmultiheme cytochrome c proteins (MHCs) and conductivepili (ie nanowires) which are mainly found in bacteriathat donate electrons extracellularly such as Geobacter andShewanella species [108ndash114] Indeed ANME-2a from seep-sediment samples seem to transfer electrons directly usinglarge MHCs [107] which were found in the metagenome ofANME-2a [107 115] ANME-1 and the associated bacterialpartner also overexpressed genes for extracellular MHCsduring AOM [116] which complements previous findings oftranscription [41] and translation [40] of ANME-1 relatedMHC genes Domain based (meta)genome analysis showsthe high abundance of MHC domains in different ANMEas compared to methanogens (Table 2) A recently isolatedbacterial partner of ANME-1 (ldquoHotSeep-1rdquo) also producedcell-to-cell connections using pili-derived nanowires [116]which explain previously detected Deltaproteobacteria-related pili genes in an AOM sample dominated by ANME-1[40]

How ANME use MHCs to donate electrons to thebacterial partner is not yet clear For ANME-2a the electronsprobably flow from methanophenazine to membrane inte-grated di-heme cytochromes (cytochrome 119887119887

6) that transfer

the electrons through the S-layer via MHCS-layer fusionproteins to extracellular MHCs (Figure 4) (Figure 4 in[107]) Exosortases and archaea-specific archaeosortases are

involved in export of cell surface proteins such as the archaealS-layer proteins These transpeptidases recognize specificsignal peptides for protein- sorting that is archaeosor-tase A recognizes the protein-sorting signal PGF-CTERMand archaeosortase C recognizes the PEF-CTERM signal[117] Both ANME-2a and 2d show presence of di-hemecytochromes archaeosortase A (IPR014522) archaeosortaseC (IPR022504) and other exosortase gene domains (Table 2)Moreover some genes of both ANME-2a and 2d containedboth MHC and PGF or PEF-CTERM domains Lastly somegenes of both ANME-2a and 2d contained both MHC andS-layer domains [107] indicating that these could form theabove-stated MHCS-layer fusion proteins

ANME-1 do not seem to have di-heme cytochromes(Table 2) [115] PGF related domains (IPR026453 andIPR026371) were present in all ANME but PEF-CTERM(IPR017474) related domains were absent in ANME-1 (Table 2) Moreover ANME-1 lacked archaeosortaseA (IPR014522) and archaeosortase C gene domains(IPR022504) as well as some other exosortases (Table 2) Asearch in NCBIrsquos conserved domains database (CCD [118])and the EMBL InterPro database [119] of amino acidssequences of all genes from ANME metagenomes thatcontain MHC domains showed that ANME-1 did not haveany protein-sorting signal or S-layer domains within thesegenes In fact S-layer domains were completely absent inANME-1 (Table 2) These results imply that ANME-1 do notuse di-heme cytochromes for electron transfer to MHCsand do not produce an S-layer (Figure 6) This implies thatANME-1 use a different mechanism for DIET and couldexplain the need for less MHCs by ANME-1 (Table 2)and the observed pili-derived nanowires produced by thebacterial partner [116] The genome of the bacterial partnerof ANME-1 (ldquoHotSeep-1rdquo) encoded 24 c-type cytochromesof which 10 were similar to secreted MHCs of Geobactersulfurreducens [120] which also uses pili for DIET [121]

In the case of ANME-2a it is not clear if pili (ienanowires) were formed during AOM It was previouslythought that electrically conductive pili seemed to be aprerequisite for current production andDIET [122 123] evenwhen syntrophs were closely associated [124] such as withinANME-2SRB aggregates However conductive materialssuch as granular activated carbon were shown to be ableto substitute pili in DIET [124] Although in previous workconductive materials such as phenazines or humic acids didnot seem to stimulate AOM rates [61] in a recent study AOMwas decoupled from SR using artificial electron acceptors[125] This indicates that conductive materials can indeedreplace pili and that ANME-2ab could possibly couple AOMto metal oxide reduction or any other suitable electronacceptor (discussed in Section 33) However it needs to beproven if in ANME-2SRB aggregates no pili are formed andif the mechanism of DIET is fundamentally different fromANME-1

As for the polysulfide shuttling theory [102] canonicalgenes for dissimilatory sulfate reduction such as adenylyl-transferase (Sat) APS reductase (Apr) and dissimilatorysulfite reductase (Dsr) which are all present in the sulfate-reducing archeon A fulgidus (Table S2) were not found in

Archaea 15

metagenomes of ANME-1 [41] and ANME-2a (Table S1)The enzymes Sat and Dsr were also not detected in ANMEcells using fluorescent immunolabelling [126] ANME-1 werepreviously found to encode most proteins for assimilatorysulfate reduction [41] ANME-2d only harbor gene domainsthat encode Sat and assimilatoryATP sulfurylase APS kinaseand sodiumsulfate symporters which were not present inANME-2a (Table S1) It is therefore clear that at least ANME-2a cannot donate electrons to sulfate but need to donateelectrons to a sulfate-reducing partner

32 Nitrate-Dependent AOM Unlike during S-AOMANME-2d that perform N-AOM do not need a bacterialpartner but transfer electrons directly to a membrane boundnitrate reductase (Nar) [28 43] (Figure 5) The ANME-2dgenomes contain most MHCs found so far in archaea[107 115] (Table 2) Of the 87 proteins that contained aCxxCH binding motif of which 43 seemed to be true c-typecytochromes [115] 23 CxxCH motif-encoding transcriptswere expressed during N-AOM [43] The function of mostof these MHCs is not known but they are likely involvedin nitrate reduction since c-type cytochromes are capableof operating in the wide range of redox potentials thatcouple nitrate reduction (11986401015840 (NO

3

minusNO2

minus) = +433mV) andmethane oxidation (11986401015840 (CoM-S-S-CoBCoM-SH+CoB-SH)= minus143mV) [43] Nitrate as terminal electron acceptor inanaerobic respiration has been found in halophilic andthermophilic archaea [127] The nar gene cluster of ldquoCaM nitroreducensrdquo comprises several genes including thecatalytic alpha (NarG molybdopterin) and beta (NarHiron sulfur cluster) subunit of nitrate reductase [28 43] The(halo)archaeal nitrate reductase complex was reported to belocated at the extracellular side of the cytoplasmic membrane[128] and in most archaea associated with the cytoplasmicmembrane via NarM [129] The ldquoCa M nitroreducensrdquogenome does not encode NarM but encodes a TAT signalpeptide at the N-terminus of NarG for translocation acrossthe cytoplasmic membrane [28 43] Interestingly theNarG and NarH seem to have been acquired from theProteobacteria via lateral gene transfer [28]

It is not yet clear at which point in themetabolism ldquoCaMnitroreducensrdquo conserves energy During reverse methano-genesis N5-methyl-H

4MPTCoM methyltransferase (Mtr)

dissipates the sodium ion potential across the cytoplasmicmembrane so subsequent steps inN-AOMhave to be coupledto the build-up of a proton or sodium motive force to makethe overall process energetically favourable The analysis ofan environmental genome [43] indicated presence of severalprotein complexes involved in electron transport and energyconservation Electrons that enter the respiratory chain couldbe transported by membrane-integral electron carriers (iemenaquinones) to a Rieske-cytochrome b complex that mayuse cytochrome c as electron acceptor This in turn maybe the electron donor for the unusual nitrate reductasecomplex Energy conservation is thermodynamically andmechanistically feasible at the F

420H2dehydrogenase and the

Rieske-cytochrome b complex (Figure 5) (Figure 2 in [43])Further investigations are needed to determine whether

nitrate reductase is also involved in energy conservationbut this working hypothesis is strengthened by the presenceof cupredoxin multicopper oxidase domains and coppercenters related to the periplasmic domain of cytochrome coxidase subunit II (HCO II) in ANME-2d (Table S1)

BothANME-2d genomes discussed here are derived frombioreactors where ldquoCaM nitroreducensrdquo formed syntrophiccultures with nitrite scavenging bacteria either with ldquoCaKuenenia stuttgartiensisrdquo (anammox bacteria) [28] or ldquoCaMethylomirabilis oxyferardquo (NC10 bacteria) [31 43]This indi-cated that ANME-2d could be dependent on those bacteriafor nitrite removal However in addition to nitrite ldquoCa Mnitroreducensrdquo may also produce ammonium during AOMby a pentaheme c-type nitrite reductase (NrfAH) encodedin the genome [43] (Figure 5) In fact both ANME-2dgenomes contain domains for NrfA (IPR003321) and NrfH(IPR017571) (Table S1) implying that both ANME-2d speciesare not necessarily dependent on a nitrite scavenger duringAOM

33 Metal-Dependent AOM Evidence for metal-dependentAOM was found in marine sediments [130ndash132] In non-marine environments AOM was also hypothesized to becoupled to iron andor manganese oxide reduction [26 133ndash136] or even coupled to the reduction of humic acids [136137] However organisms responsible for metal-dependentAOM were not identified in these studies It was speculatedthat JS1 bacteria methanogenic archaea and Methanohalo-biumANME-3 could be responsible for iron-dependentAOM [138] Other researchers speculated that either ANME-1 or MethanococcoidesANME-3 together with a bacterialpartner were responsible for manganese-dependent AOM[139] In another study where AOM was decoupled from SRANME were not detected which leaves open the possibilitythat other archaeal clades besides ANME could performmetal-dependent AOM [131]

It was recently observed that cultures containing ANME-2a and ANME-2c could decouple AOM from SR in thepresence of artificial electron acceptors humic acids andsoluble iron [125] which confirmed previous findings ofAOM not connected to SR in ANME dominated samples[140] This suggests that ANME-2 could also use insolublemetal oxide minerals as electron acceptor during AOM TheMHCs of ANME-2ab and ANME-2d are larger than thosein Shewanella and Geobacter species [107] which are knownto be capable of extracellular electron conduction It wasspeculated that both ANME-2d and Ferroglobus placidus ofwhich the latter can perform solid iron reduction can foldCxxCHmotifs into extracellular conductive structures or pili[115] Many of the MHCs of ANME-2d were not expressedwhen grown with nitrate (discussed in section 32) implyingthat these are not needed for nitrate reduction [43] Thisstrengthens the hypothesis that also ANME-2d could coupleAOM to reduction of other extracellular electron acceptorsthan nitrate and even to insoluble metal oxides Indeedrecent work showed that ANME-2d could be involved inAOM coupled to chromium(VI) reduction [141] (Table 1reaction (5)) and in AOM coupled to the reduction of soluble

16 Archaea

iron and insoluble ferrihydrite and birnessite minerals [142](Table 1 reactions (3) and (4)) ANME-2d could even possiblydonate electrons to a bacterial partner besides nitrate-richenvironments ANME-2d archaea have been found inwells ofan aquifer where sulfate and methane concentrations overlap[143] Moreover ANME-2d was the only clade detected insediments of a freshwater lake where S-AOM occurred [144]Sulfate concentrations in these studies were low but above1mM and thus higher than the lowest reported concen-trations for S-AOM to occur [145 146] Lastly sequencesof ANME-2d were relatively more abundant in freshwatersediments fed with methane and sulfate than in sedimentsfed with onlymethane or only sulfate and noN-AOMactivitywas detected when fed with nitrate and methane [27] Theseindications hold promise that direct experimental evidencefor sulfate-dependent AOM by ANME-2d could be found inthe future

TheANME-1 genome contains fewerMHCgene domainsas compared to ANME-2a and ANME-2d and some otherarchaea such as somemethylotrophicmethanogens (Table 2)and some members of the Archaeoglobales [115] The MHCsof ANME-1 also have a smaller heme count as compared toother ANME and some other archaea with the largest beingan octaheme cytochrome [107] Each hemewithin aMHChasits own redox potential and therefore structurally differentMHCs represent a large range of redox potentials that canbe used for bioenergetic electron transfer (reviewed in [147])For instance metal oxide reduction in Shewanella oneidensisMR-1 is catalyzed by a chain of a tetraheme (CymA) twodecaheme (MtrA and MtrB) and eventually extracellulardecaheme cytochromes OmcAMtrC that reduce the ironminerals [121 148 149] In Geobacter sulfurreducens ironmineral reduction seems to be catalyzed by the tetrahemecytochrome OmcE and hexaheme cytochrome OmcS trans-ferring electrons from the outer membrane to type IV pilithat transmit the electrons to iron minerals [121 150 151]Since ANME-1 lack MHCs of the correct size and lack genedomains for pili production [116] they seem unable to reduceminerals via both mechanisms present in Shewanella andGeobacter It can therefore be speculated that ANME-1 areless versatile in electron acceptor use and are not able toreduce solid metal oxides However DIET mechanisms arestill not well understood and the true differences betweenMHCs of different ANME types need to be investigated usingbiochemical methods This would allow uncovering the truecapabilities concerning DIET

34 Menaquinones and Methanophenazines ANME-2a en-coded a protein with a domain specific for PhzF which is anenzyme involved in phenazine biosynthesis in Pseudomonasfluorescens [152 153] The respective gene is not present in allmethanophenazine containing methanogens (in our genomecomparison only inM acetivorans andM formicica Table 2)so it is unclear whether this enzyme is really involved inmethanophenazine biosynthesis It is however likely thatANME-2a use methanophenazines in their respiratory chainsince gene domains for menaquinone biosynthesis wereabsent (Table 2) ldquoCa M nitroreducensrdquo probably uses

menaquinones as membrane-integral electron carrier sinceenvironmental genomes [28 43] encoded the futalosine(mqn) biosynthesis pathway as reported for Archaeoglobusfulgidus [154] (Table 2) Moreover ldquoCa M nitroreducensrdquoenrichment cultures showed absence of methanophenazines[43] ANME-1 also contained gene domains formenaquinonebiosynthesis via the futalosine (mqn) biosynthesis pathway(Table 2) Indications for a quinone biosynthesis pathwayin ANME-1 were previously found to be weak since onlysome of the Ubi homologues of the oxic ubiquinone biosyn-thesis pathway were detected [41] but the futalosine (mqn)biosynthesis pathway was overlooked in that particular anal-ysis Additionally ANME-1 have Fqo homologues similarto Archaeoglobus fulgidus [44] and expressed the catalyticsubunit FqoF [41] However since the phenazine biosynthesisdomain PhzF was also present in the ANME-1 genomes(Table 2) and Fpo and Fqo are homologues we cannotconclude on genomic information alone which redox shuttleis used by ANME-1 during AOM If ANME-1 would usemenaquinones this would have implications for subsequentelectron transfer to MHCs since methanophenazine (1198640 =minus165mV) [155] and menaquinone (1198640 = minus80mV) [156] havedifferent redox potentials

35 Cell Adhesion Some gene domains involved in cel-lular adhesion were more abundant in ANME than inmethanogens (Table 2) especially in ANME-2a and ANME-1that are known to form syntrophic interactions for electrontransfer during respiration These domains include HYR(IPR003410) and CARDB domains (IPR011635) that bothhave a direct role in cellular adhesion [157] (Table 2) Interest-ingly also domains related to the cellulosome of Clostridiumspecies termed dockerin and cohesin were highly abundantin both ANME-1 and ANME-2a as compared to ANME-2dand methanogens together with many carbohydrate bindingdomains (Table 2) In Clostridium species dockerin andcohesin form an anchor to the bacterial cell wall that containsa scaffold with cellulose-degrading enzymes and a carbohy-drate bindingmodule that binds cellulose altogether formingthe cellulosome [158] These domains have been found in alldomains of life irrespective of cellulose utilization but thefunction of such proteins outside of the cellulosome is notknown [159]Therefore dockerin cohesin and carbohydratebinding domains in ANME could hypothetically form aconstruct that binds to carbohydrates and could possibly havea function in cell-to-cell contact or MHC adhesion but thisneeds further investigation

4 Future Challenges

Advances in (meta)genomics transcriptomics and pro-teomics have produced the valuable metabolic blueprints ofdifferent ANMEwith hypotheses on how centralmetabolismelectron transport and energy conservation may functionFuture experiments are needed to biochemically demonstratethat these hypotheses are correct

The bottleneck for biochemical studies of ANME isthe lack of pure cultures due to the slow and syntrophic

Archaea 17

growth However the recent milestone discovery of directelectron transfer provides opportunities to grow ANMEas stated previously on electron accepting electrodes (ieanodes) [160] In this way pure or highly enriched culturesof different ANME without their respective syntrophic part-ner could be obtained and MHCs responsible for electricconduction could be biochemically characterized It seemsthat ANME-1 are limited by the size and abundance ofMHCs which could relate to differences in behavior onan anode The partner bacteria of ANME-1 and ANME-2could be investigated on an electron donating electrode (iecathode) with specific focus on the ability to produce pili (ienanowires) Also worth investigating is if besides ANME-2d ANME-2ab could also use insoluble electron acceptorsand if ANME-2d could donate electrons to a bacterialpartner

Another future challenge is to isolate and characterizeMcr from different ANME clades It needs to be investi-gated if Mcr abundance in ANME cells compensates forthe slow reverse activity or if modifications in the Mcrof ANME-1 also contribute to a better reverse activity ofMcr Moreover the effect of methane partial pressure onreaction rates and enzyme kinetics needs to be determined insitu

ANME-1 are potentially able to perform hydrogeno-trophic methanogenesis due to the presence of a hydrogenasein the genome Genetic indications of menaquinones aselectron carrier in ANME-1 and the various cellulosome andcell adhesion related gene domains in all ANME are alsotopics that could be explored further Methanogenic archaeaare likely not able to perform AOM but additional studieson TMO and more genetic modifications to stimulate AOMin methanogens could help in understanding the param-eters needed for AOM to occur Ultimately physiologicalunderstanding of ANME will help to explain the observedecological niche separation of different ANME clades and theoccurrence of ANMEwithout a bacterial partnerThis wouldgreatly enhance our knowledge of themethane cycle in anoxicenvironments

Competing Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors thank Stefanie Berger (RU Nijmegen) for criticalreading of the manuscript This research is supported bythe Soehngen Institute of Anaerobic Microbiology (SIAM)Gravitation grant (024002002) of the Netherlands Ministryof Education Culture and Science and the NetherlandsOrganisation for Scientific Research (NWO) Mike S MJetten was further supported by ERC AG 339880 Eco-MoMand Alfons J M Stams was supported by ERC AG 323009Novel Anaerobes

References

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[2] K-U Hinrichs J M Hayes S P Sylva P G Brewert andE F DeLong ldquoMethane-consuming archaebacteria in marinesedimentsrdquo Nature vol 398 no 6730 pp 802ndash805 1999

[3] V J Orphan C H House K-U Hinrichs K D McKeeganand E F DeLong ldquoMethane-consuming archaea revealed bydirectly coupled isotopic and phylogenetic analysisrdquo Sciencevol 293 no 5529 pp 484ndash487 2001

[4] K-U Hinrichs and A Boetius ldquoThe anaerobic oxidation ofmethane new insights in microbial ecology and biogeochem-istryrdquo inOceanMargin Systems GWefer D Billett D HebbelnB B Joslashrgensen M Schluter and T VanWeering Eds pp 457ndash477 Springer Berlin Germany 2002

[5] K Knittel T Losekann A Boetius R Kort and R AmannldquoDiversity and distribution of methanotrophic archaea at coldseepsrdquo Applied and Environmental Microbiology vol 71 no 1pp 467ndash479 2005

[6] K Knittel and A Boetius ldquoAnaerobic oxidation of methaneprogress with an unknown processrdquo Annual Review of Micro-biology vol 63 pp 311ndash334 2009

[7] V J Orphan K-U Hinrichs W Ussler III et al ldquoComparativeanalysis of methane-oxidizing archaea and sulfate-reducingbacteria in anoxic marine sedimentsrdquoApplied and Environmen-tal Microbiology vol 67 no 4 pp 1922ndash1934 2001

[8] T Losekann K Knittel T Nadalig et al ldquoDiversity andabundance of aerobic and anaerobic methane oxidizers atthe Haakon Mosby Mud Volcano Barents Seardquo Applied andEnvironmentalMicrobiology vol 73 no 10 pp 3348ndash3362 2007

[9] H Niemann T Losekann D De Beer et al ldquoNovel microbialcommunities of the Haakon Mosby mud volcano and their roleas amethane sinkrdquoNature vol 443 no 7113 pp 854ndash858 2006

[10] TNunouraHOida T Toki J Ashi K Takai andKHorikoshildquoQuantification of mcrA by quantitative fluorescent PCR insediments from methane seep of the Nankai Troughrdquo FEMSMicrobiology Ecology vol 57 no 1 pp 149ndash157 2006

[11] B Orcutt A Boetius M Elvert V Samarkin and S B JoyeldquoMolecular biogeochemistry of sulfate reduction methanogen-esis and the anaerobic oxidation of methane at Gulf of Mexicocold seepsrdquoGeochimica et Cosmochimica Acta vol 69 no 17 pp4267ndash4281 2005

[12] V J Orphan W Ussler III T H Naehr C H House K-U Hinrichs and C K Paull ldquoGeological geochemical andmicrobiological heterogeneity of the seafloor around methanevents in the Eel River Basin offshore Californiardquo ChemicalGeology vol 205 no 3-4 pp 265ndash289 2004

[13] M G Pachiadaki A Kallionaki A Dahlmann G J De Langeand K A Kormas ldquoDiversity and spatial distribution ofprokaryotic communities along a sediment vertical profile ofa deep-sea mud volcanordquo Microbial Ecology vol 62 no 3 pp655ndash668 2011

[14] I Roalkvam H Dahle Y Chen S L Joslashrgensen H Haflidasonand I H Steen ldquoFine-scale community structure analysis ofANME in Nyegga sediments with high and low methane fluxrdquoFrontiers in Microbiology vol 3 p 216 2012

[15] K Yanagawa M Sunamura M A Lever et al ldquoNiche separa-tion of methanotrophic archaea (ANME-1 and -2) in methane-seep sediments of the Eastern Japan Sea offshore JoetsurdquoGeomicrobiology Journal vol 28 no 2 pp 118ndash129 2011

18 Archaea

[16] A Pernthaler A E Dekas C T Brown S K Goffredi TEmbaye and V J Orphan ldquoDiverse syntrophic partnershipsfromdeep-seamethane vents revealed by direct cell capture andmetagenomicsrdquo Proceedings of the National Academy of Sciencesof the United States of America vol 105 no 19 pp 7052ndash70572008

[17] R Hatzenpichler S A Connon D Goudeau R R Malm-strom T Woyke and V J Orphan ldquoVisualizing in situtranslational activity for identifying and sorting slow-growingarchaealminusbacterial consortiardquo Proceedings of the NationalAcademy of Sciences vol 113 no 28 pp E4069ndashE4078 2016

[18] L Maignien R J Parkes B Cragg et al ldquoAnaerobic oxidationof methane in hypersaline cold seep sedimentsrdquo FEMS Micro-biology Ecology vol 83 no 1 pp 214ndash231 2013

[19] V J Orphan C H House K-U Hinrichs K D McKeeganand E F DeLong ldquoMultiple archaeal groups mediate methaneoxidation in anoxic cold seep sedimentsrdquo Proceedings of theNational Academy of Sciences of the United States of Americavol 99 no 11 pp 7663ndash7668 2002

[20] T TreudeM Kruger A Boetius and B B Joslashrgensen ldquoEnviron-mental control on anaerobic oxidation of methane in the gassysediments of Eckernforde Bay (German Baltic)rdquo Limnology andOceanography vol 50 no 6 pp 1771ndash1786 2005

[21] G C Jagersma R J W Meulepas I Heikamp-De Jong etal ldquoMicrobial diversity and community structure of a highlyactive anaerobic methane-oxidizing sulfate-reducing enrich-mentrdquo Environmental Microbiology vol 11 no 12 pp 3223ndash3232 2009

[22] M Blumenberg R Seifert J Reitner T Pape andWMichaelisldquoMembrane lipid patterns typify distinct anaerobic methan-otrophic consortiardquo Proceedings of the National Academy ofSciences of the United States of America vol 101 no 30 pp 11111ndash11116 2004

[23] S Bertram M Blumenberg W Michaelis M Siegert MKruger and R Seifert ldquoMethanogenic capabilities of ANME-archaea deduced from 13C-labelling approachesrdquo Environmen-tal Microbiology vol 15 no 8 pp 2384ndash2393 2013

[24] K G Lloyd M J Alperin and A Teske ldquoEnvironmental evi-dence for net methane production and oxidation in putativeANaerobic MEthanotrophic (ANME) archaeardquo EnvironmentalMicrobiology vol 13 no 9 pp 2548ndash2564 2011

[25] M Takeuchi H Yoshioka Y Seo et al ldquoA distinct freshwater-adapted subgroup of ANME-1 dominates active archaeal com-munities in terrestrial subsurfaces in Japanrdquo EnvironmentalMicrobiology vol 13 no 12 pp 3206ndash3218 2011

[26] R T Amos B A Bekins I M Cozzarelli et al ldquoEvidence foriron-mediated anaerobic methane oxidation in a crude oil-contaminated aquiferrdquo Geobiology vol 10 no 6 pp 506ndash5172012

[27] P H Timmers D A Suarez-Zuluaga M van Rossem MDiender A J Stams and C M Plugge ldquoAnaerobic oxidationof methane associated with sulfate reduction in a naturalfreshwater gas sourcerdquo ISME Journal vol 10 pp 1400ndash14122015

[28] M F Haroon S Hu Y Shi et al ldquoAnaerobic oxidation ofmethane coupled to nitrate reduction in a novel archaeallineagerdquo Nature vol 500 no 7468 pp 567ndash570 2013

[29] H J Mills C Hodges K Wilson I R MacDonald and PA Sobecky ldquoMicrobial diversity in sediments associated withsurface-breaching gas hydrate mounds in the Gulf of MexicordquoFEMS Microbiology Ecology vol 46 no 1 pp 39ndash52 2003

[30] K G Lloyd L Lapham and A Teske ldquoAn anaerobic methane-oxidizing community of ANME-1b archaea in hypersaline gulfofMexico sedimentsrdquoApplied and EnvironmentalMicrobiologyvol 72 no 11 pp 7218ndash7230 2006

[31] A A Raghoebarsing A Pol K T Van De Pas-Schoonen et alldquoA microbial consortium couples anaerobic methane oxidationto denitrificationrdquoNature vol 440 no 7086 pp 918ndash921 2006

[32] S Hu R J Zeng L C Burow P Lant J Keller and Z YuanldquoEnrichment of denitrifying anaerobic methane oxidizingmicroorganismsrdquo Environmental Microbiology Reports vol 1no 5 pp 377ndash384 2009

[33] Z-W Ding J Ding L Fu F Zhang and R J Zeng ldquoSimultane-ous enrichment of denitrifying methanotrophs and anammoxbacteriardquo Applied Microbiology and Biotechnology vol 98 no24 pp 10211ndash10221 2014

[34] R Seifert K Nauhaus M Blumenberg M Kruger and WMichaelis ldquoMethane dynamics in a microbial community ofthe Black Sea traced by stable carbon isotopes in vitrordquoOrganicGeochemistry vol 37 no 10 pp 1411ndash1419 2006

[35] J Ding Z-W Ding L Fu Y-Z Lu S H Cheng and R JZeng ldquoNew primers for detecting and quantifying denitrifyinganaerobic methane oxidation archaea in different ecologicalnichesrdquo Applied Microbiology and Biotechnology vol 99 no 22pp 9805ndash9812 2015

[36] A Vaksmaa C Luke T van Alen et al ldquoDistribution and activ-ity of the anaerobic methanotrophic community in a nitrogen-fertilized Italian paddy soilrdquo FEMS Microbiology Ecology vol92 no 12 2016

[37] P N Evans D H Parks G L Chadwick et al ldquoMethanemetabolism in the archaeal phylum Bathyarchaeota revealed bygenome-centric metagenomicsrdquo Science vol 350 no 6259 pp434ndash438 2015

[38] I Vanwonterghem P N Evans D H Parks et al ldquoMethy-lotrophic methanogenesis discovered in the archaeal phylumVerstraetearchaeotardquo Nature Microbiology vol 1 Article ID16170 2016

[39] P Worm J J Koehorst M Visser et al ldquoA genomic view onsyntrophic versus non-syntrophic lifestyle in anaerobic fattyacid degrading communitiesrdquo Biochimica et Biophysica ActamdashBioenergetics vol 1837 no 12 pp 2004ndash2016 2014

[40] R Stokke I Roalkvam A Lanzen H Haflidason and I HSteen ldquoIntegrated metagenomic and metaproteomic analysesof an ANME-1-dominated community in marine cold seepsedimentsrdquo Environmental Microbiology vol 14 no 5 pp 1333ndash1346 2012

[41] A Meyerdierks M Kube I Kostadinov et al ldquoMetagenomeand mRNA expression analyses of anaerobic methanotrophicarchaea of the ANME-1 grouprdquo Environmental Microbiologyvol 12 no 2 pp 422ndash439 2010

[42] F-P Wang Y Zhang Y Chen et al ldquoMethanotrophicarchaea possessing diverging methane-oxidizing and electron-transporting pathwaysrdquo ISME Journal vol 8 no 5 pp 1069ndash1078 2014

[43] A Arshad D R Speth R M de Graaf H J Op den Camp MS Jetten and C U Welte ldquoA metagenomics-based metabolicmodel of nitrate-dependent anaerobic oxidation of methane byMethanoperedens-like archaeardquo Frontiers inMicrobiology vol 6article1423 2015

[44] S J Hallam N Putnam CM Preston et al ldquoReversemethano-genesis testing the hypothesis with environmental genomicsrdquoScience vol 305 no 5689 pp 1457ndash1462 2004

Archaea 19

[45] R K Thauer ldquoAnaerobic oxidation of methane with sulfate onthe reversibility of the reactions that are catalyzed by enzymesalso involved inmethanogenesis fromCO

2rdquoCurrent Opinion in

Microbiology vol 14 no 3 pp 292ndash299 2011[46] U Deppenmeier V Muller and G Gottschalk ldquoPathways of

energy conservation in methanogenic archaeardquo Archives ofMicrobiology vol 165 no 3 pp 149ndash163 1996

[47] A-K Kaster J Moll K Parey and R K Thauer ldquoCoupling offerredoxin and heterodisulfide reduction via electron bifurca-tion in hydrogenotrophic methanogenic archaeardquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 108 no 7 pp 2981ndash2986 2011

[48] R K Thauer A-K Kaster H Seedorf W Buckel and RHedderich ldquoMethanogenic archaea ecologically relevant dif-ferences in energy conservationrdquo Nature Reviews Microbiologyvol 6 no 8 pp 579ndash591 2008

[49] W Ludwig O Strunk R Westram et al ldquoARB a softwareenvironment for sequence datardquoNucleic Acids Research vol 32no 4 pp 1363ndash1371 2004

[50] E Pruesse C Quast K Knittel et al ldquoSILVA a comprehensiveonline resource for quality checked and aligned ribosomal RNAsequence data compatible with ARBrdquo Nucleic Acids Researchvol 35 no 21 pp 7188ndash7196 2007

[51] J J Marlow C T Skennerton Z Li et al ldquoProteomic stableisotope probing reveals biosynthesis dynamics of slow growingmethane based microbial communitiesrdquo Frontiers in Microbiol-ogy vol 7 article 386 2016

[52] P V Welander and W W Metcalf ldquoLoss of the mtr operon inMethanosarcina blocks growth on methanol but not methano-genesis and reveals an unknown methanogenic pathwayrdquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 102 no 30 pp 10664ndash10669 2005

[53] P V Welander and W W Metcalf ldquoMutagenesis of the C1oxidation pathway inmethanosarcina barkeri new insights intothe MtrMer bypass pathwayrdquo Journal of Bacteriology vol 190no 6 pp 1928ndash1936 2008

[54] M Goenrich R K Thauer H Yurimoto and N KatoldquoFormaldehyde activating enzyme (Fae) and hexulose-6-phosphate synthase (Hps) inMethanosarcina barkeri a possiblefunction in ribose-5-phosphate biosynthesisrdquoArchives ofMicro-biology vol 184 no 1 pp 41ndash48 2005

[55] M Goenrich FMahlert E C Duin C Bauer B Jaun and R KThauer ldquoProbing the reactivity of Ni in the active site of methyl-coenzyme M reductase with substrate analoguesrdquo Journal ofBiological Inorganic Chemistry vol 9 no 6 pp 691ndash705 2004

[56] S Scheller M Goenrich R Boecher R K Thauer and BJaun ldquoThe key nickel enzyme of methanogenesis catalyses theanaerobic oxidation of methanerdquo Nature vol 465 no 7298 pp606ndash608 2010

[57] K Nauhaus A Boetius M Kruger and F Widdel ldquoIn vitrodemonstration of anaerobic oxidation of methane coupled tosulphate reduction in sediment from amarine gas hydrate areardquoEnvironmental Microbiology vol 4 no 5 pp 296ndash305 2002

[58] Y Zhang J-P Henriet J Bursens and N Boon ldquoStimulationof in vitro anaerobic oxidation of methane rate in a continuoushigh-pressure bioreactorrdquo Bioresource Technology vol 101 no9 pp 3132ndash3138 2010

[59] M Kruger T Treude H Wolters K Nauhaus and A BoetiusldquoMicrobial methane turnover in different marine habitatsrdquoPalaeogeography Palaeoclimatology Palaeoecology vol 227 no1ndash3 pp 6ndash17 2005

[60] C Deusner V Meyer and T G Ferdelman ldquoHigh-pressuresystems for gas-phase free continuous incubation of enrichedmarinemicrobial communities performing anaerobic oxidationof methanerdquo Biotechnology and Bioengineering vol 105 no 3pp 524ndash533 2010

[61] K Nauhaus T Treude A Boetius and M Kruger ldquoEnviron-mental regulation of the anaerobic oxidation of methane acomparison of ANME-I and ANME-II communitiesrdquo Environ-mental Microbiology vol 7 no 1 pp 98ndash106 2005

[62] T Treude V Orphan K Knittel A Gieseke C H House andA Boetius ldquoConsumption of methane and CO

2by methan-

otrophicmicrobial mats from gas seeps of the anoxic Black SeardquoApplied and EnvironmentalMicrobiology vol 73 no 7 pp 2271ndash2283 2007

[63] T Holler F Widdel K Knittel et al ldquoThermophilic anaerobicoxidation of methane by marine microbial consortiardquo ISMEJournal vol 5 no 12 pp 1946ndash1956 2011

[64] M Kruger M Blumenberg S Kasten et al ldquoA novel multi-layered methanotrophic microbial mat system growing on thesediment of the Black Seardquo Environmental Microbiology vol 10no 8 pp 1934ndash1947 2008

[65] R J WMeulepas C G Jagersma J Gieteling C J N BuismanA J M Stams and P N L Lens ldquoEnrichment of anaerobicmethanotrophs in sulfate-reducing membrane bioreactorsrdquoBiotechnology and Bioengineering vol 104 no 3 pp 458ndash4702009

[66] T Holler G Wegener H Niemann et al ldquoCarbon and sulfurback flux during anaerobic microbial oxidation of methane andcoupled sulfate reductionrdquo Proceedings of the National Academyof Sciences of the United States of America vol 108 no 52 ppE1484ndashE1490 2011

[67] M Kruger AMeyerdierks F O Glockner et al ldquoA conspicuousnickel protein in microbial mats that oxidize methane anaero-bicallyrdquo Nature vol 426 no 6968 pp 878ndash881 2003

[68] S Mayr C Latkoczy M Kruger et al ldquoStructure of an F430

variant from archaea associated with anaerobic oxidation ofmethanerdquo Journal of the American Chemical Society vol 130 no32 pp 10758ndash10767 2008

[69] S Shima and R K Thauer ldquoMethyl-coenzyme M reductaseand the anaerobic oxidation of methane in methanotrophicArchaeardquo Current Opinion in Microbiology vol 8 no 6 pp643ndash648 2005

[70] R K Thauer and S Shima ldquoMethane as fuel for anaerobicmicroorganismsrdquo Annals of the New York Academy of Sciencesvol 1125 pp 158ndash170 2008

[71] S Yamamoto J B Alcauskas and T E Crozier ldquoSolubility ofmethane in distilled water and seawaterrdquo Journal of Chemicaland Engineering Data vol 21 no 1 pp 78ndash80 1976

[72] P H A Timmers J Gieteling H C A Widjaja-Greefkeset al ldquoGrowth of anaerobic methane-oxidizing archaea andsulfate-reducing bacteria in a high-pressure membrane capsulebioreactorrdquoApplied and EnvironmentalMicrobiology vol 81 no4 pp 1286ndash1296 2015

[73] MKruger HWoltersMGehre S B Joye andH-H RichnowldquoTracing the slow growth of anaerobic methane-oxidizingcommunities by 15N-labelling techniquesrdquo FEMS MicrobiologyEcology vol 63 no 3 pp 401ndash411 2008

[74] R J W Meulepas C G Jagersma A F Khadem C J N Buis-man A J M Stams and P N L Lens ldquoEffect of environmentalconditions on sulfate reduction withmethane as electron donorby an Eckernforde Bay enrichmentrdquo Environmental Science andTechnology vol 43 no 17 pp 6553ndash6559 2009

20 Archaea

[75] M W Bowles V A Samarkin and S B Joye ldquoImprovedmeasurement of microbial activity in deep-sea sediments atin situ pressure and methane concentrationrdquo Limnology andOceanography Methods vol 9 pp 499ndash506 2011

[76] S Shima M Krueger T Weinert et al ldquoStructure of a methyl-coenzyme M reductase from Black Sea mats that oxidizemethane anaerobicallyrdquo Nature vol 481 no 7379 pp 98ndash1012012

[77] K D Allen G Wegener and R H White ldquoDiscovery of multi-ple modified F-430 coenzymes in methanogens and anaerobicmethanotrophic archaea suggests possible new roles for F-430in naturerdquoApplied and Environmental Microbiology vol 80 no20 pp 6403ndash6412 2014

[78] V W Soo M J McAnulty A Tripathi et al ldquoReversingmethanogenesis to capture methane for liquid biofuel precur-sorsrdquoMicrobial Cell Factories vol 15 article 11 2016

[79] D L Valentine and W S Reeburgh ldquoNew perspectives onanaerobicmethane oxidationrdquoEnvironmentalMicrobiology vol2 no 5 pp 477ndash484 2000

[80] D L Valentine ldquoBiogeochemistry and microbial ecology ofmethane oxidation in anoxic environments a reviewrdquo Antonievan Leeuwenhoek International Journal of General and Molecu-lar Microbiology vol 81 no 1-4 pp 271ndash282 2002

[81] A J B Zehnder and T D Brock ldquoMethane formation andmethane oxidation by methanogenic bacteriardquo Journal of Bac-teriology vol 137 no 1 pp 420ndash432 1979

[82] J Harder ldquoAnaerobic methane oxidation by bacteria employ-ing 14C-methane uncontaminated with 14C-carbon monoxiderdquoMarine Geology vol 137 no 1-2 pp 13ndash23 1997

[83] J J Moran C H House K H Freeman and J G FerryldquoTrace methane oxidation studied in several Euryarchaeotaunder diverse conditionsrdquo Archaea vol 1 no 5 pp 303ndash3092005

[84] J J Moran C H House B Thomas and K H FreemanldquoProducts of tracemethane oxidation during nonmethyltrophicgrowth by Methanosarcinardquo Journal of Geophysical ResearchBiogeosciences vol 112 no 2 2007

[85] R J W Meulepas C G Jagersma Y Zhang et al ldquoTracemethane oxidation and the methane dependency of sulfatereduction in anaerobic granular sludgerdquo FEMS MicrobiologyEcology vol 72 no 2 pp 261ndash271 2010

[86] A J B Zehnder andTD Brock ldquoAnaerobicmethane oxidationoccurrence and ecologyrdquoApplied and Environmental Microbiol-ogy vol 39 no 1 pp 194ndash204 1980

[87] S J Blazewicz D G Petersen M P Waldrop and M K Fire-stone ldquoAnaerobic oxidation of methane in tropical and borealsoils ecological significance in terrestrial methane cyclingrdquoJournal of Geophysical Research Biogeosciences vol 117 no 2Article ID G02033 2012

[88] K A Smemo and J B Yavitt ldquoEvidence for anaerobic CH4

oxidation in freshwater peatlandsrdquo Geomicrobiology Journalvol 24 no 7-8 pp 583ndash597 2007

[89] M J Alperin and T M Hoehler ldquoAnaerobic methane oxidationby archaeasulfate-reducing bacteria aggregates 1 Thermody-namic and physical constraintsrdquo American Journal of Sciencevol 309 no 10 pp 869ndash957 2009

[90] S L Caldwell J R Laidler E A Brewer J O Eberly S CSandborgh and F S Colwell ldquoAnaerobic oxidation of methanemechanisms bioenergetics and the ecology of associatedmicroorganismsrdquo Environmental Science and Technology vol42 no 18 pp 6791ndash6799 2008

[91] GWang A J Spivack and S DrsquoHondt ldquoGibbs energies of reac-tion and microbial mutualism in anaerobic deep subseafloorsediments of ODP Site 1226rdquoGeochimica et Cosmochimica Actavol 74 no 14 pp 3938ndash3947 2010

[92] P R Girguis A E Cozen and E F DeLong ldquoGrowth andpopulation dynamics of anaerobic methane-oxidizing archaeaand sulfate-reducing bacteria in a continuous-flow bioreactorrdquoApplied and EnvironmentalMicrobiology vol 71 no 7 pp 3725ndash3733 2005

[93] K Nauhaus M Albrecht M Elvert A Boetius and F WiddelldquoIn vitro cell growth ofmarine archaeal-bacterial consortia dur-ing anaerobic oxidation ofmethanewith sulfaterdquoEnvironmentalMicrobiology vol 9 no 1 pp 187ndash196 2007

[94] B Orcutt V Samarkin A Boetius and S Joye ldquoOn the relation-ship between methane production and oxidation by anaerobicmethanotrophic communities from cold seeps of the Gulf ofMexicordquo Environmental Microbiology vol 10 no 5 pp 1108ndash1117 2008

[95] M Y Yoshinaga T Holler T Goldhammer et al ldquoCarbon iso-tope equilibration during sulphate-limited anaerobic oxidationof methanerdquo Nature Geoscience vol 7 no 3 pp 190ndash194 2014

[96] T Treude J Niggemann J Kallmeyer et al ldquoAnaerobic oxi-dation of methane and sulfate reduction along the Chileancontinental marginrdquo Geochimica et Cosmochimica Acta vol 69no 11 pp 2767ndash2779 2005

[97] R J Parkes B A Cragg N Banning et al ldquoBiogeochemistryand biodiversity of methane cycling in subsurface marinesediments (SkagerrakDenmark)rdquoEnvironmentalMicrobiologyvol 9 no 5 pp 1146ndash1161 2007

[98] N J Knab B A Cragg E R C Hornibrook et al ldquoRegulationof anaerobic methane oxidation in sediments of the Black SeardquoBiogeosciences vol 6 no 8 pp 1505ndash1518 2009

[99] H Yoshioka A Maruyama T Nakamura et al ldquoActivities anddistribution of methanogenic and methane-oxidizing microbesin marine sediments from the Cascadia Marginrdquo Geobiologyvol 8 no 3 pp 223ndash233 2010

[100] G Wegener V Krukenberg S E Ruff M Y Kellermann andK Knittel ldquoMetabolic capabilities of microorganisms involvedin and associated with the anaerobic oxidation of methanerdquoFrontiers in Microbiology vol 7 article 46 2016

[101] R J W Meulepas C G Jagersma A F Khadem A J MStams and P N L Lens ldquoEffect of methanogenic substrateson anaerobic oxidation of methane and sulfate reduction by ananaerobic methanotrophic enrichmentrdquo Applied Microbiologyand Biotechnology vol 87 no 4 pp 1499ndash1506 2010

[102] J Milucka T G Ferdelman L Polerecky et al ldquoZero-valentsulphur is a key intermediate in marine methane oxidationrdquoNature vol 491 no 7425 pp 541ndash546 2012

[103] W Michaelis R Seifert K Nauhaus et al ldquoMicrobial reefs inthe black sea fueled by anaerobic oxidation ofmethanerdquo Sciencevol 297 no 5583 pp 1013ndash1015 2002

[104] A Vigneron P Cruaud P Pignet et al ldquoArchaeal and anaerobicmethane oxidizer communities in the Sonora Margin coldseeps Guaymas Basin (Gulf of California)rdquo ISME Journal vol7 no 8 pp 1595ndash1608 2013

[105] M Alperin and T Hoehler ldquoThe ongoing mystery of sea-floormethanerdquo Science vol 329 no 5989 pp 288ndash289 2010

[106] B Orcutt and C Meile ldquoConstraints on mechanisms and ratesof anaerobic oxidation of methane by microbial consortiaprocess-basedmodeling of ANME-2 archaea and sulfate reduc-ing bacteria interactionsrdquo Biogeosciences vol 5 no 6 pp 1587ndash1599 2008

Archaea 21

[107] S E McGlynn G L Chadwick C P Kempes and V J OrphanldquoSingle cell activity reveals direct electron transfer in methan-otrophic consortiardquoNature vol 526 no 7574 pp 531ndash535 2015

[108] D R Lovley ldquoElectromicrobiologyrdquo Annual Review of Microbi-ology vol 66 pp 391ndash409 2012

[109] S M Strycharz-Glaven R M Snider A Guiseppi-Elie andL M Tender ldquoOn the electrical conductivity of microbialnanowires and biofilmsrdquoEnergy and Environmental Science vol4 no 11 pp 4366ndash4379 2011

[110] D J Richardson J N Butt J K Fredrickson et al ldquoThe lsquoporinndashcytochromersquo model for microbe-to-mineral electron transferrdquoMolecular Microbiology vol 85 no 2 pp 201ndash212 2012

[111] A Okamoto K Hashimoto and R Nakamura ldquoLong-rangeelectron conduction of Shewanella biofilms mediated by outermembrane C-type cytochromesrdquo Bioelectrochemistry vol 85pp 61ndash65 2012

[112] M Y El-Naggar G Wanger K M Leung et al ldquoElectricaltransport along bacterial nanowires from Shewanella oneidensisMR-1rdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 107 no 42 pp 18127ndash18131 2010

[113] G Reguera K D McCarthy T Mehta J S Nicoll M TTuominen and D R Lovley ldquoExtracellular electron transfer viamicrobial nanowiresrdquo Nature vol 435 no 7045 pp 1098ndash11012005

[114] Z M Summers H E Fogarty C Leang A E Franks N SMalvankar and D R Lovley ldquoDirect exchange of electronswithin aggregates of an evolved syntrophic coculture of anaer-obic bacteriardquo Science vol 330 no 6009 pp 1413ndash1415 2010

[115] A Kletzin T Heimerl J Flechsler L V Niftrik R Rachel andA Klingl ldquoCytochromes c in archaea distribution maturationcell architecture and the special case of Ignicoccus hospitalisrdquoFrontiers in Microbiology vol 6 article 439 2015

[116] GWegener V Krukenberg D Riedel H E Tegetmeyer and ABoetius ldquoIntercellular wiring enables electron transfer betweenmethanotrophic archaea and bacteriardquo Nature vol 526 no7574 pp 587ndash590 2015

[117] D HHaft S H Payne and J D Selengut ldquoArchaeosortases andexosortases are widely distributed systems linking membranetransit with posttranslational modificationrdquo Journal of Bacteri-ology vol 194 no 1 pp 36ndash48 2012

[118] A Marchler-Bauer M K Derbyshire N R Gonzales et alldquoCDD NCBIrsquos conserved domain databaserdquo Nucleic AcidsResearch vol 43 no 1 pp D222ndashD226 2015

[119] A Mitchell H-Y Chang L Daugherty et al ldquoThe InterProprotein families database the classification resource after 15yearsrdquo Nucleic Acids Research vol 43 no 1 pp D213ndashD2212015

[120] V Krukenberg K Harding M Richter et al ldquoCandidatusdesulfofervidus auxilii a hydrogenotrophic sulfate-reducingbacterium involved in the thermophilic anaerobic oxidation ofmethanerdquo Environmental Microbiology vol 18 pp 3073ndash30912016

[121] L Shi T C Squier J M Zachara and J K Fredrickson ldquoRes-piration of metal (hydr)oxides by Shewanella and Geobactera key role for multihaem c-type cytochromesrdquo MolecularMicrobiology vol 65 no 1 pp 12ndash20 2007

[122] N S Malvankar and D R Lovley ldquoMicrobial nanowires forbioenergy applicationsrdquo Current Opinion in Biotechnology vol27 pp 88ndash95 2014

[123] A-E Rotaru T LWoodard K PNevin andDR Lovley ldquoLinkbetween capacity for current production and syntrophic growth

in Geobacter speciesrdquo Frontiers in Microbiology vol 6 article744 2015

[124] A-E Rotaru P M Shrestha F Liu et al ldquoDirect interspecieselectron transfer between Geobacter metallireducens andMethanosarcina barkerirdquo Applied and Environmental Microbi-ology vol 80 no 15 pp 4599ndash4605 2014

[125] S Scheller H Yu G L Chadwick S E McGlynn and VJ Orphan ldquoArtificial electron acceptors decouple archaealmethane oxidation from sulfate reductionrdquo Science vol 351 no6274 pp 703ndash707 2016

[126] J Milucka F Widdel and S Shima ldquoImmunological detec-tion of enzymes for sulfate reduction in anaerobic methane-oxidizing consortiardquo Environmental Microbiology vol 15 no 5pp 1561ndash1571 2013

[127] P Cabello M D Roldan and C Moreno-Vivian ldquoNitratereduction and the nitrogen cycle in archaeardquoMicrobiology vol150 no 11 pp 3527ndash3546 2004

[128] R MMartinez-Espinosa E J Dridge M J Bonete et al ldquoLookon the positive sideThe orientation identification and bioener-getics of lsquoArchaealrsquomembrane-boundnitrate reductasesrdquoFEMSMicrobiology Letters vol 276 no 2 pp 129ndash139 2007

[129] S de VriesMMomcilovicM J F Strampraad J PWhiteleggeA Baghai and I Schroder ldquoAdaptation to a high-tungsten envi-ronment pyrobaculum aerophilum contains an active tungstennitrate reductaserdquo Biochemistry vol 49 no 45 pp 9911ndash99212010

[130] M Egger O Rasigraf C J Sapart et al ldquoIron-mediated anaer-obic oxidation of methane in brackish coastal sedimentsrdquoEnvironmental Science and Technology vol 49 no 1 pp 277ndash283 2015

[131] T Treude S Krause J Maltby A W Dale R Coffin and LJ Hamdan ldquoSulfate reduction and methane oxidation activitybelow the sulfate-methane transition zone in Alaskan BeaufortSea continental margin sediments implications for deep sulfurcyclingrdquo Geochimica et Cosmochimica Acta vol 144 pp 217ndash237 2014

[132] N Riedinger M J Formolo T W Lyons S Henkel A Beckand S Kasten ldquoAn inorganic geochemical argument for coupledanaerobic oxidation of methane and iron reduction in marinesedimentsrdquo Geobiology vol 12 no 2 pp 172ndash181 2014

[133] Y-H Chang T-W Cheng W-J Lai et al ldquoMicrobial methanecycling in a terrestrialmud volcano in eastern Taiwanrdquo Environ-mental Microbiology vol 14 no 4 pp 895ndash908 2012

[134] S A Crowe S Katsev K Leslie et al ldquoThe methane cycle inferruginous Lake Matanordquo Geobiology vol 9 no 1 pp 61ndash782011

[135] O Sivan M Adler A Pearson et al ldquoGeochemical evidence foriron-mediated anaerobic oxidation of methanerdquo Limnology andOceanography vol 56 no 4 pp 1536ndash1544 2011

[136] K E A Segarra C Comerford J Slaughter and S B JoyeldquoImpact of electron acceptor availability on the anaerobic oxi-dation of methane in coastal freshwater and brackish wetlandsedimentsrdquo Geochimica et Cosmochimica Acta vol 115 pp 15ndash30 2013

[137] V Gupta K A Smemo J B Yavitt D Fowle B Branfireunand N Basiliko ldquoStable isotopes reveal widespread anaerobicmethane oxidation across latitude and peatland typerdquo Environ-mental Science and Technology vol 47 no 15 pp 8273ndash82792013

[138] O Oni T Miyatake S Kasten et al ldquoDistinct microbialpopulations are tightly linked to the profile of dissolved iron in

22 Archaea

the methanic sediments of the Helgolandmud area North SeardquoFrontiers in Microbiology vol 6 2015

[139] E J Beal C H House and V J Orphan ldquoManganese- andiron-dependent marine methane oxidationrdquo Science vol 325no 5937 pp 184ndash187 2009

[140] M W Bowles V A Samarkin K M Bowles and S B JoyeldquoWeak coupling between sulfate reduction and the anaerobicoxidation of methane in methane-rich seafloor sedimentsduring ex situ incubationrdquo Geochimica et Cosmochimica Actavol 75 no 2 pp 500ndash519 2011

[141] Y Z Lu L Fu J Ding Z Ding N Li and R J Zeng ldquoCr(VI)reduction coupled with anaerobic oxidation of methane in alaboratory reactorrdquoWater Research vol 102 pp 445ndash452 2016

[142] K F Ettwig B Zhu D Speth J T Keltjens M S Jetten and BKartal ldquoArchaea catalyze iron-dependent anaerobic oxidationof methanerdquo Proceedings of the National Academy of Sciences ofthe United States of America vol 113 no 45 pp 12792ndash127962016

[143] T M Flynn R A Sanford H Ryu et al ldquoFunctional microbialdiversity explains groundwater chemistry in a pristine aquiferrdquoBMCMicrobiology vol 13 no 1 article no 146 2013

[144] C J Schubert F Vazquez T Losekann-Behrens K KnittelM Tonolla and A Boetius ldquoEvidence for anaerobic oxidationof methane in sediments of a freshwater system (Lago diCadagno)rdquo FEMS Microbiology Ecology vol 76 no 1 pp 26ndash38 2011

[145] K E A Segarra F Schubotz V Samarkin M Y Yoshinaga K-U Hinrichs and S B Joye ldquoHigh rates of anaerobic methaneoxidation in freshwater wetlands reduce potential atmosphericmethane emissionsrdquo Nature Communications vol 6 article7477 2015

[146] E J Beal M W Claire and C H House ldquoHigh rates ofanaerobic methanotrophy at low sulfate concentrations withimplications for past and present methane levelsrdquo Geobiologyvol 9 no 2 pp 131ndash139 2011

[147] F Kracke I Vassilev and J O Kromer ldquoMicrobial electrontransport and energy conservationmdashthe foundation for opti-mizing bioelectrochemical systemsrdquo Frontiers in Microbiologyvol 6 article 575 2015

[148] C L Reardon A C Dohnalkova P Nachimuthu et al ldquoRoleof outer-membrane cytochromes MtrC and OmcA in thebiomineralization of ferrihydrite by Shewanella oneidensisMR-1rdquo Geobiology vol 8 no 1 pp 56ndash68 2010

[149] L Shi B Chen Z Wang et al ldquoIsolation of a high-affinityfunctional protein complex between OmcA and MtrC twoouter membrane decaheme c-type cytochromes of Shewanellaoneidensis MR-1rdquo Journal of Bacteriology vol 188 no 13 pp4705ndash4714 2006

[150] X Qian T Mester L Morgado et al ldquoBiochemical charac-terization of purified OmcS a c-type cytochrome requiredfor insoluble Fe(III) reduction in Geobacter sulfurreducensrdquoBiochimica et BiophysicaActamdashBioenergetics vol 1807 no 4 pp404ndash412 2011

[151] T Mehta M V Coppi S E Childers and D R Lovley ldquoOutermembrane c-type cytochromes required for Fe(III) andMn(IV)oxide reduction in Geobacter sulfurreducensrdquo Applied andEnvironmentalMicrobiology vol 71 no 12 pp 8634ndash8641 2005

[152] W Blankenfeldt A P Kuzin T Skarina et al ldquoStructure andfunction of the phenazine biosynthetic protein PhzF fromPseudomonas fluorescensrdquoProceedings of theNational Academyof Sciences of the United States of America vol 101 no 47 pp16431ndash16436 2004

[153] J F Parsons F Song L Parsons K Calabrese E Eisensteinand J E Ladner ldquoStructure and function of the phenazinebiosynthesis protein PhzF fromPseudomonas fluorescens 2-79rdquoBiochemistry vol 43 no 39 pp 12427ndash12435 2004

[154] T Hiratsuka K Furihata J Ishikawa et al ldquoAn alternativemenaquinone biosynthetic pathway operating in microorgan-ismsrdquo Science vol 321 no 5896 pp 1670ndash1673 2008

[155] M Tietze A Beuchle I Lamla et al ldquoRedox potentials ofmethanophenazine and CoB-S-S-CoM factors involved inelectron transport in methanogenic archaeardquo ChemBioChemvol 4 no 4 pp 333ndash335 2003

[156] Q H Tran and G Unden ldquoChanges in the proton potentialand the cellular energetics of Escherichia coli during growth byaerobic and anaerobic respiration or by fermentationrdquoEuropeanJournal of Biochemistry vol 251 no 1-2 pp 538ndash543 1998

[157] I Callebaut D Gilges I Vigon and J-P Mornon ldquoHYR anextracellular module involved in cellular adhesion and relatedto the immunoglobulin-like foldrdquo Protein Science vol 9 no 7pp 1382ndash1390 2000

[158] H J Gilbert ldquoCellulosomes microbial nanomachines that dis-play plasticity in quaternary structurerdquoMolecular Microbiologyvol 63 no 6 pp 1568ndash1576 2007

[159] A Peer S P Smith E A Bayer R Lamed and I BorovokldquoNoncellulosomal cohesin- and dockerin-like modules in thethree domains of liferdquo FEMS Microbiology Letters vol 291 no1 pp 1ndash16 2009

[160] M Wagner ldquoMicrobiology conductive consortiardquo Nature vol526 no 7574 pp 513ndash514 2015

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Archaea 5

Table2Con

tinued

InterPro

IDANME-1S

ANME-1M

ANME-2a

ANME-2d

HANME-2d

AAM

AM-1

M-2

M-3

H-1

H-2

H-3

H-4

SMethylotro

phicmethanogenesis

Methyltransfe

rase

MtaACmuA

IPR0

06360

00

00

07

04

56

00

10

0Methano

l-cob

alam

inmethyltransfe

raseB

subu

nit

IPR0

21079

00

00

03

02

22

00

00

0

Mon

omethylamine

methyltransfe

rase

Mtm

BIPR0

08031

30

00

012

012

2115

00

00

0

Trim

ethylaminem

ethyltransfe

rase

IPR0

10426

110

00

04

05

22

00

00

0Dim

ethylaminem

ethyltransfe

rase

MtbB

IPR0

12653

00

00

09

06

66

00

00

0

Trim

ethylaminem

ethyltransfe

rase

Methanosarcina

IPR0

12740

00

00

02

01

11

00

00

0

Methylaminem

ethyltransfe

rase

corrinoidproteinredu

ctivea

ctivase

IPR0

26339

00

00

04

02

22

00

00

0

C-type

cytochromes

Di-h

aem

cytochrome

transm

embranenitrater

eductio

nIPR0

16174

20

43

74

00

40

11

00

1

Dou

bled

CXXC

Hmotif

IPR0

10177

330

32

30

00

00

00

00

0Cy

tochromec

-like

domain

IPR0

09056

20

60

1715

04

86

00

00

4ClassIIIcytochromeC

(tetrahem

ecytochrome)

IPR0

20942

20

03

30

00

00

00

00

0

Tetrahem

ecytochrom

edom

ain

flavocytochromec

3(Shewa

nella)

IPR0

12286

40

45

42

00

10

10

00

2

Octahem

ec-ty

pecytochrome

IPR0

24673

10

20

00

00

22

00

00

1Methano

genesis

multih

emec

-type

cytochrome

IPR0

27594

00

10

01

01

11

00

00

0

Multih

emec

ytochrom

eIPR0

11031

7815

5280

733

06

814

00

01

7S-layerd

omains

S-layerfam

ilydu

plicationdo

main

IPR0

06457

130

2916

2634

1916

4417

00

00

0Sarcinarrayfamily

protein

IPR0

26476

00

60

41

00

21

00

00

0S-layerh

omolog

ydo

main

IPR0

01119

10

20

00

00

00

00

00

0Ce

llexportandcelladhesio

nHYR

domain

IPR0

03410

15

20

00

00

00

00

00

0CA

RDBdo

main

IPR0

11635

6414

156

630

41

40

90

03

8Collagen-bind

ingsurfa

ceprotein

Cna-lik

eB-type

domain

IPR0

08454

41

21

80

60

22

00

00

0

vonWillebrand

factortypeA

IPR0

02035

5528

1732

1437

2317

429

288

027

7VWAN-te

rminal

IPR0

13608

12

00

00

00

00

00

00

0Ad

hesio

nlip

oprotein

IPR0

06128

84

45

00

53

04

45

00

0Ad

hesin

BIPR0

06129

03

45

00

30

04

03

00

0

6 Archaea

Table2Con

tinued

InterPro

IDANME-1S

ANME-1M

ANME-2a

ANME-2d

HANME-2d

AAM

AM-1

M-2

M-3

H-1

H-2

H-3

H-4

SInvasin

intim

incell-adhesio

nfragments

IPR0

0896

417

03

26

70

27

01

20

22

Putativ

ecellw

allbinding

repeat2

IPR0

07253

22

00

00

00

00

00

00

0ArchaeosortaseA

IPR0

14522

20

12

21

11

11

10

02

1ArchaeosortaseB

IPR0

26430

00

00

00

00

01

00

00

0ArchaeosortaseC

IPR0

22504

00

12

10

01

10

00

00

0Ex

osortasearchaeosortased

omain

IPR0

26392

50

25

31

12

22

10

12

1Ex

osortaseE

psH

IPR0

13426

10

01

00

00

00

00

00

0Ex

osortase

EpsH

-related

IPR0

19127

42

23

21

12

11

10

12

1Archaeosortasefam

ilyproteinArtE

IPR0

26485

00

00

00

00

00

00

10

0Cellw

allhydrolaseautolysin

catalytic

IPR0

02508

22

10

00

00

00

00

01

0

PEF-CT

ERM

proteinsorting

domain

IPR0

17474

00

34

10

010

190

00

00

0

PGF-pre-PG

Fdo

main

IPR0

26453

11

189

824

07

2111

00

01

1PG

F-CT

ERM

archaeal

protein-sortingsig

nal

IPR0

26371

94

62

12

02

12

10

01

3

LPXT

Gcellwallancho

rdom

ain

IPR0

19931

30

10

00

11

00

00

00

0VPX

XXP

-CTE

RMproteinsorting

domain

IPR0

26428

00

00

00

00

05

00

00

0

Cellu

losome-relatedDockerin

Cellulosomea

ncho

ringprotein

cohesin

domain

IPR0

02102

8077

524

122

04

153

11

00

4

Dockerin

domain

IPR0

16134

149

112

444

65

172

40

90

00

2Dockerin

type

Irepeat

IPR0

02105

10

50

00

00

00

00

00

1Ca

rbohydrate-binding

domains

Carboh

ydrate-binding

domain

IPR0

08965

5042

392

62

03

132

30

10

2Ca

rboh

ydrate-binding

-like

fold

IPR0

13784

145

310

190

00

01

30

06

1Ca

rboh

ydrate-binding

CenC-

like

IPR0

03305

10

70

170

00

00

00

00

0Ca

rboh

ydrate-binding

sugar

hydrolysisdo

main

IPR0

06633

2722

52

227

37

88

05

21

8

Carboh

ydrate-binding

domain

family

9IPR0

10502

10

00

20

00

00

00

00

0

Bacteroidetes-associated

carboh

ydrate-binding

often

N-te

rminal

IPR0

24361

00

10

00

00

00

00

00

0

Carboh

ydratebind

ingmod

ule

xylan-bind

ingdo

main

IPR0

31768

00

00

10

00

00

00

00

0

Galactose-binding

domain-lik

eIPR0

08979

121

176

394

42

13

00

00

0

Archaea 7

Table2Con

tinued

InterPro

IDANME-1S

ANME-1M

ANME-2a

ANME-2d

HANME-2d

AAM

AM-1

M-2

M-3

H-1

H-2

H-3

H-4

SMenaquinones

3-Dem

ethylubiqu

inon

e-9

3-methyltransfe

rase

IPR0

28973

00

03

30

00

00

01

00

0

Succinated

ehydrogenasefu

marate

redu

ctaseflavoproteinsubu

nit

IPR0

1400

60

01

21

00

00

10

00

01

UbiECO

Q5methyltransfe

rase

IPR0

04033

30

02

21

01

00

00

00

0UbiECO

Q5methyltransfe

rase

conservedsite

IPR0

23576

30

02

20

00

10

00

00

0

NrfD

family

IPR0

05614

30

04

30

00

00

00

00

3Fu

talosin

ehydrolase

IPR0

19963

00

01

10

00

00

00

00

0Cy

clicd

ehypoxanthinefutalosine

synthase

IPR0

22431

11

01

10

00

00

00

00

1

Aminod

eoxyfutalosin

esynthase

IPR0

22432

00

01

10

00

00

00

00

0Menaquino

nesynthesis

(cho

rismate

dehydrataseamp

naph

thoatesynthase)

IPR0

03773

86

02

20

00

00

00

00

2

FOsynthasesub

unit2

IPR0

20050

33

13

32

12

12

22

22

3Ph

enazines

Phenazineb

iosynthesis

PhzF

protein

IPR0

03719

11

40

02

00

00

00

02

0

8 Archaea

Frh

Mch

Mer

Mtd

Ftr

Fmd

Mcr

MPh

Vho

Ech

Mtr

CoM-SH

CoB-S-S-CoM

CoB-SHHdrDE2H+

H2

H2

H2

MPhH2

H+

CH4

CH3-CoM

CH3-H4MPTF420H2

F420

F420H2

F420

CH2=H4MPT

CHequivH4MPT

CHO-H4MPT

CHO-MFR

CO2

Fdred

Fdox

H2O

2Na+

H2

Figure 2 Hydrogenotrophic methanogenesis in cytochrome containing Methanosarcina barkeri Black lines represent presence ofconversions See Table 3 for nomenclature

reaction thermodynamically favourable (Table 1)The reversereaction of Mcr is therefore an essential step in AOM andis discussed in Section 22 The respiratory chain that isneeded for using different terminal electron acceptors will bediscussed in Section 3

Evidence that ANME use the reverse methanogenesispathway during AOM is derived from metagenomic andmetatranscriptomic analyses This showed that all genesfor the (reverse) methanogenic pathway were present andexpressed in ANME-2a [42] (Figure 4) and ANME-2d[28] (Figure 5) ANME-1 were consistently lacking thegene encoding N5N10-methylene- tetrahydromethanopterin(H4MPT) reductase (Mer) which is an enzyme needed to

oxidize methyl-H4MPT during methane oxidation [40 41

44 51] (Figure 6 Table 2) Possible explanations could be that(1) the mer gene is present but not yet detected (2) ANME-1 used a bypass of this step and (3) Mer was replaced bya structural analogue The first possibility is highly unlikelyAlthough no closed genome of ANME-1 is publicly availableto date all ANME-1 metagenomes consistently only lackMerand no other methanogenic genes The second possibilitywas proposed previously where ANME-1 uses a bypass of

Mer via the formation of methanol or methylamine [41] aswas detected in deletion mutants ofMethanosarcina [52 53]Here CH

3-CoM was presumably converted to methanol by

a methyltransferase and subsequently to formaldehyde by amethanol dehydrogenase (Mdh) Then formaldehyde wouldbe converted to N5N10 methylene-H

4MPT using a fusion

protein of the formaldehyde-activating enzyme (Fae) and ahexulose-6-phosphate synthase (Hps) [53] (Figure 6) BothFae and Hps were found in the ANME-1 metagenome [41]and metaproteome [40 51] However no genes coding forenzymes involved in methanol metabolism were detectedin these ANME-1 datasets [40 41 51] (Table 2) indicatingthat this alternative pathway probably does not occur Thepresence of the FaeHps fusion protein in ANME-1 duringAOM could also be explained by its involvement in ribosephosphate synthesis and not in AOM [54] Indeed the Faegene domains of ANME-1 were located in between ribulose-phosphate binding barrel and ribosomal protein S5 domains(Table S2) The third possibility of a structural analogue ismost likely since an analogue of N5N10-methylene tetrahy-drofolate (H

4HF) reductase (MetF) was expressed byANME-

1 during AOM which could replace Mer [40] (Figure 6)

Archaea 9

Table 3 Nomenclature

Central methanogenic pathwayFmd Formylmethanofuran (CHO-MFR) dehydrogenaseFtr Formylmethanofuran-tetrahydromethanopterin (H

4MPT) formyltransferase

Mch N5N10-methenyl-H4MPT cyclohydrolase

Mtd F420

H2-dependent methylene -H

4MPT dehydrogenase

Mer N5N10-methylene-H4MPT reductase

Mtr N5-methyl-H4MPTcoenzyme M (CoM) methyltransferase

Mcr Methyl coenzyme M (CH3-CoM) reductase

Mdh Methanol dehydrogenaseFaeHps Fusion protein of formaldehyde activating enzyme hexulose-6-phosphate synthaseMetF N5N10-methylene tetrahydrofolate (H

4HF) reductase analogue

Electron transportMvh F

420-nonreducing hydrogenase

Vho Methanophenazine-dependent hydrogenaseFpo F

420H2phenazine oxidoreductase

Fqo F420

H2quinone oxidoreductase

Hdr Coenzyme B-coenzyme M heterodisulfide (CoB-S-S-CoM) reductaseFrh F

420-dependent hydrogenase

Ech Ferredoxin-dependent hydrogenaseMePhMePhH

2Methanophenazine

MQMQH2

MenaquinoneCyt b Cytochrome bCyt c Cytochrome cMHC Multiheme c-type cytochromeRieske Rieske cytochrome b complexOrf7 Pseudoperiplasmic b-type cytochromeNar Nitrate reductaseNap Periplasmic nitrate reductaseNrf Nitrite reductase

22 Methyl Coenzyme M Reductase (Mcr) The enzymaticreaction of a purified Mcr from ANME has not been mea-sured to date The key question is whether a methanogenicMcr can explain the observed in situ AOM rates or if theMcr of ANME is structurally altered There are three mainfactors to be considered the kinetic limitations as definedby enzyme properties (ie half-maximal activity at a specific119870119872value) the thermodynamic constraints of the enzymatic

reaction and the maximal or ambient rate of the enzymaticreaction For the Mcr from Methanothermobacter marbur-gensis kinetic parameters have been determined to illustratethe reversibility of reaction (1) In themethanogenic reactionthe purified Mcr isoform I [55] catalyzes the production ofmethane with a 119881max of 30Umgminus1 and a 119870

119872of 5mM for

CH3-CoM The same (methanogenic) enzyme was able to

oxidize methane to CH3-CoM with a rate of 00114Umgminus1

and a 119870119872for methane of sim10 mM [56]

To answer if the observed AOM rates are in accordancewith the measured methane oxidation rate for the purifiedMcr enzyme from M marburgensis the Mcr activity duringAOM is needed Estimates for AOM rates in terms of activity(per cell dry mass) range between lt1 and 20mmol dayminus1 andg cell dry massminus1 [56ndash66] This equals an activity of 07 to

sim14 nmol min and mg cell dry massminus1 About half of the celldry mass is protein so the activity for the ANME archaeawould approximate 14 to 28 nmol min and mg proteinminus1 Toestimate the activity per mg of Mcr the proportion of Mcrto cellular protein is needed It was reported that 7 of theprotein of ANMEmicrobial mats from the Black Sea [67 68]and 104 of peptides fromHydrate Ridge mesocosms is Mcr[51] As these were no pure cultures the actual percentagesof Mcr in ANME cells may be higher Transcriptome data forANME-2d [43] showed that about 19 of the total transcriptswere derived from the mcr genes indicating (though notdemonstrating) a highMcr content in ANME-2d Estimatingthat 10 of the cellular protein would be Mcr the specificactivity of the enzymewould be between 14 and 280 nmolminand mg Mcr proteinminus1 which is up to 25 times higher thanthe measured reverse reaction rate of the M marburgensisenzyme (sim12 nmol min and mg Mcrminus1 [56]) However thereverse reaction rate of the M marburgensis Mcr was deter-mined under nonsaturating substrate conditions and wastherefore not possibly representing the true maximum rateNevertheless both reverse reaction rates are in the same orderof magnitude other than the forward reaction of 30000ndash100000 nmol min and mgMcrminus1 Thus it seems that the

10 Archaea

H2

CoM-SH

Mch

Mer

Mtd

Ftr

Fmd

Mcr

MPh

MPhH2

MPh

MPh

MPhH2

MtrVho

CoM-SH

CoB-S-S-CoM

CoB-SHHdrDE

Fpo

Fpo

Ech

CH3-CoM

2H+

H2

2H+

2H+

H+

MPhH2

CH4

CH3-H4MPTF420H2

F420

F420H2

F420

CH2=H4MPT

CHequivH4MPT

CHO-H4MPT

CHO-MFR

CO2

Fdred

Fdox

H2O

2Na+

CH3-OH

Figure 3 Methylotrophic methanogenesis in cytochrome containingMethanosarcina barkeri Black lines represent presence of conversionsand red lines indicate reversal of the hydrogenotrophic methanogenic pathway See Table 3 for nomenclature

Mcr in ANME may have similar catalytic properties as themethanogenic enzyme and that the high amount of Mcr permg total cell biomass in ANME may in part compensates forthe apparently relatively slow catalysis

Considering the thermodynamic constraints the Gibbsfree energy change of the Mcr forward reaction under stan-dard conditions is around minus30 kJmolminus1 [56] Therefore thereverse reaction is endergonic under standard conditions andwill not proceed However highmethane concentrations (105according to reaction (1) [69 70]) may lead to a favourablechange in the Gibbs free energy in the direction of AOMHigh methane partial pressure prevails at many habitatswhere AOM has been detected The solubility of methaneat atmospheric pressure is only 13mM [71] Consequentlyincreased AOM rates were reported upon pressurizing sam-ples of different geographical origin [59 60 72 73] The 119870

119872

of Mcr of M marburgensis for methane was determined ator above 10mM and reported 119870

119872values of S-AOM varied

from (at least) 11mM [74] a few mM [57] to even 37mM(equivalent to 3MPa CH

4) [58] Thus high pressure and

therefore high concentrations of methane in the natural habi-tat accelerate the oxidation rate of methane by Mcr Futureresearch to accurately determine119870

119872values and rates forMcr

at differentmethane partial pressures is however neededThismay seem difficult but microbial activity measurements at insitu methane partial pressure were shown to be successful inthe laboratory [75]

It was suggested that the Mcr reaction is the rate limitingstep in reverse methanogenesis [56] which is in line withthe above described challenges Supporting these findingsthere does not seem to be a major change in the aminoacid structure that determines whether the backwards or theforward reaction of Mcr is favoured Amino acid alignments[67] and the crystal structure of ANME-1 Mcr [76] indicatedhigh overall similarity of the methanogenic and methan-otrophic enzyme and unambiguously demonstrated that

Archaea 11

MHC

MHCS-layer

2H+

minuse

cyt b

Mch

Mer

Mtd

Ftr

Fmd

Mcr

MPh

HdrABC

MPh

MHC

MHC

MPh

CoB-S-S-CoM

CoB-SH

CoM-SH

HdrDE

Mtr

Fpo

Fpo

Rnf

MPhH2

MPhH2

MPhH2

MPhH2

CH4

CH3-CoM

CH3-H4MPT

F420H2

F420

F420H2

F420

CH2=H4MPT

CHequivH4MPT

CHO-H4MPT

CHO-MFR

CO2

Fdred

Fdox

H2O

2Na+

MPh

minuse

S-layer

MHC

SRB 2H+

2H+

2Na+

minuse

minuse

minuse

Figure 4 Methanotrophic pathway during S-AOM by ANME-2a [42] Red lines indicate reversal of the hydrogenotrophic methanogenicpathway See Table 3 for nomenclature

CoM-SH and CoB-SH are substrates of the methanotrophicenzyme However several posttranslational modifications ofamino acids were different betweenmethanogens andANMEarchaea and the cofactor F

430(the prosthetic group of Mcr)

is modified in ANME-1 but not in ANME-2 or ANME-3archaea [51 63 67 68 76 77] Furthermore ANME-1 seemsto lack the noncatalytic proteinDdomain of themcr gene thatis present in all other methanogens and methanotrophs butof which the function is unknown (IPR003901 Table 2) [51]A metabolically engineered Methanosarcina acetivorans wasable to convert methane and CO

2to acetate with a plasmid

containingMcr derived from ANME-1 [78] It is thus unclearif only thermodynamic constraints and the abundance ofMcrensureAOMactivity or if also specificmodifications canhavean effect on the reverse activity of Mcr

23 Methane Oxidation by Methanogens Pure cultures ofmethanogens were not able to oxidize methane under highmethane and low hydrogen concentrations (reviewed in[79 80]) Methanogens are only able to oxidize methaneduring net methane production [81] Labeled methane addi-tion (13C or 14C) to pure cultures of methanogens showedproduction of labeled CO

2during net methane production

This characteristic was confirmed with several pure culturesof methanogens [82ndash84] The process was called ldquotracemethane oxidationrdquo (TMO) since the CO

2was formed in

trace amounts relative to the methane produced [83] It isnot clear if TMO is due to the reported reversibility ofindividual enzymes [66] or if it is an active microbial processfrom which energy can be conserved TMO was speculatedto be an active metabolic process for three reasons (1)the amount of methane oxidized varied between differentspecies of methanogens grown on the same methanogenicsubstrate (2) the amount ofmethane oxidized varied betweendifferent methanogenic substrates and (3) TMO productsvaried between different methanogenic substrates [83 84]For instance when grown on acetate Methanosarcina ace-tivorans produced labeled acetate from labeled methaneWhen grown on carbon monoxide it produced both labeledacetate and methyl sulfides from labeled methane [84] Dur-ing hydrogenotrophic and methylotrophic methanogenesisTMO mainly produced CO

2from labeled methane [83]

However in contrast with AOM TMO rates never exceededmethanogenesis rates even during long-term incubationwith methane and sulfate [85] It seems that methanogensare not able to conserve energy from TMO even under

12 Archaea

Mch

Mer

Mtd

Ftr

Fmd

Mcr

MQ

MQ

EchHdrFrh

3MQ

HdrABC

MQ

cyt b Mtr

NrfH

cyt c

NrfA

CoB-S-S-CoM

CoB-SH

CoM-SH

HdrDE

HCOIIHCOIINapHOrf7

NarGH

S-layer

Fqo

Fqo

3H+

3H+

4H+

CH4

CH3-CoM

CH3-H4MPT

F420

F420H2

F420

F420H2

CH2=H4MPT

CHequivH4MPT

CHO-H4MPT

CHO-MFR

CO2

Fdred

Fdox

H2O

2Na+

NH4+

NO2minus

NO2minus

NO3minus

3MQH2

MQH2

MQH2

MQH2eminus

eminus

Rieske

Figure 5 Methanotrophic pathway during N-AOM by ldquoCaM nitroreducensrdquo MPEBLZ (ANME-2d) [43] Red lines indicate reversal of thehydrogenotrophic methanogenic pathway See Table 3 for nomenclature

thermodynamically favourable conditions TMOoccurs bothin absence and presence of an external electron acceptor andonly during net methanogenesis It is therefore most likelycaused by the reported back flux of individual enzymes of themethanogenic pathway [66]

TMO also occurred in granular sludge and in freshwaterand terrestrial samples These mixed communities showedhigher TMO rates than pure cultures reaching up to 90of the methane produced [27 85ndash87] TMO should thereforebe carefully considered in the experimental setup and inter-pretation of results when studying AOM in environmentalsamples especially since TMO rates were like AOM stim-ulated by a high methane partial pressure [72 86 88] Sulfatereduction was also stimulated by higher methane partialpressures [85]Thus a highmethane partial pressure can havea stimulating effect on methane oxidation (either throughAOM or TMO) and SR which could be unrelated to S-AOMMoreover addition of iron sulfate (FeSO

4) or manganese

oxide (MnO2) also increased TMO rates [86] Therefore

methane-dependent SR and sulfate- or metal-dependentmethane oxidation are not necessarily indications for AOMin mixed cultures In conclusion when studying complexldquoblack-boxrdquo communities only net methane oxidation isproof for AOM activity

24 Methane Production by ANME The process of S-AOMis at the energetic limit for sustaining life with estimates

of Gibbs free energy yields between minus18 and minus35 kJmolminus1[45 79 89ndash91] and doubling times between 11 and 75months [65 72 73 92 93] Since S-AOM operates close toits thermodynamic equilibrium the reversibility of individualenzymes leads to measurable back flux producing methane(3ndash7 of AOM) and sulfate (55ndash13 of SR) during S-AOM [66] This ldquotrace methane productionrdquo was observedin situ [11] and in sediment slurries with methanogenesisaround 10 [62 94] or even as high as 50 of AOM [34]When sulfate becomes depleted Gibbs free energy yieldsbecome even lower (less negative) and the enzymatic backflux becomes even more apparent up to 78 of net AOM[95] Previous measurements of 13C depletion below thesulfate-methane transition zone (SMTZ) ofmarine sedimentsthat were thought to be indicative for methanogenesis couldtherefore instead be attributed to the back flux of AOM [95]The occurrence of ANME-1 without a bacterial partner insediment layers where sulfate was depleted was previouslyinterpreted as evidence that ANME-1 perform methanogen-esis [24] but in light of the above it could also indicate AOMThere are indeed reports of AOM activity below the SMTZin the methanogenic zone [96ndash99] In contrast AOM withother electron acceptors than sulfate operates far from thethermodynamic equilibrium with Gibbs free energy changesbetween minus5172 and minus8414 kJmolmethaneminus1 (Table 1) Herethe reported anaerobic back flux [66] is expected to be lessapparent

Archaea 13

MetFMer

Mdh

FaeHps

SRB

MHC

Mch

Mtd

Ftr

Fmd

McrMQ

Hdr1

MQ

MHC

Hdr2

CoB-S-S-CoMCoB-SHCoM-SH

Mtr

Fqo

CH4

CH3-CoMCH3-OH

CH2O CH3-H4MPT

F420F420H2

CHO-H4MPT

CHO-MFR

CO2

FdredFdox

H2O

eminus

eminus

CHequivH4MPT

CH2=H4MPT

xH+

H2

MQH2

MQH2

+xNa

Figure 6 Methanotrophic pathway during S-AOM by ANME-1 [40 41] Red lines indicate reversal of the hydrogenotrophic methanogenicpathway grey lines represent absence of conversions and blue lines indicate a bypass of the hydrogenotrophic methanogenic pathway SeeTable 3 for nomenclature

In laboratory incubations researchers were not ableto stimulate net methanogenesis through addition ofmethanogenic substrates to AOM performing sediments[62 94] In two cases researchers were successful [23 100]In one of these cases sediment-free long-term AOM enrich-ments that were dominated by ANMESRB were incubatedwith methanogenic substrates The resulting methanogenicactivity most likely came from the enrichment of a minorpopulation of methanogens (up to 7permil of total archaealgene tag sequences) that was present in the inoculum[100] In the second study methanogenic substrates wereadded to ANME-1 and ANME-2 dominated microbialmat samples and methanogenesis also occurred [23]However no information was provided for the total archaealcommunity composition which makes it impossible toexclude methanogens as the responsible organisms

Genomic information of ANME also gives indication onpotential methanogenic routes Considering methylotrophicmethanogenesis no gene homologues catalyzing methyltransfer from methylated substrates to coenzyme M weredetected in ANME (Table 2) [40ndash43] Acetoclastic methano-genesis needs either the AMP- and ADP-forming acetyl-coenzyme A synthetase (Acs and Acd resp) or proceedsvia acetate kinase and phosphotransacetylase In ANME-1only the alpha subunit of a homologue of Acd was expressed

during AOM [41] but in an ANME-1 proteome of activeAOM biomass no Acd was detected [40] The Acd gene wasdetected in the single-aggregate genome and transcriptomeof ANME-2a [42] and in ANME-2d [43] However genedomains for Acd are also present in methanogens unableto use acetate as substrate (Table 2) and are probably usedfor lipid metabolism In hydrogenotrophic methanogenesishydrogenases are used to replenish reduced coenzyme B andto recycle oxidized F

420(discussed in Section 21) Both the

cytoplasmic Mvh complex and the membrane bound Vhowere not present in ANME-2d [43] and not expressed inANME-2a (which also lackedEch andF

420-dependent hydro-

genase (Frh)) [42] making hydrogenotrophic methanogen-esis unlikely In ANME-1 both the cytoplasmic HdrABCand MvhD are present as well as homologues of Frh andEch but these were lacking catalytic subunits [40 41] Aniron hydrogenase was found in both ANME-1 metagenomesbut not in any other methanotroph or methanogen [41](Table 2) This iron hydrogenase domain is part of a genethat is 70 identical to a [FeFe]-hydrogenase of Dehalococ-coides mccartyi [FeFe]-hydrogenases catalyze reversible H

2

production and uptake but these were presumed to have nokey function in AOM [41] However the gene is part of a genecluster of three genes containing a 51 kDaNADH ubiquinoneoxidoreductase subunit (Table S3) which could potentially

14 Archaea

form a complex that generates a proton motive force duringhydrogen oxidation Therefore hydrogenotrophic methano-genesis by ANME-1 cannot be excluded yet

3 Respiration during AnaerobicOxidation of Methane

For netAOMtooccur an external electron acceptor is neededwhich results in a favourable Gibbs free energy change(Table 1) A variety of terminal electron acceptors have beendiscovered for AOM which will be discussed in Sections 31ndash33

31 Sulfate-Dependent AOM During sulfate-dependentAOM electrons are transferred from ANME to the sulfate-reducing bacterial partner Previous work tried to uncoverhow electrons were transferred and most compoundsthat could act as interspecies electron carrier (IEC) wereexcluded to be involved in AOM such as methanolhydrogen methanethiol acetate and carbon monoxide[57 61 62 94 101] Indications that polysulfide could actas IEC were found and ANME-2a archaea were thoughtto perform both AOM and sulfate reduction (SR) [102]However in marine seeps hydrothermal vents and othernondiffusion based sediments AOM rates are high andANME form close associations with SRB in dense aggregates[1 5 103 104] In these aggregates the high AOM ratescould not be explained by diffusion of an IEC whichmade direct interspecies electron transfer (DIET) a moreplausible mechanism [89 105 106] Cellular activities wereindependent of aggregate type and distance between thesyntrophic partners within the aggregate which is bestexplained by DIET [107] DIET is normally achieved usingmultiheme cytochrome c proteins (MHCs) and conductivepili (ie nanowires) which are mainly found in bacteriathat donate electrons extracellularly such as Geobacter andShewanella species [108ndash114] Indeed ANME-2a from seep-sediment samples seem to transfer electrons directly usinglarge MHCs [107] which were found in the metagenome ofANME-2a [107 115] ANME-1 and the associated bacterialpartner also overexpressed genes for extracellular MHCsduring AOM [116] which complements previous findings oftranscription [41] and translation [40] of ANME-1 relatedMHC genes Domain based (meta)genome analysis showsthe high abundance of MHC domains in different ANMEas compared to methanogens (Table 2) A recently isolatedbacterial partner of ANME-1 (ldquoHotSeep-1rdquo) also producedcell-to-cell connections using pili-derived nanowires [116]which explain previously detected Deltaproteobacteria-related pili genes in an AOM sample dominated by ANME-1[40]

How ANME use MHCs to donate electrons to thebacterial partner is not yet clear For ANME-2a the electronsprobably flow from methanophenazine to membrane inte-grated di-heme cytochromes (cytochrome 119887119887

6) that transfer

the electrons through the S-layer via MHCS-layer fusionproteins to extracellular MHCs (Figure 4) (Figure 4 in[107]) Exosortases and archaea-specific archaeosortases are

involved in export of cell surface proteins such as the archaealS-layer proteins These transpeptidases recognize specificsignal peptides for protein- sorting that is archaeosor-tase A recognizes the protein-sorting signal PGF-CTERMand archaeosortase C recognizes the PEF-CTERM signal[117] Both ANME-2a and 2d show presence of di-hemecytochromes archaeosortase A (IPR014522) archaeosortaseC (IPR022504) and other exosortase gene domains (Table 2)Moreover some genes of both ANME-2a and 2d containedboth MHC and PGF or PEF-CTERM domains Lastly somegenes of both ANME-2a and 2d contained both MHC andS-layer domains [107] indicating that these could form theabove-stated MHCS-layer fusion proteins

ANME-1 do not seem to have di-heme cytochromes(Table 2) [115] PGF related domains (IPR026453 andIPR026371) were present in all ANME but PEF-CTERM(IPR017474) related domains were absent in ANME-1 (Table 2) Moreover ANME-1 lacked archaeosortaseA (IPR014522) and archaeosortase C gene domains(IPR022504) as well as some other exosortases (Table 2) Asearch in NCBIrsquos conserved domains database (CCD [118])and the EMBL InterPro database [119] of amino acidssequences of all genes from ANME metagenomes thatcontain MHC domains showed that ANME-1 did not haveany protein-sorting signal or S-layer domains within thesegenes In fact S-layer domains were completely absent inANME-1 (Table 2) These results imply that ANME-1 do notuse di-heme cytochromes for electron transfer to MHCsand do not produce an S-layer (Figure 6) This implies thatANME-1 use a different mechanism for DIET and couldexplain the need for less MHCs by ANME-1 (Table 2)and the observed pili-derived nanowires produced by thebacterial partner [116] The genome of the bacterial partnerof ANME-1 (ldquoHotSeep-1rdquo) encoded 24 c-type cytochromesof which 10 were similar to secreted MHCs of Geobactersulfurreducens [120] which also uses pili for DIET [121]

In the case of ANME-2a it is not clear if pili (ienanowires) were formed during AOM It was previouslythought that electrically conductive pili seemed to be aprerequisite for current production andDIET [122 123] evenwhen syntrophs were closely associated [124] such as withinANME-2SRB aggregates However conductive materialssuch as granular activated carbon were shown to be ableto substitute pili in DIET [124] Although in previous workconductive materials such as phenazines or humic acids didnot seem to stimulate AOM rates [61] in a recent study AOMwas decoupled from SR using artificial electron acceptors[125] This indicates that conductive materials can indeedreplace pili and that ANME-2ab could possibly couple AOMto metal oxide reduction or any other suitable electronacceptor (discussed in Section 33) However it needs to beproven if in ANME-2SRB aggregates no pili are formed andif the mechanism of DIET is fundamentally different fromANME-1

As for the polysulfide shuttling theory [102] canonicalgenes for dissimilatory sulfate reduction such as adenylyl-transferase (Sat) APS reductase (Apr) and dissimilatorysulfite reductase (Dsr) which are all present in the sulfate-reducing archeon A fulgidus (Table S2) were not found in

Archaea 15

metagenomes of ANME-1 [41] and ANME-2a (Table S1)The enzymes Sat and Dsr were also not detected in ANMEcells using fluorescent immunolabelling [126] ANME-1 werepreviously found to encode most proteins for assimilatorysulfate reduction [41] ANME-2d only harbor gene domainsthat encode Sat and assimilatoryATP sulfurylase APS kinaseand sodiumsulfate symporters which were not present inANME-2a (Table S1) It is therefore clear that at least ANME-2a cannot donate electrons to sulfate but need to donateelectrons to a sulfate-reducing partner

32 Nitrate-Dependent AOM Unlike during S-AOMANME-2d that perform N-AOM do not need a bacterialpartner but transfer electrons directly to a membrane boundnitrate reductase (Nar) [28 43] (Figure 5) The ANME-2dgenomes contain most MHCs found so far in archaea[107 115] (Table 2) Of the 87 proteins that contained aCxxCH binding motif of which 43 seemed to be true c-typecytochromes [115] 23 CxxCH motif-encoding transcriptswere expressed during N-AOM [43] The function of mostof these MHCs is not known but they are likely involvedin nitrate reduction since c-type cytochromes are capableof operating in the wide range of redox potentials thatcouple nitrate reduction (11986401015840 (NO

3

minusNO2

minus) = +433mV) andmethane oxidation (11986401015840 (CoM-S-S-CoBCoM-SH+CoB-SH)= minus143mV) [43] Nitrate as terminal electron acceptor inanaerobic respiration has been found in halophilic andthermophilic archaea [127] The nar gene cluster of ldquoCaM nitroreducensrdquo comprises several genes including thecatalytic alpha (NarG molybdopterin) and beta (NarHiron sulfur cluster) subunit of nitrate reductase [28 43] The(halo)archaeal nitrate reductase complex was reported to belocated at the extracellular side of the cytoplasmic membrane[128] and in most archaea associated with the cytoplasmicmembrane via NarM [129] The ldquoCa M nitroreducensrdquogenome does not encode NarM but encodes a TAT signalpeptide at the N-terminus of NarG for translocation acrossthe cytoplasmic membrane [28 43] Interestingly theNarG and NarH seem to have been acquired from theProteobacteria via lateral gene transfer [28]

It is not yet clear at which point in themetabolism ldquoCaMnitroreducensrdquo conserves energy During reverse methano-genesis N5-methyl-H

4MPTCoM methyltransferase (Mtr)

dissipates the sodium ion potential across the cytoplasmicmembrane so subsequent steps inN-AOMhave to be coupledto the build-up of a proton or sodium motive force to makethe overall process energetically favourable The analysis ofan environmental genome [43] indicated presence of severalprotein complexes involved in electron transport and energyconservation Electrons that enter the respiratory chain couldbe transported by membrane-integral electron carriers (iemenaquinones) to a Rieske-cytochrome b complex that mayuse cytochrome c as electron acceptor This in turn maybe the electron donor for the unusual nitrate reductasecomplex Energy conservation is thermodynamically andmechanistically feasible at the F

420H2dehydrogenase and the

Rieske-cytochrome b complex (Figure 5) (Figure 2 in [43])Further investigations are needed to determine whether

nitrate reductase is also involved in energy conservationbut this working hypothesis is strengthened by the presenceof cupredoxin multicopper oxidase domains and coppercenters related to the periplasmic domain of cytochrome coxidase subunit II (HCO II) in ANME-2d (Table S1)

BothANME-2d genomes discussed here are derived frombioreactors where ldquoCaM nitroreducensrdquo formed syntrophiccultures with nitrite scavenging bacteria either with ldquoCaKuenenia stuttgartiensisrdquo (anammox bacteria) [28] or ldquoCaMethylomirabilis oxyferardquo (NC10 bacteria) [31 43]This indi-cated that ANME-2d could be dependent on those bacteriafor nitrite removal However in addition to nitrite ldquoCa Mnitroreducensrdquo may also produce ammonium during AOMby a pentaheme c-type nitrite reductase (NrfAH) encodedin the genome [43] (Figure 5) In fact both ANME-2dgenomes contain domains for NrfA (IPR003321) and NrfH(IPR017571) (Table S1) implying that both ANME-2d speciesare not necessarily dependent on a nitrite scavenger duringAOM

33 Metal-Dependent AOM Evidence for metal-dependentAOM was found in marine sediments [130ndash132] In non-marine environments AOM was also hypothesized to becoupled to iron andor manganese oxide reduction [26 133ndash136] or even coupled to the reduction of humic acids [136137] However organisms responsible for metal-dependentAOM were not identified in these studies It was speculatedthat JS1 bacteria methanogenic archaea and Methanohalo-biumANME-3 could be responsible for iron-dependentAOM [138] Other researchers speculated that either ANME-1 or MethanococcoidesANME-3 together with a bacterialpartner were responsible for manganese-dependent AOM[139] In another study where AOM was decoupled from SRANME were not detected which leaves open the possibilitythat other archaeal clades besides ANME could performmetal-dependent AOM [131]

It was recently observed that cultures containing ANME-2a and ANME-2c could decouple AOM from SR in thepresence of artificial electron acceptors humic acids andsoluble iron [125] which confirmed previous findings ofAOM not connected to SR in ANME dominated samples[140] This suggests that ANME-2 could also use insolublemetal oxide minerals as electron acceptor during AOM TheMHCs of ANME-2ab and ANME-2d are larger than thosein Shewanella and Geobacter species [107] which are knownto be capable of extracellular electron conduction It wasspeculated that both ANME-2d and Ferroglobus placidus ofwhich the latter can perform solid iron reduction can foldCxxCHmotifs into extracellular conductive structures or pili[115] Many of the MHCs of ANME-2d were not expressedwhen grown with nitrate (discussed in section 32) implyingthat these are not needed for nitrate reduction [43] Thisstrengthens the hypothesis that also ANME-2d could coupleAOM to reduction of other extracellular electron acceptorsthan nitrate and even to insoluble metal oxides Indeedrecent work showed that ANME-2d could be involved inAOM coupled to chromium(VI) reduction [141] (Table 1reaction (5)) and in AOM coupled to the reduction of soluble

16 Archaea

iron and insoluble ferrihydrite and birnessite minerals [142](Table 1 reactions (3) and (4)) ANME-2d could even possiblydonate electrons to a bacterial partner besides nitrate-richenvironments ANME-2d archaea have been found inwells ofan aquifer where sulfate and methane concentrations overlap[143] Moreover ANME-2d was the only clade detected insediments of a freshwater lake where S-AOM occurred [144]Sulfate concentrations in these studies were low but above1mM and thus higher than the lowest reported concen-trations for S-AOM to occur [145 146] Lastly sequencesof ANME-2d were relatively more abundant in freshwatersediments fed with methane and sulfate than in sedimentsfed with onlymethane or only sulfate and noN-AOMactivitywas detected when fed with nitrate and methane [27] Theseindications hold promise that direct experimental evidencefor sulfate-dependent AOM by ANME-2d could be found inthe future

TheANME-1 genome contains fewerMHCgene domainsas compared to ANME-2a and ANME-2d and some otherarchaea such as somemethylotrophicmethanogens (Table 2)and some members of the Archaeoglobales [115] The MHCsof ANME-1 also have a smaller heme count as compared toother ANME and some other archaea with the largest beingan octaheme cytochrome [107] Each hemewithin aMHChasits own redox potential and therefore structurally differentMHCs represent a large range of redox potentials that canbe used for bioenergetic electron transfer (reviewed in [147])For instance metal oxide reduction in Shewanella oneidensisMR-1 is catalyzed by a chain of a tetraheme (CymA) twodecaheme (MtrA and MtrB) and eventually extracellulardecaheme cytochromes OmcAMtrC that reduce the ironminerals [121 148 149] In Geobacter sulfurreducens ironmineral reduction seems to be catalyzed by the tetrahemecytochrome OmcE and hexaheme cytochrome OmcS trans-ferring electrons from the outer membrane to type IV pilithat transmit the electrons to iron minerals [121 150 151]Since ANME-1 lack MHCs of the correct size and lack genedomains for pili production [116] they seem unable to reduceminerals via both mechanisms present in Shewanella andGeobacter It can therefore be speculated that ANME-1 areless versatile in electron acceptor use and are not able toreduce solid metal oxides However DIET mechanisms arestill not well understood and the true differences betweenMHCs of different ANME types need to be investigated usingbiochemical methods This would allow uncovering the truecapabilities concerning DIET

34 Menaquinones and Methanophenazines ANME-2a en-coded a protein with a domain specific for PhzF which is anenzyme involved in phenazine biosynthesis in Pseudomonasfluorescens [152 153] The respective gene is not present in allmethanophenazine containing methanogens (in our genomecomparison only inM acetivorans andM formicica Table 2)so it is unclear whether this enzyme is really involved inmethanophenazine biosynthesis It is however likely thatANME-2a use methanophenazines in their respiratory chainsince gene domains for menaquinone biosynthesis wereabsent (Table 2) ldquoCa M nitroreducensrdquo probably uses

menaquinones as membrane-integral electron carrier sinceenvironmental genomes [28 43] encoded the futalosine(mqn) biosynthesis pathway as reported for Archaeoglobusfulgidus [154] (Table 2) Moreover ldquoCa M nitroreducensrdquoenrichment cultures showed absence of methanophenazines[43] ANME-1 also contained gene domains formenaquinonebiosynthesis via the futalosine (mqn) biosynthesis pathway(Table 2) Indications for a quinone biosynthesis pathwayin ANME-1 were previously found to be weak since onlysome of the Ubi homologues of the oxic ubiquinone biosyn-thesis pathway were detected [41] but the futalosine (mqn)biosynthesis pathway was overlooked in that particular anal-ysis Additionally ANME-1 have Fqo homologues similarto Archaeoglobus fulgidus [44] and expressed the catalyticsubunit FqoF [41] However since the phenazine biosynthesisdomain PhzF was also present in the ANME-1 genomes(Table 2) and Fpo and Fqo are homologues we cannotconclude on genomic information alone which redox shuttleis used by ANME-1 during AOM If ANME-1 would usemenaquinones this would have implications for subsequentelectron transfer to MHCs since methanophenazine (1198640 =minus165mV) [155] and menaquinone (1198640 = minus80mV) [156] havedifferent redox potentials

35 Cell Adhesion Some gene domains involved in cel-lular adhesion were more abundant in ANME than inmethanogens (Table 2) especially in ANME-2a and ANME-1that are known to form syntrophic interactions for electrontransfer during respiration These domains include HYR(IPR003410) and CARDB domains (IPR011635) that bothhave a direct role in cellular adhesion [157] (Table 2) Interest-ingly also domains related to the cellulosome of Clostridiumspecies termed dockerin and cohesin were highly abundantin both ANME-1 and ANME-2a as compared to ANME-2dand methanogens together with many carbohydrate bindingdomains (Table 2) In Clostridium species dockerin andcohesin form an anchor to the bacterial cell wall that containsa scaffold with cellulose-degrading enzymes and a carbohy-drate bindingmodule that binds cellulose altogether formingthe cellulosome [158] These domains have been found in alldomains of life irrespective of cellulose utilization but thefunction of such proteins outside of the cellulosome is notknown [159]Therefore dockerin cohesin and carbohydratebinding domains in ANME could hypothetically form aconstruct that binds to carbohydrates and could possibly havea function in cell-to-cell contact or MHC adhesion but thisneeds further investigation

4 Future Challenges

Advances in (meta)genomics transcriptomics and pro-teomics have produced the valuable metabolic blueprints ofdifferent ANMEwith hypotheses on how centralmetabolismelectron transport and energy conservation may functionFuture experiments are needed to biochemically demonstratethat these hypotheses are correct

The bottleneck for biochemical studies of ANME isthe lack of pure cultures due to the slow and syntrophic

Archaea 17

growth However the recent milestone discovery of directelectron transfer provides opportunities to grow ANMEas stated previously on electron accepting electrodes (ieanodes) [160] In this way pure or highly enriched culturesof different ANME without their respective syntrophic part-ner could be obtained and MHCs responsible for electricconduction could be biochemically characterized It seemsthat ANME-1 are limited by the size and abundance ofMHCs which could relate to differences in behavior onan anode The partner bacteria of ANME-1 and ANME-2could be investigated on an electron donating electrode (iecathode) with specific focus on the ability to produce pili (ienanowires) Also worth investigating is if besides ANME-2d ANME-2ab could also use insoluble electron acceptorsand if ANME-2d could donate electrons to a bacterialpartner

Another future challenge is to isolate and characterizeMcr from different ANME clades It needs to be investi-gated if Mcr abundance in ANME cells compensates forthe slow reverse activity or if modifications in the Mcrof ANME-1 also contribute to a better reverse activity ofMcr Moreover the effect of methane partial pressure onreaction rates and enzyme kinetics needs to be determined insitu

ANME-1 are potentially able to perform hydrogeno-trophic methanogenesis due to the presence of a hydrogenasein the genome Genetic indications of menaquinones aselectron carrier in ANME-1 and the various cellulosome andcell adhesion related gene domains in all ANME are alsotopics that could be explored further Methanogenic archaeaare likely not able to perform AOM but additional studieson TMO and more genetic modifications to stimulate AOMin methanogens could help in understanding the param-eters needed for AOM to occur Ultimately physiologicalunderstanding of ANME will help to explain the observedecological niche separation of different ANME clades and theoccurrence of ANMEwithout a bacterial partnerThis wouldgreatly enhance our knowledge of themethane cycle in anoxicenvironments

Competing Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors thank Stefanie Berger (RU Nijmegen) for criticalreading of the manuscript This research is supported bythe Soehngen Institute of Anaerobic Microbiology (SIAM)Gravitation grant (024002002) of the Netherlands Ministryof Education Culture and Science and the NetherlandsOrganisation for Scientific Research (NWO) Mike S MJetten was further supported by ERC AG 339880 Eco-MoMand Alfons J M Stams was supported by ERC AG 323009Novel Anaerobes

References

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[2] K-U Hinrichs J M Hayes S P Sylva P G Brewert andE F DeLong ldquoMethane-consuming archaebacteria in marinesedimentsrdquo Nature vol 398 no 6730 pp 802ndash805 1999

[3] V J Orphan C H House K-U Hinrichs K D McKeeganand E F DeLong ldquoMethane-consuming archaea revealed bydirectly coupled isotopic and phylogenetic analysisrdquo Sciencevol 293 no 5529 pp 484ndash487 2001

[4] K-U Hinrichs and A Boetius ldquoThe anaerobic oxidation ofmethane new insights in microbial ecology and biogeochem-istryrdquo inOceanMargin Systems GWefer D Billett D HebbelnB B Joslashrgensen M Schluter and T VanWeering Eds pp 457ndash477 Springer Berlin Germany 2002

[5] K Knittel T Losekann A Boetius R Kort and R AmannldquoDiversity and distribution of methanotrophic archaea at coldseepsrdquo Applied and Environmental Microbiology vol 71 no 1pp 467ndash479 2005

[6] K Knittel and A Boetius ldquoAnaerobic oxidation of methaneprogress with an unknown processrdquo Annual Review of Micro-biology vol 63 pp 311ndash334 2009

[7] V J Orphan K-U Hinrichs W Ussler III et al ldquoComparativeanalysis of methane-oxidizing archaea and sulfate-reducingbacteria in anoxic marine sedimentsrdquoApplied and Environmen-tal Microbiology vol 67 no 4 pp 1922ndash1934 2001

[8] T Losekann K Knittel T Nadalig et al ldquoDiversity andabundance of aerobic and anaerobic methane oxidizers atthe Haakon Mosby Mud Volcano Barents Seardquo Applied andEnvironmentalMicrobiology vol 73 no 10 pp 3348ndash3362 2007

[9] H Niemann T Losekann D De Beer et al ldquoNovel microbialcommunities of the Haakon Mosby mud volcano and their roleas amethane sinkrdquoNature vol 443 no 7113 pp 854ndash858 2006

[10] TNunouraHOida T Toki J Ashi K Takai andKHorikoshildquoQuantification of mcrA by quantitative fluorescent PCR insediments from methane seep of the Nankai Troughrdquo FEMSMicrobiology Ecology vol 57 no 1 pp 149ndash157 2006

[11] B Orcutt A Boetius M Elvert V Samarkin and S B JoyeldquoMolecular biogeochemistry of sulfate reduction methanogen-esis and the anaerobic oxidation of methane at Gulf of Mexicocold seepsrdquoGeochimica et Cosmochimica Acta vol 69 no 17 pp4267ndash4281 2005

[12] V J Orphan W Ussler III T H Naehr C H House K-U Hinrichs and C K Paull ldquoGeological geochemical andmicrobiological heterogeneity of the seafloor around methanevents in the Eel River Basin offshore Californiardquo ChemicalGeology vol 205 no 3-4 pp 265ndash289 2004

[13] M G Pachiadaki A Kallionaki A Dahlmann G J De Langeand K A Kormas ldquoDiversity and spatial distribution ofprokaryotic communities along a sediment vertical profile ofa deep-sea mud volcanordquo Microbial Ecology vol 62 no 3 pp655ndash668 2011

[14] I Roalkvam H Dahle Y Chen S L Joslashrgensen H Haflidasonand I H Steen ldquoFine-scale community structure analysis ofANME in Nyegga sediments with high and low methane fluxrdquoFrontiers in Microbiology vol 3 p 216 2012

[15] K Yanagawa M Sunamura M A Lever et al ldquoNiche separa-tion of methanotrophic archaea (ANME-1 and -2) in methane-seep sediments of the Eastern Japan Sea offshore JoetsurdquoGeomicrobiology Journal vol 28 no 2 pp 118ndash129 2011

18 Archaea

[16] A Pernthaler A E Dekas C T Brown S K Goffredi TEmbaye and V J Orphan ldquoDiverse syntrophic partnershipsfromdeep-seamethane vents revealed by direct cell capture andmetagenomicsrdquo Proceedings of the National Academy of Sciencesof the United States of America vol 105 no 19 pp 7052ndash70572008

[17] R Hatzenpichler S A Connon D Goudeau R R Malm-strom T Woyke and V J Orphan ldquoVisualizing in situtranslational activity for identifying and sorting slow-growingarchaealminusbacterial consortiardquo Proceedings of the NationalAcademy of Sciences vol 113 no 28 pp E4069ndashE4078 2016

[18] L Maignien R J Parkes B Cragg et al ldquoAnaerobic oxidationof methane in hypersaline cold seep sedimentsrdquo FEMS Micro-biology Ecology vol 83 no 1 pp 214ndash231 2013

[19] V J Orphan C H House K-U Hinrichs K D McKeeganand E F DeLong ldquoMultiple archaeal groups mediate methaneoxidation in anoxic cold seep sedimentsrdquo Proceedings of theNational Academy of Sciences of the United States of Americavol 99 no 11 pp 7663ndash7668 2002

[20] T TreudeM Kruger A Boetius and B B Joslashrgensen ldquoEnviron-mental control on anaerobic oxidation of methane in the gassysediments of Eckernforde Bay (German Baltic)rdquo Limnology andOceanography vol 50 no 6 pp 1771ndash1786 2005

[21] G C Jagersma R J W Meulepas I Heikamp-De Jong etal ldquoMicrobial diversity and community structure of a highlyactive anaerobic methane-oxidizing sulfate-reducing enrich-mentrdquo Environmental Microbiology vol 11 no 12 pp 3223ndash3232 2009

[22] M Blumenberg R Seifert J Reitner T Pape andWMichaelisldquoMembrane lipid patterns typify distinct anaerobic methan-otrophic consortiardquo Proceedings of the National Academy ofSciences of the United States of America vol 101 no 30 pp 11111ndash11116 2004

[23] S Bertram M Blumenberg W Michaelis M Siegert MKruger and R Seifert ldquoMethanogenic capabilities of ANME-archaea deduced from 13C-labelling approachesrdquo Environmen-tal Microbiology vol 15 no 8 pp 2384ndash2393 2013

[24] K G Lloyd M J Alperin and A Teske ldquoEnvironmental evi-dence for net methane production and oxidation in putativeANaerobic MEthanotrophic (ANME) archaeardquo EnvironmentalMicrobiology vol 13 no 9 pp 2548ndash2564 2011

[25] M Takeuchi H Yoshioka Y Seo et al ldquoA distinct freshwater-adapted subgroup of ANME-1 dominates active archaeal com-munities in terrestrial subsurfaces in Japanrdquo EnvironmentalMicrobiology vol 13 no 12 pp 3206ndash3218 2011

[26] R T Amos B A Bekins I M Cozzarelli et al ldquoEvidence foriron-mediated anaerobic methane oxidation in a crude oil-contaminated aquiferrdquo Geobiology vol 10 no 6 pp 506ndash5172012

[27] P H Timmers D A Suarez-Zuluaga M van Rossem MDiender A J Stams and C M Plugge ldquoAnaerobic oxidationof methane associated with sulfate reduction in a naturalfreshwater gas sourcerdquo ISME Journal vol 10 pp 1400ndash14122015

[28] M F Haroon S Hu Y Shi et al ldquoAnaerobic oxidation ofmethane coupled to nitrate reduction in a novel archaeallineagerdquo Nature vol 500 no 7468 pp 567ndash570 2013

[29] H J Mills C Hodges K Wilson I R MacDonald and PA Sobecky ldquoMicrobial diversity in sediments associated withsurface-breaching gas hydrate mounds in the Gulf of MexicordquoFEMS Microbiology Ecology vol 46 no 1 pp 39ndash52 2003

[30] K G Lloyd L Lapham and A Teske ldquoAn anaerobic methane-oxidizing community of ANME-1b archaea in hypersaline gulfofMexico sedimentsrdquoApplied and EnvironmentalMicrobiologyvol 72 no 11 pp 7218ndash7230 2006

[31] A A Raghoebarsing A Pol K T Van De Pas-Schoonen et alldquoA microbial consortium couples anaerobic methane oxidationto denitrificationrdquoNature vol 440 no 7086 pp 918ndash921 2006

[32] S Hu R J Zeng L C Burow P Lant J Keller and Z YuanldquoEnrichment of denitrifying anaerobic methane oxidizingmicroorganismsrdquo Environmental Microbiology Reports vol 1no 5 pp 377ndash384 2009

[33] Z-W Ding J Ding L Fu F Zhang and R J Zeng ldquoSimultane-ous enrichment of denitrifying methanotrophs and anammoxbacteriardquo Applied Microbiology and Biotechnology vol 98 no24 pp 10211ndash10221 2014

[34] R Seifert K Nauhaus M Blumenberg M Kruger and WMichaelis ldquoMethane dynamics in a microbial community ofthe Black Sea traced by stable carbon isotopes in vitrordquoOrganicGeochemistry vol 37 no 10 pp 1411ndash1419 2006

[35] J Ding Z-W Ding L Fu Y-Z Lu S H Cheng and R JZeng ldquoNew primers for detecting and quantifying denitrifyinganaerobic methane oxidation archaea in different ecologicalnichesrdquo Applied Microbiology and Biotechnology vol 99 no 22pp 9805ndash9812 2015

[36] A Vaksmaa C Luke T van Alen et al ldquoDistribution and activ-ity of the anaerobic methanotrophic community in a nitrogen-fertilized Italian paddy soilrdquo FEMS Microbiology Ecology vol92 no 12 2016

[37] P N Evans D H Parks G L Chadwick et al ldquoMethanemetabolism in the archaeal phylum Bathyarchaeota revealed bygenome-centric metagenomicsrdquo Science vol 350 no 6259 pp434ndash438 2015

[38] I Vanwonterghem P N Evans D H Parks et al ldquoMethy-lotrophic methanogenesis discovered in the archaeal phylumVerstraetearchaeotardquo Nature Microbiology vol 1 Article ID16170 2016

[39] P Worm J J Koehorst M Visser et al ldquoA genomic view onsyntrophic versus non-syntrophic lifestyle in anaerobic fattyacid degrading communitiesrdquo Biochimica et Biophysica ActamdashBioenergetics vol 1837 no 12 pp 2004ndash2016 2014

[40] R Stokke I Roalkvam A Lanzen H Haflidason and I HSteen ldquoIntegrated metagenomic and metaproteomic analysesof an ANME-1-dominated community in marine cold seepsedimentsrdquo Environmental Microbiology vol 14 no 5 pp 1333ndash1346 2012

[41] A Meyerdierks M Kube I Kostadinov et al ldquoMetagenomeand mRNA expression analyses of anaerobic methanotrophicarchaea of the ANME-1 grouprdquo Environmental Microbiologyvol 12 no 2 pp 422ndash439 2010

[42] F-P Wang Y Zhang Y Chen et al ldquoMethanotrophicarchaea possessing diverging methane-oxidizing and electron-transporting pathwaysrdquo ISME Journal vol 8 no 5 pp 1069ndash1078 2014

[43] A Arshad D R Speth R M de Graaf H J Op den Camp MS Jetten and C U Welte ldquoA metagenomics-based metabolicmodel of nitrate-dependent anaerobic oxidation of methane byMethanoperedens-like archaeardquo Frontiers inMicrobiology vol 6article1423 2015

[44] S J Hallam N Putnam CM Preston et al ldquoReversemethano-genesis testing the hypothesis with environmental genomicsrdquoScience vol 305 no 5689 pp 1457ndash1462 2004

Archaea 19

[45] R K Thauer ldquoAnaerobic oxidation of methane with sulfate onthe reversibility of the reactions that are catalyzed by enzymesalso involved inmethanogenesis fromCO

2rdquoCurrent Opinion in

Microbiology vol 14 no 3 pp 292ndash299 2011[46] U Deppenmeier V Muller and G Gottschalk ldquoPathways of

energy conservation in methanogenic archaeardquo Archives ofMicrobiology vol 165 no 3 pp 149ndash163 1996

[47] A-K Kaster J Moll K Parey and R K Thauer ldquoCoupling offerredoxin and heterodisulfide reduction via electron bifurca-tion in hydrogenotrophic methanogenic archaeardquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 108 no 7 pp 2981ndash2986 2011

[48] R K Thauer A-K Kaster H Seedorf W Buckel and RHedderich ldquoMethanogenic archaea ecologically relevant dif-ferences in energy conservationrdquo Nature Reviews Microbiologyvol 6 no 8 pp 579ndash591 2008

[49] W Ludwig O Strunk R Westram et al ldquoARB a softwareenvironment for sequence datardquoNucleic Acids Research vol 32no 4 pp 1363ndash1371 2004

[50] E Pruesse C Quast K Knittel et al ldquoSILVA a comprehensiveonline resource for quality checked and aligned ribosomal RNAsequence data compatible with ARBrdquo Nucleic Acids Researchvol 35 no 21 pp 7188ndash7196 2007

[51] J J Marlow C T Skennerton Z Li et al ldquoProteomic stableisotope probing reveals biosynthesis dynamics of slow growingmethane based microbial communitiesrdquo Frontiers in Microbiol-ogy vol 7 article 386 2016

[52] P V Welander and W W Metcalf ldquoLoss of the mtr operon inMethanosarcina blocks growth on methanol but not methano-genesis and reveals an unknown methanogenic pathwayrdquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 102 no 30 pp 10664ndash10669 2005

[53] P V Welander and W W Metcalf ldquoMutagenesis of the C1oxidation pathway inmethanosarcina barkeri new insights intothe MtrMer bypass pathwayrdquo Journal of Bacteriology vol 190no 6 pp 1928ndash1936 2008

[54] M Goenrich R K Thauer H Yurimoto and N KatoldquoFormaldehyde activating enzyme (Fae) and hexulose-6-phosphate synthase (Hps) inMethanosarcina barkeri a possiblefunction in ribose-5-phosphate biosynthesisrdquoArchives ofMicro-biology vol 184 no 1 pp 41ndash48 2005

[55] M Goenrich FMahlert E C Duin C Bauer B Jaun and R KThauer ldquoProbing the reactivity of Ni in the active site of methyl-coenzyme M reductase with substrate analoguesrdquo Journal ofBiological Inorganic Chemistry vol 9 no 6 pp 691ndash705 2004

[56] S Scheller M Goenrich R Boecher R K Thauer and BJaun ldquoThe key nickel enzyme of methanogenesis catalyses theanaerobic oxidation of methanerdquo Nature vol 465 no 7298 pp606ndash608 2010

[57] K Nauhaus A Boetius M Kruger and F Widdel ldquoIn vitrodemonstration of anaerobic oxidation of methane coupled tosulphate reduction in sediment from amarine gas hydrate areardquoEnvironmental Microbiology vol 4 no 5 pp 296ndash305 2002

[58] Y Zhang J-P Henriet J Bursens and N Boon ldquoStimulationof in vitro anaerobic oxidation of methane rate in a continuoushigh-pressure bioreactorrdquo Bioresource Technology vol 101 no9 pp 3132ndash3138 2010

[59] M Kruger T Treude H Wolters K Nauhaus and A BoetiusldquoMicrobial methane turnover in different marine habitatsrdquoPalaeogeography Palaeoclimatology Palaeoecology vol 227 no1ndash3 pp 6ndash17 2005

[60] C Deusner V Meyer and T G Ferdelman ldquoHigh-pressuresystems for gas-phase free continuous incubation of enrichedmarinemicrobial communities performing anaerobic oxidationof methanerdquo Biotechnology and Bioengineering vol 105 no 3pp 524ndash533 2010

[61] K Nauhaus T Treude A Boetius and M Kruger ldquoEnviron-mental regulation of the anaerobic oxidation of methane acomparison of ANME-I and ANME-II communitiesrdquo Environ-mental Microbiology vol 7 no 1 pp 98ndash106 2005

[62] T Treude V Orphan K Knittel A Gieseke C H House andA Boetius ldquoConsumption of methane and CO

2by methan-

otrophicmicrobial mats from gas seeps of the anoxic Black SeardquoApplied and EnvironmentalMicrobiology vol 73 no 7 pp 2271ndash2283 2007

[63] T Holler F Widdel K Knittel et al ldquoThermophilic anaerobicoxidation of methane by marine microbial consortiardquo ISMEJournal vol 5 no 12 pp 1946ndash1956 2011

[64] M Kruger M Blumenberg S Kasten et al ldquoA novel multi-layered methanotrophic microbial mat system growing on thesediment of the Black Seardquo Environmental Microbiology vol 10no 8 pp 1934ndash1947 2008

[65] R J WMeulepas C G Jagersma J Gieteling C J N BuismanA J M Stams and P N L Lens ldquoEnrichment of anaerobicmethanotrophs in sulfate-reducing membrane bioreactorsrdquoBiotechnology and Bioengineering vol 104 no 3 pp 458ndash4702009

[66] T Holler G Wegener H Niemann et al ldquoCarbon and sulfurback flux during anaerobic microbial oxidation of methane andcoupled sulfate reductionrdquo Proceedings of the National Academyof Sciences of the United States of America vol 108 no 52 ppE1484ndashE1490 2011

[67] M Kruger AMeyerdierks F O Glockner et al ldquoA conspicuousnickel protein in microbial mats that oxidize methane anaero-bicallyrdquo Nature vol 426 no 6968 pp 878ndash881 2003

[68] S Mayr C Latkoczy M Kruger et al ldquoStructure of an F430

variant from archaea associated with anaerobic oxidation ofmethanerdquo Journal of the American Chemical Society vol 130 no32 pp 10758ndash10767 2008

[69] S Shima and R K Thauer ldquoMethyl-coenzyme M reductaseand the anaerobic oxidation of methane in methanotrophicArchaeardquo Current Opinion in Microbiology vol 8 no 6 pp643ndash648 2005

[70] R K Thauer and S Shima ldquoMethane as fuel for anaerobicmicroorganismsrdquo Annals of the New York Academy of Sciencesvol 1125 pp 158ndash170 2008

[71] S Yamamoto J B Alcauskas and T E Crozier ldquoSolubility ofmethane in distilled water and seawaterrdquo Journal of Chemicaland Engineering Data vol 21 no 1 pp 78ndash80 1976

[72] P H A Timmers J Gieteling H C A Widjaja-Greefkeset al ldquoGrowth of anaerobic methane-oxidizing archaea andsulfate-reducing bacteria in a high-pressure membrane capsulebioreactorrdquoApplied and EnvironmentalMicrobiology vol 81 no4 pp 1286ndash1296 2015

[73] MKruger HWoltersMGehre S B Joye andH-H RichnowldquoTracing the slow growth of anaerobic methane-oxidizingcommunities by 15N-labelling techniquesrdquo FEMS MicrobiologyEcology vol 63 no 3 pp 401ndash411 2008

[74] R J W Meulepas C G Jagersma A F Khadem C J N Buis-man A J M Stams and P N L Lens ldquoEffect of environmentalconditions on sulfate reduction withmethane as electron donorby an Eckernforde Bay enrichmentrdquo Environmental Science andTechnology vol 43 no 17 pp 6553ndash6559 2009

20 Archaea

[75] M W Bowles V A Samarkin and S B Joye ldquoImprovedmeasurement of microbial activity in deep-sea sediments atin situ pressure and methane concentrationrdquo Limnology andOceanography Methods vol 9 pp 499ndash506 2011

[76] S Shima M Krueger T Weinert et al ldquoStructure of a methyl-coenzyme M reductase from Black Sea mats that oxidizemethane anaerobicallyrdquo Nature vol 481 no 7379 pp 98ndash1012012

[77] K D Allen G Wegener and R H White ldquoDiscovery of multi-ple modified F-430 coenzymes in methanogens and anaerobicmethanotrophic archaea suggests possible new roles for F-430in naturerdquoApplied and Environmental Microbiology vol 80 no20 pp 6403ndash6412 2014

[78] V W Soo M J McAnulty A Tripathi et al ldquoReversingmethanogenesis to capture methane for liquid biofuel precur-sorsrdquoMicrobial Cell Factories vol 15 article 11 2016

[79] D L Valentine and W S Reeburgh ldquoNew perspectives onanaerobicmethane oxidationrdquoEnvironmentalMicrobiology vol2 no 5 pp 477ndash484 2000

[80] D L Valentine ldquoBiogeochemistry and microbial ecology ofmethane oxidation in anoxic environments a reviewrdquo Antonievan Leeuwenhoek International Journal of General and Molecu-lar Microbiology vol 81 no 1-4 pp 271ndash282 2002

[81] A J B Zehnder and T D Brock ldquoMethane formation andmethane oxidation by methanogenic bacteriardquo Journal of Bac-teriology vol 137 no 1 pp 420ndash432 1979

[82] J Harder ldquoAnaerobic methane oxidation by bacteria employ-ing 14C-methane uncontaminated with 14C-carbon monoxiderdquoMarine Geology vol 137 no 1-2 pp 13ndash23 1997

[83] J J Moran C H House K H Freeman and J G FerryldquoTrace methane oxidation studied in several Euryarchaeotaunder diverse conditionsrdquo Archaea vol 1 no 5 pp 303ndash3092005

[84] J J Moran C H House B Thomas and K H FreemanldquoProducts of tracemethane oxidation during nonmethyltrophicgrowth by Methanosarcinardquo Journal of Geophysical ResearchBiogeosciences vol 112 no 2 2007

[85] R J W Meulepas C G Jagersma Y Zhang et al ldquoTracemethane oxidation and the methane dependency of sulfatereduction in anaerobic granular sludgerdquo FEMS MicrobiologyEcology vol 72 no 2 pp 261ndash271 2010

[86] A J B Zehnder andTD Brock ldquoAnaerobicmethane oxidationoccurrence and ecologyrdquoApplied and Environmental Microbiol-ogy vol 39 no 1 pp 194ndash204 1980

[87] S J Blazewicz D G Petersen M P Waldrop and M K Fire-stone ldquoAnaerobic oxidation of methane in tropical and borealsoils ecological significance in terrestrial methane cyclingrdquoJournal of Geophysical Research Biogeosciences vol 117 no 2Article ID G02033 2012

[88] K A Smemo and J B Yavitt ldquoEvidence for anaerobic CH4

oxidation in freshwater peatlandsrdquo Geomicrobiology Journalvol 24 no 7-8 pp 583ndash597 2007

[89] M J Alperin and T M Hoehler ldquoAnaerobic methane oxidationby archaeasulfate-reducing bacteria aggregates 1 Thermody-namic and physical constraintsrdquo American Journal of Sciencevol 309 no 10 pp 869ndash957 2009

[90] S L Caldwell J R Laidler E A Brewer J O Eberly S CSandborgh and F S Colwell ldquoAnaerobic oxidation of methanemechanisms bioenergetics and the ecology of associatedmicroorganismsrdquo Environmental Science and Technology vol42 no 18 pp 6791ndash6799 2008

[91] GWang A J Spivack and S DrsquoHondt ldquoGibbs energies of reac-tion and microbial mutualism in anaerobic deep subseafloorsediments of ODP Site 1226rdquoGeochimica et Cosmochimica Actavol 74 no 14 pp 3938ndash3947 2010

[92] P R Girguis A E Cozen and E F DeLong ldquoGrowth andpopulation dynamics of anaerobic methane-oxidizing archaeaand sulfate-reducing bacteria in a continuous-flow bioreactorrdquoApplied and EnvironmentalMicrobiology vol 71 no 7 pp 3725ndash3733 2005

[93] K Nauhaus M Albrecht M Elvert A Boetius and F WiddelldquoIn vitro cell growth ofmarine archaeal-bacterial consortia dur-ing anaerobic oxidation ofmethanewith sulfaterdquoEnvironmentalMicrobiology vol 9 no 1 pp 187ndash196 2007

[94] B Orcutt V Samarkin A Boetius and S Joye ldquoOn the relation-ship between methane production and oxidation by anaerobicmethanotrophic communities from cold seeps of the Gulf ofMexicordquo Environmental Microbiology vol 10 no 5 pp 1108ndash1117 2008

[95] M Y Yoshinaga T Holler T Goldhammer et al ldquoCarbon iso-tope equilibration during sulphate-limited anaerobic oxidationof methanerdquo Nature Geoscience vol 7 no 3 pp 190ndash194 2014

[96] T Treude J Niggemann J Kallmeyer et al ldquoAnaerobic oxi-dation of methane and sulfate reduction along the Chileancontinental marginrdquo Geochimica et Cosmochimica Acta vol 69no 11 pp 2767ndash2779 2005

[97] R J Parkes B A Cragg N Banning et al ldquoBiogeochemistryand biodiversity of methane cycling in subsurface marinesediments (SkagerrakDenmark)rdquoEnvironmentalMicrobiologyvol 9 no 5 pp 1146ndash1161 2007

[98] N J Knab B A Cragg E R C Hornibrook et al ldquoRegulationof anaerobic methane oxidation in sediments of the Black SeardquoBiogeosciences vol 6 no 8 pp 1505ndash1518 2009

[99] H Yoshioka A Maruyama T Nakamura et al ldquoActivities anddistribution of methanogenic and methane-oxidizing microbesin marine sediments from the Cascadia Marginrdquo Geobiologyvol 8 no 3 pp 223ndash233 2010

[100] G Wegener V Krukenberg S E Ruff M Y Kellermann andK Knittel ldquoMetabolic capabilities of microorganisms involvedin and associated with the anaerobic oxidation of methanerdquoFrontiers in Microbiology vol 7 article 46 2016

[101] R J W Meulepas C G Jagersma A F Khadem A J MStams and P N L Lens ldquoEffect of methanogenic substrateson anaerobic oxidation of methane and sulfate reduction by ananaerobic methanotrophic enrichmentrdquo Applied Microbiologyand Biotechnology vol 87 no 4 pp 1499ndash1506 2010

[102] J Milucka T G Ferdelman L Polerecky et al ldquoZero-valentsulphur is a key intermediate in marine methane oxidationrdquoNature vol 491 no 7425 pp 541ndash546 2012

[103] W Michaelis R Seifert K Nauhaus et al ldquoMicrobial reefs inthe black sea fueled by anaerobic oxidation ofmethanerdquo Sciencevol 297 no 5583 pp 1013ndash1015 2002

[104] A Vigneron P Cruaud P Pignet et al ldquoArchaeal and anaerobicmethane oxidizer communities in the Sonora Margin coldseeps Guaymas Basin (Gulf of California)rdquo ISME Journal vol7 no 8 pp 1595ndash1608 2013

[105] M Alperin and T Hoehler ldquoThe ongoing mystery of sea-floormethanerdquo Science vol 329 no 5989 pp 288ndash289 2010

[106] B Orcutt and C Meile ldquoConstraints on mechanisms and ratesof anaerobic oxidation of methane by microbial consortiaprocess-basedmodeling of ANME-2 archaea and sulfate reduc-ing bacteria interactionsrdquo Biogeosciences vol 5 no 6 pp 1587ndash1599 2008

Archaea 21

[107] S E McGlynn G L Chadwick C P Kempes and V J OrphanldquoSingle cell activity reveals direct electron transfer in methan-otrophic consortiardquoNature vol 526 no 7574 pp 531ndash535 2015

[108] D R Lovley ldquoElectromicrobiologyrdquo Annual Review of Microbi-ology vol 66 pp 391ndash409 2012

[109] S M Strycharz-Glaven R M Snider A Guiseppi-Elie andL M Tender ldquoOn the electrical conductivity of microbialnanowires and biofilmsrdquoEnergy and Environmental Science vol4 no 11 pp 4366ndash4379 2011

[110] D J Richardson J N Butt J K Fredrickson et al ldquoThe lsquoporinndashcytochromersquo model for microbe-to-mineral electron transferrdquoMolecular Microbiology vol 85 no 2 pp 201ndash212 2012

[111] A Okamoto K Hashimoto and R Nakamura ldquoLong-rangeelectron conduction of Shewanella biofilms mediated by outermembrane C-type cytochromesrdquo Bioelectrochemistry vol 85pp 61ndash65 2012

[112] M Y El-Naggar G Wanger K M Leung et al ldquoElectricaltransport along bacterial nanowires from Shewanella oneidensisMR-1rdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 107 no 42 pp 18127ndash18131 2010

[113] G Reguera K D McCarthy T Mehta J S Nicoll M TTuominen and D R Lovley ldquoExtracellular electron transfer viamicrobial nanowiresrdquo Nature vol 435 no 7045 pp 1098ndash11012005

[114] Z M Summers H E Fogarty C Leang A E Franks N SMalvankar and D R Lovley ldquoDirect exchange of electronswithin aggregates of an evolved syntrophic coculture of anaer-obic bacteriardquo Science vol 330 no 6009 pp 1413ndash1415 2010

[115] A Kletzin T Heimerl J Flechsler L V Niftrik R Rachel andA Klingl ldquoCytochromes c in archaea distribution maturationcell architecture and the special case of Ignicoccus hospitalisrdquoFrontiers in Microbiology vol 6 article 439 2015

[116] GWegener V Krukenberg D Riedel H E Tegetmeyer and ABoetius ldquoIntercellular wiring enables electron transfer betweenmethanotrophic archaea and bacteriardquo Nature vol 526 no7574 pp 587ndash590 2015

[117] D HHaft S H Payne and J D Selengut ldquoArchaeosortases andexosortases are widely distributed systems linking membranetransit with posttranslational modificationrdquo Journal of Bacteri-ology vol 194 no 1 pp 36ndash48 2012

[118] A Marchler-Bauer M K Derbyshire N R Gonzales et alldquoCDD NCBIrsquos conserved domain databaserdquo Nucleic AcidsResearch vol 43 no 1 pp D222ndashD226 2015

[119] A Mitchell H-Y Chang L Daugherty et al ldquoThe InterProprotein families database the classification resource after 15yearsrdquo Nucleic Acids Research vol 43 no 1 pp D213ndashD2212015

[120] V Krukenberg K Harding M Richter et al ldquoCandidatusdesulfofervidus auxilii a hydrogenotrophic sulfate-reducingbacterium involved in the thermophilic anaerobic oxidation ofmethanerdquo Environmental Microbiology vol 18 pp 3073ndash30912016

[121] L Shi T C Squier J M Zachara and J K Fredrickson ldquoRes-piration of metal (hydr)oxides by Shewanella and Geobactera key role for multihaem c-type cytochromesrdquo MolecularMicrobiology vol 65 no 1 pp 12ndash20 2007

[122] N S Malvankar and D R Lovley ldquoMicrobial nanowires forbioenergy applicationsrdquo Current Opinion in Biotechnology vol27 pp 88ndash95 2014

[123] A-E Rotaru T LWoodard K PNevin andDR Lovley ldquoLinkbetween capacity for current production and syntrophic growth

in Geobacter speciesrdquo Frontiers in Microbiology vol 6 article744 2015

[124] A-E Rotaru P M Shrestha F Liu et al ldquoDirect interspecieselectron transfer between Geobacter metallireducens andMethanosarcina barkerirdquo Applied and Environmental Microbi-ology vol 80 no 15 pp 4599ndash4605 2014

[125] S Scheller H Yu G L Chadwick S E McGlynn and VJ Orphan ldquoArtificial electron acceptors decouple archaealmethane oxidation from sulfate reductionrdquo Science vol 351 no6274 pp 703ndash707 2016

[126] J Milucka F Widdel and S Shima ldquoImmunological detec-tion of enzymes for sulfate reduction in anaerobic methane-oxidizing consortiardquo Environmental Microbiology vol 15 no 5pp 1561ndash1571 2013

[127] P Cabello M D Roldan and C Moreno-Vivian ldquoNitratereduction and the nitrogen cycle in archaeardquoMicrobiology vol150 no 11 pp 3527ndash3546 2004

[128] R MMartinez-Espinosa E J Dridge M J Bonete et al ldquoLookon the positive sideThe orientation identification and bioener-getics of lsquoArchaealrsquomembrane-boundnitrate reductasesrdquoFEMSMicrobiology Letters vol 276 no 2 pp 129ndash139 2007

[129] S de VriesMMomcilovicM J F Strampraad J PWhiteleggeA Baghai and I Schroder ldquoAdaptation to a high-tungsten envi-ronment pyrobaculum aerophilum contains an active tungstennitrate reductaserdquo Biochemistry vol 49 no 45 pp 9911ndash99212010

[130] M Egger O Rasigraf C J Sapart et al ldquoIron-mediated anaer-obic oxidation of methane in brackish coastal sedimentsrdquoEnvironmental Science and Technology vol 49 no 1 pp 277ndash283 2015

[131] T Treude S Krause J Maltby A W Dale R Coffin and LJ Hamdan ldquoSulfate reduction and methane oxidation activitybelow the sulfate-methane transition zone in Alaskan BeaufortSea continental margin sediments implications for deep sulfurcyclingrdquo Geochimica et Cosmochimica Acta vol 144 pp 217ndash237 2014

[132] N Riedinger M J Formolo T W Lyons S Henkel A Beckand S Kasten ldquoAn inorganic geochemical argument for coupledanaerobic oxidation of methane and iron reduction in marinesedimentsrdquo Geobiology vol 12 no 2 pp 172ndash181 2014

[133] Y-H Chang T-W Cheng W-J Lai et al ldquoMicrobial methanecycling in a terrestrialmud volcano in eastern Taiwanrdquo Environ-mental Microbiology vol 14 no 4 pp 895ndash908 2012

[134] S A Crowe S Katsev K Leslie et al ldquoThe methane cycle inferruginous Lake Matanordquo Geobiology vol 9 no 1 pp 61ndash782011

[135] O Sivan M Adler A Pearson et al ldquoGeochemical evidence foriron-mediated anaerobic oxidation of methanerdquo Limnology andOceanography vol 56 no 4 pp 1536ndash1544 2011

[136] K E A Segarra C Comerford J Slaughter and S B JoyeldquoImpact of electron acceptor availability on the anaerobic oxi-dation of methane in coastal freshwater and brackish wetlandsedimentsrdquo Geochimica et Cosmochimica Acta vol 115 pp 15ndash30 2013

[137] V Gupta K A Smemo J B Yavitt D Fowle B Branfireunand N Basiliko ldquoStable isotopes reveal widespread anaerobicmethane oxidation across latitude and peatland typerdquo Environ-mental Science and Technology vol 47 no 15 pp 8273ndash82792013

[138] O Oni T Miyatake S Kasten et al ldquoDistinct microbialpopulations are tightly linked to the profile of dissolved iron in

22 Archaea

the methanic sediments of the Helgolandmud area North SeardquoFrontiers in Microbiology vol 6 2015

[139] E J Beal C H House and V J Orphan ldquoManganese- andiron-dependent marine methane oxidationrdquo Science vol 325no 5937 pp 184ndash187 2009

[140] M W Bowles V A Samarkin K M Bowles and S B JoyeldquoWeak coupling between sulfate reduction and the anaerobicoxidation of methane in methane-rich seafloor sedimentsduring ex situ incubationrdquo Geochimica et Cosmochimica Actavol 75 no 2 pp 500ndash519 2011

[141] Y Z Lu L Fu J Ding Z Ding N Li and R J Zeng ldquoCr(VI)reduction coupled with anaerobic oxidation of methane in alaboratory reactorrdquoWater Research vol 102 pp 445ndash452 2016

[142] K F Ettwig B Zhu D Speth J T Keltjens M S Jetten and BKartal ldquoArchaea catalyze iron-dependent anaerobic oxidationof methanerdquo Proceedings of the National Academy of Sciences ofthe United States of America vol 113 no 45 pp 12792ndash127962016

[143] T M Flynn R A Sanford H Ryu et al ldquoFunctional microbialdiversity explains groundwater chemistry in a pristine aquiferrdquoBMCMicrobiology vol 13 no 1 article no 146 2013

[144] C J Schubert F Vazquez T Losekann-Behrens K KnittelM Tonolla and A Boetius ldquoEvidence for anaerobic oxidationof methane in sediments of a freshwater system (Lago diCadagno)rdquo FEMS Microbiology Ecology vol 76 no 1 pp 26ndash38 2011

[145] K E A Segarra F Schubotz V Samarkin M Y Yoshinaga K-U Hinrichs and S B Joye ldquoHigh rates of anaerobic methaneoxidation in freshwater wetlands reduce potential atmosphericmethane emissionsrdquo Nature Communications vol 6 article7477 2015

[146] E J Beal M W Claire and C H House ldquoHigh rates ofanaerobic methanotrophy at low sulfate concentrations withimplications for past and present methane levelsrdquo Geobiologyvol 9 no 2 pp 131ndash139 2011

[147] F Kracke I Vassilev and J O Kromer ldquoMicrobial electrontransport and energy conservationmdashthe foundation for opti-mizing bioelectrochemical systemsrdquo Frontiers in Microbiologyvol 6 article 575 2015

[148] C L Reardon A C Dohnalkova P Nachimuthu et al ldquoRoleof outer-membrane cytochromes MtrC and OmcA in thebiomineralization of ferrihydrite by Shewanella oneidensisMR-1rdquo Geobiology vol 8 no 1 pp 56ndash68 2010

[149] L Shi B Chen Z Wang et al ldquoIsolation of a high-affinityfunctional protein complex between OmcA and MtrC twoouter membrane decaheme c-type cytochromes of Shewanellaoneidensis MR-1rdquo Journal of Bacteriology vol 188 no 13 pp4705ndash4714 2006

[150] X Qian T Mester L Morgado et al ldquoBiochemical charac-terization of purified OmcS a c-type cytochrome requiredfor insoluble Fe(III) reduction in Geobacter sulfurreducensrdquoBiochimica et BiophysicaActamdashBioenergetics vol 1807 no 4 pp404ndash412 2011

[151] T Mehta M V Coppi S E Childers and D R Lovley ldquoOutermembrane c-type cytochromes required for Fe(III) andMn(IV)oxide reduction in Geobacter sulfurreducensrdquo Applied andEnvironmentalMicrobiology vol 71 no 12 pp 8634ndash8641 2005

[152] W Blankenfeldt A P Kuzin T Skarina et al ldquoStructure andfunction of the phenazine biosynthetic protein PhzF fromPseudomonas fluorescensrdquoProceedings of theNational Academyof Sciences of the United States of America vol 101 no 47 pp16431ndash16436 2004

[153] J F Parsons F Song L Parsons K Calabrese E Eisensteinand J E Ladner ldquoStructure and function of the phenazinebiosynthesis protein PhzF fromPseudomonas fluorescens 2-79rdquoBiochemistry vol 43 no 39 pp 12427ndash12435 2004

[154] T Hiratsuka K Furihata J Ishikawa et al ldquoAn alternativemenaquinone biosynthetic pathway operating in microorgan-ismsrdquo Science vol 321 no 5896 pp 1670ndash1673 2008

[155] M Tietze A Beuchle I Lamla et al ldquoRedox potentials ofmethanophenazine and CoB-S-S-CoM factors involved inelectron transport in methanogenic archaeardquo ChemBioChemvol 4 no 4 pp 333ndash335 2003

[156] Q H Tran and G Unden ldquoChanges in the proton potentialand the cellular energetics of Escherichia coli during growth byaerobic and anaerobic respiration or by fermentationrdquoEuropeanJournal of Biochemistry vol 251 no 1-2 pp 538ndash543 1998

[157] I Callebaut D Gilges I Vigon and J-P Mornon ldquoHYR anextracellular module involved in cellular adhesion and relatedto the immunoglobulin-like foldrdquo Protein Science vol 9 no 7pp 1382ndash1390 2000

[158] H J Gilbert ldquoCellulosomes microbial nanomachines that dis-play plasticity in quaternary structurerdquoMolecular Microbiologyvol 63 no 6 pp 1568ndash1576 2007

[159] A Peer S P Smith E A Bayer R Lamed and I BorovokldquoNoncellulosomal cohesin- and dockerin-like modules in thethree domains of liferdquo FEMS Microbiology Letters vol 291 no1 pp 1ndash16 2009

[160] M Wagner ldquoMicrobiology conductive consortiardquo Nature vol526 no 7574 pp 513ndash514 2015

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

6 Archaea

Table2Con

tinued

InterPro

IDANME-1S

ANME-1M

ANME-2a

ANME-2d

HANME-2d

AAM

AM-1

M-2

M-3

H-1

H-2

H-3

H-4

SInvasin

intim

incell-adhesio

nfragments

IPR0

0896

417

03

26

70

27

01

20

22

Putativ

ecellw

allbinding

repeat2

IPR0

07253

22

00

00

00

00

00

00

0ArchaeosortaseA

IPR0

14522

20

12

21

11

11

10

02

1ArchaeosortaseB

IPR0

26430

00

00

00

00

01

00

00

0ArchaeosortaseC

IPR0

22504

00

12

10

01

10

00

00

0Ex

osortasearchaeosortased

omain

IPR0

26392

50

25

31

12

22

10

12

1Ex

osortaseE

psH

IPR0

13426

10

01

00

00

00

00

00

0Ex

osortase

EpsH

-related

IPR0

19127

42

23

21

12

11

10

12

1Archaeosortasefam

ilyproteinArtE

IPR0

26485

00

00

00

00

00

00

10

0Cellw

allhydrolaseautolysin

catalytic

IPR0

02508

22

10

00

00

00

00

01

0

PEF-CT

ERM

proteinsorting

domain

IPR0

17474

00

34

10

010

190

00

00

0

PGF-pre-PG

Fdo

main

IPR0

26453

11

189

824

07

2111

00

01

1PG

F-CT

ERM

archaeal

protein-sortingsig

nal

IPR0

26371

94

62

12

02

12

10

01

3

LPXT

Gcellwallancho

rdom

ain

IPR0

19931

30

10

00

11

00

00

00

0VPX

XXP

-CTE

RMproteinsorting

domain

IPR0

26428

00

00

00

00

05

00

00

0

Cellu

losome-relatedDockerin

Cellulosomea

ncho

ringprotein

cohesin

domain

IPR0

02102

8077

524

122

04

153

11

00

4

Dockerin

domain

IPR0

16134

149

112

444

65

172

40

90

00

2Dockerin

type

Irepeat

IPR0

02105

10

50

00

00

00

00

00

1Ca

rbohydrate-binding

domains

Carboh

ydrate-binding

domain

IPR0

08965

5042

392

62

03

132

30

10

2Ca

rboh

ydrate-binding

-like

fold

IPR0

13784

145

310

190

00

01

30

06

1Ca

rboh

ydrate-binding

CenC-

like

IPR0

03305

10

70

170

00

00

00

00

0Ca

rboh

ydrate-binding

sugar

hydrolysisdo

main

IPR0

06633

2722

52

227

37

88

05

21

8

Carboh

ydrate-binding

domain

family

9IPR0

10502

10

00

20

00

00

00

00

0

Bacteroidetes-associated

carboh

ydrate-binding

often

N-te

rminal

IPR0

24361

00

10

00

00

00

00

00

0

Carboh

ydratebind

ingmod

ule

xylan-bind

ingdo

main

IPR0

31768

00

00

10

00

00

00

00

0

Galactose-binding

domain-lik

eIPR0

08979

121

176

394

42

13

00

00

0

Archaea 7

Table2Con

tinued

InterPro

IDANME-1S

ANME-1M

ANME-2a

ANME-2d

HANME-2d

AAM

AM-1

M-2

M-3

H-1

H-2

H-3

H-4

SMenaquinones

3-Dem

ethylubiqu

inon

e-9

3-methyltransfe

rase

IPR0

28973

00

03

30

00

00

01

00

0

Succinated

ehydrogenasefu

marate

redu

ctaseflavoproteinsubu

nit

IPR0

1400

60

01

21

00

00

10

00

01

UbiECO

Q5methyltransfe

rase

IPR0

04033

30

02

21

01

00

00

00

0UbiECO

Q5methyltransfe

rase

conservedsite

IPR0

23576

30

02

20

00

10

00

00

0

NrfD

family

IPR0

05614

30

04

30

00

00

00

00

3Fu

talosin

ehydrolase

IPR0

19963

00

01

10

00

00

00

00

0Cy

clicd

ehypoxanthinefutalosine

synthase

IPR0

22431

11

01

10

00

00

00

00

1

Aminod

eoxyfutalosin

esynthase

IPR0

22432

00

01

10

00

00

00

00

0Menaquino

nesynthesis

(cho

rismate

dehydrataseamp

naph

thoatesynthase)

IPR0

03773

86

02

20

00

00

00

00

2

FOsynthasesub

unit2

IPR0

20050

33

13

32

12

12

22

22

3Ph

enazines

Phenazineb

iosynthesis

PhzF

protein

IPR0

03719

11

40

02

00

00

00

02

0

8 Archaea

Frh

Mch

Mer

Mtd

Ftr

Fmd

Mcr

MPh

Vho

Ech

Mtr

CoM-SH

CoB-S-S-CoM

CoB-SHHdrDE2H+

H2

H2

H2

MPhH2

H+

CH4

CH3-CoM

CH3-H4MPTF420H2

F420

F420H2

F420

CH2=H4MPT

CHequivH4MPT

CHO-H4MPT

CHO-MFR

CO2

Fdred

Fdox

H2O

2Na+

H2

Figure 2 Hydrogenotrophic methanogenesis in cytochrome containing Methanosarcina barkeri Black lines represent presence ofconversions See Table 3 for nomenclature

reaction thermodynamically favourable (Table 1)The reversereaction of Mcr is therefore an essential step in AOM andis discussed in Section 22 The respiratory chain that isneeded for using different terminal electron acceptors will bediscussed in Section 3

Evidence that ANME use the reverse methanogenesispathway during AOM is derived from metagenomic andmetatranscriptomic analyses This showed that all genesfor the (reverse) methanogenic pathway were present andexpressed in ANME-2a [42] (Figure 4) and ANME-2d[28] (Figure 5) ANME-1 were consistently lacking thegene encoding N5N10-methylene- tetrahydromethanopterin(H4MPT) reductase (Mer) which is an enzyme needed to

oxidize methyl-H4MPT during methane oxidation [40 41

44 51] (Figure 6 Table 2) Possible explanations could be that(1) the mer gene is present but not yet detected (2) ANME-1 used a bypass of this step and (3) Mer was replaced bya structural analogue The first possibility is highly unlikelyAlthough no closed genome of ANME-1 is publicly availableto date all ANME-1 metagenomes consistently only lackMerand no other methanogenic genes The second possibilitywas proposed previously where ANME-1 uses a bypass of

Mer via the formation of methanol or methylamine [41] aswas detected in deletion mutants ofMethanosarcina [52 53]Here CH

3-CoM was presumably converted to methanol by

a methyltransferase and subsequently to formaldehyde by amethanol dehydrogenase (Mdh) Then formaldehyde wouldbe converted to N5N10 methylene-H

4MPT using a fusion

protein of the formaldehyde-activating enzyme (Fae) and ahexulose-6-phosphate synthase (Hps) [53] (Figure 6) BothFae and Hps were found in the ANME-1 metagenome [41]and metaproteome [40 51] However no genes coding forenzymes involved in methanol metabolism were detectedin these ANME-1 datasets [40 41 51] (Table 2) indicatingthat this alternative pathway probably does not occur Thepresence of the FaeHps fusion protein in ANME-1 duringAOM could also be explained by its involvement in ribosephosphate synthesis and not in AOM [54] Indeed the Faegene domains of ANME-1 were located in between ribulose-phosphate binding barrel and ribosomal protein S5 domains(Table S2) The third possibility of a structural analogue ismost likely since an analogue of N5N10-methylene tetrahy-drofolate (H

4HF) reductase (MetF) was expressed byANME-

1 during AOM which could replace Mer [40] (Figure 6)

Archaea 9

Table 3 Nomenclature

Central methanogenic pathwayFmd Formylmethanofuran (CHO-MFR) dehydrogenaseFtr Formylmethanofuran-tetrahydromethanopterin (H

4MPT) formyltransferase

Mch N5N10-methenyl-H4MPT cyclohydrolase

Mtd F420

H2-dependent methylene -H

4MPT dehydrogenase

Mer N5N10-methylene-H4MPT reductase

Mtr N5-methyl-H4MPTcoenzyme M (CoM) methyltransferase

Mcr Methyl coenzyme M (CH3-CoM) reductase

Mdh Methanol dehydrogenaseFaeHps Fusion protein of formaldehyde activating enzyme hexulose-6-phosphate synthaseMetF N5N10-methylene tetrahydrofolate (H

4HF) reductase analogue

Electron transportMvh F

420-nonreducing hydrogenase

Vho Methanophenazine-dependent hydrogenaseFpo F

420H2phenazine oxidoreductase

Fqo F420

H2quinone oxidoreductase

Hdr Coenzyme B-coenzyme M heterodisulfide (CoB-S-S-CoM) reductaseFrh F

420-dependent hydrogenase

Ech Ferredoxin-dependent hydrogenaseMePhMePhH

2Methanophenazine

MQMQH2

MenaquinoneCyt b Cytochrome bCyt c Cytochrome cMHC Multiheme c-type cytochromeRieske Rieske cytochrome b complexOrf7 Pseudoperiplasmic b-type cytochromeNar Nitrate reductaseNap Periplasmic nitrate reductaseNrf Nitrite reductase

22 Methyl Coenzyme M Reductase (Mcr) The enzymaticreaction of a purified Mcr from ANME has not been mea-sured to date The key question is whether a methanogenicMcr can explain the observed in situ AOM rates or if theMcr of ANME is structurally altered There are three mainfactors to be considered the kinetic limitations as definedby enzyme properties (ie half-maximal activity at a specific119870119872value) the thermodynamic constraints of the enzymatic

reaction and the maximal or ambient rate of the enzymaticreaction For the Mcr from Methanothermobacter marbur-gensis kinetic parameters have been determined to illustratethe reversibility of reaction (1) In themethanogenic reactionthe purified Mcr isoform I [55] catalyzes the production ofmethane with a 119881max of 30Umgminus1 and a 119870

119872of 5mM for

CH3-CoM The same (methanogenic) enzyme was able to

oxidize methane to CH3-CoM with a rate of 00114Umgminus1

and a 119870119872for methane of sim10 mM [56]

To answer if the observed AOM rates are in accordancewith the measured methane oxidation rate for the purifiedMcr enzyme from M marburgensis the Mcr activity duringAOM is needed Estimates for AOM rates in terms of activity(per cell dry mass) range between lt1 and 20mmol dayminus1 andg cell dry massminus1 [56ndash66] This equals an activity of 07 to

sim14 nmol min and mg cell dry massminus1 About half of the celldry mass is protein so the activity for the ANME archaeawould approximate 14 to 28 nmol min and mg proteinminus1 Toestimate the activity per mg of Mcr the proportion of Mcrto cellular protein is needed It was reported that 7 of theprotein of ANMEmicrobial mats from the Black Sea [67 68]and 104 of peptides fromHydrate Ridge mesocosms is Mcr[51] As these were no pure cultures the actual percentagesof Mcr in ANME cells may be higher Transcriptome data forANME-2d [43] showed that about 19 of the total transcriptswere derived from the mcr genes indicating (though notdemonstrating) a highMcr content in ANME-2d Estimatingthat 10 of the cellular protein would be Mcr the specificactivity of the enzymewould be between 14 and 280 nmolminand mg Mcr proteinminus1 which is up to 25 times higher thanthe measured reverse reaction rate of the M marburgensisenzyme (sim12 nmol min and mg Mcrminus1 [56]) However thereverse reaction rate of the M marburgensis Mcr was deter-mined under nonsaturating substrate conditions and wastherefore not possibly representing the true maximum rateNevertheless both reverse reaction rates are in the same orderof magnitude other than the forward reaction of 30000ndash100000 nmol min and mgMcrminus1 Thus it seems that the

10 Archaea

H2

CoM-SH

Mch

Mer

Mtd

Ftr

Fmd

Mcr

MPh

MPhH2

MPh

MPh

MPhH2

MtrVho

CoM-SH

CoB-S-S-CoM

CoB-SHHdrDE

Fpo

Fpo

Ech

CH3-CoM

2H+

H2

2H+

2H+

H+

MPhH2

CH4

CH3-H4MPTF420H2

F420

F420H2

F420

CH2=H4MPT

CHequivH4MPT

CHO-H4MPT

CHO-MFR

CO2

Fdred

Fdox

H2O

2Na+

CH3-OH

Figure 3 Methylotrophic methanogenesis in cytochrome containingMethanosarcina barkeri Black lines represent presence of conversionsand red lines indicate reversal of the hydrogenotrophic methanogenic pathway See Table 3 for nomenclature

Mcr in ANME may have similar catalytic properties as themethanogenic enzyme and that the high amount of Mcr permg total cell biomass in ANME may in part compensates forthe apparently relatively slow catalysis

Considering the thermodynamic constraints the Gibbsfree energy change of the Mcr forward reaction under stan-dard conditions is around minus30 kJmolminus1 [56] Therefore thereverse reaction is endergonic under standard conditions andwill not proceed However highmethane concentrations (105according to reaction (1) [69 70]) may lead to a favourablechange in the Gibbs free energy in the direction of AOMHigh methane partial pressure prevails at many habitatswhere AOM has been detected The solubility of methaneat atmospheric pressure is only 13mM [71] Consequentlyincreased AOM rates were reported upon pressurizing sam-ples of different geographical origin [59 60 72 73] The 119870

119872

of Mcr of M marburgensis for methane was determined ator above 10mM and reported 119870

119872values of S-AOM varied

from (at least) 11mM [74] a few mM [57] to even 37mM(equivalent to 3MPa CH

4) [58] Thus high pressure and

therefore high concentrations of methane in the natural habi-tat accelerate the oxidation rate of methane by Mcr Futureresearch to accurately determine119870

119872values and rates forMcr

at differentmethane partial pressures is however neededThismay seem difficult but microbial activity measurements at insitu methane partial pressure were shown to be successful inthe laboratory [75]

It was suggested that the Mcr reaction is the rate limitingstep in reverse methanogenesis [56] which is in line withthe above described challenges Supporting these findingsthere does not seem to be a major change in the aminoacid structure that determines whether the backwards or theforward reaction of Mcr is favoured Amino acid alignments[67] and the crystal structure of ANME-1 Mcr [76] indicatedhigh overall similarity of the methanogenic and methan-otrophic enzyme and unambiguously demonstrated that

Archaea 11

MHC

MHCS-layer

2H+

minuse

cyt b

Mch

Mer

Mtd

Ftr

Fmd

Mcr

MPh

HdrABC

MPh

MHC

MHC

MPh

CoB-S-S-CoM

CoB-SH

CoM-SH

HdrDE

Mtr

Fpo

Fpo

Rnf

MPhH2

MPhH2

MPhH2

MPhH2

CH4

CH3-CoM

CH3-H4MPT

F420H2

F420

F420H2

F420

CH2=H4MPT

CHequivH4MPT

CHO-H4MPT

CHO-MFR

CO2

Fdred

Fdox

H2O

2Na+

MPh

minuse

S-layer

MHC

SRB 2H+

2H+

2Na+

minuse

minuse

minuse

Figure 4 Methanotrophic pathway during S-AOM by ANME-2a [42] Red lines indicate reversal of the hydrogenotrophic methanogenicpathway See Table 3 for nomenclature

CoM-SH and CoB-SH are substrates of the methanotrophicenzyme However several posttranslational modifications ofamino acids were different betweenmethanogens andANMEarchaea and the cofactor F

430(the prosthetic group of Mcr)

is modified in ANME-1 but not in ANME-2 or ANME-3archaea [51 63 67 68 76 77] Furthermore ANME-1 seemsto lack the noncatalytic proteinDdomain of themcr gene thatis present in all other methanogens and methanotrophs butof which the function is unknown (IPR003901 Table 2) [51]A metabolically engineered Methanosarcina acetivorans wasable to convert methane and CO

2to acetate with a plasmid

containingMcr derived from ANME-1 [78] It is thus unclearif only thermodynamic constraints and the abundance ofMcrensureAOMactivity or if also specificmodifications canhavean effect on the reverse activity of Mcr

23 Methane Oxidation by Methanogens Pure cultures ofmethanogens were not able to oxidize methane under highmethane and low hydrogen concentrations (reviewed in[79 80]) Methanogens are only able to oxidize methaneduring net methane production [81] Labeled methane addi-tion (13C or 14C) to pure cultures of methanogens showedproduction of labeled CO

2during net methane production

This characteristic was confirmed with several pure culturesof methanogens [82ndash84] The process was called ldquotracemethane oxidationrdquo (TMO) since the CO

2was formed in

trace amounts relative to the methane produced [83] It isnot clear if TMO is due to the reported reversibility ofindividual enzymes [66] or if it is an active microbial processfrom which energy can be conserved TMO was speculatedto be an active metabolic process for three reasons (1)the amount of methane oxidized varied between differentspecies of methanogens grown on the same methanogenicsubstrate (2) the amount ofmethane oxidized varied betweendifferent methanogenic substrates and (3) TMO productsvaried between different methanogenic substrates [83 84]For instance when grown on acetate Methanosarcina ace-tivorans produced labeled acetate from labeled methaneWhen grown on carbon monoxide it produced both labeledacetate and methyl sulfides from labeled methane [84] Dur-ing hydrogenotrophic and methylotrophic methanogenesisTMO mainly produced CO

2from labeled methane [83]

However in contrast with AOM TMO rates never exceededmethanogenesis rates even during long-term incubationwith methane and sulfate [85] It seems that methanogensare not able to conserve energy from TMO even under

12 Archaea

Mch

Mer

Mtd

Ftr

Fmd

Mcr

MQ

MQ

EchHdrFrh

3MQ

HdrABC

MQ

cyt b Mtr

NrfH

cyt c

NrfA

CoB-S-S-CoM

CoB-SH

CoM-SH

HdrDE

HCOIIHCOIINapHOrf7

NarGH

S-layer

Fqo

Fqo

3H+

3H+

4H+

CH4

CH3-CoM

CH3-H4MPT

F420

F420H2

F420

F420H2

CH2=H4MPT

CHequivH4MPT

CHO-H4MPT

CHO-MFR

CO2

Fdred

Fdox

H2O

2Na+

NH4+

NO2minus

NO2minus

NO3minus

3MQH2

MQH2

MQH2

MQH2eminus

eminus

Rieske

Figure 5 Methanotrophic pathway during N-AOM by ldquoCaM nitroreducensrdquo MPEBLZ (ANME-2d) [43] Red lines indicate reversal of thehydrogenotrophic methanogenic pathway See Table 3 for nomenclature

thermodynamically favourable conditions TMOoccurs bothin absence and presence of an external electron acceptor andonly during net methanogenesis It is therefore most likelycaused by the reported back flux of individual enzymes of themethanogenic pathway [66]

TMO also occurred in granular sludge and in freshwaterand terrestrial samples These mixed communities showedhigher TMO rates than pure cultures reaching up to 90of the methane produced [27 85ndash87] TMO should thereforebe carefully considered in the experimental setup and inter-pretation of results when studying AOM in environmentalsamples especially since TMO rates were like AOM stim-ulated by a high methane partial pressure [72 86 88] Sulfatereduction was also stimulated by higher methane partialpressures [85]Thus a highmethane partial pressure can havea stimulating effect on methane oxidation (either throughAOM or TMO) and SR which could be unrelated to S-AOMMoreover addition of iron sulfate (FeSO

4) or manganese

oxide (MnO2) also increased TMO rates [86] Therefore

methane-dependent SR and sulfate- or metal-dependentmethane oxidation are not necessarily indications for AOMin mixed cultures In conclusion when studying complexldquoblack-boxrdquo communities only net methane oxidation isproof for AOM activity

24 Methane Production by ANME The process of S-AOMis at the energetic limit for sustaining life with estimates

of Gibbs free energy yields between minus18 and minus35 kJmolminus1[45 79 89ndash91] and doubling times between 11 and 75months [65 72 73 92 93] Since S-AOM operates close toits thermodynamic equilibrium the reversibility of individualenzymes leads to measurable back flux producing methane(3ndash7 of AOM) and sulfate (55ndash13 of SR) during S-AOM [66] This ldquotrace methane productionrdquo was observedin situ [11] and in sediment slurries with methanogenesisaround 10 [62 94] or even as high as 50 of AOM [34]When sulfate becomes depleted Gibbs free energy yieldsbecome even lower (less negative) and the enzymatic backflux becomes even more apparent up to 78 of net AOM[95] Previous measurements of 13C depletion below thesulfate-methane transition zone (SMTZ) ofmarine sedimentsthat were thought to be indicative for methanogenesis couldtherefore instead be attributed to the back flux of AOM [95]The occurrence of ANME-1 without a bacterial partner insediment layers where sulfate was depleted was previouslyinterpreted as evidence that ANME-1 perform methanogen-esis [24] but in light of the above it could also indicate AOMThere are indeed reports of AOM activity below the SMTZin the methanogenic zone [96ndash99] In contrast AOM withother electron acceptors than sulfate operates far from thethermodynamic equilibrium with Gibbs free energy changesbetween minus5172 and minus8414 kJmolmethaneminus1 (Table 1) Herethe reported anaerobic back flux [66] is expected to be lessapparent

Archaea 13

MetFMer

Mdh

FaeHps

SRB

MHC

Mch

Mtd

Ftr

Fmd

McrMQ

Hdr1

MQ

MHC

Hdr2

CoB-S-S-CoMCoB-SHCoM-SH

Mtr

Fqo

CH4

CH3-CoMCH3-OH

CH2O CH3-H4MPT

F420F420H2

CHO-H4MPT

CHO-MFR

CO2

FdredFdox

H2O

eminus

eminus

CHequivH4MPT

CH2=H4MPT

xH+

H2

MQH2

MQH2

+xNa

Figure 6 Methanotrophic pathway during S-AOM by ANME-1 [40 41] Red lines indicate reversal of the hydrogenotrophic methanogenicpathway grey lines represent absence of conversions and blue lines indicate a bypass of the hydrogenotrophic methanogenic pathway SeeTable 3 for nomenclature

In laboratory incubations researchers were not ableto stimulate net methanogenesis through addition ofmethanogenic substrates to AOM performing sediments[62 94] In two cases researchers were successful [23 100]In one of these cases sediment-free long-term AOM enrich-ments that were dominated by ANMESRB were incubatedwith methanogenic substrates The resulting methanogenicactivity most likely came from the enrichment of a minorpopulation of methanogens (up to 7permil of total archaealgene tag sequences) that was present in the inoculum[100] In the second study methanogenic substrates wereadded to ANME-1 and ANME-2 dominated microbialmat samples and methanogenesis also occurred [23]However no information was provided for the total archaealcommunity composition which makes it impossible toexclude methanogens as the responsible organisms

Genomic information of ANME also gives indication onpotential methanogenic routes Considering methylotrophicmethanogenesis no gene homologues catalyzing methyltransfer from methylated substrates to coenzyme M weredetected in ANME (Table 2) [40ndash43] Acetoclastic methano-genesis needs either the AMP- and ADP-forming acetyl-coenzyme A synthetase (Acs and Acd resp) or proceedsvia acetate kinase and phosphotransacetylase In ANME-1only the alpha subunit of a homologue of Acd was expressed

during AOM [41] but in an ANME-1 proteome of activeAOM biomass no Acd was detected [40] The Acd gene wasdetected in the single-aggregate genome and transcriptomeof ANME-2a [42] and in ANME-2d [43] However genedomains for Acd are also present in methanogens unableto use acetate as substrate (Table 2) and are probably usedfor lipid metabolism In hydrogenotrophic methanogenesishydrogenases are used to replenish reduced coenzyme B andto recycle oxidized F

420(discussed in Section 21) Both the

cytoplasmic Mvh complex and the membrane bound Vhowere not present in ANME-2d [43] and not expressed inANME-2a (which also lackedEch andF

420-dependent hydro-

genase (Frh)) [42] making hydrogenotrophic methanogen-esis unlikely In ANME-1 both the cytoplasmic HdrABCand MvhD are present as well as homologues of Frh andEch but these were lacking catalytic subunits [40 41] Aniron hydrogenase was found in both ANME-1 metagenomesbut not in any other methanotroph or methanogen [41](Table 2) This iron hydrogenase domain is part of a genethat is 70 identical to a [FeFe]-hydrogenase of Dehalococ-coides mccartyi [FeFe]-hydrogenases catalyze reversible H

2

production and uptake but these were presumed to have nokey function in AOM [41] However the gene is part of a genecluster of three genes containing a 51 kDaNADH ubiquinoneoxidoreductase subunit (Table S3) which could potentially

14 Archaea

form a complex that generates a proton motive force duringhydrogen oxidation Therefore hydrogenotrophic methano-genesis by ANME-1 cannot be excluded yet

3 Respiration during AnaerobicOxidation of Methane

For netAOMtooccur an external electron acceptor is neededwhich results in a favourable Gibbs free energy change(Table 1) A variety of terminal electron acceptors have beendiscovered for AOM which will be discussed in Sections 31ndash33

31 Sulfate-Dependent AOM During sulfate-dependentAOM electrons are transferred from ANME to the sulfate-reducing bacterial partner Previous work tried to uncoverhow electrons were transferred and most compoundsthat could act as interspecies electron carrier (IEC) wereexcluded to be involved in AOM such as methanolhydrogen methanethiol acetate and carbon monoxide[57 61 62 94 101] Indications that polysulfide could actas IEC were found and ANME-2a archaea were thoughtto perform both AOM and sulfate reduction (SR) [102]However in marine seeps hydrothermal vents and othernondiffusion based sediments AOM rates are high andANME form close associations with SRB in dense aggregates[1 5 103 104] In these aggregates the high AOM ratescould not be explained by diffusion of an IEC whichmade direct interspecies electron transfer (DIET) a moreplausible mechanism [89 105 106] Cellular activities wereindependent of aggregate type and distance between thesyntrophic partners within the aggregate which is bestexplained by DIET [107] DIET is normally achieved usingmultiheme cytochrome c proteins (MHCs) and conductivepili (ie nanowires) which are mainly found in bacteriathat donate electrons extracellularly such as Geobacter andShewanella species [108ndash114] Indeed ANME-2a from seep-sediment samples seem to transfer electrons directly usinglarge MHCs [107] which were found in the metagenome ofANME-2a [107 115] ANME-1 and the associated bacterialpartner also overexpressed genes for extracellular MHCsduring AOM [116] which complements previous findings oftranscription [41] and translation [40] of ANME-1 relatedMHC genes Domain based (meta)genome analysis showsthe high abundance of MHC domains in different ANMEas compared to methanogens (Table 2) A recently isolatedbacterial partner of ANME-1 (ldquoHotSeep-1rdquo) also producedcell-to-cell connections using pili-derived nanowires [116]which explain previously detected Deltaproteobacteria-related pili genes in an AOM sample dominated by ANME-1[40]

How ANME use MHCs to donate electrons to thebacterial partner is not yet clear For ANME-2a the electronsprobably flow from methanophenazine to membrane inte-grated di-heme cytochromes (cytochrome 119887119887

6) that transfer

the electrons through the S-layer via MHCS-layer fusionproteins to extracellular MHCs (Figure 4) (Figure 4 in[107]) Exosortases and archaea-specific archaeosortases are

involved in export of cell surface proteins such as the archaealS-layer proteins These transpeptidases recognize specificsignal peptides for protein- sorting that is archaeosor-tase A recognizes the protein-sorting signal PGF-CTERMand archaeosortase C recognizes the PEF-CTERM signal[117] Both ANME-2a and 2d show presence of di-hemecytochromes archaeosortase A (IPR014522) archaeosortaseC (IPR022504) and other exosortase gene domains (Table 2)Moreover some genes of both ANME-2a and 2d containedboth MHC and PGF or PEF-CTERM domains Lastly somegenes of both ANME-2a and 2d contained both MHC andS-layer domains [107] indicating that these could form theabove-stated MHCS-layer fusion proteins

ANME-1 do not seem to have di-heme cytochromes(Table 2) [115] PGF related domains (IPR026453 andIPR026371) were present in all ANME but PEF-CTERM(IPR017474) related domains were absent in ANME-1 (Table 2) Moreover ANME-1 lacked archaeosortaseA (IPR014522) and archaeosortase C gene domains(IPR022504) as well as some other exosortases (Table 2) Asearch in NCBIrsquos conserved domains database (CCD [118])and the EMBL InterPro database [119] of amino acidssequences of all genes from ANME metagenomes thatcontain MHC domains showed that ANME-1 did not haveany protein-sorting signal or S-layer domains within thesegenes In fact S-layer domains were completely absent inANME-1 (Table 2) These results imply that ANME-1 do notuse di-heme cytochromes for electron transfer to MHCsand do not produce an S-layer (Figure 6) This implies thatANME-1 use a different mechanism for DIET and couldexplain the need for less MHCs by ANME-1 (Table 2)and the observed pili-derived nanowires produced by thebacterial partner [116] The genome of the bacterial partnerof ANME-1 (ldquoHotSeep-1rdquo) encoded 24 c-type cytochromesof which 10 were similar to secreted MHCs of Geobactersulfurreducens [120] which also uses pili for DIET [121]

In the case of ANME-2a it is not clear if pili (ienanowires) were formed during AOM It was previouslythought that electrically conductive pili seemed to be aprerequisite for current production andDIET [122 123] evenwhen syntrophs were closely associated [124] such as withinANME-2SRB aggregates However conductive materialssuch as granular activated carbon were shown to be ableto substitute pili in DIET [124] Although in previous workconductive materials such as phenazines or humic acids didnot seem to stimulate AOM rates [61] in a recent study AOMwas decoupled from SR using artificial electron acceptors[125] This indicates that conductive materials can indeedreplace pili and that ANME-2ab could possibly couple AOMto metal oxide reduction or any other suitable electronacceptor (discussed in Section 33) However it needs to beproven if in ANME-2SRB aggregates no pili are formed andif the mechanism of DIET is fundamentally different fromANME-1

As for the polysulfide shuttling theory [102] canonicalgenes for dissimilatory sulfate reduction such as adenylyl-transferase (Sat) APS reductase (Apr) and dissimilatorysulfite reductase (Dsr) which are all present in the sulfate-reducing archeon A fulgidus (Table S2) were not found in

Archaea 15

metagenomes of ANME-1 [41] and ANME-2a (Table S1)The enzymes Sat and Dsr were also not detected in ANMEcells using fluorescent immunolabelling [126] ANME-1 werepreviously found to encode most proteins for assimilatorysulfate reduction [41] ANME-2d only harbor gene domainsthat encode Sat and assimilatoryATP sulfurylase APS kinaseand sodiumsulfate symporters which were not present inANME-2a (Table S1) It is therefore clear that at least ANME-2a cannot donate electrons to sulfate but need to donateelectrons to a sulfate-reducing partner

32 Nitrate-Dependent AOM Unlike during S-AOMANME-2d that perform N-AOM do not need a bacterialpartner but transfer electrons directly to a membrane boundnitrate reductase (Nar) [28 43] (Figure 5) The ANME-2dgenomes contain most MHCs found so far in archaea[107 115] (Table 2) Of the 87 proteins that contained aCxxCH binding motif of which 43 seemed to be true c-typecytochromes [115] 23 CxxCH motif-encoding transcriptswere expressed during N-AOM [43] The function of mostof these MHCs is not known but they are likely involvedin nitrate reduction since c-type cytochromes are capableof operating in the wide range of redox potentials thatcouple nitrate reduction (11986401015840 (NO

3

minusNO2

minus) = +433mV) andmethane oxidation (11986401015840 (CoM-S-S-CoBCoM-SH+CoB-SH)= minus143mV) [43] Nitrate as terminal electron acceptor inanaerobic respiration has been found in halophilic andthermophilic archaea [127] The nar gene cluster of ldquoCaM nitroreducensrdquo comprises several genes including thecatalytic alpha (NarG molybdopterin) and beta (NarHiron sulfur cluster) subunit of nitrate reductase [28 43] The(halo)archaeal nitrate reductase complex was reported to belocated at the extracellular side of the cytoplasmic membrane[128] and in most archaea associated with the cytoplasmicmembrane via NarM [129] The ldquoCa M nitroreducensrdquogenome does not encode NarM but encodes a TAT signalpeptide at the N-terminus of NarG for translocation acrossthe cytoplasmic membrane [28 43] Interestingly theNarG and NarH seem to have been acquired from theProteobacteria via lateral gene transfer [28]

It is not yet clear at which point in themetabolism ldquoCaMnitroreducensrdquo conserves energy During reverse methano-genesis N5-methyl-H

4MPTCoM methyltransferase (Mtr)

dissipates the sodium ion potential across the cytoplasmicmembrane so subsequent steps inN-AOMhave to be coupledto the build-up of a proton or sodium motive force to makethe overall process energetically favourable The analysis ofan environmental genome [43] indicated presence of severalprotein complexes involved in electron transport and energyconservation Electrons that enter the respiratory chain couldbe transported by membrane-integral electron carriers (iemenaquinones) to a Rieske-cytochrome b complex that mayuse cytochrome c as electron acceptor This in turn maybe the electron donor for the unusual nitrate reductasecomplex Energy conservation is thermodynamically andmechanistically feasible at the F

420H2dehydrogenase and the

Rieske-cytochrome b complex (Figure 5) (Figure 2 in [43])Further investigations are needed to determine whether

nitrate reductase is also involved in energy conservationbut this working hypothesis is strengthened by the presenceof cupredoxin multicopper oxidase domains and coppercenters related to the periplasmic domain of cytochrome coxidase subunit II (HCO II) in ANME-2d (Table S1)

BothANME-2d genomes discussed here are derived frombioreactors where ldquoCaM nitroreducensrdquo formed syntrophiccultures with nitrite scavenging bacteria either with ldquoCaKuenenia stuttgartiensisrdquo (anammox bacteria) [28] or ldquoCaMethylomirabilis oxyferardquo (NC10 bacteria) [31 43]This indi-cated that ANME-2d could be dependent on those bacteriafor nitrite removal However in addition to nitrite ldquoCa Mnitroreducensrdquo may also produce ammonium during AOMby a pentaheme c-type nitrite reductase (NrfAH) encodedin the genome [43] (Figure 5) In fact both ANME-2dgenomes contain domains for NrfA (IPR003321) and NrfH(IPR017571) (Table S1) implying that both ANME-2d speciesare not necessarily dependent on a nitrite scavenger duringAOM

33 Metal-Dependent AOM Evidence for metal-dependentAOM was found in marine sediments [130ndash132] In non-marine environments AOM was also hypothesized to becoupled to iron andor manganese oxide reduction [26 133ndash136] or even coupled to the reduction of humic acids [136137] However organisms responsible for metal-dependentAOM were not identified in these studies It was speculatedthat JS1 bacteria methanogenic archaea and Methanohalo-biumANME-3 could be responsible for iron-dependentAOM [138] Other researchers speculated that either ANME-1 or MethanococcoidesANME-3 together with a bacterialpartner were responsible for manganese-dependent AOM[139] In another study where AOM was decoupled from SRANME were not detected which leaves open the possibilitythat other archaeal clades besides ANME could performmetal-dependent AOM [131]

It was recently observed that cultures containing ANME-2a and ANME-2c could decouple AOM from SR in thepresence of artificial electron acceptors humic acids andsoluble iron [125] which confirmed previous findings ofAOM not connected to SR in ANME dominated samples[140] This suggests that ANME-2 could also use insolublemetal oxide minerals as electron acceptor during AOM TheMHCs of ANME-2ab and ANME-2d are larger than thosein Shewanella and Geobacter species [107] which are knownto be capable of extracellular electron conduction It wasspeculated that both ANME-2d and Ferroglobus placidus ofwhich the latter can perform solid iron reduction can foldCxxCHmotifs into extracellular conductive structures or pili[115] Many of the MHCs of ANME-2d were not expressedwhen grown with nitrate (discussed in section 32) implyingthat these are not needed for nitrate reduction [43] Thisstrengthens the hypothesis that also ANME-2d could coupleAOM to reduction of other extracellular electron acceptorsthan nitrate and even to insoluble metal oxides Indeedrecent work showed that ANME-2d could be involved inAOM coupled to chromium(VI) reduction [141] (Table 1reaction (5)) and in AOM coupled to the reduction of soluble

16 Archaea

iron and insoluble ferrihydrite and birnessite minerals [142](Table 1 reactions (3) and (4)) ANME-2d could even possiblydonate electrons to a bacterial partner besides nitrate-richenvironments ANME-2d archaea have been found inwells ofan aquifer where sulfate and methane concentrations overlap[143] Moreover ANME-2d was the only clade detected insediments of a freshwater lake where S-AOM occurred [144]Sulfate concentrations in these studies were low but above1mM and thus higher than the lowest reported concen-trations for S-AOM to occur [145 146] Lastly sequencesof ANME-2d were relatively more abundant in freshwatersediments fed with methane and sulfate than in sedimentsfed with onlymethane or only sulfate and noN-AOMactivitywas detected when fed with nitrate and methane [27] Theseindications hold promise that direct experimental evidencefor sulfate-dependent AOM by ANME-2d could be found inthe future

TheANME-1 genome contains fewerMHCgene domainsas compared to ANME-2a and ANME-2d and some otherarchaea such as somemethylotrophicmethanogens (Table 2)and some members of the Archaeoglobales [115] The MHCsof ANME-1 also have a smaller heme count as compared toother ANME and some other archaea with the largest beingan octaheme cytochrome [107] Each hemewithin aMHChasits own redox potential and therefore structurally differentMHCs represent a large range of redox potentials that canbe used for bioenergetic electron transfer (reviewed in [147])For instance metal oxide reduction in Shewanella oneidensisMR-1 is catalyzed by a chain of a tetraheme (CymA) twodecaheme (MtrA and MtrB) and eventually extracellulardecaheme cytochromes OmcAMtrC that reduce the ironminerals [121 148 149] In Geobacter sulfurreducens ironmineral reduction seems to be catalyzed by the tetrahemecytochrome OmcE and hexaheme cytochrome OmcS trans-ferring electrons from the outer membrane to type IV pilithat transmit the electrons to iron minerals [121 150 151]Since ANME-1 lack MHCs of the correct size and lack genedomains for pili production [116] they seem unable to reduceminerals via both mechanisms present in Shewanella andGeobacter It can therefore be speculated that ANME-1 areless versatile in electron acceptor use and are not able toreduce solid metal oxides However DIET mechanisms arestill not well understood and the true differences betweenMHCs of different ANME types need to be investigated usingbiochemical methods This would allow uncovering the truecapabilities concerning DIET

34 Menaquinones and Methanophenazines ANME-2a en-coded a protein with a domain specific for PhzF which is anenzyme involved in phenazine biosynthesis in Pseudomonasfluorescens [152 153] The respective gene is not present in allmethanophenazine containing methanogens (in our genomecomparison only inM acetivorans andM formicica Table 2)so it is unclear whether this enzyme is really involved inmethanophenazine biosynthesis It is however likely thatANME-2a use methanophenazines in their respiratory chainsince gene domains for menaquinone biosynthesis wereabsent (Table 2) ldquoCa M nitroreducensrdquo probably uses

menaquinones as membrane-integral electron carrier sinceenvironmental genomes [28 43] encoded the futalosine(mqn) biosynthesis pathway as reported for Archaeoglobusfulgidus [154] (Table 2) Moreover ldquoCa M nitroreducensrdquoenrichment cultures showed absence of methanophenazines[43] ANME-1 also contained gene domains formenaquinonebiosynthesis via the futalosine (mqn) biosynthesis pathway(Table 2) Indications for a quinone biosynthesis pathwayin ANME-1 were previously found to be weak since onlysome of the Ubi homologues of the oxic ubiquinone biosyn-thesis pathway were detected [41] but the futalosine (mqn)biosynthesis pathway was overlooked in that particular anal-ysis Additionally ANME-1 have Fqo homologues similarto Archaeoglobus fulgidus [44] and expressed the catalyticsubunit FqoF [41] However since the phenazine biosynthesisdomain PhzF was also present in the ANME-1 genomes(Table 2) and Fpo and Fqo are homologues we cannotconclude on genomic information alone which redox shuttleis used by ANME-1 during AOM If ANME-1 would usemenaquinones this would have implications for subsequentelectron transfer to MHCs since methanophenazine (1198640 =minus165mV) [155] and menaquinone (1198640 = minus80mV) [156] havedifferent redox potentials

35 Cell Adhesion Some gene domains involved in cel-lular adhesion were more abundant in ANME than inmethanogens (Table 2) especially in ANME-2a and ANME-1that are known to form syntrophic interactions for electrontransfer during respiration These domains include HYR(IPR003410) and CARDB domains (IPR011635) that bothhave a direct role in cellular adhesion [157] (Table 2) Interest-ingly also domains related to the cellulosome of Clostridiumspecies termed dockerin and cohesin were highly abundantin both ANME-1 and ANME-2a as compared to ANME-2dand methanogens together with many carbohydrate bindingdomains (Table 2) In Clostridium species dockerin andcohesin form an anchor to the bacterial cell wall that containsa scaffold with cellulose-degrading enzymes and a carbohy-drate bindingmodule that binds cellulose altogether formingthe cellulosome [158] These domains have been found in alldomains of life irrespective of cellulose utilization but thefunction of such proteins outside of the cellulosome is notknown [159]Therefore dockerin cohesin and carbohydratebinding domains in ANME could hypothetically form aconstruct that binds to carbohydrates and could possibly havea function in cell-to-cell contact or MHC adhesion but thisneeds further investigation

4 Future Challenges

Advances in (meta)genomics transcriptomics and pro-teomics have produced the valuable metabolic blueprints ofdifferent ANMEwith hypotheses on how centralmetabolismelectron transport and energy conservation may functionFuture experiments are needed to biochemically demonstratethat these hypotheses are correct

The bottleneck for biochemical studies of ANME isthe lack of pure cultures due to the slow and syntrophic

Archaea 17

growth However the recent milestone discovery of directelectron transfer provides opportunities to grow ANMEas stated previously on electron accepting electrodes (ieanodes) [160] In this way pure or highly enriched culturesof different ANME without their respective syntrophic part-ner could be obtained and MHCs responsible for electricconduction could be biochemically characterized It seemsthat ANME-1 are limited by the size and abundance ofMHCs which could relate to differences in behavior onan anode The partner bacteria of ANME-1 and ANME-2could be investigated on an electron donating electrode (iecathode) with specific focus on the ability to produce pili (ienanowires) Also worth investigating is if besides ANME-2d ANME-2ab could also use insoluble electron acceptorsand if ANME-2d could donate electrons to a bacterialpartner

Another future challenge is to isolate and characterizeMcr from different ANME clades It needs to be investi-gated if Mcr abundance in ANME cells compensates forthe slow reverse activity or if modifications in the Mcrof ANME-1 also contribute to a better reverse activity ofMcr Moreover the effect of methane partial pressure onreaction rates and enzyme kinetics needs to be determined insitu

ANME-1 are potentially able to perform hydrogeno-trophic methanogenesis due to the presence of a hydrogenasein the genome Genetic indications of menaquinones aselectron carrier in ANME-1 and the various cellulosome andcell adhesion related gene domains in all ANME are alsotopics that could be explored further Methanogenic archaeaare likely not able to perform AOM but additional studieson TMO and more genetic modifications to stimulate AOMin methanogens could help in understanding the param-eters needed for AOM to occur Ultimately physiologicalunderstanding of ANME will help to explain the observedecological niche separation of different ANME clades and theoccurrence of ANMEwithout a bacterial partnerThis wouldgreatly enhance our knowledge of themethane cycle in anoxicenvironments

Competing Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors thank Stefanie Berger (RU Nijmegen) for criticalreading of the manuscript This research is supported bythe Soehngen Institute of Anaerobic Microbiology (SIAM)Gravitation grant (024002002) of the Netherlands Ministryof Education Culture and Science and the NetherlandsOrganisation for Scientific Research (NWO) Mike S MJetten was further supported by ERC AG 339880 Eco-MoMand Alfons J M Stams was supported by ERC AG 323009Novel Anaerobes

References

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[2] K-U Hinrichs J M Hayes S P Sylva P G Brewert andE F DeLong ldquoMethane-consuming archaebacteria in marinesedimentsrdquo Nature vol 398 no 6730 pp 802ndash805 1999

[3] V J Orphan C H House K-U Hinrichs K D McKeeganand E F DeLong ldquoMethane-consuming archaea revealed bydirectly coupled isotopic and phylogenetic analysisrdquo Sciencevol 293 no 5529 pp 484ndash487 2001

[4] K-U Hinrichs and A Boetius ldquoThe anaerobic oxidation ofmethane new insights in microbial ecology and biogeochem-istryrdquo inOceanMargin Systems GWefer D Billett D HebbelnB B Joslashrgensen M Schluter and T VanWeering Eds pp 457ndash477 Springer Berlin Germany 2002

[5] K Knittel T Losekann A Boetius R Kort and R AmannldquoDiversity and distribution of methanotrophic archaea at coldseepsrdquo Applied and Environmental Microbiology vol 71 no 1pp 467ndash479 2005

[6] K Knittel and A Boetius ldquoAnaerobic oxidation of methaneprogress with an unknown processrdquo Annual Review of Micro-biology vol 63 pp 311ndash334 2009

[7] V J Orphan K-U Hinrichs W Ussler III et al ldquoComparativeanalysis of methane-oxidizing archaea and sulfate-reducingbacteria in anoxic marine sedimentsrdquoApplied and Environmen-tal Microbiology vol 67 no 4 pp 1922ndash1934 2001

[8] T Losekann K Knittel T Nadalig et al ldquoDiversity andabundance of aerobic and anaerobic methane oxidizers atthe Haakon Mosby Mud Volcano Barents Seardquo Applied andEnvironmentalMicrobiology vol 73 no 10 pp 3348ndash3362 2007

[9] H Niemann T Losekann D De Beer et al ldquoNovel microbialcommunities of the Haakon Mosby mud volcano and their roleas amethane sinkrdquoNature vol 443 no 7113 pp 854ndash858 2006

[10] TNunouraHOida T Toki J Ashi K Takai andKHorikoshildquoQuantification of mcrA by quantitative fluorescent PCR insediments from methane seep of the Nankai Troughrdquo FEMSMicrobiology Ecology vol 57 no 1 pp 149ndash157 2006

[11] B Orcutt A Boetius M Elvert V Samarkin and S B JoyeldquoMolecular biogeochemistry of sulfate reduction methanogen-esis and the anaerobic oxidation of methane at Gulf of Mexicocold seepsrdquoGeochimica et Cosmochimica Acta vol 69 no 17 pp4267ndash4281 2005

[12] V J Orphan W Ussler III T H Naehr C H House K-U Hinrichs and C K Paull ldquoGeological geochemical andmicrobiological heterogeneity of the seafloor around methanevents in the Eel River Basin offshore Californiardquo ChemicalGeology vol 205 no 3-4 pp 265ndash289 2004

[13] M G Pachiadaki A Kallionaki A Dahlmann G J De Langeand K A Kormas ldquoDiversity and spatial distribution ofprokaryotic communities along a sediment vertical profile ofa deep-sea mud volcanordquo Microbial Ecology vol 62 no 3 pp655ndash668 2011

[14] I Roalkvam H Dahle Y Chen S L Joslashrgensen H Haflidasonand I H Steen ldquoFine-scale community structure analysis ofANME in Nyegga sediments with high and low methane fluxrdquoFrontiers in Microbiology vol 3 p 216 2012

[15] K Yanagawa M Sunamura M A Lever et al ldquoNiche separa-tion of methanotrophic archaea (ANME-1 and -2) in methane-seep sediments of the Eastern Japan Sea offshore JoetsurdquoGeomicrobiology Journal vol 28 no 2 pp 118ndash129 2011

18 Archaea

[16] A Pernthaler A E Dekas C T Brown S K Goffredi TEmbaye and V J Orphan ldquoDiverse syntrophic partnershipsfromdeep-seamethane vents revealed by direct cell capture andmetagenomicsrdquo Proceedings of the National Academy of Sciencesof the United States of America vol 105 no 19 pp 7052ndash70572008

[17] R Hatzenpichler S A Connon D Goudeau R R Malm-strom T Woyke and V J Orphan ldquoVisualizing in situtranslational activity for identifying and sorting slow-growingarchaealminusbacterial consortiardquo Proceedings of the NationalAcademy of Sciences vol 113 no 28 pp E4069ndashE4078 2016

[18] L Maignien R J Parkes B Cragg et al ldquoAnaerobic oxidationof methane in hypersaline cold seep sedimentsrdquo FEMS Micro-biology Ecology vol 83 no 1 pp 214ndash231 2013

[19] V J Orphan C H House K-U Hinrichs K D McKeeganand E F DeLong ldquoMultiple archaeal groups mediate methaneoxidation in anoxic cold seep sedimentsrdquo Proceedings of theNational Academy of Sciences of the United States of Americavol 99 no 11 pp 7663ndash7668 2002

[20] T TreudeM Kruger A Boetius and B B Joslashrgensen ldquoEnviron-mental control on anaerobic oxidation of methane in the gassysediments of Eckernforde Bay (German Baltic)rdquo Limnology andOceanography vol 50 no 6 pp 1771ndash1786 2005

[21] G C Jagersma R J W Meulepas I Heikamp-De Jong etal ldquoMicrobial diversity and community structure of a highlyactive anaerobic methane-oxidizing sulfate-reducing enrich-mentrdquo Environmental Microbiology vol 11 no 12 pp 3223ndash3232 2009

[22] M Blumenberg R Seifert J Reitner T Pape andWMichaelisldquoMembrane lipid patterns typify distinct anaerobic methan-otrophic consortiardquo Proceedings of the National Academy ofSciences of the United States of America vol 101 no 30 pp 11111ndash11116 2004

[23] S Bertram M Blumenberg W Michaelis M Siegert MKruger and R Seifert ldquoMethanogenic capabilities of ANME-archaea deduced from 13C-labelling approachesrdquo Environmen-tal Microbiology vol 15 no 8 pp 2384ndash2393 2013

[24] K G Lloyd M J Alperin and A Teske ldquoEnvironmental evi-dence for net methane production and oxidation in putativeANaerobic MEthanotrophic (ANME) archaeardquo EnvironmentalMicrobiology vol 13 no 9 pp 2548ndash2564 2011

[25] M Takeuchi H Yoshioka Y Seo et al ldquoA distinct freshwater-adapted subgroup of ANME-1 dominates active archaeal com-munities in terrestrial subsurfaces in Japanrdquo EnvironmentalMicrobiology vol 13 no 12 pp 3206ndash3218 2011

[26] R T Amos B A Bekins I M Cozzarelli et al ldquoEvidence foriron-mediated anaerobic methane oxidation in a crude oil-contaminated aquiferrdquo Geobiology vol 10 no 6 pp 506ndash5172012

[27] P H Timmers D A Suarez-Zuluaga M van Rossem MDiender A J Stams and C M Plugge ldquoAnaerobic oxidationof methane associated with sulfate reduction in a naturalfreshwater gas sourcerdquo ISME Journal vol 10 pp 1400ndash14122015

[28] M F Haroon S Hu Y Shi et al ldquoAnaerobic oxidation ofmethane coupled to nitrate reduction in a novel archaeallineagerdquo Nature vol 500 no 7468 pp 567ndash570 2013

[29] H J Mills C Hodges K Wilson I R MacDonald and PA Sobecky ldquoMicrobial diversity in sediments associated withsurface-breaching gas hydrate mounds in the Gulf of MexicordquoFEMS Microbiology Ecology vol 46 no 1 pp 39ndash52 2003

[30] K G Lloyd L Lapham and A Teske ldquoAn anaerobic methane-oxidizing community of ANME-1b archaea in hypersaline gulfofMexico sedimentsrdquoApplied and EnvironmentalMicrobiologyvol 72 no 11 pp 7218ndash7230 2006

[31] A A Raghoebarsing A Pol K T Van De Pas-Schoonen et alldquoA microbial consortium couples anaerobic methane oxidationto denitrificationrdquoNature vol 440 no 7086 pp 918ndash921 2006

[32] S Hu R J Zeng L C Burow P Lant J Keller and Z YuanldquoEnrichment of denitrifying anaerobic methane oxidizingmicroorganismsrdquo Environmental Microbiology Reports vol 1no 5 pp 377ndash384 2009

[33] Z-W Ding J Ding L Fu F Zhang and R J Zeng ldquoSimultane-ous enrichment of denitrifying methanotrophs and anammoxbacteriardquo Applied Microbiology and Biotechnology vol 98 no24 pp 10211ndash10221 2014

[34] R Seifert K Nauhaus M Blumenberg M Kruger and WMichaelis ldquoMethane dynamics in a microbial community ofthe Black Sea traced by stable carbon isotopes in vitrordquoOrganicGeochemistry vol 37 no 10 pp 1411ndash1419 2006

[35] J Ding Z-W Ding L Fu Y-Z Lu S H Cheng and R JZeng ldquoNew primers for detecting and quantifying denitrifyinganaerobic methane oxidation archaea in different ecologicalnichesrdquo Applied Microbiology and Biotechnology vol 99 no 22pp 9805ndash9812 2015

[36] A Vaksmaa C Luke T van Alen et al ldquoDistribution and activ-ity of the anaerobic methanotrophic community in a nitrogen-fertilized Italian paddy soilrdquo FEMS Microbiology Ecology vol92 no 12 2016

[37] P N Evans D H Parks G L Chadwick et al ldquoMethanemetabolism in the archaeal phylum Bathyarchaeota revealed bygenome-centric metagenomicsrdquo Science vol 350 no 6259 pp434ndash438 2015

[38] I Vanwonterghem P N Evans D H Parks et al ldquoMethy-lotrophic methanogenesis discovered in the archaeal phylumVerstraetearchaeotardquo Nature Microbiology vol 1 Article ID16170 2016

[39] P Worm J J Koehorst M Visser et al ldquoA genomic view onsyntrophic versus non-syntrophic lifestyle in anaerobic fattyacid degrading communitiesrdquo Biochimica et Biophysica ActamdashBioenergetics vol 1837 no 12 pp 2004ndash2016 2014

[40] R Stokke I Roalkvam A Lanzen H Haflidason and I HSteen ldquoIntegrated metagenomic and metaproteomic analysesof an ANME-1-dominated community in marine cold seepsedimentsrdquo Environmental Microbiology vol 14 no 5 pp 1333ndash1346 2012

[41] A Meyerdierks M Kube I Kostadinov et al ldquoMetagenomeand mRNA expression analyses of anaerobic methanotrophicarchaea of the ANME-1 grouprdquo Environmental Microbiologyvol 12 no 2 pp 422ndash439 2010

[42] F-P Wang Y Zhang Y Chen et al ldquoMethanotrophicarchaea possessing diverging methane-oxidizing and electron-transporting pathwaysrdquo ISME Journal vol 8 no 5 pp 1069ndash1078 2014

[43] A Arshad D R Speth R M de Graaf H J Op den Camp MS Jetten and C U Welte ldquoA metagenomics-based metabolicmodel of nitrate-dependent anaerobic oxidation of methane byMethanoperedens-like archaeardquo Frontiers inMicrobiology vol 6article1423 2015

[44] S J Hallam N Putnam CM Preston et al ldquoReversemethano-genesis testing the hypothesis with environmental genomicsrdquoScience vol 305 no 5689 pp 1457ndash1462 2004

Archaea 19

[45] R K Thauer ldquoAnaerobic oxidation of methane with sulfate onthe reversibility of the reactions that are catalyzed by enzymesalso involved inmethanogenesis fromCO

2rdquoCurrent Opinion in

Microbiology vol 14 no 3 pp 292ndash299 2011[46] U Deppenmeier V Muller and G Gottschalk ldquoPathways of

energy conservation in methanogenic archaeardquo Archives ofMicrobiology vol 165 no 3 pp 149ndash163 1996

[47] A-K Kaster J Moll K Parey and R K Thauer ldquoCoupling offerredoxin and heterodisulfide reduction via electron bifurca-tion in hydrogenotrophic methanogenic archaeardquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 108 no 7 pp 2981ndash2986 2011

[48] R K Thauer A-K Kaster H Seedorf W Buckel and RHedderich ldquoMethanogenic archaea ecologically relevant dif-ferences in energy conservationrdquo Nature Reviews Microbiologyvol 6 no 8 pp 579ndash591 2008

[49] W Ludwig O Strunk R Westram et al ldquoARB a softwareenvironment for sequence datardquoNucleic Acids Research vol 32no 4 pp 1363ndash1371 2004

[50] E Pruesse C Quast K Knittel et al ldquoSILVA a comprehensiveonline resource for quality checked and aligned ribosomal RNAsequence data compatible with ARBrdquo Nucleic Acids Researchvol 35 no 21 pp 7188ndash7196 2007

[51] J J Marlow C T Skennerton Z Li et al ldquoProteomic stableisotope probing reveals biosynthesis dynamics of slow growingmethane based microbial communitiesrdquo Frontiers in Microbiol-ogy vol 7 article 386 2016

[52] P V Welander and W W Metcalf ldquoLoss of the mtr operon inMethanosarcina blocks growth on methanol but not methano-genesis and reveals an unknown methanogenic pathwayrdquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 102 no 30 pp 10664ndash10669 2005

[53] P V Welander and W W Metcalf ldquoMutagenesis of the C1oxidation pathway inmethanosarcina barkeri new insights intothe MtrMer bypass pathwayrdquo Journal of Bacteriology vol 190no 6 pp 1928ndash1936 2008

[54] M Goenrich R K Thauer H Yurimoto and N KatoldquoFormaldehyde activating enzyme (Fae) and hexulose-6-phosphate synthase (Hps) inMethanosarcina barkeri a possiblefunction in ribose-5-phosphate biosynthesisrdquoArchives ofMicro-biology vol 184 no 1 pp 41ndash48 2005

[55] M Goenrich FMahlert E C Duin C Bauer B Jaun and R KThauer ldquoProbing the reactivity of Ni in the active site of methyl-coenzyme M reductase with substrate analoguesrdquo Journal ofBiological Inorganic Chemistry vol 9 no 6 pp 691ndash705 2004

[56] S Scheller M Goenrich R Boecher R K Thauer and BJaun ldquoThe key nickel enzyme of methanogenesis catalyses theanaerobic oxidation of methanerdquo Nature vol 465 no 7298 pp606ndash608 2010

[57] K Nauhaus A Boetius M Kruger and F Widdel ldquoIn vitrodemonstration of anaerobic oxidation of methane coupled tosulphate reduction in sediment from amarine gas hydrate areardquoEnvironmental Microbiology vol 4 no 5 pp 296ndash305 2002

[58] Y Zhang J-P Henriet J Bursens and N Boon ldquoStimulationof in vitro anaerobic oxidation of methane rate in a continuoushigh-pressure bioreactorrdquo Bioresource Technology vol 101 no9 pp 3132ndash3138 2010

[59] M Kruger T Treude H Wolters K Nauhaus and A BoetiusldquoMicrobial methane turnover in different marine habitatsrdquoPalaeogeography Palaeoclimatology Palaeoecology vol 227 no1ndash3 pp 6ndash17 2005

[60] C Deusner V Meyer and T G Ferdelman ldquoHigh-pressuresystems for gas-phase free continuous incubation of enrichedmarinemicrobial communities performing anaerobic oxidationof methanerdquo Biotechnology and Bioengineering vol 105 no 3pp 524ndash533 2010

[61] K Nauhaus T Treude A Boetius and M Kruger ldquoEnviron-mental regulation of the anaerobic oxidation of methane acomparison of ANME-I and ANME-II communitiesrdquo Environ-mental Microbiology vol 7 no 1 pp 98ndash106 2005

[62] T Treude V Orphan K Knittel A Gieseke C H House andA Boetius ldquoConsumption of methane and CO

2by methan-

otrophicmicrobial mats from gas seeps of the anoxic Black SeardquoApplied and EnvironmentalMicrobiology vol 73 no 7 pp 2271ndash2283 2007

[63] T Holler F Widdel K Knittel et al ldquoThermophilic anaerobicoxidation of methane by marine microbial consortiardquo ISMEJournal vol 5 no 12 pp 1946ndash1956 2011

[64] M Kruger M Blumenberg S Kasten et al ldquoA novel multi-layered methanotrophic microbial mat system growing on thesediment of the Black Seardquo Environmental Microbiology vol 10no 8 pp 1934ndash1947 2008

[65] R J WMeulepas C G Jagersma J Gieteling C J N BuismanA J M Stams and P N L Lens ldquoEnrichment of anaerobicmethanotrophs in sulfate-reducing membrane bioreactorsrdquoBiotechnology and Bioengineering vol 104 no 3 pp 458ndash4702009

[66] T Holler G Wegener H Niemann et al ldquoCarbon and sulfurback flux during anaerobic microbial oxidation of methane andcoupled sulfate reductionrdquo Proceedings of the National Academyof Sciences of the United States of America vol 108 no 52 ppE1484ndashE1490 2011

[67] M Kruger AMeyerdierks F O Glockner et al ldquoA conspicuousnickel protein in microbial mats that oxidize methane anaero-bicallyrdquo Nature vol 426 no 6968 pp 878ndash881 2003

[68] S Mayr C Latkoczy M Kruger et al ldquoStructure of an F430

variant from archaea associated with anaerobic oxidation ofmethanerdquo Journal of the American Chemical Society vol 130 no32 pp 10758ndash10767 2008

[69] S Shima and R K Thauer ldquoMethyl-coenzyme M reductaseand the anaerobic oxidation of methane in methanotrophicArchaeardquo Current Opinion in Microbiology vol 8 no 6 pp643ndash648 2005

[70] R K Thauer and S Shima ldquoMethane as fuel for anaerobicmicroorganismsrdquo Annals of the New York Academy of Sciencesvol 1125 pp 158ndash170 2008

[71] S Yamamoto J B Alcauskas and T E Crozier ldquoSolubility ofmethane in distilled water and seawaterrdquo Journal of Chemicaland Engineering Data vol 21 no 1 pp 78ndash80 1976

[72] P H A Timmers J Gieteling H C A Widjaja-Greefkeset al ldquoGrowth of anaerobic methane-oxidizing archaea andsulfate-reducing bacteria in a high-pressure membrane capsulebioreactorrdquoApplied and EnvironmentalMicrobiology vol 81 no4 pp 1286ndash1296 2015

[73] MKruger HWoltersMGehre S B Joye andH-H RichnowldquoTracing the slow growth of anaerobic methane-oxidizingcommunities by 15N-labelling techniquesrdquo FEMS MicrobiologyEcology vol 63 no 3 pp 401ndash411 2008

[74] R J W Meulepas C G Jagersma A F Khadem C J N Buis-man A J M Stams and P N L Lens ldquoEffect of environmentalconditions on sulfate reduction withmethane as electron donorby an Eckernforde Bay enrichmentrdquo Environmental Science andTechnology vol 43 no 17 pp 6553ndash6559 2009

20 Archaea

[75] M W Bowles V A Samarkin and S B Joye ldquoImprovedmeasurement of microbial activity in deep-sea sediments atin situ pressure and methane concentrationrdquo Limnology andOceanography Methods vol 9 pp 499ndash506 2011

[76] S Shima M Krueger T Weinert et al ldquoStructure of a methyl-coenzyme M reductase from Black Sea mats that oxidizemethane anaerobicallyrdquo Nature vol 481 no 7379 pp 98ndash1012012

[77] K D Allen G Wegener and R H White ldquoDiscovery of multi-ple modified F-430 coenzymes in methanogens and anaerobicmethanotrophic archaea suggests possible new roles for F-430in naturerdquoApplied and Environmental Microbiology vol 80 no20 pp 6403ndash6412 2014

[78] V W Soo M J McAnulty A Tripathi et al ldquoReversingmethanogenesis to capture methane for liquid biofuel precur-sorsrdquoMicrobial Cell Factories vol 15 article 11 2016

[79] D L Valentine and W S Reeburgh ldquoNew perspectives onanaerobicmethane oxidationrdquoEnvironmentalMicrobiology vol2 no 5 pp 477ndash484 2000

[80] D L Valentine ldquoBiogeochemistry and microbial ecology ofmethane oxidation in anoxic environments a reviewrdquo Antonievan Leeuwenhoek International Journal of General and Molecu-lar Microbiology vol 81 no 1-4 pp 271ndash282 2002

[81] A J B Zehnder and T D Brock ldquoMethane formation andmethane oxidation by methanogenic bacteriardquo Journal of Bac-teriology vol 137 no 1 pp 420ndash432 1979

[82] J Harder ldquoAnaerobic methane oxidation by bacteria employ-ing 14C-methane uncontaminated with 14C-carbon monoxiderdquoMarine Geology vol 137 no 1-2 pp 13ndash23 1997

[83] J J Moran C H House K H Freeman and J G FerryldquoTrace methane oxidation studied in several Euryarchaeotaunder diverse conditionsrdquo Archaea vol 1 no 5 pp 303ndash3092005

[84] J J Moran C H House B Thomas and K H FreemanldquoProducts of tracemethane oxidation during nonmethyltrophicgrowth by Methanosarcinardquo Journal of Geophysical ResearchBiogeosciences vol 112 no 2 2007

[85] R J W Meulepas C G Jagersma Y Zhang et al ldquoTracemethane oxidation and the methane dependency of sulfatereduction in anaerobic granular sludgerdquo FEMS MicrobiologyEcology vol 72 no 2 pp 261ndash271 2010

[86] A J B Zehnder andTD Brock ldquoAnaerobicmethane oxidationoccurrence and ecologyrdquoApplied and Environmental Microbiol-ogy vol 39 no 1 pp 194ndash204 1980

[87] S J Blazewicz D G Petersen M P Waldrop and M K Fire-stone ldquoAnaerobic oxidation of methane in tropical and borealsoils ecological significance in terrestrial methane cyclingrdquoJournal of Geophysical Research Biogeosciences vol 117 no 2Article ID G02033 2012

[88] K A Smemo and J B Yavitt ldquoEvidence for anaerobic CH4

oxidation in freshwater peatlandsrdquo Geomicrobiology Journalvol 24 no 7-8 pp 583ndash597 2007

[89] M J Alperin and T M Hoehler ldquoAnaerobic methane oxidationby archaeasulfate-reducing bacteria aggregates 1 Thermody-namic and physical constraintsrdquo American Journal of Sciencevol 309 no 10 pp 869ndash957 2009

[90] S L Caldwell J R Laidler E A Brewer J O Eberly S CSandborgh and F S Colwell ldquoAnaerobic oxidation of methanemechanisms bioenergetics and the ecology of associatedmicroorganismsrdquo Environmental Science and Technology vol42 no 18 pp 6791ndash6799 2008

[91] GWang A J Spivack and S DrsquoHondt ldquoGibbs energies of reac-tion and microbial mutualism in anaerobic deep subseafloorsediments of ODP Site 1226rdquoGeochimica et Cosmochimica Actavol 74 no 14 pp 3938ndash3947 2010

[92] P R Girguis A E Cozen and E F DeLong ldquoGrowth andpopulation dynamics of anaerobic methane-oxidizing archaeaand sulfate-reducing bacteria in a continuous-flow bioreactorrdquoApplied and EnvironmentalMicrobiology vol 71 no 7 pp 3725ndash3733 2005

[93] K Nauhaus M Albrecht M Elvert A Boetius and F WiddelldquoIn vitro cell growth ofmarine archaeal-bacterial consortia dur-ing anaerobic oxidation ofmethanewith sulfaterdquoEnvironmentalMicrobiology vol 9 no 1 pp 187ndash196 2007

[94] B Orcutt V Samarkin A Boetius and S Joye ldquoOn the relation-ship between methane production and oxidation by anaerobicmethanotrophic communities from cold seeps of the Gulf ofMexicordquo Environmental Microbiology vol 10 no 5 pp 1108ndash1117 2008

[95] M Y Yoshinaga T Holler T Goldhammer et al ldquoCarbon iso-tope equilibration during sulphate-limited anaerobic oxidationof methanerdquo Nature Geoscience vol 7 no 3 pp 190ndash194 2014

[96] T Treude J Niggemann J Kallmeyer et al ldquoAnaerobic oxi-dation of methane and sulfate reduction along the Chileancontinental marginrdquo Geochimica et Cosmochimica Acta vol 69no 11 pp 2767ndash2779 2005

[97] R J Parkes B A Cragg N Banning et al ldquoBiogeochemistryand biodiversity of methane cycling in subsurface marinesediments (SkagerrakDenmark)rdquoEnvironmentalMicrobiologyvol 9 no 5 pp 1146ndash1161 2007

[98] N J Knab B A Cragg E R C Hornibrook et al ldquoRegulationof anaerobic methane oxidation in sediments of the Black SeardquoBiogeosciences vol 6 no 8 pp 1505ndash1518 2009

[99] H Yoshioka A Maruyama T Nakamura et al ldquoActivities anddistribution of methanogenic and methane-oxidizing microbesin marine sediments from the Cascadia Marginrdquo Geobiologyvol 8 no 3 pp 223ndash233 2010

[100] G Wegener V Krukenberg S E Ruff M Y Kellermann andK Knittel ldquoMetabolic capabilities of microorganisms involvedin and associated with the anaerobic oxidation of methanerdquoFrontiers in Microbiology vol 7 article 46 2016

[101] R J W Meulepas C G Jagersma A F Khadem A J MStams and P N L Lens ldquoEffect of methanogenic substrateson anaerobic oxidation of methane and sulfate reduction by ananaerobic methanotrophic enrichmentrdquo Applied Microbiologyand Biotechnology vol 87 no 4 pp 1499ndash1506 2010

[102] J Milucka T G Ferdelman L Polerecky et al ldquoZero-valentsulphur is a key intermediate in marine methane oxidationrdquoNature vol 491 no 7425 pp 541ndash546 2012

[103] W Michaelis R Seifert K Nauhaus et al ldquoMicrobial reefs inthe black sea fueled by anaerobic oxidation ofmethanerdquo Sciencevol 297 no 5583 pp 1013ndash1015 2002

[104] A Vigneron P Cruaud P Pignet et al ldquoArchaeal and anaerobicmethane oxidizer communities in the Sonora Margin coldseeps Guaymas Basin (Gulf of California)rdquo ISME Journal vol7 no 8 pp 1595ndash1608 2013

[105] M Alperin and T Hoehler ldquoThe ongoing mystery of sea-floormethanerdquo Science vol 329 no 5989 pp 288ndash289 2010

[106] B Orcutt and C Meile ldquoConstraints on mechanisms and ratesof anaerobic oxidation of methane by microbial consortiaprocess-basedmodeling of ANME-2 archaea and sulfate reduc-ing bacteria interactionsrdquo Biogeosciences vol 5 no 6 pp 1587ndash1599 2008

Archaea 21

[107] S E McGlynn G L Chadwick C P Kempes and V J OrphanldquoSingle cell activity reveals direct electron transfer in methan-otrophic consortiardquoNature vol 526 no 7574 pp 531ndash535 2015

[108] D R Lovley ldquoElectromicrobiologyrdquo Annual Review of Microbi-ology vol 66 pp 391ndash409 2012

[109] S M Strycharz-Glaven R M Snider A Guiseppi-Elie andL M Tender ldquoOn the electrical conductivity of microbialnanowires and biofilmsrdquoEnergy and Environmental Science vol4 no 11 pp 4366ndash4379 2011

[110] D J Richardson J N Butt J K Fredrickson et al ldquoThe lsquoporinndashcytochromersquo model for microbe-to-mineral electron transferrdquoMolecular Microbiology vol 85 no 2 pp 201ndash212 2012

[111] A Okamoto K Hashimoto and R Nakamura ldquoLong-rangeelectron conduction of Shewanella biofilms mediated by outermembrane C-type cytochromesrdquo Bioelectrochemistry vol 85pp 61ndash65 2012

[112] M Y El-Naggar G Wanger K M Leung et al ldquoElectricaltransport along bacterial nanowires from Shewanella oneidensisMR-1rdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 107 no 42 pp 18127ndash18131 2010

[113] G Reguera K D McCarthy T Mehta J S Nicoll M TTuominen and D R Lovley ldquoExtracellular electron transfer viamicrobial nanowiresrdquo Nature vol 435 no 7045 pp 1098ndash11012005

[114] Z M Summers H E Fogarty C Leang A E Franks N SMalvankar and D R Lovley ldquoDirect exchange of electronswithin aggregates of an evolved syntrophic coculture of anaer-obic bacteriardquo Science vol 330 no 6009 pp 1413ndash1415 2010

[115] A Kletzin T Heimerl J Flechsler L V Niftrik R Rachel andA Klingl ldquoCytochromes c in archaea distribution maturationcell architecture and the special case of Ignicoccus hospitalisrdquoFrontiers in Microbiology vol 6 article 439 2015

[116] GWegener V Krukenberg D Riedel H E Tegetmeyer and ABoetius ldquoIntercellular wiring enables electron transfer betweenmethanotrophic archaea and bacteriardquo Nature vol 526 no7574 pp 587ndash590 2015

[117] D HHaft S H Payne and J D Selengut ldquoArchaeosortases andexosortases are widely distributed systems linking membranetransit with posttranslational modificationrdquo Journal of Bacteri-ology vol 194 no 1 pp 36ndash48 2012

[118] A Marchler-Bauer M K Derbyshire N R Gonzales et alldquoCDD NCBIrsquos conserved domain databaserdquo Nucleic AcidsResearch vol 43 no 1 pp D222ndashD226 2015

[119] A Mitchell H-Y Chang L Daugherty et al ldquoThe InterProprotein families database the classification resource after 15yearsrdquo Nucleic Acids Research vol 43 no 1 pp D213ndashD2212015

[120] V Krukenberg K Harding M Richter et al ldquoCandidatusdesulfofervidus auxilii a hydrogenotrophic sulfate-reducingbacterium involved in the thermophilic anaerobic oxidation ofmethanerdquo Environmental Microbiology vol 18 pp 3073ndash30912016

[121] L Shi T C Squier J M Zachara and J K Fredrickson ldquoRes-piration of metal (hydr)oxides by Shewanella and Geobactera key role for multihaem c-type cytochromesrdquo MolecularMicrobiology vol 65 no 1 pp 12ndash20 2007

[122] N S Malvankar and D R Lovley ldquoMicrobial nanowires forbioenergy applicationsrdquo Current Opinion in Biotechnology vol27 pp 88ndash95 2014

[123] A-E Rotaru T LWoodard K PNevin andDR Lovley ldquoLinkbetween capacity for current production and syntrophic growth

in Geobacter speciesrdquo Frontiers in Microbiology vol 6 article744 2015

[124] A-E Rotaru P M Shrestha F Liu et al ldquoDirect interspecieselectron transfer between Geobacter metallireducens andMethanosarcina barkerirdquo Applied and Environmental Microbi-ology vol 80 no 15 pp 4599ndash4605 2014

[125] S Scheller H Yu G L Chadwick S E McGlynn and VJ Orphan ldquoArtificial electron acceptors decouple archaealmethane oxidation from sulfate reductionrdquo Science vol 351 no6274 pp 703ndash707 2016

[126] J Milucka F Widdel and S Shima ldquoImmunological detec-tion of enzymes for sulfate reduction in anaerobic methane-oxidizing consortiardquo Environmental Microbiology vol 15 no 5pp 1561ndash1571 2013

[127] P Cabello M D Roldan and C Moreno-Vivian ldquoNitratereduction and the nitrogen cycle in archaeardquoMicrobiology vol150 no 11 pp 3527ndash3546 2004

[128] R MMartinez-Espinosa E J Dridge M J Bonete et al ldquoLookon the positive sideThe orientation identification and bioener-getics of lsquoArchaealrsquomembrane-boundnitrate reductasesrdquoFEMSMicrobiology Letters vol 276 no 2 pp 129ndash139 2007

[129] S de VriesMMomcilovicM J F Strampraad J PWhiteleggeA Baghai and I Schroder ldquoAdaptation to a high-tungsten envi-ronment pyrobaculum aerophilum contains an active tungstennitrate reductaserdquo Biochemistry vol 49 no 45 pp 9911ndash99212010

[130] M Egger O Rasigraf C J Sapart et al ldquoIron-mediated anaer-obic oxidation of methane in brackish coastal sedimentsrdquoEnvironmental Science and Technology vol 49 no 1 pp 277ndash283 2015

[131] T Treude S Krause J Maltby A W Dale R Coffin and LJ Hamdan ldquoSulfate reduction and methane oxidation activitybelow the sulfate-methane transition zone in Alaskan BeaufortSea continental margin sediments implications for deep sulfurcyclingrdquo Geochimica et Cosmochimica Acta vol 144 pp 217ndash237 2014

[132] N Riedinger M J Formolo T W Lyons S Henkel A Beckand S Kasten ldquoAn inorganic geochemical argument for coupledanaerobic oxidation of methane and iron reduction in marinesedimentsrdquo Geobiology vol 12 no 2 pp 172ndash181 2014

[133] Y-H Chang T-W Cheng W-J Lai et al ldquoMicrobial methanecycling in a terrestrialmud volcano in eastern Taiwanrdquo Environ-mental Microbiology vol 14 no 4 pp 895ndash908 2012

[134] S A Crowe S Katsev K Leslie et al ldquoThe methane cycle inferruginous Lake Matanordquo Geobiology vol 9 no 1 pp 61ndash782011

[135] O Sivan M Adler A Pearson et al ldquoGeochemical evidence foriron-mediated anaerobic oxidation of methanerdquo Limnology andOceanography vol 56 no 4 pp 1536ndash1544 2011

[136] K E A Segarra C Comerford J Slaughter and S B JoyeldquoImpact of electron acceptor availability on the anaerobic oxi-dation of methane in coastal freshwater and brackish wetlandsedimentsrdquo Geochimica et Cosmochimica Acta vol 115 pp 15ndash30 2013

[137] V Gupta K A Smemo J B Yavitt D Fowle B Branfireunand N Basiliko ldquoStable isotopes reveal widespread anaerobicmethane oxidation across latitude and peatland typerdquo Environ-mental Science and Technology vol 47 no 15 pp 8273ndash82792013

[138] O Oni T Miyatake S Kasten et al ldquoDistinct microbialpopulations are tightly linked to the profile of dissolved iron in

22 Archaea

the methanic sediments of the Helgolandmud area North SeardquoFrontiers in Microbiology vol 6 2015

[139] E J Beal C H House and V J Orphan ldquoManganese- andiron-dependent marine methane oxidationrdquo Science vol 325no 5937 pp 184ndash187 2009

[140] M W Bowles V A Samarkin K M Bowles and S B JoyeldquoWeak coupling between sulfate reduction and the anaerobicoxidation of methane in methane-rich seafloor sedimentsduring ex situ incubationrdquo Geochimica et Cosmochimica Actavol 75 no 2 pp 500ndash519 2011

[141] Y Z Lu L Fu J Ding Z Ding N Li and R J Zeng ldquoCr(VI)reduction coupled with anaerobic oxidation of methane in alaboratory reactorrdquoWater Research vol 102 pp 445ndash452 2016

[142] K F Ettwig B Zhu D Speth J T Keltjens M S Jetten and BKartal ldquoArchaea catalyze iron-dependent anaerobic oxidationof methanerdquo Proceedings of the National Academy of Sciences ofthe United States of America vol 113 no 45 pp 12792ndash127962016

[143] T M Flynn R A Sanford H Ryu et al ldquoFunctional microbialdiversity explains groundwater chemistry in a pristine aquiferrdquoBMCMicrobiology vol 13 no 1 article no 146 2013

[144] C J Schubert F Vazquez T Losekann-Behrens K KnittelM Tonolla and A Boetius ldquoEvidence for anaerobic oxidationof methane in sediments of a freshwater system (Lago diCadagno)rdquo FEMS Microbiology Ecology vol 76 no 1 pp 26ndash38 2011

[145] K E A Segarra F Schubotz V Samarkin M Y Yoshinaga K-U Hinrichs and S B Joye ldquoHigh rates of anaerobic methaneoxidation in freshwater wetlands reduce potential atmosphericmethane emissionsrdquo Nature Communications vol 6 article7477 2015

[146] E J Beal M W Claire and C H House ldquoHigh rates ofanaerobic methanotrophy at low sulfate concentrations withimplications for past and present methane levelsrdquo Geobiologyvol 9 no 2 pp 131ndash139 2011

[147] F Kracke I Vassilev and J O Kromer ldquoMicrobial electrontransport and energy conservationmdashthe foundation for opti-mizing bioelectrochemical systemsrdquo Frontiers in Microbiologyvol 6 article 575 2015

[148] C L Reardon A C Dohnalkova P Nachimuthu et al ldquoRoleof outer-membrane cytochromes MtrC and OmcA in thebiomineralization of ferrihydrite by Shewanella oneidensisMR-1rdquo Geobiology vol 8 no 1 pp 56ndash68 2010

[149] L Shi B Chen Z Wang et al ldquoIsolation of a high-affinityfunctional protein complex between OmcA and MtrC twoouter membrane decaheme c-type cytochromes of Shewanellaoneidensis MR-1rdquo Journal of Bacteriology vol 188 no 13 pp4705ndash4714 2006

[150] X Qian T Mester L Morgado et al ldquoBiochemical charac-terization of purified OmcS a c-type cytochrome requiredfor insoluble Fe(III) reduction in Geobacter sulfurreducensrdquoBiochimica et BiophysicaActamdashBioenergetics vol 1807 no 4 pp404ndash412 2011

[151] T Mehta M V Coppi S E Childers and D R Lovley ldquoOutermembrane c-type cytochromes required for Fe(III) andMn(IV)oxide reduction in Geobacter sulfurreducensrdquo Applied andEnvironmentalMicrobiology vol 71 no 12 pp 8634ndash8641 2005

[152] W Blankenfeldt A P Kuzin T Skarina et al ldquoStructure andfunction of the phenazine biosynthetic protein PhzF fromPseudomonas fluorescensrdquoProceedings of theNational Academyof Sciences of the United States of America vol 101 no 47 pp16431ndash16436 2004

[153] J F Parsons F Song L Parsons K Calabrese E Eisensteinand J E Ladner ldquoStructure and function of the phenazinebiosynthesis protein PhzF fromPseudomonas fluorescens 2-79rdquoBiochemistry vol 43 no 39 pp 12427ndash12435 2004

[154] T Hiratsuka K Furihata J Ishikawa et al ldquoAn alternativemenaquinone biosynthetic pathway operating in microorgan-ismsrdquo Science vol 321 no 5896 pp 1670ndash1673 2008

[155] M Tietze A Beuchle I Lamla et al ldquoRedox potentials ofmethanophenazine and CoB-S-S-CoM factors involved inelectron transport in methanogenic archaeardquo ChemBioChemvol 4 no 4 pp 333ndash335 2003

[156] Q H Tran and G Unden ldquoChanges in the proton potentialand the cellular energetics of Escherichia coli during growth byaerobic and anaerobic respiration or by fermentationrdquoEuropeanJournal of Biochemistry vol 251 no 1-2 pp 538ndash543 1998

[157] I Callebaut D Gilges I Vigon and J-P Mornon ldquoHYR anextracellular module involved in cellular adhesion and relatedto the immunoglobulin-like foldrdquo Protein Science vol 9 no 7pp 1382ndash1390 2000

[158] H J Gilbert ldquoCellulosomes microbial nanomachines that dis-play plasticity in quaternary structurerdquoMolecular Microbiologyvol 63 no 6 pp 1568ndash1576 2007

[159] A Peer S P Smith E A Bayer R Lamed and I BorovokldquoNoncellulosomal cohesin- and dockerin-like modules in thethree domains of liferdquo FEMS Microbiology Letters vol 291 no1 pp 1ndash16 2009

[160] M Wagner ldquoMicrobiology conductive consortiardquo Nature vol526 no 7574 pp 513ndash514 2015

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Archaea 7

Table2Con

tinued

InterPro

IDANME-1S

ANME-1M

ANME-2a

ANME-2d

HANME-2d

AAM

AM-1

M-2

M-3

H-1

H-2

H-3

H-4

SMenaquinones

3-Dem

ethylubiqu

inon

e-9

3-methyltransfe

rase

IPR0

28973

00

03

30

00

00

01

00

0

Succinated

ehydrogenasefu

marate

redu

ctaseflavoproteinsubu

nit

IPR0

1400

60

01

21

00

00

10

00

01

UbiECO

Q5methyltransfe

rase

IPR0

04033

30

02

21

01

00

00

00

0UbiECO

Q5methyltransfe

rase

conservedsite

IPR0

23576

30

02

20

00

10

00

00

0

NrfD

family

IPR0

05614

30

04

30

00

00

00

00

3Fu

talosin

ehydrolase

IPR0

19963

00

01

10

00

00

00

00

0Cy

clicd

ehypoxanthinefutalosine

synthase

IPR0

22431

11

01

10

00

00

00

00

1

Aminod

eoxyfutalosin

esynthase

IPR0

22432

00

01

10

00

00

00

00

0Menaquino

nesynthesis

(cho

rismate

dehydrataseamp

naph

thoatesynthase)

IPR0

03773

86

02

20

00

00

00

00

2

FOsynthasesub

unit2

IPR0

20050

33

13

32

12

12

22

22

3Ph

enazines

Phenazineb

iosynthesis

PhzF

protein

IPR0

03719

11

40

02

00

00

00

02

0

8 Archaea

Frh

Mch

Mer

Mtd

Ftr

Fmd

Mcr

MPh

Vho

Ech

Mtr

CoM-SH

CoB-S-S-CoM

CoB-SHHdrDE2H+

H2

H2

H2

MPhH2

H+

CH4

CH3-CoM

CH3-H4MPTF420H2

F420

F420H2

F420

CH2=H4MPT

CHequivH4MPT

CHO-H4MPT

CHO-MFR

CO2

Fdred

Fdox

H2O

2Na+

H2

Figure 2 Hydrogenotrophic methanogenesis in cytochrome containing Methanosarcina barkeri Black lines represent presence ofconversions See Table 3 for nomenclature

reaction thermodynamically favourable (Table 1)The reversereaction of Mcr is therefore an essential step in AOM andis discussed in Section 22 The respiratory chain that isneeded for using different terminal electron acceptors will bediscussed in Section 3

Evidence that ANME use the reverse methanogenesispathway during AOM is derived from metagenomic andmetatranscriptomic analyses This showed that all genesfor the (reverse) methanogenic pathway were present andexpressed in ANME-2a [42] (Figure 4) and ANME-2d[28] (Figure 5) ANME-1 were consistently lacking thegene encoding N5N10-methylene- tetrahydromethanopterin(H4MPT) reductase (Mer) which is an enzyme needed to

oxidize methyl-H4MPT during methane oxidation [40 41

44 51] (Figure 6 Table 2) Possible explanations could be that(1) the mer gene is present but not yet detected (2) ANME-1 used a bypass of this step and (3) Mer was replaced bya structural analogue The first possibility is highly unlikelyAlthough no closed genome of ANME-1 is publicly availableto date all ANME-1 metagenomes consistently only lackMerand no other methanogenic genes The second possibilitywas proposed previously where ANME-1 uses a bypass of

Mer via the formation of methanol or methylamine [41] aswas detected in deletion mutants ofMethanosarcina [52 53]Here CH

3-CoM was presumably converted to methanol by

a methyltransferase and subsequently to formaldehyde by amethanol dehydrogenase (Mdh) Then formaldehyde wouldbe converted to N5N10 methylene-H

4MPT using a fusion

protein of the formaldehyde-activating enzyme (Fae) and ahexulose-6-phosphate synthase (Hps) [53] (Figure 6) BothFae and Hps were found in the ANME-1 metagenome [41]and metaproteome [40 51] However no genes coding forenzymes involved in methanol metabolism were detectedin these ANME-1 datasets [40 41 51] (Table 2) indicatingthat this alternative pathway probably does not occur Thepresence of the FaeHps fusion protein in ANME-1 duringAOM could also be explained by its involvement in ribosephosphate synthesis and not in AOM [54] Indeed the Faegene domains of ANME-1 were located in between ribulose-phosphate binding barrel and ribosomal protein S5 domains(Table S2) The third possibility of a structural analogue ismost likely since an analogue of N5N10-methylene tetrahy-drofolate (H

4HF) reductase (MetF) was expressed byANME-

1 during AOM which could replace Mer [40] (Figure 6)

Archaea 9

Table 3 Nomenclature

Central methanogenic pathwayFmd Formylmethanofuran (CHO-MFR) dehydrogenaseFtr Formylmethanofuran-tetrahydromethanopterin (H

4MPT) formyltransferase

Mch N5N10-methenyl-H4MPT cyclohydrolase

Mtd F420

H2-dependent methylene -H

4MPT dehydrogenase

Mer N5N10-methylene-H4MPT reductase

Mtr N5-methyl-H4MPTcoenzyme M (CoM) methyltransferase

Mcr Methyl coenzyme M (CH3-CoM) reductase

Mdh Methanol dehydrogenaseFaeHps Fusion protein of formaldehyde activating enzyme hexulose-6-phosphate synthaseMetF N5N10-methylene tetrahydrofolate (H

4HF) reductase analogue

Electron transportMvh F

420-nonreducing hydrogenase

Vho Methanophenazine-dependent hydrogenaseFpo F

420H2phenazine oxidoreductase

Fqo F420

H2quinone oxidoreductase

Hdr Coenzyme B-coenzyme M heterodisulfide (CoB-S-S-CoM) reductaseFrh F

420-dependent hydrogenase

Ech Ferredoxin-dependent hydrogenaseMePhMePhH

2Methanophenazine

MQMQH2

MenaquinoneCyt b Cytochrome bCyt c Cytochrome cMHC Multiheme c-type cytochromeRieske Rieske cytochrome b complexOrf7 Pseudoperiplasmic b-type cytochromeNar Nitrate reductaseNap Periplasmic nitrate reductaseNrf Nitrite reductase

22 Methyl Coenzyme M Reductase (Mcr) The enzymaticreaction of a purified Mcr from ANME has not been mea-sured to date The key question is whether a methanogenicMcr can explain the observed in situ AOM rates or if theMcr of ANME is structurally altered There are three mainfactors to be considered the kinetic limitations as definedby enzyme properties (ie half-maximal activity at a specific119870119872value) the thermodynamic constraints of the enzymatic

reaction and the maximal or ambient rate of the enzymaticreaction For the Mcr from Methanothermobacter marbur-gensis kinetic parameters have been determined to illustratethe reversibility of reaction (1) In themethanogenic reactionthe purified Mcr isoform I [55] catalyzes the production ofmethane with a 119881max of 30Umgminus1 and a 119870

119872of 5mM for

CH3-CoM The same (methanogenic) enzyme was able to

oxidize methane to CH3-CoM with a rate of 00114Umgminus1

and a 119870119872for methane of sim10 mM [56]

To answer if the observed AOM rates are in accordancewith the measured methane oxidation rate for the purifiedMcr enzyme from M marburgensis the Mcr activity duringAOM is needed Estimates for AOM rates in terms of activity(per cell dry mass) range between lt1 and 20mmol dayminus1 andg cell dry massminus1 [56ndash66] This equals an activity of 07 to

sim14 nmol min and mg cell dry massminus1 About half of the celldry mass is protein so the activity for the ANME archaeawould approximate 14 to 28 nmol min and mg proteinminus1 Toestimate the activity per mg of Mcr the proportion of Mcrto cellular protein is needed It was reported that 7 of theprotein of ANMEmicrobial mats from the Black Sea [67 68]and 104 of peptides fromHydrate Ridge mesocosms is Mcr[51] As these were no pure cultures the actual percentagesof Mcr in ANME cells may be higher Transcriptome data forANME-2d [43] showed that about 19 of the total transcriptswere derived from the mcr genes indicating (though notdemonstrating) a highMcr content in ANME-2d Estimatingthat 10 of the cellular protein would be Mcr the specificactivity of the enzymewould be between 14 and 280 nmolminand mg Mcr proteinminus1 which is up to 25 times higher thanthe measured reverse reaction rate of the M marburgensisenzyme (sim12 nmol min and mg Mcrminus1 [56]) However thereverse reaction rate of the M marburgensis Mcr was deter-mined under nonsaturating substrate conditions and wastherefore not possibly representing the true maximum rateNevertheless both reverse reaction rates are in the same orderof magnitude other than the forward reaction of 30000ndash100000 nmol min and mgMcrminus1 Thus it seems that the

10 Archaea

H2

CoM-SH

Mch

Mer

Mtd

Ftr

Fmd

Mcr

MPh

MPhH2

MPh

MPh

MPhH2

MtrVho

CoM-SH

CoB-S-S-CoM

CoB-SHHdrDE

Fpo

Fpo

Ech

CH3-CoM

2H+

H2

2H+

2H+

H+

MPhH2

CH4

CH3-H4MPTF420H2

F420

F420H2

F420

CH2=H4MPT

CHequivH4MPT

CHO-H4MPT

CHO-MFR

CO2

Fdred

Fdox

H2O

2Na+

CH3-OH

Figure 3 Methylotrophic methanogenesis in cytochrome containingMethanosarcina barkeri Black lines represent presence of conversionsand red lines indicate reversal of the hydrogenotrophic methanogenic pathway See Table 3 for nomenclature

Mcr in ANME may have similar catalytic properties as themethanogenic enzyme and that the high amount of Mcr permg total cell biomass in ANME may in part compensates forthe apparently relatively slow catalysis

Considering the thermodynamic constraints the Gibbsfree energy change of the Mcr forward reaction under stan-dard conditions is around minus30 kJmolminus1 [56] Therefore thereverse reaction is endergonic under standard conditions andwill not proceed However highmethane concentrations (105according to reaction (1) [69 70]) may lead to a favourablechange in the Gibbs free energy in the direction of AOMHigh methane partial pressure prevails at many habitatswhere AOM has been detected The solubility of methaneat atmospheric pressure is only 13mM [71] Consequentlyincreased AOM rates were reported upon pressurizing sam-ples of different geographical origin [59 60 72 73] The 119870

119872

of Mcr of M marburgensis for methane was determined ator above 10mM and reported 119870

119872values of S-AOM varied

from (at least) 11mM [74] a few mM [57] to even 37mM(equivalent to 3MPa CH

4) [58] Thus high pressure and

therefore high concentrations of methane in the natural habi-tat accelerate the oxidation rate of methane by Mcr Futureresearch to accurately determine119870

119872values and rates forMcr

at differentmethane partial pressures is however neededThismay seem difficult but microbial activity measurements at insitu methane partial pressure were shown to be successful inthe laboratory [75]

It was suggested that the Mcr reaction is the rate limitingstep in reverse methanogenesis [56] which is in line withthe above described challenges Supporting these findingsthere does not seem to be a major change in the aminoacid structure that determines whether the backwards or theforward reaction of Mcr is favoured Amino acid alignments[67] and the crystal structure of ANME-1 Mcr [76] indicatedhigh overall similarity of the methanogenic and methan-otrophic enzyme and unambiguously demonstrated that

Archaea 11

MHC

MHCS-layer

2H+

minuse

cyt b

Mch

Mer

Mtd

Ftr

Fmd

Mcr

MPh

HdrABC

MPh

MHC

MHC

MPh

CoB-S-S-CoM

CoB-SH

CoM-SH

HdrDE

Mtr

Fpo

Fpo

Rnf

MPhH2

MPhH2

MPhH2

MPhH2

CH4

CH3-CoM

CH3-H4MPT

F420H2

F420

F420H2

F420

CH2=H4MPT

CHequivH4MPT

CHO-H4MPT

CHO-MFR

CO2

Fdred

Fdox

H2O

2Na+

MPh

minuse

S-layer

MHC

SRB 2H+

2H+

2Na+

minuse

minuse

minuse

Figure 4 Methanotrophic pathway during S-AOM by ANME-2a [42] Red lines indicate reversal of the hydrogenotrophic methanogenicpathway See Table 3 for nomenclature

CoM-SH and CoB-SH are substrates of the methanotrophicenzyme However several posttranslational modifications ofamino acids were different betweenmethanogens andANMEarchaea and the cofactor F

430(the prosthetic group of Mcr)

is modified in ANME-1 but not in ANME-2 or ANME-3archaea [51 63 67 68 76 77] Furthermore ANME-1 seemsto lack the noncatalytic proteinDdomain of themcr gene thatis present in all other methanogens and methanotrophs butof which the function is unknown (IPR003901 Table 2) [51]A metabolically engineered Methanosarcina acetivorans wasable to convert methane and CO

2to acetate with a plasmid

containingMcr derived from ANME-1 [78] It is thus unclearif only thermodynamic constraints and the abundance ofMcrensureAOMactivity or if also specificmodifications canhavean effect on the reverse activity of Mcr

23 Methane Oxidation by Methanogens Pure cultures ofmethanogens were not able to oxidize methane under highmethane and low hydrogen concentrations (reviewed in[79 80]) Methanogens are only able to oxidize methaneduring net methane production [81] Labeled methane addi-tion (13C or 14C) to pure cultures of methanogens showedproduction of labeled CO

2during net methane production

This characteristic was confirmed with several pure culturesof methanogens [82ndash84] The process was called ldquotracemethane oxidationrdquo (TMO) since the CO

2was formed in

trace amounts relative to the methane produced [83] It isnot clear if TMO is due to the reported reversibility ofindividual enzymes [66] or if it is an active microbial processfrom which energy can be conserved TMO was speculatedto be an active metabolic process for three reasons (1)the amount of methane oxidized varied between differentspecies of methanogens grown on the same methanogenicsubstrate (2) the amount ofmethane oxidized varied betweendifferent methanogenic substrates and (3) TMO productsvaried between different methanogenic substrates [83 84]For instance when grown on acetate Methanosarcina ace-tivorans produced labeled acetate from labeled methaneWhen grown on carbon monoxide it produced both labeledacetate and methyl sulfides from labeled methane [84] Dur-ing hydrogenotrophic and methylotrophic methanogenesisTMO mainly produced CO

2from labeled methane [83]

However in contrast with AOM TMO rates never exceededmethanogenesis rates even during long-term incubationwith methane and sulfate [85] It seems that methanogensare not able to conserve energy from TMO even under

12 Archaea

Mch

Mer

Mtd

Ftr

Fmd

Mcr

MQ

MQ

EchHdrFrh

3MQ

HdrABC

MQ

cyt b Mtr

NrfH

cyt c

NrfA

CoB-S-S-CoM

CoB-SH

CoM-SH

HdrDE

HCOIIHCOIINapHOrf7

NarGH

S-layer

Fqo

Fqo

3H+

3H+

4H+

CH4

CH3-CoM

CH3-H4MPT

F420

F420H2

F420

F420H2

CH2=H4MPT

CHequivH4MPT

CHO-H4MPT

CHO-MFR

CO2

Fdred

Fdox

H2O

2Na+

NH4+

NO2minus

NO2minus

NO3minus

3MQH2

MQH2

MQH2

MQH2eminus

eminus

Rieske

Figure 5 Methanotrophic pathway during N-AOM by ldquoCaM nitroreducensrdquo MPEBLZ (ANME-2d) [43] Red lines indicate reversal of thehydrogenotrophic methanogenic pathway See Table 3 for nomenclature

thermodynamically favourable conditions TMOoccurs bothin absence and presence of an external electron acceptor andonly during net methanogenesis It is therefore most likelycaused by the reported back flux of individual enzymes of themethanogenic pathway [66]

TMO also occurred in granular sludge and in freshwaterand terrestrial samples These mixed communities showedhigher TMO rates than pure cultures reaching up to 90of the methane produced [27 85ndash87] TMO should thereforebe carefully considered in the experimental setup and inter-pretation of results when studying AOM in environmentalsamples especially since TMO rates were like AOM stim-ulated by a high methane partial pressure [72 86 88] Sulfatereduction was also stimulated by higher methane partialpressures [85]Thus a highmethane partial pressure can havea stimulating effect on methane oxidation (either throughAOM or TMO) and SR which could be unrelated to S-AOMMoreover addition of iron sulfate (FeSO

4) or manganese

oxide (MnO2) also increased TMO rates [86] Therefore

methane-dependent SR and sulfate- or metal-dependentmethane oxidation are not necessarily indications for AOMin mixed cultures In conclusion when studying complexldquoblack-boxrdquo communities only net methane oxidation isproof for AOM activity

24 Methane Production by ANME The process of S-AOMis at the energetic limit for sustaining life with estimates

of Gibbs free energy yields between minus18 and minus35 kJmolminus1[45 79 89ndash91] and doubling times between 11 and 75months [65 72 73 92 93] Since S-AOM operates close toits thermodynamic equilibrium the reversibility of individualenzymes leads to measurable back flux producing methane(3ndash7 of AOM) and sulfate (55ndash13 of SR) during S-AOM [66] This ldquotrace methane productionrdquo was observedin situ [11] and in sediment slurries with methanogenesisaround 10 [62 94] or even as high as 50 of AOM [34]When sulfate becomes depleted Gibbs free energy yieldsbecome even lower (less negative) and the enzymatic backflux becomes even more apparent up to 78 of net AOM[95] Previous measurements of 13C depletion below thesulfate-methane transition zone (SMTZ) ofmarine sedimentsthat were thought to be indicative for methanogenesis couldtherefore instead be attributed to the back flux of AOM [95]The occurrence of ANME-1 without a bacterial partner insediment layers where sulfate was depleted was previouslyinterpreted as evidence that ANME-1 perform methanogen-esis [24] but in light of the above it could also indicate AOMThere are indeed reports of AOM activity below the SMTZin the methanogenic zone [96ndash99] In contrast AOM withother electron acceptors than sulfate operates far from thethermodynamic equilibrium with Gibbs free energy changesbetween minus5172 and minus8414 kJmolmethaneminus1 (Table 1) Herethe reported anaerobic back flux [66] is expected to be lessapparent

Archaea 13

MetFMer

Mdh

FaeHps

SRB

MHC

Mch

Mtd

Ftr

Fmd

McrMQ

Hdr1

MQ

MHC

Hdr2

CoB-S-S-CoMCoB-SHCoM-SH

Mtr

Fqo

CH4

CH3-CoMCH3-OH

CH2O CH3-H4MPT

F420F420H2

CHO-H4MPT

CHO-MFR

CO2

FdredFdox

H2O

eminus

eminus

CHequivH4MPT

CH2=H4MPT

xH+

H2

MQH2

MQH2

+xNa

Figure 6 Methanotrophic pathway during S-AOM by ANME-1 [40 41] Red lines indicate reversal of the hydrogenotrophic methanogenicpathway grey lines represent absence of conversions and blue lines indicate a bypass of the hydrogenotrophic methanogenic pathway SeeTable 3 for nomenclature

In laboratory incubations researchers were not ableto stimulate net methanogenesis through addition ofmethanogenic substrates to AOM performing sediments[62 94] In two cases researchers were successful [23 100]In one of these cases sediment-free long-term AOM enrich-ments that were dominated by ANMESRB were incubatedwith methanogenic substrates The resulting methanogenicactivity most likely came from the enrichment of a minorpopulation of methanogens (up to 7permil of total archaealgene tag sequences) that was present in the inoculum[100] In the second study methanogenic substrates wereadded to ANME-1 and ANME-2 dominated microbialmat samples and methanogenesis also occurred [23]However no information was provided for the total archaealcommunity composition which makes it impossible toexclude methanogens as the responsible organisms

Genomic information of ANME also gives indication onpotential methanogenic routes Considering methylotrophicmethanogenesis no gene homologues catalyzing methyltransfer from methylated substrates to coenzyme M weredetected in ANME (Table 2) [40ndash43] Acetoclastic methano-genesis needs either the AMP- and ADP-forming acetyl-coenzyme A synthetase (Acs and Acd resp) or proceedsvia acetate kinase and phosphotransacetylase In ANME-1only the alpha subunit of a homologue of Acd was expressed

during AOM [41] but in an ANME-1 proteome of activeAOM biomass no Acd was detected [40] The Acd gene wasdetected in the single-aggregate genome and transcriptomeof ANME-2a [42] and in ANME-2d [43] However genedomains for Acd are also present in methanogens unableto use acetate as substrate (Table 2) and are probably usedfor lipid metabolism In hydrogenotrophic methanogenesishydrogenases are used to replenish reduced coenzyme B andto recycle oxidized F

420(discussed in Section 21) Both the

cytoplasmic Mvh complex and the membrane bound Vhowere not present in ANME-2d [43] and not expressed inANME-2a (which also lackedEch andF

420-dependent hydro-

genase (Frh)) [42] making hydrogenotrophic methanogen-esis unlikely In ANME-1 both the cytoplasmic HdrABCand MvhD are present as well as homologues of Frh andEch but these were lacking catalytic subunits [40 41] Aniron hydrogenase was found in both ANME-1 metagenomesbut not in any other methanotroph or methanogen [41](Table 2) This iron hydrogenase domain is part of a genethat is 70 identical to a [FeFe]-hydrogenase of Dehalococ-coides mccartyi [FeFe]-hydrogenases catalyze reversible H

2

production and uptake but these were presumed to have nokey function in AOM [41] However the gene is part of a genecluster of three genes containing a 51 kDaNADH ubiquinoneoxidoreductase subunit (Table S3) which could potentially

14 Archaea

form a complex that generates a proton motive force duringhydrogen oxidation Therefore hydrogenotrophic methano-genesis by ANME-1 cannot be excluded yet

3 Respiration during AnaerobicOxidation of Methane

For netAOMtooccur an external electron acceptor is neededwhich results in a favourable Gibbs free energy change(Table 1) A variety of terminal electron acceptors have beendiscovered for AOM which will be discussed in Sections 31ndash33

31 Sulfate-Dependent AOM During sulfate-dependentAOM electrons are transferred from ANME to the sulfate-reducing bacterial partner Previous work tried to uncoverhow electrons were transferred and most compoundsthat could act as interspecies electron carrier (IEC) wereexcluded to be involved in AOM such as methanolhydrogen methanethiol acetate and carbon monoxide[57 61 62 94 101] Indications that polysulfide could actas IEC were found and ANME-2a archaea were thoughtto perform both AOM and sulfate reduction (SR) [102]However in marine seeps hydrothermal vents and othernondiffusion based sediments AOM rates are high andANME form close associations with SRB in dense aggregates[1 5 103 104] In these aggregates the high AOM ratescould not be explained by diffusion of an IEC whichmade direct interspecies electron transfer (DIET) a moreplausible mechanism [89 105 106] Cellular activities wereindependent of aggregate type and distance between thesyntrophic partners within the aggregate which is bestexplained by DIET [107] DIET is normally achieved usingmultiheme cytochrome c proteins (MHCs) and conductivepili (ie nanowires) which are mainly found in bacteriathat donate electrons extracellularly such as Geobacter andShewanella species [108ndash114] Indeed ANME-2a from seep-sediment samples seem to transfer electrons directly usinglarge MHCs [107] which were found in the metagenome ofANME-2a [107 115] ANME-1 and the associated bacterialpartner also overexpressed genes for extracellular MHCsduring AOM [116] which complements previous findings oftranscription [41] and translation [40] of ANME-1 relatedMHC genes Domain based (meta)genome analysis showsthe high abundance of MHC domains in different ANMEas compared to methanogens (Table 2) A recently isolatedbacterial partner of ANME-1 (ldquoHotSeep-1rdquo) also producedcell-to-cell connections using pili-derived nanowires [116]which explain previously detected Deltaproteobacteria-related pili genes in an AOM sample dominated by ANME-1[40]

How ANME use MHCs to donate electrons to thebacterial partner is not yet clear For ANME-2a the electronsprobably flow from methanophenazine to membrane inte-grated di-heme cytochromes (cytochrome 119887119887

6) that transfer

the electrons through the S-layer via MHCS-layer fusionproteins to extracellular MHCs (Figure 4) (Figure 4 in[107]) Exosortases and archaea-specific archaeosortases are

involved in export of cell surface proteins such as the archaealS-layer proteins These transpeptidases recognize specificsignal peptides for protein- sorting that is archaeosor-tase A recognizes the protein-sorting signal PGF-CTERMand archaeosortase C recognizes the PEF-CTERM signal[117] Both ANME-2a and 2d show presence of di-hemecytochromes archaeosortase A (IPR014522) archaeosortaseC (IPR022504) and other exosortase gene domains (Table 2)Moreover some genes of both ANME-2a and 2d containedboth MHC and PGF or PEF-CTERM domains Lastly somegenes of both ANME-2a and 2d contained both MHC andS-layer domains [107] indicating that these could form theabove-stated MHCS-layer fusion proteins

ANME-1 do not seem to have di-heme cytochromes(Table 2) [115] PGF related domains (IPR026453 andIPR026371) were present in all ANME but PEF-CTERM(IPR017474) related domains were absent in ANME-1 (Table 2) Moreover ANME-1 lacked archaeosortaseA (IPR014522) and archaeosortase C gene domains(IPR022504) as well as some other exosortases (Table 2) Asearch in NCBIrsquos conserved domains database (CCD [118])and the EMBL InterPro database [119] of amino acidssequences of all genes from ANME metagenomes thatcontain MHC domains showed that ANME-1 did not haveany protein-sorting signal or S-layer domains within thesegenes In fact S-layer domains were completely absent inANME-1 (Table 2) These results imply that ANME-1 do notuse di-heme cytochromes for electron transfer to MHCsand do not produce an S-layer (Figure 6) This implies thatANME-1 use a different mechanism for DIET and couldexplain the need for less MHCs by ANME-1 (Table 2)and the observed pili-derived nanowires produced by thebacterial partner [116] The genome of the bacterial partnerof ANME-1 (ldquoHotSeep-1rdquo) encoded 24 c-type cytochromesof which 10 were similar to secreted MHCs of Geobactersulfurreducens [120] which also uses pili for DIET [121]

In the case of ANME-2a it is not clear if pili (ienanowires) were formed during AOM It was previouslythought that electrically conductive pili seemed to be aprerequisite for current production andDIET [122 123] evenwhen syntrophs were closely associated [124] such as withinANME-2SRB aggregates However conductive materialssuch as granular activated carbon were shown to be ableto substitute pili in DIET [124] Although in previous workconductive materials such as phenazines or humic acids didnot seem to stimulate AOM rates [61] in a recent study AOMwas decoupled from SR using artificial electron acceptors[125] This indicates that conductive materials can indeedreplace pili and that ANME-2ab could possibly couple AOMto metal oxide reduction or any other suitable electronacceptor (discussed in Section 33) However it needs to beproven if in ANME-2SRB aggregates no pili are formed andif the mechanism of DIET is fundamentally different fromANME-1

As for the polysulfide shuttling theory [102] canonicalgenes for dissimilatory sulfate reduction such as adenylyl-transferase (Sat) APS reductase (Apr) and dissimilatorysulfite reductase (Dsr) which are all present in the sulfate-reducing archeon A fulgidus (Table S2) were not found in

Archaea 15

metagenomes of ANME-1 [41] and ANME-2a (Table S1)The enzymes Sat and Dsr were also not detected in ANMEcells using fluorescent immunolabelling [126] ANME-1 werepreviously found to encode most proteins for assimilatorysulfate reduction [41] ANME-2d only harbor gene domainsthat encode Sat and assimilatoryATP sulfurylase APS kinaseand sodiumsulfate symporters which were not present inANME-2a (Table S1) It is therefore clear that at least ANME-2a cannot donate electrons to sulfate but need to donateelectrons to a sulfate-reducing partner

32 Nitrate-Dependent AOM Unlike during S-AOMANME-2d that perform N-AOM do not need a bacterialpartner but transfer electrons directly to a membrane boundnitrate reductase (Nar) [28 43] (Figure 5) The ANME-2dgenomes contain most MHCs found so far in archaea[107 115] (Table 2) Of the 87 proteins that contained aCxxCH binding motif of which 43 seemed to be true c-typecytochromes [115] 23 CxxCH motif-encoding transcriptswere expressed during N-AOM [43] The function of mostof these MHCs is not known but they are likely involvedin nitrate reduction since c-type cytochromes are capableof operating in the wide range of redox potentials thatcouple nitrate reduction (11986401015840 (NO

3

minusNO2

minus) = +433mV) andmethane oxidation (11986401015840 (CoM-S-S-CoBCoM-SH+CoB-SH)= minus143mV) [43] Nitrate as terminal electron acceptor inanaerobic respiration has been found in halophilic andthermophilic archaea [127] The nar gene cluster of ldquoCaM nitroreducensrdquo comprises several genes including thecatalytic alpha (NarG molybdopterin) and beta (NarHiron sulfur cluster) subunit of nitrate reductase [28 43] The(halo)archaeal nitrate reductase complex was reported to belocated at the extracellular side of the cytoplasmic membrane[128] and in most archaea associated with the cytoplasmicmembrane via NarM [129] The ldquoCa M nitroreducensrdquogenome does not encode NarM but encodes a TAT signalpeptide at the N-terminus of NarG for translocation acrossthe cytoplasmic membrane [28 43] Interestingly theNarG and NarH seem to have been acquired from theProteobacteria via lateral gene transfer [28]

It is not yet clear at which point in themetabolism ldquoCaMnitroreducensrdquo conserves energy During reverse methano-genesis N5-methyl-H

4MPTCoM methyltransferase (Mtr)

dissipates the sodium ion potential across the cytoplasmicmembrane so subsequent steps inN-AOMhave to be coupledto the build-up of a proton or sodium motive force to makethe overall process energetically favourable The analysis ofan environmental genome [43] indicated presence of severalprotein complexes involved in electron transport and energyconservation Electrons that enter the respiratory chain couldbe transported by membrane-integral electron carriers (iemenaquinones) to a Rieske-cytochrome b complex that mayuse cytochrome c as electron acceptor This in turn maybe the electron donor for the unusual nitrate reductasecomplex Energy conservation is thermodynamically andmechanistically feasible at the F

420H2dehydrogenase and the

Rieske-cytochrome b complex (Figure 5) (Figure 2 in [43])Further investigations are needed to determine whether

nitrate reductase is also involved in energy conservationbut this working hypothesis is strengthened by the presenceof cupredoxin multicopper oxidase domains and coppercenters related to the periplasmic domain of cytochrome coxidase subunit II (HCO II) in ANME-2d (Table S1)

BothANME-2d genomes discussed here are derived frombioreactors where ldquoCaM nitroreducensrdquo formed syntrophiccultures with nitrite scavenging bacteria either with ldquoCaKuenenia stuttgartiensisrdquo (anammox bacteria) [28] or ldquoCaMethylomirabilis oxyferardquo (NC10 bacteria) [31 43]This indi-cated that ANME-2d could be dependent on those bacteriafor nitrite removal However in addition to nitrite ldquoCa Mnitroreducensrdquo may also produce ammonium during AOMby a pentaheme c-type nitrite reductase (NrfAH) encodedin the genome [43] (Figure 5) In fact both ANME-2dgenomes contain domains for NrfA (IPR003321) and NrfH(IPR017571) (Table S1) implying that both ANME-2d speciesare not necessarily dependent on a nitrite scavenger duringAOM

33 Metal-Dependent AOM Evidence for metal-dependentAOM was found in marine sediments [130ndash132] In non-marine environments AOM was also hypothesized to becoupled to iron andor manganese oxide reduction [26 133ndash136] or even coupled to the reduction of humic acids [136137] However organisms responsible for metal-dependentAOM were not identified in these studies It was speculatedthat JS1 bacteria methanogenic archaea and Methanohalo-biumANME-3 could be responsible for iron-dependentAOM [138] Other researchers speculated that either ANME-1 or MethanococcoidesANME-3 together with a bacterialpartner were responsible for manganese-dependent AOM[139] In another study where AOM was decoupled from SRANME were not detected which leaves open the possibilitythat other archaeal clades besides ANME could performmetal-dependent AOM [131]

It was recently observed that cultures containing ANME-2a and ANME-2c could decouple AOM from SR in thepresence of artificial electron acceptors humic acids andsoluble iron [125] which confirmed previous findings ofAOM not connected to SR in ANME dominated samples[140] This suggests that ANME-2 could also use insolublemetal oxide minerals as electron acceptor during AOM TheMHCs of ANME-2ab and ANME-2d are larger than thosein Shewanella and Geobacter species [107] which are knownto be capable of extracellular electron conduction It wasspeculated that both ANME-2d and Ferroglobus placidus ofwhich the latter can perform solid iron reduction can foldCxxCHmotifs into extracellular conductive structures or pili[115] Many of the MHCs of ANME-2d were not expressedwhen grown with nitrate (discussed in section 32) implyingthat these are not needed for nitrate reduction [43] Thisstrengthens the hypothesis that also ANME-2d could coupleAOM to reduction of other extracellular electron acceptorsthan nitrate and even to insoluble metal oxides Indeedrecent work showed that ANME-2d could be involved inAOM coupled to chromium(VI) reduction [141] (Table 1reaction (5)) and in AOM coupled to the reduction of soluble

16 Archaea

iron and insoluble ferrihydrite and birnessite minerals [142](Table 1 reactions (3) and (4)) ANME-2d could even possiblydonate electrons to a bacterial partner besides nitrate-richenvironments ANME-2d archaea have been found inwells ofan aquifer where sulfate and methane concentrations overlap[143] Moreover ANME-2d was the only clade detected insediments of a freshwater lake where S-AOM occurred [144]Sulfate concentrations in these studies were low but above1mM and thus higher than the lowest reported concen-trations for S-AOM to occur [145 146] Lastly sequencesof ANME-2d were relatively more abundant in freshwatersediments fed with methane and sulfate than in sedimentsfed with onlymethane or only sulfate and noN-AOMactivitywas detected when fed with nitrate and methane [27] Theseindications hold promise that direct experimental evidencefor sulfate-dependent AOM by ANME-2d could be found inthe future

TheANME-1 genome contains fewerMHCgene domainsas compared to ANME-2a and ANME-2d and some otherarchaea such as somemethylotrophicmethanogens (Table 2)and some members of the Archaeoglobales [115] The MHCsof ANME-1 also have a smaller heme count as compared toother ANME and some other archaea with the largest beingan octaheme cytochrome [107] Each hemewithin aMHChasits own redox potential and therefore structurally differentMHCs represent a large range of redox potentials that canbe used for bioenergetic electron transfer (reviewed in [147])For instance metal oxide reduction in Shewanella oneidensisMR-1 is catalyzed by a chain of a tetraheme (CymA) twodecaheme (MtrA and MtrB) and eventually extracellulardecaheme cytochromes OmcAMtrC that reduce the ironminerals [121 148 149] In Geobacter sulfurreducens ironmineral reduction seems to be catalyzed by the tetrahemecytochrome OmcE and hexaheme cytochrome OmcS trans-ferring electrons from the outer membrane to type IV pilithat transmit the electrons to iron minerals [121 150 151]Since ANME-1 lack MHCs of the correct size and lack genedomains for pili production [116] they seem unable to reduceminerals via both mechanisms present in Shewanella andGeobacter It can therefore be speculated that ANME-1 areless versatile in electron acceptor use and are not able toreduce solid metal oxides However DIET mechanisms arestill not well understood and the true differences betweenMHCs of different ANME types need to be investigated usingbiochemical methods This would allow uncovering the truecapabilities concerning DIET

34 Menaquinones and Methanophenazines ANME-2a en-coded a protein with a domain specific for PhzF which is anenzyme involved in phenazine biosynthesis in Pseudomonasfluorescens [152 153] The respective gene is not present in allmethanophenazine containing methanogens (in our genomecomparison only inM acetivorans andM formicica Table 2)so it is unclear whether this enzyme is really involved inmethanophenazine biosynthesis It is however likely thatANME-2a use methanophenazines in their respiratory chainsince gene domains for menaquinone biosynthesis wereabsent (Table 2) ldquoCa M nitroreducensrdquo probably uses

menaquinones as membrane-integral electron carrier sinceenvironmental genomes [28 43] encoded the futalosine(mqn) biosynthesis pathway as reported for Archaeoglobusfulgidus [154] (Table 2) Moreover ldquoCa M nitroreducensrdquoenrichment cultures showed absence of methanophenazines[43] ANME-1 also contained gene domains formenaquinonebiosynthesis via the futalosine (mqn) biosynthesis pathway(Table 2) Indications for a quinone biosynthesis pathwayin ANME-1 were previously found to be weak since onlysome of the Ubi homologues of the oxic ubiquinone biosyn-thesis pathway were detected [41] but the futalosine (mqn)biosynthesis pathway was overlooked in that particular anal-ysis Additionally ANME-1 have Fqo homologues similarto Archaeoglobus fulgidus [44] and expressed the catalyticsubunit FqoF [41] However since the phenazine biosynthesisdomain PhzF was also present in the ANME-1 genomes(Table 2) and Fpo and Fqo are homologues we cannotconclude on genomic information alone which redox shuttleis used by ANME-1 during AOM If ANME-1 would usemenaquinones this would have implications for subsequentelectron transfer to MHCs since methanophenazine (1198640 =minus165mV) [155] and menaquinone (1198640 = minus80mV) [156] havedifferent redox potentials

35 Cell Adhesion Some gene domains involved in cel-lular adhesion were more abundant in ANME than inmethanogens (Table 2) especially in ANME-2a and ANME-1that are known to form syntrophic interactions for electrontransfer during respiration These domains include HYR(IPR003410) and CARDB domains (IPR011635) that bothhave a direct role in cellular adhesion [157] (Table 2) Interest-ingly also domains related to the cellulosome of Clostridiumspecies termed dockerin and cohesin were highly abundantin both ANME-1 and ANME-2a as compared to ANME-2dand methanogens together with many carbohydrate bindingdomains (Table 2) In Clostridium species dockerin andcohesin form an anchor to the bacterial cell wall that containsa scaffold with cellulose-degrading enzymes and a carbohy-drate bindingmodule that binds cellulose altogether formingthe cellulosome [158] These domains have been found in alldomains of life irrespective of cellulose utilization but thefunction of such proteins outside of the cellulosome is notknown [159]Therefore dockerin cohesin and carbohydratebinding domains in ANME could hypothetically form aconstruct that binds to carbohydrates and could possibly havea function in cell-to-cell contact or MHC adhesion but thisneeds further investigation

4 Future Challenges

Advances in (meta)genomics transcriptomics and pro-teomics have produced the valuable metabolic blueprints ofdifferent ANMEwith hypotheses on how centralmetabolismelectron transport and energy conservation may functionFuture experiments are needed to biochemically demonstratethat these hypotheses are correct

The bottleneck for biochemical studies of ANME isthe lack of pure cultures due to the slow and syntrophic

Archaea 17

growth However the recent milestone discovery of directelectron transfer provides opportunities to grow ANMEas stated previously on electron accepting electrodes (ieanodes) [160] In this way pure or highly enriched culturesof different ANME without their respective syntrophic part-ner could be obtained and MHCs responsible for electricconduction could be biochemically characterized It seemsthat ANME-1 are limited by the size and abundance ofMHCs which could relate to differences in behavior onan anode The partner bacteria of ANME-1 and ANME-2could be investigated on an electron donating electrode (iecathode) with specific focus on the ability to produce pili (ienanowires) Also worth investigating is if besides ANME-2d ANME-2ab could also use insoluble electron acceptorsand if ANME-2d could donate electrons to a bacterialpartner

Another future challenge is to isolate and characterizeMcr from different ANME clades It needs to be investi-gated if Mcr abundance in ANME cells compensates forthe slow reverse activity or if modifications in the Mcrof ANME-1 also contribute to a better reverse activity ofMcr Moreover the effect of methane partial pressure onreaction rates and enzyme kinetics needs to be determined insitu

ANME-1 are potentially able to perform hydrogeno-trophic methanogenesis due to the presence of a hydrogenasein the genome Genetic indications of menaquinones aselectron carrier in ANME-1 and the various cellulosome andcell adhesion related gene domains in all ANME are alsotopics that could be explored further Methanogenic archaeaare likely not able to perform AOM but additional studieson TMO and more genetic modifications to stimulate AOMin methanogens could help in understanding the param-eters needed for AOM to occur Ultimately physiologicalunderstanding of ANME will help to explain the observedecological niche separation of different ANME clades and theoccurrence of ANMEwithout a bacterial partnerThis wouldgreatly enhance our knowledge of themethane cycle in anoxicenvironments

Competing Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors thank Stefanie Berger (RU Nijmegen) for criticalreading of the manuscript This research is supported bythe Soehngen Institute of Anaerobic Microbiology (SIAM)Gravitation grant (024002002) of the Netherlands Ministryof Education Culture and Science and the NetherlandsOrganisation for Scientific Research (NWO) Mike S MJetten was further supported by ERC AG 339880 Eco-MoMand Alfons J M Stams was supported by ERC AG 323009Novel Anaerobes

References

[1] A Boetius K Ravenschlag C J Schubert et al ldquoA marinemicrobial consortium apparently mediating anaerobic oxida-tion of methanerdquo Nature vol 407 no 6804 pp 623ndash626 2000

[2] K-U Hinrichs J M Hayes S P Sylva P G Brewert andE F DeLong ldquoMethane-consuming archaebacteria in marinesedimentsrdquo Nature vol 398 no 6730 pp 802ndash805 1999

[3] V J Orphan C H House K-U Hinrichs K D McKeeganand E F DeLong ldquoMethane-consuming archaea revealed bydirectly coupled isotopic and phylogenetic analysisrdquo Sciencevol 293 no 5529 pp 484ndash487 2001

[4] K-U Hinrichs and A Boetius ldquoThe anaerobic oxidation ofmethane new insights in microbial ecology and biogeochem-istryrdquo inOceanMargin Systems GWefer D Billett D HebbelnB B Joslashrgensen M Schluter and T VanWeering Eds pp 457ndash477 Springer Berlin Germany 2002

[5] K Knittel T Losekann A Boetius R Kort and R AmannldquoDiversity and distribution of methanotrophic archaea at coldseepsrdquo Applied and Environmental Microbiology vol 71 no 1pp 467ndash479 2005

[6] K Knittel and A Boetius ldquoAnaerobic oxidation of methaneprogress with an unknown processrdquo Annual Review of Micro-biology vol 63 pp 311ndash334 2009

[7] V J Orphan K-U Hinrichs W Ussler III et al ldquoComparativeanalysis of methane-oxidizing archaea and sulfate-reducingbacteria in anoxic marine sedimentsrdquoApplied and Environmen-tal Microbiology vol 67 no 4 pp 1922ndash1934 2001

[8] T Losekann K Knittel T Nadalig et al ldquoDiversity andabundance of aerobic and anaerobic methane oxidizers atthe Haakon Mosby Mud Volcano Barents Seardquo Applied andEnvironmentalMicrobiology vol 73 no 10 pp 3348ndash3362 2007

[9] H Niemann T Losekann D De Beer et al ldquoNovel microbialcommunities of the Haakon Mosby mud volcano and their roleas amethane sinkrdquoNature vol 443 no 7113 pp 854ndash858 2006

[10] TNunouraHOida T Toki J Ashi K Takai andKHorikoshildquoQuantification of mcrA by quantitative fluorescent PCR insediments from methane seep of the Nankai Troughrdquo FEMSMicrobiology Ecology vol 57 no 1 pp 149ndash157 2006

[11] B Orcutt A Boetius M Elvert V Samarkin and S B JoyeldquoMolecular biogeochemistry of sulfate reduction methanogen-esis and the anaerobic oxidation of methane at Gulf of Mexicocold seepsrdquoGeochimica et Cosmochimica Acta vol 69 no 17 pp4267ndash4281 2005

[12] V J Orphan W Ussler III T H Naehr C H House K-U Hinrichs and C K Paull ldquoGeological geochemical andmicrobiological heterogeneity of the seafloor around methanevents in the Eel River Basin offshore Californiardquo ChemicalGeology vol 205 no 3-4 pp 265ndash289 2004

[13] M G Pachiadaki A Kallionaki A Dahlmann G J De Langeand K A Kormas ldquoDiversity and spatial distribution ofprokaryotic communities along a sediment vertical profile ofa deep-sea mud volcanordquo Microbial Ecology vol 62 no 3 pp655ndash668 2011

[14] I Roalkvam H Dahle Y Chen S L Joslashrgensen H Haflidasonand I H Steen ldquoFine-scale community structure analysis ofANME in Nyegga sediments with high and low methane fluxrdquoFrontiers in Microbiology vol 3 p 216 2012

[15] K Yanagawa M Sunamura M A Lever et al ldquoNiche separa-tion of methanotrophic archaea (ANME-1 and -2) in methane-seep sediments of the Eastern Japan Sea offshore JoetsurdquoGeomicrobiology Journal vol 28 no 2 pp 118ndash129 2011

18 Archaea

[16] A Pernthaler A E Dekas C T Brown S K Goffredi TEmbaye and V J Orphan ldquoDiverse syntrophic partnershipsfromdeep-seamethane vents revealed by direct cell capture andmetagenomicsrdquo Proceedings of the National Academy of Sciencesof the United States of America vol 105 no 19 pp 7052ndash70572008

[17] R Hatzenpichler S A Connon D Goudeau R R Malm-strom T Woyke and V J Orphan ldquoVisualizing in situtranslational activity for identifying and sorting slow-growingarchaealminusbacterial consortiardquo Proceedings of the NationalAcademy of Sciences vol 113 no 28 pp E4069ndashE4078 2016

[18] L Maignien R J Parkes B Cragg et al ldquoAnaerobic oxidationof methane in hypersaline cold seep sedimentsrdquo FEMS Micro-biology Ecology vol 83 no 1 pp 214ndash231 2013

[19] V J Orphan C H House K-U Hinrichs K D McKeeganand E F DeLong ldquoMultiple archaeal groups mediate methaneoxidation in anoxic cold seep sedimentsrdquo Proceedings of theNational Academy of Sciences of the United States of Americavol 99 no 11 pp 7663ndash7668 2002

[20] T TreudeM Kruger A Boetius and B B Joslashrgensen ldquoEnviron-mental control on anaerobic oxidation of methane in the gassysediments of Eckernforde Bay (German Baltic)rdquo Limnology andOceanography vol 50 no 6 pp 1771ndash1786 2005

[21] G C Jagersma R J W Meulepas I Heikamp-De Jong etal ldquoMicrobial diversity and community structure of a highlyactive anaerobic methane-oxidizing sulfate-reducing enrich-mentrdquo Environmental Microbiology vol 11 no 12 pp 3223ndash3232 2009

[22] M Blumenberg R Seifert J Reitner T Pape andWMichaelisldquoMembrane lipid patterns typify distinct anaerobic methan-otrophic consortiardquo Proceedings of the National Academy ofSciences of the United States of America vol 101 no 30 pp 11111ndash11116 2004

[23] S Bertram M Blumenberg W Michaelis M Siegert MKruger and R Seifert ldquoMethanogenic capabilities of ANME-archaea deduced from 13C-labelling approachesrdquo Environmen-tal Microbiology vol 15 no 8 pp 2384ndash2393 2013

[24] K G Lloyd M J Alperin and A Teske ldquoEnvironmental evi-dence for net methane production and oxidation in putativeANaerobic MEthanotrophic (ANME) archaeardquo EnvironmentalMicrobiology vol 13 no 9 pp 2548ndash2564 2011

[25] M Takeuchi H Yoshioka Y Seo et al ldquoA distinct freshwater-adapted subgroup of ANME-1 dominates active archaeal com-munities in terrestrial subsurfaces in Japanrdquo EnvironmentalMicrobiology vol 13 no 12 pp 3206ndash3218 2011

[26] R T Amos B A Bekins I M Cozzarelli et al ldquoEvidence foriron-mediated anaerobic methane oxidation in a crude oil-contaminated aquiferrdquo Geobiology vol 10 no 6 pp 506ndash5172012

[27] P H Timmers D A Suarez-Zuluaga M van Rossem MDiender A J Stams and C M Plugge ldquoAnaerobic oxidationof methane associated with sulfate reduction in a naturalfreshwater gas sourcerdquo ISME Journal vol 10 pp 1400ndash14122015

[28] M F Haroon S Hu Y Shi et al ldquoAnaerobic oxidation ofmethane coupled to nitrate reduction in a novel archaeallineagerdquo Nature vol 500 no 7468 pp 567ndash570 2013

[29] H J Mills C Hodges K Wilson I R MacDonald and PA Sobecky ldquoMicrobial diversity in sediments associated withsurface-breaching gas hydrate mounds in the Gulf of MexicordquoFEMS Microbiology Ecology vol 46 no 1 pp 39ndash52 2003

[30] K G Lloyd L Lapham and A Teske ldquoAn anaerobic methane-oxidizing community of ANME-1b archaea in hypersaline gulfofMexico sedimentsrdquoApplied and EnvironmentalMicrobiologyvol 72 no 11 pp 7218ndash7230 2006

[31] A A Raghoebarsing A Pol K T Van De Pas-Schoonen et alldquoA microbial consortium couples anaerobic methane oxidationto denitrificationrdquoNature vol 440 no 7086 pp 918ndash921 2006

[32] S Hu R J Zeng L C Burow P Lant J Keller and Z YuanldquoEnrichment of denitrifying anaerobic methane oxidizingmicroorganismsrdquo Environmental Microbiology Reports vol 1no 5 pp 377ndash384 2009

[33] Z-W Ding J Ding L Fu F Zhang and R J Zeng ldquoSimultane-ous enrichment of denitrifying methanotrophs and anammoxbacteriardquo Applied Microbiology and Biotechnology vol 98 no24 pp 10211ndash10221 2014

[34] R Seifert K Nauhaus M Blumenberg M Kruger and WMichaelis ldquoMethane dynamics in a microbial community ofthe Black Sea traced by stable carbon isotopes in vitrordquoOrganicGeochemistry vol 37 no 10 pp 1411ndash1419 2006

[35] J Ding Z-W Ding L Fu Y-Z Lu S H Cheng and R JZeng ldquoNew primers for detecting and quantifying denitrifyinganaerobic methane oxidation archaea in different ecologicalnichesrdquo Applied Microbiology and Biotechnology vol 99 no 22pp 9805ndash9812 2015

[36] A Vaksmaa C Luke T van Alen et al ldquoDistribution and activ-ity of the anaerobic methanotrophic community in a nitrogen-fertilized Italian paddy soilrdquo FEMS Microbiology Ecology vol92 no 12 2016

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[40] R Stokke I Roalkvam A Lanzen H Haflidason and I HSteen ldquoIntegrated metagenomic and metaproteomic analysesof an ANME-1-dominated community in marine cold seepsedimentsrdquo Environmental Microbiology vol 14 no 5 pp 1333ndash1346 2012

[41] A Meyerdierks M Kube I Kostadinov et al ldquoMetagenomeand mRNA expression analyses of anaerobic methanotrophicarchaea of the ANME-1 grouprdquo Environmental Microbiologyvol 12 no 2 pp 422ndash439 2010

[42] F-P Wang Y Zhang Y Chen et al ldquoMethanotrophicarchaea possessing diverging methane-oxidizing and electron-transporting pathwaysrdquo ISME Journal vol 8 no 5 pp 1069ndash1078 2014

[43] A Arshad D R Speth R M de Graaf H J Op den Camp MS Jetten and C U Welte ldquoA metagenomics-based metabolicmodel of nitrate-dependent anaerobic oxidation of methane byMethanoperedens-like archaeardquo Frontiers inMicrobiology vol 6article1423 2015

[44] S J Hallam N Putnam CM Preston et al ldquoReversemethano-genesis testing the hypothesis with environmental genomicsrdquoScience vol 305 no 5689 pp 1457ndash1462 2004

Archaea 19

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energy conservation in methanogenic archaeardquo Archives ofMicrobiology vol 165 no 3 pp 149ndash163 1996

[47] A-K Kaster J Moll K Parey and R K Thauer ldquoCoupling offerredoxin and heterodisulfide reduction via electron bifurca-tion in hydrogenotrophic methanogenic archaeardquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 108 no 7 pp 2981ndash2986 2011

[48] R K Thauer A-K Kaster H Seedorf W Buckel and RHedderich ldquoMethanogenic archaea ecologically relevant dif-ferences in energy conservationrdquo Nature Reviews Microbiologyvol 6 no 8 pp 579ndash591 2008

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[52] P V Welander and W W Metcalf ldquoLoss of the mtr operon inMethanosarcina blocks growth on methanol but not methano-genesis and reveals an unknown methanogenic pathwayrdquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 102 no 30 pp 10664ndash10669 2005

[53] P V Welander and W W Metcalf ldquoMutagenesis of the C1oxidation pathway inmethanosarcina barkeri new insights intothe MtrMer bypass pathwayrdquo Journal of Bacteriology vol 190no 6 pp 1928ndash1936 2008

[54] M Goenrich R K Thauer H Yurimoto and N KatoldquoFormaldehyde activating enzyme (Fae) and hexulose-6-phosphate synthase (Hps) inMethanosarcina barkeri a possiblefunction in ribose-5-phosphate biosynthesisrdquoArchives ofMicro-biology vol 184 no 1 pp 41ndash48 2005

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[57] K Nauhaus A Boetius M Kruger and F Widdel ldquoIn vitrodemonstration of anaerobic oxidation of methane coupled tosulphate reduction in sediment from amarine gas hydrate areardquoEnvironmental Microbiology vol 4 no 5 pp 296ndash305 2002

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[59] M Kruger T Treude H Wolters K Nauhaus and A BoetiusldquoMicrobial methane turnover in different marine habitatsrdquoPalaeogeography Palaeoclimatology Palaeoecology vol 227 no1ndash3 pp 6ndash17 2005

[60] C Deusner V Meyer and T G Ferdelman ldquoHigh-pressuresystems for gas-phase free continuous incubation of enrichedmarinemicrobial communities performing anaerobic oxidationof methanerdquo Biotechnology and Bioengineering vol 105 no 3pp 524ndash533 2010

[61] K Nauhaus T Treude A Boetius and M Kruger ldquoEnviron-mental regulation of the anaerobic oxidation of methane acomparison of ANME-I and ANME-II communitiesrdquo Environ-mental Microbiology vol 7 no 1 pp 98ndash106 2005

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2by methan-

otrophicmicrobial mats from gas seeps of the anoxic Black SeardquoApplied and EnvironmentalMicrobiology vol 73 no 7 pp 2271ndash2283 2007

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[65] R J WMeulepas C G Jagersma J Gieteling C J N BuismanA J M Stams and P N L Lens ldquoEnrichment of anaerobicmethanotrophs in sulfate-reducing membrane bioreactorsrdquoBiotechnology and Bioengineering vol 104 no 3 pp 458ndash4702009

[66] T Holler G Wegener H Niemann et al ldquoCarbon and sulfurback flux during anaerobic microbial oxidation of methane andcoupled sulfate reductionrdquo Proceedings of the National Academyof Sciences of the United States of America vol 108 no 52 ppE1484ndashE1490 2011

[67] M Kruger AMeyerdierks F O Glockner et al ldquoA conspicuousnickel protein in microbial mats that oxidize methane anaero-bicallyrdquo Nature vol 426 no 6968 pp 878ndash881 2003

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variant from archaea associated with anaerobic oxidation ofmethanerdquo Journal of the American Chemical Society vol 130 no32 pp 10758ndash10767 2008

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[70] R K Thauer and S Shima ldquoMethane as fuel for anaerobicmicroorganismsrdquo Annals of the New York Academy of Sciencesvol 1125 pp 158ndash170 2008

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[72] P H A Timmers J Gieteling H C A Widjaja-Greefkeset al ldquoGrowth of anaerobic methane-oxidizing archaea andsulfate-reducing bacteria in a high-pressure membrane capsulebioreactorrdquoApplied and EnvironmentalMicrobiology vol 81 no4 pp 1286ndash1296 2015

[73] MKruger HWoltersMGehre S B Joye andH-H RichnowldquoTracing the slow growth of anaerobic methane-oxidizingcommunities by 15N-labelling techniquesrdquo FEMS MicrobiologyEcology vol 63 no 3 pp 401ndash411 2008

[74] R J W Meulepas C G Jagersma A F Khadem C J N Buis-man A J M Stams and P N L Lens ldquoEffect of environmentalconditions on sulfate reduction withmethane as electron donorby an Eckernforde Bay enrichmentrdquo Environmental Science andTechnology vol 43 no 17 pp 6553ndash6559 2009

20 Archaea

[75] M W Bowles V A Samarkin and S B Joye ldquoImprovedmeasurement of microbial activity in deep-sea sediments atin situ pressure and methane concentrationrdquo Limnology andOceanography Methods vol 9 pp 499ndash506 2011

[76] S Shima M Krueger T Weinert et al ldquoStructure of a methyl-coenzyme M reductase from Black Sea mats that oxidizemethane anaerobicallyrdquo Nature vol 481 no 7379 pp 98ndash1012012

[77] K D Allen G Wegener and R H White ldquoDiscovery of multi-ple modified F-430 coenzymes in methanogens and anaerobicmethanotrophic archaea suggests possible new roles for F-430in naturerdquoApplied and Environmental Microbiology vol 80 no20 pp 6403ndash6412 2014

[78] V W Soo M J McAnulty A Tripathi et al ldquoReversingmethanogenesis to capture methane for liquid biofuel precur-sorsrdquoMicrobial Cell Factories vol 15 article 11 2016

[79] D L Valentine and W S Reeburgh ldquoNew perspectives onanaerobicmethane oxidationrdquoEnvironmentalMicrobiology vol2 no 5 pp 477ndash484 2000

[80] D L Valentine ldquoBiogeochemistry and microbial ecology ofmethane oxidation in anoxic environments a reviewrdquo Antonievan Leeuwenhoek International Journal of General and Molecu-lar Microbiology vol 81 no 1-4 pp 271ndash282 2002

[81] A J B Zehnder and T D Brock ldquoMethane formation andmethane oxidation by methanogenic bacteriardquo Journal of Bac-teriology vol 137 no 1 pp 420ndash432 1979

[82] J Harder ldquoAnaerobic methane oxidation by bacteria employ-ing 14C-methane uncontaminated with 14C-carbon monoxiderdquoMarine Geology vol 137 no 1-2 pp 13ndash23 1997

[83] J J Moran C H House K H Freeman and J G FerryldquoTrace methane oxidation studied in several Euryarchaeotaunder diverse conditionsrdquo Archaea vol 1 no 5 pp 303ndash3092005

[84] J J Moran C H House B Thomas and K H FreemanldquoProducts of tracemethane oxidation during nonmethyltrophicgrowth by Methanosarcinardquo Journal of Geophysical ResearchBiogeosciences vol 112 no 2 2007

[85] R J W Meulepas C G Jagersma Y Zhang et al ldquoTracemethane oxidation and the methane dependency of sulfatereduction in anaerobic granular sludgerdquo FEMS MicrobiologyEcology vol 72 no 2 pp 261ndash271 2010

[86] A J B Zehnder andTD Brock ldquoAnaerobicmethane oxidationoccurrence and ecologyrdquoApplied and Environmental Microbiol-ogy vol 39 no 1 pp 194ndash204 1980

[87] S J Blazewicz D G Petersen M P Waldrop and M K Fire-stone ldquoAnaerobic oxidation of methane in tropical and borealsoils ecological significance in terrestrial methane cyclingrdquoJournal of Geophysical Research Biogeosciences vol 117 no 2Article ID G02033 2012

[88] K A Smemo and J B Yavitt ldquoEvidence for anaerobic CH4

oxidation in freshwater peatlandsrdquo Geomicrobiology Journalvol 24 no 7-8 pp 583ndash597 2007

[89] M J Alperin and T M Hoehler ldquoAnaerobic methane oxidationby archaeasulfate-reducing bacteria aggregates 1 Thermody-namic and physical constraintsrdquo American Journal of Sciencevol 309 no 10 pp 869ndash957 2009

[90] S L Caldwell J R Laidler E A Brewer J O Eberly S CSandborgh and F S Colwell ldquoAnaerobic oxidation of methanemechanisms bioenergetics and the ecology of associatedmicroorganismsrdquo Environmental Science and Technology vol42 no 18 pp 6791ndash6799 2008

[91] GWang A J Spivack and S DrsquoHondt ldquoGibbs energies of reac-tion and microbial mutualism in anaerobic deep subseafloorsediments of ODP Site 1226rdquoGeochimica et Cosmochimica Actavol 74 no 14 pp 3938ndash3947 2010

[92] P R Girguis A E Cozen and E F DeLong ldquoGrowth andpopulation dynamics of anaerobic methane-oxidizing archaeaand sulfate-reducing bacteria in a continuous-flow bioreactorrdquoApplied and EnvironmentalMicrobiology vol 71 no 7 pp 3725ndash3733 2005

[93] K Nauhaus M Albrecht M Elvert A Boetius and F WiddelldquoIn vitro cell growth ofmarine archaeal-bacterial consortia dur-ing anaerobic oxidation ofmethanewith sulfaterdquoEnvironmentalMicrobiology vol 9 no 1 pp 187ndash196 2007

[94] B Orcutt V Samarkin A Boetius and S Joye ldquoOn the relation-ship between methane production and oxidation by anaerobicmethanotrophic communities from cold seeps of the Gulf ofMexicordquo Environmental Microbiology vol 10 no 5 pp 1108ndash1117 2008

[95] M Y Yoshinaga T Holler T Goldhammer et al ldquoCarbon iso-tope equilibration during sulphate-limited anaerobic oxidationof methanerdquo Nature Geoscience vol 7 no 3 pp 190ndash194 2014

[96] T Treude J Niggemann J Kallmeyer et al ldquoAnaerobic oxi-dation of methane and sulfate reduction along the Chileancontinental marginrdquo Geochimica et Cosmochimica Acta vol 69no 11 pp 2767ndash2779 2005

[97] R J Parkes B A Cragg N Banning et al ldquoBiogeochemistryand biodiversity of methane cycling in subsurface marinesediments (SkagerrakDenmark)rdquoEnvironmentalMicrobiologyvol 9 no 5 pp 1146ndash1161 2007

[98] N J Knab B A Cragg E R C Hornibrook et al ldquoRegulationof anaerobic methane oxidation in sediments of the Black SeardquoBiogeosciences vol 6 no 8 pp 1505ndash1518 2009

[99] H Yoshioka A Maruyama T Nakamura et al ldquoActivities anddistribution of methanogenic and methane-oxidizing microbesin marine sediments from the Cascadia Marginrdquo Geobiologyvol 8 no 3 pp 223ndash233 2010

[100] G Wegener V Krukenberg S E Ruff M Y Kellermann andK Knittel ldquoMetabolic capabilities of microorganisms involvedin and associated with the anaerobic oxidation of methanerdquoFrontiers in Microbiology vol 7 article 46 2016

[101] R J W Meulepas C G Jagersma A F Khadem A J MStams and P N L Lens ldquoEffect of methanogenic substrateson anaerobic oxidation of methane and sulfate reduction by ananaerobic methanotrophic enrichmentrdquo Applied Microbiologyand Biotechnology vol 87 no 4 pp 1499ndash1506 2010

[102] J Milucka T G Ferdelman L Polerecky et al ldquoZero-valentsulphur is a key intermediate in marine methane oxidationrdquoNature vol 491 no 7425 pp 541ndash546 2012

[103] W Michaelis R Seifert K Nauhaus et al ldquoMicrobial reefs inthe black sea fueled by anaerobic oxidation ofmethanerdquo Sciencevol 297 no 5583 pp 1013ndash1015 2002

[104] A Vigneron P Cruaud P Pignet et al ldquoArchaeal and anaerobicmethane oxidizer communities in the Sonora Margin coldseeps Guaymas Basin (Gulf of California)rdquo ISME Journal vol7 no 8 pp 1595ndash1608 2013

[105] M Alperin and T Hoehler ldquoThe ongoing mystery of sea-floormethanerdquo Science vol 329 no 5989 pp 288ndash289 2010

[106] B Orcutt and C Meile ldquoConstraints on mechanisms and ratesof anaerobic oxidation of methane by microbial consortiaprocess-basedmodeling of ANME-2 archaea and sulfate reduc-ing bacteria interactionsrdquo Biogeosciences vol 5 no 6 pp 1587ndash1599 2008

Archaea 21

[107] S E McGlynn G L Chadwick C P Kempes and V J OrphanldquoSingle cell activity reveals direct electron transfer in methan-otrophic consortiardquoNature vol 526 no 7574 pp 531ndash535 2015

[108] D R Lovley ldquoElectromicrobiologyrdquo Annual Review of Microbi-ology vol 66 pp 391ndash409 2012

[109] S M Strycharz-Glaven R M Snider A Guiseppi-Elie andL M Tender ldquoOn the electrical conductivity of microbialnanowires and biofilmsrdquoEnergy and Environmental Science vol4 no 11 pp 4366ndash4379 2011

[110] D J Richardson J N Butt J K Fredrickson et al ldquoThe lsquoporinndashcytochromersquo model for microbe-to-mineral electron transferrdquoMolecular Microbiology vol 85 no 2 pp 201ndash212 2012

[111] A Okamoto K Hashimoto and R Nakamura ldquoLong-rangeelectron conduction of Shewanella biofilms mediated by outermembrane C-type cytochromesrdquo Bioelectrochemistry vol 85pp 61ndash65 2012

[112] M Y El-Naggar G Wanger K M Leung et al ldquoElectricaltransport along bacterial nanowires from Shewanella oneidensisMR-1rdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 107 no 42 pp 18127ndash18131 2010

[113] G Reguera K D McCarthy T Mehta J S Nicoll M TTuominen and D R Lovley ldquoExtracellular electron transfer viamicrobial nanowiresrdquo Nature vol 435 no 7045 pp 1098ndash11012005

[114] Z M Summers H E Fogarty C Leang A E Franks N SMalvankar and D R Lovley ldquoDirect exchange of electronswithin aggregates of an evolved syntrophic coculture of anaer-obic bacteriardquo Science vol 330 no 6009 pp 1413ndash1415 2010

[115] A Kletzin T Heimerl J Flechsler L V Niftrik R Rachel andA Klingl ldquoCytochromes c in archaea distribution maturationcell architecture and the special case of Ignicoccus hospitalisrdquoFrontiers in Microbiology vol 6 article 439 2015

[116] GWegener V Krukenberg D Riedel H E Tegetmeyer and ABoetius ldquoIntercellular wiring enables electron transfer betweenmethanotrophic archaea and bacteriardquo Nature vol 526 no7574 pp 587ndash590 2015

[117] D HHaft S H Payne and J D Selengut ldquoArchaeosortases andexosortases are widely distributed systems linking membranetransit with posttranslational modificationrdquo Journal of Bacteri-ology vol 194 no 1 pp 36ndash48 2012

[118] A Marchler-Bauer M K Derbyshire N R Gonzales et alldquoCDD NCBIrsquos conserved domain databaserdquo Nucleic AcidsResearch vol 43 no 1 pp D222ndashD226 2015

[119] A Mitchell H-Y Chang L Daugherty et al ldquoThe InterProprotein families database the classification resource after 15yearsrdquo Nucleic Acids Research vol 43 no 1 pp D213ndashD2212015

[120] V Krukenberg K Harding M Richter et al ldquoCandidatusdesulfofervidus auxilii a hydrogenotrophic sulfate-reducingbacterium involved in the thermophilic anaerobic oxidation ofmethanerdquo Environmental Microbiology vol 18 pp 3073ndash30912016

[121] L Shi T C Squier J M Zachara and J K Fredrickson ldquoRes-piration of metal (hydr)oxides by Shewanella and Geobactera key role for multihaem c-type cytochromesrdquo MolecularMicrobiology vol 65 no 1 pp 12ndash20 2007

[122] N S Malvankar and D R Lovley ldquoMicrobial nanowires forbioenergy applicationsrdquo Current Opinion in Biotechnology vol27 pp 88ndash95 2014

[123] A-E Rotaru T LWoodard K PNevin andDR Lovley ldquoLinkbetween capacity for current production and syntrophic growth

in Geobacter speciesrdquo Frontiers in Microbiology vol 6 article744 2015

[124] A-E Rotaru P M Shrestha F Liu et al ldquoDirect interspecieselectron transfer between Geobacter metallireducens andMethanosarcina barkerirdquo Applied and Environmental Microbi-ology vol 80 no 15 pp 4599ndash4605 2014

[125] S Scheller H Yu G L Chadwick S E McGlynn and VJ Orphan ldquoArtificial electron acceptors decouple archaealmethane oxidation from sulfate reductionrdquo Science vol 351 no6274 pp 703ndash707 2016

[126] J Milucka F Widdel and S Shima ldquoImmunological detec-tion of enzymes for sulfate reduction in anaerobic methane-oxidizing consortiardquo Environmental Microbiology vol 15 no 5pp 1561ndash1571 2013

[127] P Cabello M D Roldan and C Moreno-Vivian ldquoNitratereduction and the nitrogen cycle in archaeardquoMicrobiology vol150 no 11 pp 3527ndash3546 2004

[128] R MMartinez-Espinosa E J Dridge M J Bonete et al ldquoLookon the positive sideThe orientation identification and bioener-getics of lsquoArchaealrsquomembrane-boundnitrate reductasesrdquoFEMSMicrobiology Letters vol 276 no 2 pp 129ndash139 2007

[129] S de VriesMMomcilovicM J F Strampraad J PWhiteleggeA Baghai and I Schroder ldquoAdaptation to a high-tungsten envi-ronment pyrobaculum aerophilum contains an active tungstennitrate reductaserdquo Biochemistry vol 49 no 45 pp 9911ndash99212010

[130] M Egger O Rasigraf C J Sapart et al ldquoIron-mediated anaer-obic oxidation of methane in brackish coastal sedimentsrdquoEnvironmental Science and Technology vol 49 no 1 pp 277ndash283 2015

[131] T Treude S Krause J Maltby A W Dale R Coffin and LJ Hamdan ldquoSulfate reduction and methane oxidation activitybelow the sulfate-methane transition zone in Alaskan BeaufortSea continental margin sediments implications for deep sulfurcyclingrdquo Geochimica et Cosmochimica Acta vol 144 pp 217ndash237 2014

[132] N Riedinger M J Formolo T W Lyons S Henkel A Beckand S Kasten ldquoAn inorganic geochemical argument for coupledanaerobic oxidation of methane and iron reduction in marinesedimentsrdquo Geobiology vol 12 no 2 pp 172ndash181 2014

[133] Y-H Chang T-W Cheng W-J Lai et al ldquoMicrobial methanecycling in a terrestrialmud volcano in eastern Taiwanrdquo Environ-mental Microbiology vol 14 no 4 pp 895ndash908 2012

[134] S A Crowe S Katsev K Leslie et al ldquoThe methane cycle inferruginous Lake Matanordquo Geobiology vol 9 no 1 pp 61ndash782011

[135] O Sivan M Adler A Pearson et al ldquoGeochemical evidence foriron-mediated anaerobic oxidation of methanerdquo Limnology andOceanography vol 56 no 4 pp 1536ndash1544 2011

[136] K E A Segarra C Comerford J Slaughter and S B JoyeldquoImpact of electron acceptor availability on the anaerobic oxi-dation of methane in coastal freshwater and brackish wetlandsedimentsrdquo Geochimica et Cosmochimica Acta vol 115 pp 15ndash30 2013

[137] V Gupta K A Smemo J B Yavitt D Fowle B Branfireunand N Basiliko ldquoStable isotopes reveal widespread anaerobicmethane oxidation across latitude and peatland typerdquo Environ-mental Science and Technology vol 47 no 15 pp 8273ndash82792013

[138] O Oni T Miyatake S Kasten et al ldquoDistinct microbialpopulations are tightly linked to the profile of dissolved iron in

22 Archaea

the methanic sediments of the Helgolandmud area North SeardquoFrontiers in Microbiology vol 6 2015

[139] E J Beal C H House and V J Orphan ldquoManganese- andiron-dependent marine methane oxidationrdquo Science vol 325no 5937 pp 184ndash187 2009

[140] M W Bowles V A Samarkin K M Bowles and S B JoyeldquoWeak coupling between sulfate reduction and the anaerobicoxidation of methane in methane-rich seafloor sedimentsduring ex situ incubationrdquo Geochimica et Cosmochimica Actavol 75 no 2 pp 500ndash519 2011

[141] Y Z Lu L Fu J Ding Z Ding N Li and R J Zeng ldquoCr(VI)reduction coupled with anaerobic oxidation of methane in alaboratory reactorrdquoWater Research vol 102 pp 445ndash452 2016

[142] K F Ettwig B Zhu D Speth J T Keltjens M S Jetten and BKartal ldquoArchaea catalyze iron-dependent anaerobic oxidationof methanerdquo Proceedings of the National Academy of Sciences ofthe United States of America vol 113 no 45 pp 12792ndash127962016

[143] T M Flynn R A Sanford H Ryu et al ldquoFunctional microbialdiversity explains groundwater chemistry in a pristine aquiferrdquoBMCMicrobiology vol 13 no 1 article no 146 2013

[144] C J Schubert F Vazquez T Losekann-Behrens K KnittelM Tonolla and A Boetius ldquoEvidence for anaerobic oxidationof methane in sediments of a freshwater system (Lago diCadagno)rdquo FEMS Microbiology Ecology vol 76 no 1 pp 26ndash38 2011

[145] K E A Segarra F Schubotz V Samarkin M Y Yoshinaga K-U Hinrichs and S B Joye ldquoHigh rates of anaerobic methaneoxidation in freshwater wetlands reduce potential atmosphericmethane emissionsrdquo Nature Communications vol 6 article7477 2015

[146] E J Beal M W Claire and C H House ldquoHigh rates ofanaerobic methanotrophy at low sulfate concentrations withimplications for past and present methane levelsrdquo Geobiologyvol 9 no 2 pp 131ndash139 2011

[147] F Kracke I Vassilev and J O Kromer ldquoMicrobial electrontransport and energy conservationmdashthe foundation for opti-mizing bioelectrochemical systemsrdquo Frontiers in Microbiologyvol 6 article 575 2015

[148] C L Reardon A C Dohnalkova P Nachimuthu et al ldquoRoleof outer-membrane cytochromes MtrC and OmcA in thebiomineralization of ferrihydrite by Shewanella oneidensisMR-1rdquo Geobiology vol 8 no 1 pp 56ndash68 2010

[149] L Shi B Chen Z Wang et al ldquoIsolation of a high-affinityfunctional protein complex between OmcA and MtrC twoouter membrane decaheme c-type cytochromes of Shewanellaoneidensis MR-1rdquo Journal of Bacteriology vol 188 no 13 pp4705ndash4714 2006

[150] X Qian T Mester L Morgado et al ldquoBiochemical charac-terization of purified OmcS a c-type cytochrome requiredfor insoluble Fe(III) reduction in Geobacter sulfurreducensrdquoBiochimica et BiophysicaActamdashBioenergetics vol 1807 no 4 pp404ndash412 2011

[151] T Mehta M V Coppi S E Childers and D R Lovley ldquoOutermembrane c-type cytochromes required for Fe(III) andMn(IV)oxide reduction in Geobacter sulfurreducensrdquo Applied andEnvironmentalMicrobiology vol 71 no 12 pp 8634ndash8641 2005

[152] W Blankenfeldt A P Kuzin T Skarina et al ldquoStructure andfunction of the phenazine biosynthetic protein PhzF fromPseudomonas fluorescensrdquoProceedings of theNational Academyof Sciences of the United States of America vol 101 no 47 pp16431ndash16436 2004

[153] J F Parsons F Song L Parsons K Calabrese E Eisensteinand J E Ladner ldquoStructure and function of the phenazinebiosynthesis protein PhzF fromPseudomonas fluorescens 2-79rdquoBiochemistry vol 43 no 39 pp 12427ndash12435 2004

[154] T Hiratsuka K Furihata J Ishikawa et al ldquoAn alternativemenaquinone biosynthetic pathway operating in microorgan-ismsrdquo Science vol 321 no 5896 pp 1670ndash1673 2008

[155] M Tietze A Beuchle I Lamla et al ldquoRedox potentials ofmethanophenazine and CoB-S-S-CoM factors involved inelectron transport in methanogenic archaeardquo ChemBioChemvol 4 no 4 pp 333ndash335 2003

[156] Q H Tran and G Unden ldquoChanges in the proton potentialand the cellular energetics of Escherichia coli during growth byaerobic and anaerobic respiration or by fermentationrdquoEuropeanJournal of Biochemistry vol 251 no 1-2 pp 538ndash543 1998

[157] I Callebaut D Gilges I Vigon and J-P Mornon ldquoHYR anextracellular module involved in cellular adhesion and relatedto the immunoglobulin-like foldrdquo Protein Science vol 9 no 7pp 1382ndash1390 2000

[158] H J Gilbert ldquoCellulosomes microbial nanomachines that dis-play plasticity in quaternary structurerdquoMolecular Microbiologyvol 63 no 6 pp 1568ndash1576 2007

[159] A Peer S P Smith E A Bayer R Lamed and I BorovokldquoNoncellulosomal cohesin- and dockerin-like modules in thethree domains of liferdquo FEMS Microbiology Letters vol 291 no1 pp 1ndash16 2009

[160] M Wagner ldquoMicrobiology conductive consortiardquo Nature vol526 no 7574 pp 513ndash514 2015

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

8 Archaea

Frh

Mch

Mer

Mtd

Ftr

Fmd

Mcr

MPh

Vho

Ech

Mtr

CoM-SH

CoB-S-S-CoM

CoB-SHHdrDE2H+

H2

H2

H2

MPhH2

H+

CH4

CH3-CoM

CH3-H4MPTF420H2

F420

F420H2

F420

CH2=H4MPT

CHequivH4MPT

CHO-H4MPT

CHO-MFR

CO2

Fdred

Fdox

H2O

2Na+

H2

Figure 2 Hydrogenotrophic methanogenesis in cytochrome containing Methanosarcina barkeri Black lines represent presence ofconversions See Table 3 for nomenclature

reaction thermodynamically favourable (Table 1)The reversereaction of Mcr is therefore an essential step in AOM andis discussed in Section 22 The respiratory chain that isneeded for using different terminal electron acceptors will bediscussed in Section 3

Evidence that ANME use the reverse methanogenesispathway during AOM is derived from metagenomic andmetatranscriptomic analyses This showed that all genesfor the (reverse) methanogenic pathway were present andexpressed in ANME-2a [42] (Figure 4) and ANME-2d[28] (Figure 5) ANME-1 were consistently lacking thegene encoding N5N10-methylene- tetrahydromethanopterin(H4MPT) reductase (Mer) which is an enzyme needed to

oxidize methyl-H4MPT during methane oxidation [40 41

44 51] (Figure 6 Table 2) Possible explanations could be that(1) the mer gene is present but not yet detected (2) ANME-1 used a bypass of this step and (3) Mer was replaced bya structural analogue The first possibility is highly unlikelyAlthough no closed genome of ANME-1 is publicly availableto date all ANME-1 metagenomes consistently only lackMerand no other methanogenic genes The second possibilitywas proposed previously where ANME-1 uses a bypass of

Mer via the formation of methanol or methylamine [41] aswas detected in deletion mutants ofMethanosarcina [52 53]Here CH

3-CoM was presumably converted to methanol by

a methyltransferase and subsequently to formaldehyde by amethanol dehydrogenase (Mdh) Then formaldehyde wouldbe converted to N5N10 methylene-H

4MPT using a fusion

protein of the formaldehyde-activating enzyme (Fae) and ahexulose-6-phosphate synthase (Hps) [53] (Figure 6) BothFae and Hps were found in the ANME-1 metagenome [41]and metaproteome [40 51] However no genes coding forenzymes involved in methanol metabolism were detectedin these ANME-1 datasets [40 41 51] (Table 2) indicatingthat this alternative pathway probably does not occur Thepresence of the FaeHps fusion protein in ANME-1 duringAOM could also be explained by its involvement in ribosephosphate synthesis and not in AOM [54] Indeed the Faegene domains of ANME-1 were located in between ribulose-phosphate binding barrel and ribosomal protein S5 domains(Table S2) The third possibility of a structural analogue ismost likely since an analogue of N5N10-methylene tetrahy-drofolate (H

4HF) reductase (MetF) was expressed byANME-

1 during AOM which could replace Mer [40] (Figure 6)

Archaea 9

Table 3 Nomenclature

Central methanogenic pathwayFmd Formylmethanofuran (CHO-MFR) dehydrogenaseFtr Formylmethanofuran-tetrahydromethanopterin (H

4MPT) formyltransferase

Mch N5N10-methenyl-H4MPT cyclohydrolase

Mtd F420

H2-dependent methylene -H

4MPT dehydrogenase

Mer N5N10-methylene-H4MPT reductase

Mtr N5-methyl-H4MPTcoenzyme M (CoM) methyltransferase

Mcr Methyl coenzyme M (CH3-CoM) reductase

Mdh Methanol dehydrogenaseFaeHps Fusion protein of formaldehyde activating enzyme hexulose-6-phosphate synthaseMetF N5N10-methylene tetrahydrofolate (H

4HF) reductase analogue

Electron transportMvh F

420-nonreducing hydrogenase

Vho Methanophenazine-dependent hydrogenaseFpo F

420H2phenazine oxidoreductase

Fqo F420

H2quinone oxidoreductase

Hdr Coenzyme B-coenzyme M heterodisulfide (CoB-S-S-CoM) reductaseFrh F

420-dependent hydrogenase

Ech Ferredoxin-dependent hydrogenaseMePhMePhH

2Methanophenazine

MQMQH2

MenaquinoneCyt b Cytochrome bCyt c Cytochrome cMHC Multiheme c-type cytochromeRieske Rieske cytochrome b complexOrf7 Pseudoperiplasmic b-type cytochromeNar Nitrate reductaseNap Periplasmic nitrate reductaseNrf Nitrite reductase

22 Methyl Coenzyme M Reductase (Mcr) The enzymaticreaction of a purified Mcr from ANME has not been mea-sured to date The key question is whether a methanogenicMcr can explain the observed in situ AOM rates or if theMcr of ANME is structurally altered There are three mainfactors to be considered the kinetic limitations as definedby enzyme properties (ie half-maximal activity at a specific119870119872value) the thermodynamic constraints of the enzymatic

reaction and the maximal or ambient rate of the enzymaticreaction For the Mcr from Methanothermobacter marbur-gensis kinetic parameters have been determined to illustratethe reversibility of reaction (1) In themethanogenic reactionthe purified Mcr isoform I [55] catalyzes the production ofmethane with a 119881max of 30Umgminus1 and a 119870

119872of 5mM for

CH3-CoM The same (methanogenic) enzyme was able to

oxidize methane to CH3-CoM with a rate of 00114Umgminus1

and a 119870119872for methane of sim10 mM [56]

To answer if the observed AOM rates are in accordancewith the measured methane oxidation rate for the purifiedMcr enzyme from M marburgensis the Mcr activity duringAOM is needed Estimates for AOM rates in terms of activity(per cell dry mass) range between lt1 and 20mmol dayminus1 andg cell dry massminus1 [56ndash66] This equals an activity of 07 to

sim14 nmol min and mg cell dry massminus1 About half of the celldry mass is protein so the activity for the ANME archaeawould approximate 14 to 28 nmol min and mg proteinminus1 Toestimate the activity per mg of Mcr the proportion of Mcrto cellular protein is needed It was reported that 7 of theprotein of ANMEmicrobial mats from the Black Sea [67 68]and 104 of peptides fromHydrate Ridge mesocosms is Mcr[51] As these were no pure cultures the actual percentagesof Mcr in ANME cells may be higher Transcriptome data forANME-2d [43] showed that about 19 of the total transcriptswere derived from the mcr genes indicating (though notdemonstrating) a highMcr content in ANME-2d Estimatingthat 10 of the cellular protein would be Mcr the specificactivity of the enzymewould be between 14 and 280 nmolminand mg Mcr proteinminus1 which is up to 25 times higher thanthe measured reverse reaction rate of the M marburgensisenzyme (sim12 nmol min and mg Mcrminus1 [56]) However thereverse reaction rate of the M marburgensis Mcr was deter-mined under nonsaturating substrate conditions and wastherefore not possibly representing the true maximum rateNevertheless both reverse reaction rates are in the same orderof magnitude other than the forward reaction of 30000ndash100000 nmol min and mgMcrminus1 Thus it seems that the

10 Archaea

H2

CoM-SH

Mch

Mer

Mtd

Ftr

Fmd

Mcr

MPh

MPhH2

MPh

MPh

MPhH2

MtrVho

CoM-SH

CoB-S-S-CoM

CoB-SHHdrDE

Fpo

Fpo

Ech

CH3-CoM

2H+

H2

2H+

2H+

H+

MPhH2

CH4

CH3-H4MPTF420H2

F420

F420H2

F420

CH2=H4MPT

CHequivH4MPT

CHO-H4MPT

CHO-MFR

CO2

Fdred

Fdox

H2O

2Na+

CH3-OH

Figure 3 Methylotrophic methanogenesis in cytochrome containingMethanosarcina barkeri Black lines represent presence of conversionsand red lines indicate reversal of the hydrogenotrophic methanogenic pathway See Table 3 for nomenclature

Mcr in ANME may have similar catalytic properties as themethanogenic enzyme and that the high amount of Mcr permg total cell biomass in ANME may in part compensates forthe apparently relatively slow catalysis

Considering the thermodynamic constraints the Gibbsfree energy change of the Mcr forward reaction under stan-dard conditions is around minus30 kJmolminus1 [56] Therefore thereverse reaction is endergonic under standard conditions andwill not proceed However highmethane concentrations (105according to reaction (1) [69 70]) may lead to a favourablechange in the Gibbs free energy in the direction of AOMHigh methane partial pressure prevails at many habitatswhere AOM has been detected The solubility of methaneat atmospheric pressure is only 13mM [71] Consequentlyincreased AOM rates were reported upon pressurizing sam-ples of different geographical origin [59 60 72 73] The 119870

119872

of Mcr of M marburgensis for methane was determined ator above 10mM and reported 119870

119872values of S-AOM varied

from (at least) 11mM [74] a few mM [57] to even 37mM(equivalent to 3MPa CH

4) [58] Thus high pressure and

therefore high concentrations of methane in the natural habi-tat accelerate the oxidation rate of methane by Mcr Futureresearch to accurately determine119870

119872values and rates forMcr

at differentmethane partial pressures is however neededThismay seem difficult but microbial activity measurements at insitu methane partial pressure were shown to be successful inthe laboratory [75]

It was suggested that the Mcr reaction is the rate limitingstep in reverse methanogenesis [56] which is in line withthe above described challenges Supporting these findingsthere does not seem to be a major change in the aminoacid structure that determines whether the backwards or theforward reaction of Mcr is favoured Amino acid alignments[67] and the crystal structure of ANME-1 Mcr [76] indicatedhigh overall similarity of the methanogenic and methan-otrophic enzyme and unambiguously demonstrated that

Archaea 11

MHC

MHCS-layer

2H+

minuse

cyt b

Mch

Mer

Mtd

Ftr

Fmd

Mcr

MPh

HdrABC

MPh

MHC

MHC

MPh

CoB-S-S-CoM

CoB-SH

CoM-SH

HdrDE

Mtr

Fpo

Fpo

Rnf

MPhH2

MPhH2

MPhH2

MPhH2

CH4

CH3-CoM

CH3-H4MPT

F420H2

F420

F420H2

F420

CH2=H4MPT

CHequivH4MPT

CHO-H4MPT

CHO-MFR

CO2

Fdred

Fdox

H2O

2Na+

MPh

minuse

S-layer

MHC

SRB 2H+

2H+

2Na+

minuse

minuse

minuse

Figure 4 Methanotrophic pathway during S-AOM by ANME-2a [42] Red lines indicate reversal of the hydrogenotrophic methanogenicpathway See Table 3 for nomenclature

CoM-SH and CoB-SH are substrates of the methanotrophicenzyme However several posttranslational modifications ofamino acids were different betweenmethanogens andANMEarchaea and the cofactor F

430(the prosthetic group of Mcr)

is modified in ANME-1 but not in ANME-2 or ANME-3archaea [51 63 67 68 76 77] Furthermore ANME-1 seemsto lack the noncatalytic proteinDdomain of themcr gene thatis present in all other methanogens and methanotrophs butof which the function is unknown (IPR003901 Table 2) [51]A metabolically engineered Methanosarcina acetivorans wasable to convert methane and CO

2to acetate with a plasmid

containingMcr derived from ANME-1 [78] It is thus unclearif only thermodynamic constraints and the abundance ofMcrensureAOMactivity or if also specificmodifications canhavean effect on the reverse activity of Mcr

23 Methane Oxidation by Methanogens Pure cultures ofmethanogens were not able to oxidize methane under highmethane and low hydrogen concentrations (reviewed in[79 80]) Methanogens are only able to oxidize methaneduring net methane production [81] Labeled methane addi-tion (13C or 14C) to pure cultures of methanogens showedproduction of labeled CO

2during net methane production

This characteristic was confirmed with several pure culturesof methanogens [82ndash84] The process was called ldquotracemethane oxidationrdquo (TMO) since the CO

2was formed in

trace amounts relative to the methane produced [83] It isnot clear if TMO is due to the reported reversibility ofindividual enzymes [66] or if it is an active microbial processfrom which energy can be conserved TMO was speculatedto be an active metabolic process for three reasons (1)the amount of methane oxidized varied between differentspecies of methanogens grown on the same methanogenicsubstrate (2) the amount ofmethane oxidized varied betweendifferent methanogenic substrates and (3) TMO productsvaried between different methanogenic substrates [83 84]For instance when grown on acetate Methanosarcina ace-tivorans produced labeled acetate from labeled methaneWhen grown on carbon monoxide it produced both labeledacetate and methyl sulfides from labeled methane [84] Dur-ing hydrogenotrophic and methylotrophic methanogenesisTMO mainly produced CO

2from labeled methane [83]

However in contrast with AOM TMO rates never exceededmethanogenesis rates even during long-term incubationwith methane and sulfate [85] It seems that methanogensare not able to conserve energy from TMO even under

12 Archaea

Mch

Mer

Mtd

Ftr

Fmd

Mcr

MQ

MQ

EchHdrFrh

3MQ

HdrABC

MQ

cyt b Mtr

NrfH

cyt c

NrfA

CoB-S-S-CoM

CoB-SH

CoM-SH

HdrDE

HCOIIHCOIINapHOrf7

NarGH

S-layer

Fqo

Fqo

3H+

3H+

4H+

CH4

CH3-CoM

CH3-H4MPT

F420

F420H2

F420

F420H2

CH2=H4MPT

CHequivH4MPT

CHO-H4MPT

CHO-MFR

CO2

Fdred

Fdox

H2O

2Na+

NH4+

NO2minus

NO2minus

NO3minus

3MQH2

MQH2

MQH2

MQH2eminus

eminus

Rieske

Figure 5 Methanotrophic pathway during N-AOM by ldquoCaM nitroreducensrdquo MPEBLZ (ANME-2d) [43] Red lines indicate reversal of thehydrogenotrophic methanogenic pathway See Table 3 for nomenclature

thermodynamically favourable conditions TMOoccurs bothin absence and presence of an external electron acceptor andonly during net methanogenesis It is therefore most likelycaused by the reported back flux of individual enzymes of themethanogenic pathway [66]

TMO also occurred in granular sludge and in freshwaterand terrestrial samples These mixed communities showedhigher TMO rates than pure cultures reaching up to 90of the methane produced [27 85ndash87] TMO should thereforebe carefully considered in the experimental setup and inter-pretation of results when studying AOM in environmentalsamples especially since TMO rates were like AOM stim-ulated by a high methane partial pressure [72 86 88] Sulfatereduction was also stimulated by higher methane partialpressures [85]Thus a highmethane partial pressure can havea stimulating effect on methane oxidation (either throughAOM or TMO) and SR which could be unrelated to S-AOMMoreover addition of iron sulfate (FeSO

4) or manganese

oxide (MnO2) also increased TMO rates [86] Therefore

methane-dependent SR and sulfate- or metal-dependentmethane oxidation are not necessarily indications for AOMin mixed cultures In conclusion when studying complexldquoblack-boxrdquo communities only net methane oxidation isproof for AOM activity

24 Methane Production by ANME The process of S-AOMis at the energetic limit for sustaining life with estimates

of Gibbs free energy yields between minus18 and minus35 kJmolminus1[45 79 89ndash91] and doubling times between 11 and 75months [65 72 73 92 93] Since S-AOM operates close toits thermodynamic equilibrium the reversibility of individualenzymes leads to measurable back flux producing methane(3ndash7 of AOM) and sulfate (55ndash13 of SR) during S-AOM [66] This ldquotrace methane productionrdquo was observedin situ [11] and in sediment slurries with methanogenesisaround 10 [62 94] or even as high as 50 of AOM [34]When sulfate becomes depleted Gibbs free energy yieldsbecome even lower (less negative) and the enzymatic backflux becomes even more apparent up to 78 of net AOM[95] Previous measurements of 13C depletion below thesulfate-methane transition zone (SMTZ) ofmarine sedimentsthat were thought to be indicative for methanogenesis couldtherefore instead be attributed to the back flux of AOM [95]The occurrence of ANME-1 without a bacterial partner insediment layers where sulfate was depleted was previouslyinterpreted as evidence that ANME-1 perform methanogen-esis [24] but in light of the above it could also indicate AOMThere are indeed reports of AOM activity below the SMTZin the methanogenic zone [96ndash99] In contrast AOM withother electron acceptors than sulfate operates far from thethermodynamic equilibrium with Gibbs free energy changesbetween minus5172 and minus8414 kJmolmethaneminus1 (Table 1) Herethe reported anaerobic back flux [66] is expected to be lessapparent

Archaea 13

MetFMer

Mdh

FaeHps

SRB

MHC

Mch

Mtd

Ftr

Fmd

McrMQ

Hdr1

MQ

MHC

Hdr2

CoB-S-S-CoMCoB-SHCoM-SH

Mtr

Fqo

CH4

CH3-CoMCH3-OH

CH2O CH3-H4MPT

F420F420H2

CHO-H4MPT

CHO-MFR

CO2

FdredFdox

H2O

eminus

eminus

CHequivH4MPT

CH2=H4MPT

xH+

H2

MQH2

MQH2

+xNa

Figure 6 Methanotrophic pathway during S-AOM by ANME-1 [40 41] Red lines indicate reversal of the hydrogenotrophic methanogenicpathway grey lines represent absence of conversions and blue lines indicate a bypass of the hydrogenotrophic methanogenic pathway SeeTable 3 for nomenclature

In laboratory incubations researchers were not ableto stimulate net methanogenesis through addition ofmethanogenic substrates to AOM performing sediments[62 94] In two cases researchers were successful [23 100]In one of these cases sediment-free long-term AOM enrich-ments that were dominated by ANMESRB were incubatedwith methanogenic substrates The resulting methanogenicactivity most likely came from the enrichment of a minorpopulation of methanogens (up to 7permil of total archaealgene tag sequences) that was present in the inoculum[100] In the second study methanogenic substrates wereadded to ANME-1 and ANME-2 dominated microbialmat samples and methanogenesis also occurred [23]However no information was provided for the total archaealcommunity composition which makes it impossible toexclude methanogens as the responsible organisms

Genomic information of ANME also gives indication onpotential methanogenic routes Considering methylotrophicmethanogenesis no gene homologues catalyzing methyltransfer from methylated substrates to coenzyme M weredetected in ANME (Table 2) [40ndash43] Acetoclastic methano-genesis needs either the AMP- and ADP-forming acetyl-coenzyme A synthetase (Acs and Acd resp) or proceedsvia acetate kinase and phosphotransacetylase In ANME-1only the alpha subunit of a homologue of Acd was expressed

during AOM [41] but in an ANME-1 proteome of activeAOM biomass no Acd was detected [40] The Acd gene wasdetected in the single-aggregate genome and transcriptomeof ANME-2a [42] and in ANME-2d [43] However genedomains for Acd are also present in methanogens unableto use acetate as substrate (Table 2) and are probably usedfor lipid metabolism In hydrogenotrophic methanogenesishydrogenases are used to replenish reduced coenzyme B andto recycle oxidized F

420(discussed in Section 21) Both the

cytoplasmic Mvh complex and the membrane bound Vhowere not present in ANME-2d [43] and not expressed inANME-2a (which also lackedEch andF

420-dependent hydro-

genase (Frh)) [42] making hydrogenotrophic methanogen-esis unlikely In ANME-1 both the cytoplasmic HdrABCand MvhD are present as well as homologues of Frh andEch but these were lacking catalytic subunits [40 41] Aniron hydrogenase was found in both ANME-1 metagenomesbut not in any other methanotroph or methanogen [41](Table 2) This iron hydrogenase domain is part of a genethat is 70 identical to a [FeFe]-hydrogenase of Dehalococ-coides mccartyi [FeFe]-hydrogenases catalyze reversible H

2

production and uptake but these were presumed to have nokey function in AOM [41] However the gene is part of a genecluster of three genes containing a 51 kDaNADH ubiquinoneoxidoreductase subunit (Table S3) which could potentially

14 Archaea

form a complex that generates a proton motive force duringhydrogen oxidation Therefore hydrogenotrophic methano-genesis by ANME-1 cannot be excluded yet

3 Respiration during AnaerobicOxidation of Methane

For netAOMtooccur an external electron acceptor is neededwhich results in a favourable Gibbs free energy change(Table 1) A variety of terminal electron acceptors have beendiscovered for AOM which will be discussed in Sections 31ndash33

31 Sulfate-Dependent AOM During sulfate-dependentAOM electrons are transferred from ANME to the sulfate-reducing bacterial partner Previous work tried to uncoverhow electrons were transferred and most compoundsthat could act as interspecies electron carrier (IEC) wereexcluded to be involved in AOM such as methanolhydrogen methanethiol acetate and carbon monoxide[57 61 62 94 101] Indications that polysulfide could actas IEC were found and ANME-2a archaea were thoughtto perform both AOM and sulfate reduction (SR) [102]However in marine seeps hydrothermal vents and othernondiffusion based sediments AOM rates are high andANME form close associations with SRB in dense aggregates[1 5 103 104] In these aggregates the high AOM ratescould not be explained by diffusion of an IEC whichmade direct interspecies electron transfer (DIET) a moreplausible mechanism [89 105 106] Cellular activities wereindependent of aggregate type and distance between thesyntrophic partners within the aggregate which is bestexplained by DIET [107] DIET is normally achieved usingmultiheme cytochrome c proteins (MHCs) and conductivepili (ie nanowires) which are mainly found in bacteriathat donate electrons extracellularly such as Geobacter andShewanella species [108ndash114] Indeed ANME-2a from seep-sediment samples seem to transfer electrons directly usinglarge MHCs [107] which were found in the metagenome ofANME-2a [107 115] ANME-1 and the associated bacterialpartner also overexpressed genes for extracellular MHCsduring AOM [116] which complements previous findings oftranscription [41] and translation [40] of ANME-1 relatedMHC genes Domain based (meta)genome analysis showsthe high abundance of MHC domains in different ANMEas compared to methanogens (Table 2) A recently isolatedbacterial partner of ANME-1 (ldquoHotSeep-1rdquo) also producedcell-to-cell connections using pili-derived nanowires [116]which explain previously detected Deltaproteobacteria-related pili genes in an AOM sample dominated by ANME-1[40]

How ANME use MHCs to donate electrons to thebacterial partner is not yet clear For ANME-2a the electronsprobably flow from methanophenazine to membrane inte-grated di-heme cytochromes (cytochrome 119887119887

6) that transfer

the electrons through the S-layer via MHCS-layer fusionproteins to extracellular MHCs (Figure 4) (Figure 4 in[107]) Exosortases and archaea-specific archaeosortases are

involved in export of cell surface proteins such as the archaealS-layer proteins These transpeptidases recognize specificsignal peptides for protein- sorting that is archaeosor-tase A recognizes the protein-sorting signal PGF-CTERMand archaeosortase C recognizes the PEF-CTERM signal[117] Both ANME-2a and 2d show presence of di-hemecytochromes archaeosortase A (IPR014522) archaeosortaseC (IPR022504) and other exosortase gene domains (Table 2)Moreover some genes of both ANME-2a and 2d containedboth MHC and PGF or PEF-CTERM domains Lastly somegenes of both ANME-2a and 2d contained both MHC andS-layer domains [107] indicating that these could form theabove-stated MHCS-layer fusion proteins

ANME-1 do not seem to have di-heme cytochromes(Table 2) [115] PGF related domains (IPR026453 andIPR026371) were present in all ANME but PEF-CTERM(IPR017474) related domains were absent in ANME-1 (Table 2) Moreover ANME-1 lacked archaeosortaseA (IPR014522) and archaeosortase C gene domains(IPR022504) as well as some other exosortases (Table 2) Asearch in NCBIrsquos conserved domains database (CCD [118])and the EMBL InterPro database [119] of amino acidssequences of all genes from ANME metagenomes thatcontain MHC domains showed that ANME-1 did not haveany protein-sorting signal or S-layer domains within thesegenes In fact S-layer domains were completely absent inANME-1 (Table 2) These results imply that ANME-1 do notuse di-heme cytochromes for electron transfer to MHCsand do not produce an S-layer (Figure 6) This implies thatANME-1 use a different mechanism for DIET and couldexplain the need for less MHCs by ANME-1 (Table 2)and the observed pili-derived nanowires produced by thebacterial partner [116] The genome of the bacterial partnerof ANME-1 (ldquoHotSeep-1rdquo) encoded 24 c-type cytochromesof which 10 were similar to secreted MHCs of Geobactersulfurreducens [120] which also uses pili for DIET [121]

In the case of ANME-2a it is not clear if pili (ienanowires) were formed during AOM It was previouslythought that electrically conductive pili seemed to be aprerequisite for current production andDIET [122 123] evenwhen syntrophs were closely associated [124] such as withinANME-2SRB aggregates However conductive materialssuch as granular activated carbon were shown to be ableto substitute pili in DIET [124] Although in previous workconductive materials such as phenazines or humic acids didnot seem to stimulate AOM rates [61] in a recent study AOMwas decoupled from SR using artificial electron acceptors[125] This indicates that conductive materials can indeedreplace pili and that ANME-2ab could possibly couple AOMto metal oxide reduction or any other suitable electronacceptor (discussed in Section 33) However it needs to beproven if in ANME-2SRB aggregates no pili are formed andif the mechanism of DIET is fundamentally different fromANME-1

As for the polysulfide shuttling theory [102] canonicalgenes for dissimilatory sulfate reduction such as adenylyl-transferase (Sat) APS reductase (Apr) and dissimilatorysulfite reductase (Dsr) which are all present in the sulfate-reducing archeon A fulgidus (Table S2) were not found in

Archaea 15

metagenomes of ANME-1 [41] and ANME-2a (Table S1)The enzymes Sat and Dsr were also not detected in ANMEcells using fluorescent immunolabelling [126] ANME-1 werepreviously found to encode most proteins for assimilatorysulfate reduction [41] ANME-2d only harbor gene domainsthat encode Sat and assimilatoryATP sulfurylase APS kinaseand sodiumsulfate symporters which were not present inANME-2a (Table S1) It is therefore clear that at least ANME-2a cannot donate electrons to sulfate but need to donateelectrons to a sulfate-reducing partner

32 Nitrate-Dependent AOM Unlike during S-AOMANME-2d that perform N-AOM do not need a bacterialpartner but transfer electrons directly to a membrane boundnitrate reductase (Nar) [28 43] (Figure 5) The ANME-2dgenomes contain most MHCs found so far in archaea[107 115] (Table 2) Of the 87 proteins that contained aCxxCH binding motif of which 43 seemed to be true c-typecytochromes [115] 23 CxxCH motif-encoding transcriptswere expressed during N-AOM [43] The function of mostof these MHCs is not known but they are likely involvedin nitrate reduction since c-type cytochromes are capableof operating in the wide range of redox potentials thatcouple nitrate reduction (11986401015840 (NO

3

minusNO2

minus) = +433mV) andmethane oxidation (11986401015840 (CoM-S-S-CoBCoM-SH+CoB-SH)= minus143mV) [43] Nitrate as terminal electron acceptor inanaerobic respiration has been found in halophilic andthermophilic archaea [127] The nar gene cluster of ldquoCaM nitroreducensrdquo comprises several genes including thecatalytic alpha (NarG molybdopterin) and beta (NarHiron sulfur cluster) subunit of nitrate reductase [28 43] The(halo)archaeal nitrate reductase complex was reported to belocated at the extracellular side of the cytoplasmic membrane[128] and in most archaea associated with the cytoplasmicmembrane via NarM [129] The ldquoCa M nitroreducensrdquogenome does not encode NarM but encodes a TAT signalpeptide at the N-terminus of NarG for translocation acrossthe cytoplasmic membrane [28 43] Interestingly theNarG and NarH seem to have been acquired from theProteobacteria via lateral gene transfer [28]

It is not yet clear at which point in themetabolism ldquoCaMnitroreducensrdquo conserves energy During reverse methano-genesis N5-methyl-H

4MPTCoM methyltransferase (Mtr)

dissipates the sodium ion potential across the cytoplasmicmembrane so subsequent steps inN-AOMhave to be coupledto the build-up of a proton or sodium motive force to makethe overall process energetically favourable The analysis ofan environmental genome [43] indicated presence of severalprotein complexes involved in electron transport and energyconservation Electrons that enter the respiratory chain couldbe transported by membrane-integral electron carriers (iemenaquinones) to a Rieske-cytochrome b complex that mayuse cytochrome c as electron acceptor This in turn maybe the electron donor for the unusual nitrate reductasecomplex Energy conservation is thermodynamically andmechanistically feasible at the F

420H2dehydrogenase and the

Rieske-cytochrome b complex (Figure 5) (Figure 2 in [43])Further investigations are needed to determine whether

nitrate reductase is also involved in energy conservationbut this working hypothesis is strengthened by the presenceof cupredoxin multicopper oxidase domains and coppercenters related to the periplasmic domain of cytochrome coxidase subunit II (HCO II) in ANME-2d (Table S1)

BothANME-2d genomes discussed here are derived frombioreactors where ldquoCaM nitroreducensrdquo formed syntrophiccultures with nitrite scavenging bacteria either with ldquoCaKuenenia stuttgartiensisrdquo (anammox bacteria) [28] or ldquoCaMethylomirabilis oxyferardquo (NC10 bacteria) [31 43]This indi-cated that ANME-2d could be dependent on those bacteriafor nitrite removal However in addition to nitrite ldquoCa Mnitroreducensrdquo may also produce ammonium during AOMby a pentaheme c-type nitrite reductase (NrfAH) encodedin the genome [43] (Figure 5) In fact both ANME-2dgenomes contain domains for NrfA (IPR003321) and NrfH(IPR017571) (Table S1) implying that both ANME-2d speciesare not necessarily dependent on a nitrite scavenger duringAOM

33 Metal-Dependent AOM Evidence for metal-dependentAOM was found in marine sediments [130ndash132] In non-marine environments AOM was also hypothesized to becoupled to iron andor manganese oxide reduction [26 133ndash136] or even coupled to the reduction of humic acids [136137] However organisms responsible for metal-dependentAOM were not identified in these studies It was speculatedthat JS1 bacteria methanogenic archaea and Methanohalo-biumANME-3 could be responsible for iron-dependentAOM [138] Other researchers speculated that either ANME-1 or MethanococcoidesANME-3 together with a bacterialpartner were responsible for manganese-dependent AOM[139] In another study where AOM was decoupled from SRANME were not detected which leaves open the possibilitythat other archaeal clades besides ANME could performmetal-dependent AOM [131]

It was recently observed that cultures containing ANME-2a and ANME-2c could decouple AOM from SR in thepresence of artificial electron acceptors humic acids andsoluble iron [125] which confirmed previous findings ofAOM not connected to SR in ANME dominated samples[140] This suggests that ANME-2 could also use insolublemetal oxide minerals as electron acceptor during AOM TheMHCs of ANME-2ab and ANME-2d are larger than thosein Shewanella and Geobacter species [107] which are knownto be capable of extracellular electron conduction It wasspeculated that both ANME-2d and Ferroglobus placidus ofwhich the latter can perform solid iron reduction can foldCxxCHmotifs into extracellular conductive structures or pili[115] Many of the MHCs of ANME-2d were not expressedwhen grown with nitrate (discussed in section 32) implyingthat these are not needed for nitrate reduction [43] Thisstrengthens the hypothesis that also ANME-2d could coupleAOM to reduction of other extracellular electron acceptorsthan nitrate and even to insoluble metal oxides Indeedrecent work showed that ANME-2d could be involved inAOM coupled to chromium(VI) reduction [141] (Table 1reaction (5)) and in AOM coupled to the reduction of soluble

16 Archaea

iron and insoluble ferrihydrite and birnessite minerals [142](Table 1 reactions (3) and (4)) ANME-2d could even possiblydonate electrons to a bacterial partner besides nitrate-richenvironments ANME-2d archaea have been found inwells ofan aquifer where sulfate and methane concentrations overlap[143] Moreover ANME-2d was the only clade detected insediments of a freshwater lake where S-AOM occurred [144]Sulfate concentrations in these studies were low but above1mM and thus higher than the lowest reported concen-trations for S-AOM to occur [145 146] Lastly sequencesof ANME-2d were relatively more abundant in freshwatersediments fed with methane and sulfate than in sedimentsfed with onlymethane or only sulfate and noN-AOMactivitywas detected when fed with nitrate and methane [27] Theseindications hold promise that direct experimental evidencefor sulfate-dependent AOM by ANME-2d could be found inthe future

TheANME-1 genome contains fewerMHCgene domainsas compared to ANME-2a and ANME-2d and some otherarchaea such as somemethylotrophicmethanogens (Table 2)and some members of the Archaeoglobales [115] The MHCsof ANME-1 also have a smaller heme count as compared toother ANME and some other archaea with the largest beingan octaheme cytochrome [107] Each hemewithin aMHChasits own redox potential and therefore structurally differentMHCs represent a large range of redox potentials that canbe used for bioenergetic electron transfer (reviewed in [147])For instance metal oxide reduction in Shewanella oneidensisMR-1 is catalyzed by a chain of a tetraheme (CymA) twodecaheme (MtrA and MtrB) and eventually extracellulardecaheme cytochromes OmcAMtrC that reduce the ironminerals [121 148 149] In Geobacter sulfurreducens ironmineral reduction seems to be catalyzed by the tetrahemecytochrome OmcE and hexaheme cytochrome OmcS trans-ferring electrons from the outer membrane to type IV pilithat transmit the electrons to iron minerals [121 150 151]Since ANME-1 lack MHCs of the correct size and lack genedomains for pili production [116] they seem unable to reduceminerals via both mechanisms present in Shewanella andGeobacter It can therefore be speculated that ANME-1 areless versatile in electron acceptor use and are not able toreduce solid metal oxides However DIET mechanisms arestill not well understood and the true differences betweenMHCs of different ANME types need to be investigated usingbiochemical methods This would allow uncovering the truecapabilities concerning DIET

34 Menaquinones and Methanophenazines ANME-2a en-coded a protein with a domain specific for PhzF which is anenzyme involved in phenazine biosynthesis in Pseudomonasfluorescens [152 153] The respective gene is not present in allmethanophenazine containing methanogens (in our genomecomparison only inM acetivorans andM formicica Table 2)so it is unclear whether this enzyme is really involved inmethanophenazine biosynthesis It is however likely thatANME-2a use methanophenazines in their respiratory chainsince gene domains for menaquinone biosynthesis wereabsent (Table 2) ldquoCa M nitroreducensrdquo probably uses

menaquinones as membrane-integral electron carrier sinceenvironmental genomes [28 43] encoded the futalosine(mqn) biosynthesis pathway as reported for Archaeoglobusfulgidus [154] (Table 2) Moreover ldquoCa M nitroreducensrdquoenrichment cultures showed absence of methanophenazines[43] ANME-1 also contained gene domains formenaquinonebiosynthesis via the futalosine (mqn) biosynthesis pathway(Table 2) Indications for a quinone biosynthesis pathwayin ANME-1 were previously found to be weak since onlysome of the Ubi homologues of the oxic ubiquinone biosyn-thesis pathway were detected [41] but the futalosine (mqn)biosynthesis pathway was overlooked in that particular anal-ysis Additionally ANME-1 have Fqo homologues similarto Archaeoglobus fulgidus [44] and expressed the catalyticsubunit FqoF [41] However since the phenazine biosynthesisdomain PhzF was also present in the ANME-1 genomes(Table 2) and Fpo and Fqo are homologues we cannotconclude on genomic information alone which redox shuttleis used by ANME-1 during AOM If ANME-1 would usemenaquinones this would have implications for subsequentelectron transfer to MHCs since methanophenazine (1198640 =minus165mV) [155] and menaquinone (1198640 = minus80mV) [156] havedifferent redox potentials

35 Cell Adhesion Some gene domains involved in cel-lular adhesion were more abundant in ANME than inmethanogens (Table 2) especially in ANME-2a and ANME-1that are known to form syntrophic interactions for electrontransfer during respiration These domains include HYR(IPR003410) and CARDB domains (IPR011635) that bothhave a direct role in cellular adhesion [157] (Table 2) Interest-ingly also domains related to the cellulosome of Clostridiumspecies termed dockerin and cohesin were highly abundantin both ANME-1 and ANME-2a as compared to ANME-2dand methanogens together with many carbohydrate bindingdomains (Table 2) In Clostridium species dockerin andcohesin form an anchor to the bacterial cell wall that containsa scaffold with cellulose-degrading enzymes and a carbohy-drate bindingmodule that binds cellulose altogether formingthe cellulosome [158] These domains have been found in alldomains of life irrespective of cellulose utilization but thefunction of such proteins outside of the cellulosome is notknown [159]Therefore dockerin cohesin and carbohydratebinding domains in ANME could hypothetically form aconstruct that binds to carbohydrates and could possibly havea function in cell-to-cell contact or MHC adhesion but thisneeds further investigation

4 Future Challenges

Advances in (meta)genomics transcriptomics and pro-teomics have produced the valuable metabolic blueprints ofdifferent ANMEwith hypotheses on how centralmetabolismelectron transport and energy conservation may functionFuture experiments are needed to biochemically demonstratethat these hypotheses are correct

The bottleneck for biochemical studies of ANME isthe lack of pure cultures due to the slow and syntrophic

Archaea 17

growth However the recent milestone discovery of directelectron transfer provides opportunities to grow ANMEas stated previously on electron accepting electrodes (ieanodes) [160] In this way pure or highly enriched culturesof different ANME without their respective syntrophic part-ner could be obtained and MHCs responsible for electricconduction could be biochemically characterized It seemsthat ANME-1 are limited by the size and abundance ofMHCs which could relate to differences in behavior onan anode The partner bacteria of ANME-1 and ANME-2could be investigated on an electron donating electrode (iecathode) with specific focus on the ability to produce pili (ienanowires) Also worth investigating is if besides ANME-2d ANME-2ab could also use insoluble electron acceptorsand if ANME-2d could donate electrons to a bacterialpartner

Another future challenge is to isolate and characterizeMcr from different ANME clades It needs to be investi-gated if Mcr abundance in ANME cells compensates forthe slow reverse activity or if modifications in the Mcrof ANME-1 also contribute to a better reverse activity ofMcr Moreover the effect of methane partial pressure onreaction rates and enzyme kinetics needs to be determined insitu

ANME-1 are potentially able to perform hydrogeno-trophic methanogenesis due to the presence of a hydrogenasein the genome Genetic indications of menaquinones aselectron carrier in ANME-1 and the various cellulosome andcell adhesion related gene domains in all ANME are alsotopics that could be explored further Methanogenic archaeaare likely not able to perform AOM but additional studieson TMO and more genetic modifications to stimulate AOMin methanogens could help in understanding the param-eters needed for AOM to occur Ultimately physiologicalunderstanding of ANME will help to explain the observedecological niche separation of different ANME clades and theoccurrence of ANMEwithout a bacterial partnerThis wouldgreatly enhance our knowledge of themethane cycle in anoxicenvironments

Competing Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors thank Stefanie Berger (RU Nijmegen) for criticalreading of the manuscript This research is supported bythe Soehngen Institute of Anaerobic Microbiology (SIAM)Gravitation grant (024002002) of the Netherlands Ministryof Education Culture and Science and the NetherlandsOrganisation for Scientific Research (NWO) Mike S MJetten was further supported by ERC AG 339880 Eco-MoMand Alfons J M Stams was supported by ERC AG 323009Novel Anaerobes

References

[1] A Boetius K Ravenschlag C J Schubert et al ldquoA marinemicrobial consortium apparently mediating anaerobic oxida-tion of methanerdquo Nature vol 407 no 6804 pp 623ndash626 2000

[2] K-U Hinrichs J M Hayes S P Sylva P G Brewert andE F DeLong ldquoMethane-consuming archaebacteria in marinesedimentsrdquo Nature vol 398 no 6730 pp 802ndash805 1999

[3] V J Orphan C H House K-U Hinrichs K D McKeeganand E F DeLong ldquoMethane-consuming archaea revealed bydirectly coupled isotopic and phylogenetic analysisrdquo Sciencevol 293 no 5529 pp 484ndash487 2001

[4] K-U Hinrichs and A Boetius ldquoThe anaerobic oxidation ofmethane new insights in microbial ecology and biogeochem-istryrdquo inOceanMargin Systems GWefer D Billett D HebbelnB B Joslashrgensen M Schluter and T VanWeering Eds pp 457ndash477 Springer Berlin Germany 2002

[5] K Knittel T Losekann A Boetius R Kort and R AmannldquoDiversity and distribution of methanotrophic archaea at coldseepsrdquo Applied and Environmental Microbiology vol 71 no 1pp 467ndash479 2005

[6] K Knittel and A Boetius ldquoAnaerobic oxidation of methaneprogress with an unknown processrdquo Annual Review of Micro-biology vol 63 pp 311ndash334 2009

[7] V J Orphan K-U Hinrichs W Ussler III et al ldquoComparativeanalysis of methane-oxidizing archaea and sulfate-reducingbacteria in anoxic marine sedimentsrdquoApplied and Environmen-tal Microbiology vol 67 no 4 pp 1922ndash1934 2001

[8] T Losekann K Knittel T Nadalig et al ldquoDiversity andabundance of aerobic and anaerobic methane oxidizers atthe Haakon Mosby Mud Volcano Barents Seardquo Applied andEnvironmentalMicrobiology vol 73 no 10 pp 3348ndash3362 2007

[9] H Niemann T Losekann D De Beer et al ldquoNovel microbialcommunities of the Haakon Mosby mud volcano and their roleas amethane sinkrdquoNature vol 443 no 7113 pp 854ndash858 2006

[10] TNunouraHOida T Toki J Ashi K Takai andKHorikoshildquoQuantification of mcrA by quantitative fluorescent PCR insediments from methane seep of the Nankai Troughrdquo FEMSMicrobiology Ecology vol 57 no 1 pp 149ndash157 2006

[11] B Orcutt A Boetius M Elvert V Samarkin and S B JoyeldquoMolecular biogeochemistry of sulfate reduction methanogen-esis and the anaerobic oxidation of methane at Gulf of Mexicocold seepsrdquoGeochimica et Cosmochimica Acta vol 69 no 17 pp4267ndash4281 2005

[12] V J Orphan W Ussler III T H Naehr C H House K-U Hinrichs and C K Paull ldquoGeological geochemical andmicrobiological heterogeneity of the seafloor around methanevents in the Eel River Basin offshore Californiardquo ChemicalGeology vol 205 no 3-4 pp 265ndash289 2004

[13] M G Pachiadaki A Kallionaki A Dahlmann G J De Langeand K A Kormas ldquoDiversity and spatial distribution ofprokaryotic communities along a sediment vertical profile ofa deep-sea mud volcanordquo Microbial Ecology vol 62 no 3 pp655ndash668 2011

[14] I Roalkvam H Dahle Y Chen S L Joslashrgensen H Haflidasonand I H Steen ldquoFine-scale community structure analysis ofANME in Nyegga sediments with high and low methane fluxrdquoFrontiers in Microbiology vol 3 p 216 2012

[15] K Yanagawa M Sunamura M A Lever et al ldquoNiche separa-tion of methanotrophic archaea (ANME-1 and -2) in methane-seep sediments of the Eastern Japan Sea offshore JoetsurdquoGeomicrobiology Journal vol 28 no 2 pp 118ndash129 2011

18 Archaea

[16] A Pernthaler A E Dekas C T Brown S K Goffredi TEmbaye and V J Orphan ldquoDiverse syntrophic partnershipsfromdeep-seamethane vents revealed by direct cell capture andmetagenomicsrdquo Proceedings of the National Academy of Sciencesof the United States of America vol 105 no 19 pp 7052ndash70572008

[17] R Hatzenpichler S A Connon D Goudeau R R Malm-strom T Woyke and V J Orphan ldquoVisualizing in situtranslational activity for identifying and sorting slow-growingarchaealminusbacterial consortiardquo Proceedings of the NationalAcademy of Sciences vol 113 no 28 pp E4069ndashE4078 2016

[18] L Maignien R J Parkes B Cragg et al ldquoAnaerobic oxidationof methane in hypersaline cold seep sedimentsrdquo FEMS Micro-biology Ecology vol 83 no 1 pp 214ndash231 2013

[19] V J Orphan C H House K-U Hinrichs K D McKeeganand E F DeLong ldquoMultiple archaeal groups mediate methaneoxidation in anoxic cold seep sedimentsrdquo Proceedings of theNational Academy of Sciences of the United States of Americavol 99 no 11 pp 7663ndash7668 2002

[20] T TreudeM Kruger A Boetius and B B Joslashrgensen ldquoEnviron-mental control on anaerobic oxidation of methane in the gassysediments of Eckernforde Bay (German Baltic)rdquo Limnology andOceanography vol 50 no 6 pp 1771ndash1786 2005

[21] G C Jagersma R J W Meulepas I Heikamp-De Jong etal ldquoMicrobial diversity and community structure of a highlyactive anaerobic methane-oxidizing sulfate-reducing enrich-mentrdquo Environmental Microbiology vol 11 no 12 pp 3223ndash3232 2009

[22] M Blumenberg R Seifert J Reitner T Pape andWMichaelisldquoMembrane lipid patterns typify distinct anaerobic methan-otrophic consortiardquo Proceedings of the National Academy ofSciences of the United States of America vol 101 no 30 pp 11111ndash11116 2004

[23] S Bertram M Blumenberg W Michaelis M Siegert MKruger and R Seifert ldquoMethanogenic capabilities of ANME-archaea deduced from 13C-labelling approachesrdquo Environmen-tal Microbiology vol 15 no 8 pp 2384ndash2393 2013

[24] K G Lloyd M J Alperin and A Teske ldquoEnvironmental evi-dence for net methane production and oxidation in putativeANaerobic MEthanotrophic (ANME) archaeardquo EnvironmentalMicrobiology vol 13 no 9 pp 2548ndash2564 2011

[25] M Takeuchi H Yoshioka Y Seo et al ldquoA distinct freshwater-adapted subgroup of ANME-1 dominates active archaeal com-munities in terrestrial subsurfaces in Japanrdquo EnvironmentalMicrobiology vol 13 no 12 pp 3206ndash3218 2011

[26] R T Amos B A Bekins I M Cozzarelli et al ldquoEvidence foriron-mediated anaerobic methane oxidation in a crude oil-contaminated aquiferrdquo Geobiology vol 10 no 6 pp 506ndash5172012

[27] P H Timmers D A Suarez-Zuluaga M van Rossem MDiender A J Stams and C M Plugge ldquoAnaerobic oxidationof methane associated with sulfate reduction in a naturalfreshwater gas sourcerdquo ISME Journal vol 10 pp 1400ndash14122015

[28] M F Haroon S Hu Y Shi et al ldquoAnaerobic oxidation ofmethane coupled to nitrate reduction in a novel archaeallineagerdquo Nature vol 500 no 7468 pp 567ndash570 2013

[29] H J Mills C Hodges K Wilson I R MacDonald and PA Sobecky ldquoMicrobial diversity in sediments associated withsurface-breaching gas hydrate mounds in the Gulf of MexicordquoFEMS Microbiology Ecology vol 46 no 1 pp 39ndash52 2003

[30] K G Lloyd L Lapham and A Teske ldquoAn anaerobic methane-oxidizing community of ANME-1b archaea in hypersaline gulfofMexico sedimentsrdquoApplied and EnvironmentalMicrobiologyvol 72 no 11 pp 7218ndash7230 2006

[31] A A Raghoebarsing A Pol K T Van De Pas-Schoonen et alldquoA microbial consortium couples anaerobic methane oxidationto denitrificationrdquoNature vol 440 no 7086 pp 918ndash921 2006

[32] S Hu R J Zeng L C Burow P Lant J Keller and Z YuanldquoEnrichment of denitrifying anaerobic methane oxidizingmicroorganismsrdquo Environmental Microbiology Reports vol 1no 5 pp 377ndash384 2009

[33] Z-W Ding J Ding L Fu F Zhang and R J Zeng ldquoSimultane-ous enrichment of denitrifying methanotrophs and anammoxbacteriardquo Applied Microbiology and Biotechnology vol 98 no24 pp 10211ndash10221 2014

[34] R Seifert K Nauhaus M Blumenberg M Kruger and WMichaelis ldquoMethane dynamics in a microbial community ofthe Black Sea traced by stable carbon isotopes in vitrordquoOrganicGeochemistry vol 37 no 10 pp 1411ndash1419 2006

[35] J Ding Z-W Ding L Fu Y-Z Lu S H Cheng and R JZeng ldquoNew primers for detecting and quantifying denitrifyinganaerobic methane oxidation archaea in different ecologicalnichesrdquo Applied Microbiology and Biotechnology vol 99 no 22pp 9805ndash9812 2015

[36] A Vaksmaa C Luke T van Alen et al ldquoDistribution and activ-ity of the anaerobic methanotrophic community in a nitrogen-fertilized Italian paddy soilrdquo FEMS Microbiology Ecology vol92 no 12 2016

[37] P N Evans D H Parks G L Chadwick et al ldquoMethanemetabolism in the archaeal phylum Bathyarchaeota revealed bygenome-centric metagenomicsrdquo Science vol 350 no 6259 pp434ndash438 2015

[38] I Vanwonterghem P N Evans D H Parks et al ldquoMethy-lotrophic methanogenesis discovered in the archaeal phylumVerstraetearchaeotardquo Nature Microbiology vol 1 Article ID16170 2016

[39] P Worm J J Koehorst M Visser et al ldquoA genomic view onsyntrophic versus non-syntrophic lifestyle in anaerobic fattyacid degrading communitiesrdquo Biochimica et Biophysica ActamdashBioenergetics vol 1837 no 12 pp 2004ndash2016 2014

[40] R Stokke I Roalkvam A Lanzen H Haflidason and I HSteen ldquoIntegrated metagenomic and metaproteomic analysesof an ANME-1-dominated community in marine cold seepsedimentsrdquo Environmental Microbiology vol 14 no 5 pp 1333ndash1346 2012

[41] A Meyerdierks M Kube I Kostadinov et al ldquoMetagenomeand mRNA expression analyses of anaerobic methanotrophicarchaea of the ANME-1 grouprdquo Environmental Microbiologyvol 12 no 2 pp 422ndash439 2010

[42] F-P Wang Y Zhang Y Chen et al ldquoMethanotrophicarchaea possessing diverging methane-oxidizing and electron-transporting pathwaysrdquo ISME Journal vol 8 no 5 pp 1069ndash1078 2014

[43] A Arshad D R Speth R M de Graaf H J Op den Camp MS Jetten and C U Welte ldquoA metagenomics-based metabolicmodel of nitrate-dependent anaerobic oxidation of methane byMethanoperedens-like archaeardquo Frontiers inMicrobiology vol 6article1423 2015

[44] S J Hallam N Putnam CM Preston et al ldquoReversemethano-genesis testing the hypothesis with environmental genomicsrdquoScience vol 305 no 5689 pp 1457ndash1462 2004

Archaea 19

[45] R K Thauer ldquoAnaerobic oxidation of methane with sulfate onthe reversibility of the reactions that are catalyzed by enzymesalso involved inmethanogenesis fromCO

2rdquoCurrent Opinion in

Microbiology vol 14 no 3 pp 292ndash299 2011[46] U Deppenmeier V Muller and G Gottschalk ldquoPathways of

energy conservation in methanogenic archaeardquo Archives ofMicrobiology vol 165 no 3 pp 149ndash163 1996

[47] A-K Kaster J Moll K Parey and R K Thauer ldquoCoupling offerredoxin and heterodisulfide reduction via electron bifurca-tion in hydrogenotrophic methanogenic archaeardquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 108 no 7 pp 2981ndash2986 2011

[48] R K Thauer A-K Kaster H Seedorf W Buckel and RHedderich ldquoMethanogenic archaea ecologically relevant dif-ferences in energy conservationrdquo Nature Reviews Microbiologyvol 6 no 8 pp 579ndash591 2008

[49] W Ludwig O Strunk R Westram et al ldquoARB a softwareenvironment for sequence datardquoNucleic Acids Research vol 32no 4 pp 1363ndash1371 2004

[50] E Pruesse C Quast K Knittel et al ldquoSILVA a comprehensiveonline resource for quality checked and aligned ribosomal RNAsequence data compatible with ARBrdquo Nucleic Acids Researchvol 35 no 21 pp 7188ndash7196 2007

[51] J J Marlow C T Skennerton Z Li et al ldquoProteomic stableisotope probing reveals biosynthesis dynamics of slow growingmethane based microbial communitiesrdquo Frontiers in Microbiol-ogy vol 7 article 386 2016

[52] P V Welander and W W Metcalf ldquoLoss of the mtr operon inMethanosarcina blocks growth on methanol but not methano-genesis and reveals an unknown methanogenic pathwayrdquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 102 no 30 pp 10664ndash10669 2005

[53] P V Welander and W W Metcalf ldquoMutagenesis of the C1oxidation pathway inmethanosarcina barkeri new insights intothe MtrMer bypass pathwayrdquo Journal of Bacteriology vol 190no 6 pp 1928ndash1936 2008

[54] M Goenrich R K Thauer H Yurimoto and N KatoldquoFormaldehyde activating enzyme (Fae) and hexulose-6-phosphate synthase (Hps) inMethanosarcina barkeri a possiblefunction in ribose-5-phosphate biosynthesisrdquoArchives ofMicro-biology vol 184 no 1 pp 41ndash48 2005

[55] M Goenrich FMahlert E C Duin C Bauer B Jaun and R KThauer ldquoProbing the reactivity of Ni in the active site of methyl-coenzyme M reductase with substrate analoguesrdquo Journal ofBiological Inorganic Chemistry vol 9 no 6 pp 691ndash705 2004

[56] S Scheller M Goenrich R Boecher R K Thauer and BJaun ldquoThe key nickel enzyme of methanogenesis catalyses theanaerobic oxidation of methanerdquo Nature vol 465 no 7298 pp606ndash608 2010

[57] K Nauhaus A Boetius M Kruger and F Widdel ldquoIn vitrodemonstration of anaerobic oxidation of methane coupled tosulphate reduction in sediment from amarine gas hydrate areardquoEnvironmental Microbiology vol 4 no 5 pp 296ndash305 2002

[58] Y Zhang J-P Henriet J Bursens and N Boon ldquoStimulationof in vitro anaerobic oxidation of methane rate in a continuoushigh-pressure bioreactorrdquo Bioresource Technology vol 101 no9 pp 3132ndash3138 2010

[59] M Kruger T Treude H Wolters K Nauhaus and A BoetiusldquoMicrobial methane turnover in different marine habitatsrdquoPalaeogeography Palaeoclimatology Palaeoecology vol 227 no1ndash3 pp 6ndash17 2005

[60] C Deusner V Meyer and T G Ferdelman ldquoHigh-pressuresystems for gas-phase free continuous incubation of enrichedmarinemicrobial communities performing anaerobic oxidationof methanerdquo Biotechnology and Bioengineering vol 105 no 3pp 524ndash533 2010

[61] K Nauhaus T Treude A Boetius and M Kruger ldquoEnviron-mental regulation of the anaerobic oxidation of methane acomparison of ANME-I and ANME-II communitiesrdquo Environ-mental Microbiology vol 7 no 1 pp 98ndash106 2005

[62] T Treude V Orphan K Knittel A Gieseke C H House andA Boetius ldquoConsumption of methane and CO

2by methan-

otrophicmicrobial mats from gas seeps of the anoxic Black SeardquoApplied and EnvironmentalMicrobiology vol 73 no 7 pp 2271ndash2283 2007

[63] T Holler F Widdel K Knittel et al ldquoThermophilic anaerobicoxidation of methane by marine microbial consortiardquo ISMEJournal vol 5 no 12 pp 1946ndash1956 2011

[64] M Kruger M Blumenberg S Kasten et al ldquoA novel multi-layered methanotrophic microbial mat system growing on thesediment of the Black Seardquo Environmental Microbiology vol 10no 8 pp 1934ndash1947 2008

[65] R J WMeulepas C G Jagersma J Gieteling C J N BuismanA J M Stams and P N L Lens ldquoEnrichment of anaerobicmethanotrophs in sulfate-reducing membrane bioreactorsrdquoBiotechnology and Bioengineering vol 104 no 3 pp 458ndash4702009

[66] T Holler G Wegener H Niemann et al ldquoCarbon and sulfurback flux during anaerobic microbial oxidation of methane andcoupled sulfate reductionrdquo Proceedings of the National Academyof Sciences of the United States of America vol 108 no 52 ppE1484ndashE1490 2011

[67] M Kruger AMeyerdierks F O Glockner et al ldquoA conspicuousnickel protein in microbial mats that oxidize methane anaero-bicallyrdquo Nature vol 426 no 6968 pp 878ndash881 2003

[68] S Mayr C Latkoczy M Kruger et al ldquoStructure of an F430

variant from archaea associated with anaerobic oxidation ofmethanerdquo Journal of the American Chemical Society vol 130 no32 pp 10758ndash10767 2008

[69] S Shima and R K Thauer ldquoMethyl-coenzyme M reductaseand the anaerobic oxidation of methane in methanotrophicArchaeardquo Current Opinion in Microbiology vol 8 no 6 pp643ndash648 2005

[70] R K Thauer and S Shima ldquoMethane as fuel for anaerobicmicroorganismsrdquo Annals of the New York Academy of Sciencesvol 1125 pp 158ndash170 2008

[71] S Yamamoto J B Alcauskas and T E Crozier ldquoSolubility ofmethane in distilled water and seawaterrdquo Journal of Chemicaland Engineering Data vol 21 no 1 pp 78ndash80 1976

[72] P H A Timmers J Gieteling H C A Widjaja-Greefkeset al ldquoGrowth of anaerobic methane-oxidizing archaea andsulfate-reducing bacteria in a high-pressure membrane capsulebioreactorrdquoApplied and EnvironmentalMicrobiology vol 81 no4 pp 1286ndash1296 2015

[73] MKruger HWoltersMGehre S B Joye andH-H RichnowldquoTracing the slow growth of anaerobic methane-oxidizingcommunities by 15N-labelling techniquesrdquo FEMS MicrobiologyEcology vol 63 no 3 pp 401ndash411 2008

[74] R J W Meulepas C G Jagersma A F Khadem C J N Buis-man A J M Stams and P N L Lens ldquoEffect of environmentalconditions on sulfate reduction withmethane as electron donorby an Eckernforde Bay enrichmentrdquo Environmental Science andTechnology vol 43 no 17 pp 6553ndash6559 2009

20 Archaea

[75] M W Bowles V A Samarkin and S B Joye ldquoImprovedmeasurement of microbial activity in deep-sea sediments atin situ pressure and methane concentrationrdquo Limnology andOceanography Methods vol 9 pp 499ndash506 2011

[76] S Shima M Krueger T Weinert et al ldquoStructure of a methyl-coenzyme M reductase from Black Sea mats that oxidizemethane anaerobicallyrdquo Nature vol 481 no 7379 pp 98ndash1012012

[77] K D Allen G Wegener and R H White ldquoDiscovery of multi-ple modified F-430 coenzymes in methanogens and anaerobicmethanotrophic archaea suggests possible new roles for F-430in naturerdquoApplied and Environmental Microbiology vol 80 no20 pp 6403ndash6412 2014

[78] V W Soo M J McAnulty A Tripathi et al ldquoReversingmethanogenesis to capture methane for liquid biofuel precur-sorsrdquoMicrobial Cell Factories vol 15 article 11 2016

[79] D L Valentine and W S Reeburgh ldquoNew perspectives onanaerobicmethane oxidationrdquoEnvironmentalMicrobiology vol2 no 5 pp 477ndash484 2000

[80] D L Valentine ldquoBiogeochemistry and microbial ecology ofmethane oxidation in anoxic environments a reviewrdquo Antonievan Leeuwenhoek International Journal of General and Molecu-lar Microbiology vol 81 no 1-4 pp 271ndash282 2002

[81] A J B Zehnder and T D Brock ldquoMethane formation andmethane oxidation by methanogenic bacteriardquo Journal of Bac-teriology vol 137 no 1 pp 420ndash432 1979

[82] J Harder ldquoAnaerobic methane oxidation by bacteria employ-ing 14C-methane uncontaminated with 14C-carbon monoxiderdquoMarine Geology vol 137 no 1-2 pp 13ndash23 1997

[83] J J Moran C H House K H Freeman and J G FerryldquoTrace methane oxidation studied in several Euryarchaeotaunder diverse conditionsrdquo Archaea vol 1 no 5 pp 303ndash3092005

[84] J J Moran C H House B Thomas and K H FreemanldquoProducts of tracemethane oxidation during nonmethyltrophicgrowth by Methanosarcinardquo Journal of Geophysical ResearchBiogeosciences vol 112 no 2 2007

[85] R J W Meulepas C G Jagersma Y Zhang et al ldquoTracemethane oxidation and the methane dependency of sulfatereduction in anaerobic granular sludgerdquo FEMS MicrobiologyEcology vol 72 no 2 pp 261ndash271 2010

[86] A J B Zehnder andTD Brock ldquoAnaerobicmethane oxidationoccurrence and ecologyrdquoApplied and Environmental Microbiol-ogy vol 39 no 1 pp 194ndash204 1980

[87] S J Blazewicz D G Petersen M P Waldrop and M K Fire-stone ldquoAnaerobic oxidation of methane in tropical and borealsoils ecological significance in terrestrial methane cyclingrdquoJournal of Geophysical Research Biogeosciences vol 117 no 2Article ID G02033 2012

[88] K A Smemo and J B Yavitt ldquoEvidence for anaerobic CH4

oxidation in freshwater peatlandsrdquo Geomicrobiology Journalvol 24 no 7-8 pp 583ndash597 2007

[89] M J Alperin and T M Hoehler ldquoAnaerobic methane oxidationby archaeasulfate-reducing bacteria aggregates 1 Thermody-namic and physical constraintsrdquo American Journal of Sciencevol 309 no 10 pp 869ndash957 2009

[90] S L Caldwell J R Laidler E A Brewer J O Eberly S CSandborgh and F S Colwell ldquoAnaerobic oxidation of methanemechanisms bioenergetics and the ecology of associatedmicroorganismsrdquo Environmental Science and Technology vol42 no 18 pp 6791ndash6799 2008

[91] GWang A J Spivack and S DrsquoHondt ldquoGibbs energies of reac-tion and microbial mutualism in anaerobic deep subseafloorsediments of ODP Site 1226rdquoGeochimica et Cosmochimica Actavol 74 no 14 pp 3938ndash3947 2010

[92] P R Girguis A E Cozen and E F DeLong ldquoGrowth andpopulation dynamics of anaerobic methane-oxidizing archaeaand sulfate-reducing bacteria in a continuous-flow bioreactorrdquoApplied and EnvironmentalMicrobiology vol 71 no 7 pp 3725ndash3733 2005

[93] K Nauhaus M Albrecht M Elvert A Boetius and F WiddelldquoIn vitro cell growth ofmarine archaeal-bacterial consortia dur-ing anaerobic oxidation ofmethanewith sulfaterdquoEnvironmentalMicrobiology vol 9 no 1 pp 187ndash196 2007

[94] B Orcutt V Samarkin A Boetius and S Joye ldquoOn the relation-ship between methane production and oxidation by anaerobicmethanotrophic communities from cold seeps of the Gulf ofMexicordquo Environmental Microbiology vol 10 no 5 pp 1108ndash1117 2008

[95] M Y Yoshinaga T Holler T Goldhammer et al ldquoCarbon iso-tope equilibration during sulphate-limited anaerobic oxidationof methanerdquo Nature Geoscience vol 7 no 3 pp 190ndash194 2014

[96] T Treude J Niggemann J Kallmeyer et al ldquoAnaerobic oxi-dation of methane and sulfate reduction along the Chileancontinental marginrdquo Geochimica et Cosmochimica Acta vol 69no 11 pp 2767ndash2779 2005

[97] R J Parkes B A Cragg N Banning et al ldquoBiogeochemistryand biodiversity of methane cycling in subsurface marinesediments (SkagerrakDenmark)rdquoEnvironmentalMicrobiologyvol 9 no 5 pp 1146ndash1161 2007

[98] N J Knab B A Cragg E R C Hornibrook et al ldquoRegulationof anaerobic methane oxidation in sediments of the Black SeardquoBiogeosciences vol 6 no 8 pp 1505ndash1518 2009

[99] H Yoshioka A Maruyama T Nakamura et al ldquoActivities anddistribution of methanogenic and methane-oxidizing microbesin marine sediments from the Cascadia Marginrdquo Geobiologyvol 8 no 3 pp 223ndash233 2010

[100] G Wegener V Krukenberg S E Ruff M Y Kellermann andK Knittel ldquoMetabolic capabilities of microorganisms involvedin and associated with the anaerobic oxidation of methanerdquoFrontiers in Microbiology vol 7 article 46 2016

[101] R J W Meulepas C G Jagersma A F Khadem A J MStams and P N L Lens ldquoEffect of methanogenic substrateson anaerobic oxidation of methane and sulfate reduction by ananaerobic methanotrophic enrichmentrdquo Applied Microbiologyand Biotechnology vol 87 no 4 pp 1499ndash1506 2010

[102] J Milucka T G Ferdelman L Polerecky et al ldquoZero-valentsulphur is a key intermediate in marine methane oxidationrdquoNature vol 491 no 7425 pp 541ndash546 2012

[103] W Michaelis R Seifert K Nauhaus et al ldquoMicrobial reefs inthe black sea fueled by anaerobic oxidation ofmethanerdquo Sciencevol 297 no 5583 pp 1013ndash1015 2002

[104] A Vigneron P Cruaud P Pignet et al ldquoArchaeal and anaerobicmethane oxidizer communities in the Sonora Margin coldseeps Guaymas Basin (Gulf of California)rdquo ISME Journal vol7 no 8 pp 1595ndash1608 2013

[105] M Alperin and T Hoehler ldquoThe ongoing mystery of sea-floormethanerdquo Science vol 329 no 5989 pp 288ndash289 2010

[106] B Orcutt and C Meile ldquoConstraints on mechanisms and ratesof anaerobic oxidation of methane by microbial consortiaprocess-basedmodeling of ANME-2 archaea and sulfate reduc-ing bacteria interactionsrdquo Biogeosciences vol 5 no 6 pp 1587ndash1599 2008

Archaea 21

[107] S E McGlynn G L Chadwick C P Kempes and V J OrphanldquoSingle cell activity reveals direct electron transfer in methan-otrophic consortiardquoNature vol 526 no 7574 pp 531ndash535 2015

[108] D R Lovley ldquoElectromicrobiologyrdquo Annual Review of Microbi-ology vol 66 pp 391ndash409 2012

[109] S M Strycharz-Glaven R M Snider A Guiseppi-Elie andL M Tender ldquoOn the electrical conductivity of microbialnanowires and biofilmsrdquoEnergy and Environmental Science vol4 no 11 pp 4366ndash4379 2011

[110] D J Richardson J N Butt J K Fredrickson et al ldquoThe lsquoporinndashcytochromersquo model for microbe-to-mineral electron transferrdquoMolecular Microbiology vol 85 no 2 pp 201ndash212 2012

[111] A Okamoto K Hashimoto and R Nakamura ldquoLong-rangeelectron conduction of Shewanella biofilms mediated by outermembrane C-type cytochromesrdquo Bioelectrochemistry vol 85pp 61ndash65 2012

[112] M Y El-Naggar G Wanger K M Leung et al ldquoElectricaltransport along bacterial nanowires from Shewanella oneidensisMR-1rdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 107 no 42 pp 18127ndash18131 2010

[113] G Reguera K D McCarthy T Mehta J S Nicoll M TTuominen and D R Lovley ldquoExtracellular electron transfer viamicrobial nanowiresrdquo Nature vol 435 no 7045 pp 1098ndash11012005

[114] Z M Summers H E Fogarty C Leang A E Franks N SMalvankar and D R Lovley ldquoDirect exchange of electronswithin aggregates of an evolved syntrophic coculture of anaer-obic bacteriardquo Science vol 330 no 6009 pp 1413ndash1415 2010

[115] A Kletzin T Heimerl J Flechsler L V Niftrik R Rachel andA Klingl ldquoCytochromes c in archaea distribution maturationcell architecture and the special case of Ignicoccus hospitalisrdquoFrontiers in Microbiology vol 6 article 439 2015

[116] GWegener V Krukenberg D Riedel H E Tegetmeyer and ABoetius ldquoIntercellular wiring enables electron transfer betweenmethanotrophic archaea and bacteriardquo Nature vol 526 no7574 pp 587ndash590 2015

[117] D HHaft S H Payne and J D Selengut ldquoArchaeosortases andexosortases are widely distributed systems linking membranetransit with posttranslational modificationrdquo Journal of Bacteri-ology vol 194 no 1 pp 36ndash48 2012

[118] A Marchler-Bauer M K Derbyshire N R Gonzales et alldquoCDD NCBIrsquos conserved domain databaserdquo Nucleic AcidsResearch vol 43 no 1 pp D222ndashD226 2015

[119] A Mitchell H-Y Chang L Daugherty et al ldquoThe InterProprotein families database the classification resource after 15yearsrdquo Nucleic Acids Research vol 43 no 1 pp D213ndashD2212015

[120] V Krukenberg K Harding M Richter et al ldquoCandidatusdesulfofervidus auxilii a hydrogenotrophic sulfate-reducingbacterium involved in the thermophilic anaerobic oxidation ofmethanerdquo Environmental Microbiology vol 18 pp 3073ndash30912016

[121] L Shi T C Squier J M Zachara and J K Fredrickson ldquoRes-piration of metal (hydr)oxides by Shewanella and Geobactera key role for multihaem c-type cytochromesrdquo MolecularMicrobiology vol 65 no 1 pp 12ndash20 2007

[122] N S Malvankar and D R Lovley ldquoMicrobial nanowires forbioenergy applicationsrdquo Current Opinion in Biotechnology vol27 pp 88ndash95 2014

[123] A-E Rotaru T LWoodard K PNevin andDR Lovley ldquoLinkbetween capacity for current production and syntrophic growth

in Geobacter speciesrdquo Frontiers in Microbiology vol 6 article744 2015

[124] A-E Rotaru P M Shrestha F Liu et al ldquoDirect interspecieselectron transfer between Geobacter metallireducens andMethanosarcina barkerirdquo Applied and Environmental Microbi-ology vol 80 no 15 pp 4599ndash4605 2014

[125] S Scheller H Yu G L Chadwick S E McGlynn and VJ Orphan ldquoArtificial electron acceptors decouple archaealmethane oxidation from sulfate reductionrdquo Science vol 351 no6274 pp 703ndash707 2016

[126] J Milucka F Widdel and S Shima ldquoImmunological detec-tion of enzymes for sulfate reduction in anaerobic methane-oxidizing consortiardquo Environmental Microbiology vol 15 no 5pp 1561ndash1571 2013

[127] P Cabello M D Roldan and C Moreno-Vivian ldquoNitratereduction and the nitrogen cycle in archaeardquoMicrobiology vol150 no 11 pp 3527ndash3546 2004

[128] R MMartinez-Espinosa E J Dridge M J Bonete et al ldquoLookon the positive sideThe orientation identification and bioener-getics of lsquoArchaealrsquomembrane-boundnitrate reductasesrdquoFEMSMicrobiology Letters vol 276 no 2 pp 129ndash139 2007

[129] S de VriesMMomcilovicM J F Strampraad J PWhiteleggeA Baghai and I Schroder ldquoAdaptation to a high-tungsten envi-ronment pyrobaculum aerophilum contains an active tungstennitrate reductaserdquo Biochemistry vol 49 no 45 pp 9911ndash99212010

[130] M Egger O Rasigraf C J Sapart et al ldquoIron-mediated anaer-obic oxidation of methane in brackish coastal sedimentsrdquoEnvironmental Science and Technology vol 49 no 1 pp 277ndash283 2015

[131] T Treude S Krause J Maltby A W Dale R Coffin and LJ Hamdan ldquoSulfate reduction and methane oxidation activitybelow the sulfate-methane transition zone in Alaskan BeaufortSea continental margin sediments implications for deep sulfurcyclingrdquo Geochimica et Cosmochimica Acta vol 144 pp 217ndash237 2014

[132] N Riedinger M J Formolo T W Lyons S Henkel A Beckand S Kasten ldquoAn inorganic geochemical argument for coupledanaerobic oxidation of methane and iron reduction in marinesedimentsrdquo Geobiology vol 12 no 2 pp 172ndash181 2014

[133] Y-H Chang T-W Cheng W-J Lai et al ldquoMicrobial methanecycling in a terrestrialmud volcano in eastern Taiwanrdquo Environ-mental Microbiology vol 14 no 4 pp 895ndash908 2012

[134] S A Crowe S Katsev K Leslie et al ldquoThe methane cycle inferruginous Lake Matanordquo Geobiology vol 9 no 1 pp 61ndash782011

[135] O Sivan M Adler A Pearson et al ldquoGeochemical evidence foriron-mediated anaerobic oxidation of methanerdquo Limnology andOceanography vol 56 no 4 pp 1536ndash1544 2011

[136] K E A Segarra C Comerford J Slaughter and S B JoyeldquoImpact of electron acceptor availability on the anaerobic oxi-dation of methane in coastal freshwater and brackish wetlandsedimentsrdquo Geochimica et Cosmochimica Acta vol 115 pp 15ndash30 2013

[137] V Gupta K A Smemo J B Yavitt D Fowle B Branfireunand N Basiliko ldquoStable isotopes reveal widespread anaerobicmethane oxidation across latitude and peatland typerdquo Environ-mental Science and Technology vol 47 no 15 pp 8273ndash82792013

[138] O Oni T Miyatake S Kasten et al ldquoDistinct microbialpopulations are tightly linked to the profile of dissolved iron in

22 Archaea

the methanic sediments of the Helgolandmud area North SeardquoFrontiers in Microbiology vol 6 2015

[139] E J Beal C H House and V J Orphan ldquoManganese- andiron-dependent marine methane oxidationrdquo Science vol 325no 5937 pp 184ndash187 2009

[140] M W Bowles V A Samarkin K M Bowles and S B JoyeldquoWeak coupling between sulfate reduction and the anaerobicoxidation of methane in methane-rich seafloor sedimentsduring ex situ incubationrdquo Geochimica et Cosmochimica Actavol 75 no 2 pp 500ndash519 2011

[141] Y Z Lu L Fu J Ding Z Ding N Li and R J Zeng ldquoCr(VI)reduction coupled with anaerobic oxidation of methane in alaboratory reactorrdquoWater Research vol 102 pp 445ndash452 2016

[142] K F Ettwig B Zhu D Speth J T Keltjens M S Jetten and BKartal ldquoArchaea catalyze iron-dependent anaerobic oxidationof methanerdquo Proceedings of the National Academy of Sciences ofthe United States of America vol 113 no 45 pp 12792ndash127962016

[143] T M Flynn R A Sanford H Ryu et al ldquoFunctional microbialdiversity explains groundwater chemistry in a pristine aquiferrdquoBMCMicrobiology vol 13 no 1 article no 146 2013

[144] C J Schubert F Vazquez T Losekann-Behrens K KnittelM Tonolla and A Boetius ldquoEvidence for anaerobic oxidationof methane in sediments of a freshwater system (Lago diCadagno)rdquo FEMS Microbiology Ecology vol 76 no 1 pp 26ndash38 2011

[145] K E A Segarra F Schubotz V Samarkin M Y Yoshinaga K-U Hinrichs and S B Joye ldquoHigh rates of anaerobic methaneoxidation in freshwater wetlands reduce potential atmosphericmethane emissionsrdquo Nature Communications vol 6 article7477 2015

[146] E J Beal M W Claire and C H House ldquoHigh rates ofanaerobic methanotrophy at low sulfate concentrations withimplications for past and present methane levelsrdquo Geobiologyvol 9 no 2 pp 131ndash139 2011

[147] F Kracke I Vassilev and J O Kromer ldquoMicrobial electrontransport and energy conservationmdashthe foundation for opti-mizing bioelectrochemical systemsrdquo Frontiers in Microbiologyvol 6 article 575 2015

[148] C L Reardon A C Dohnalkova P Nachimuthu et al ldquoRoleof outer-membrane cytochromes MtrC and OmcA in thebiomineralization of ferrihydrite by Shewanella oneidensisMR-1rdquo Geobiology vol 8 no 1 pp 56ndash68 2010

[149] L Shi B Chen Z Wang et al ldquoIsolation of a high-affinityfunctional protein complex between OmcA and MtrC twoouter membrane decaheme c-type cytochromes of Shewanellaoneidensis MR-1rdquo Journal of Bacteriology vol 188 no 13 pp4705ndash4714 2006

[150] X Qian T Mester L Morgado et al ldquoBiochemical charac-terization of purified OmcS a c-type cytochrome requiredfor insoluble Fe(III) reduction in Geobacter sulfurreducensrdquoBiochimica et BiophysicaActamdashBioenergetics vol 1807 no 4 pp404ndash412 2011

[151] T Mehta M V Coppi S E Childers and D R Lovley ldquoOutermembrane c-type cytochromes required for Fe(III) andMn(IV)oxide reduction in Geobacter sulfurreducensrdquo Applied andEnvironmentalMicrobiology vol 71 no 12 pp 8634ndash8641 2005

[152] W Blankenfeldt A P Kuzin T Skarina et al ldquoStructure andfunction of the phenazine biosynthetic protein PhzF fromPseudomonas fluorescensrdquoProceedings of theNational Academyof Sciences of the United States of America vol 101 no 47 pp16431ndash16436 2004

[153] J F Parsons F Song L Parsons K Calabrese E Eisensteinand J E Ladner ldquoStructure and function of the phenazinebiosynthesis protein PhzF fromPseudomonas fluorescens 2-79rdquoBiochemistry vol 43 no 39 pp 12427ndash12435 2004

[154] T Hiratsuka K Furihata J Ishikawa et al ldquoAn alternativemenaquinone biosynthetic pathway operating in microorgan-ismsrdquo Science vol 321 no 5896 pp 1670ndash1673 2008

[155] M Tietze A Beuchle I Lamla et al ldquoRedox potentials ofmethanophenazine and CoB-S-S-CoM factors involved inelectron transport in methanogenic archaeardquo ChemBioChemvol 4 no 4 pp 333ndash335 2003

[156] Q H Tran and G Unden ldquoChanges in the proton potentialand the cellular energetics of Escherichia coli during growth byaerobic and anaerobic respiration or by fermentationrdquoEuropeanJournal of Biochemistry vol 251 no 1-2 pp 538ndash543 1998

[157] I Callebaut D Gilges I Vigon and J-P Mornon ldquoHYR anextracellular module involved in cellular adhesion and relatedto the immunoglobulin-like foldrdquo Protein Science vol 9 no 7pp 1382ndash1390 2000

[158] H J Gilbert ldquoCellulosomes microbial nanomachines that dis-play plasticity in quaternary structurerdquoMolecular Microbiologyvol 63 no 6 pp 1568ndash1576 2007

[159] A Peer S P Smith E A Bayer R Lamed and I BorovokldquoNoncellulosomal cohesin- and dockerin-like modules in thethree domains of liferdquo FEMS Microbiology Letters vol 291 no1 pp 1ndash16 2009

[160] M Wagner ldquoMicrobiology conductive consortiardquo Nature vol526 no 7574 pp 513ndash514 2015

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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International Journal of

Microbiology

Archaea 9

Table 3 Nomenclature

Central methanogenic pathwayFmd Formylmethanofuran (CHO-MFR) dehydrogenaseFtr Formylmethanofuran-tetrahydromethanopterin (H

4MPT) formyltransferase

Mch N5N10-methenyl-H4MPT cyclohydrolase

Mtd F420

H2-dependent methylene -H

4MPT dehydrogenase

Mer N5N10-methylene-H4MPT reductase

Mtr N5-methyl-H4MPTcoenzyme M (CoM) methyltransferase

Mcr Methyl coenzyme M (CH3-CoM) reductase

Mdh Methanol dehydrogenaseFaeHps Fusion protein of formaldehyde activating enzyme hexulose-6-phosphate synthaseMetF N5N10-methylene tetrahydrofolate (H

4HF) reductase analogue

Electron transportMvh F

420-nonreducing hydrogenase

Vho Methanophenazine-dependent hydrogenaseFpo F

420H2phenazine oxidoreductase

Fqo F420

H2quinone oxidoreductase

Hdr Coenzyme B-coenzyme M heterodisulfide (CoB-S-S-CoM) reductaseFrh F

420-dependent hydrogenase

Ech Ferredoxin-dependent hydrogenaseMePhMePhH

2Methanophenazine

MQMQH2

MenaquinoneCyt b Cytochrome bCyt c Cytochrome cMHC Multiheme c-type cytochromeRieske Rieske cytochrome b complexOrf7 Pseudoperiplasmic b-type cytochromeNar Nitrate reductaseNap Periplasmic nitrate reductaseNrf Nitrite reductase

22 Methyl Coenzyme M Reductase (Mcr) The enzymaticreaction of a purified Mcr from ANME has not been mea-sured to date The key question is whether a methanogenicMcr can explain the observed in situ AOM rates or if theMcr of ANME is structurally altered There are three mainfactors to be considered the kinetic limitations as definedby enzyme properties (ie half-maximal activity at a specific119870119872value) the thermodynamic constraints of the enzymatic

reaction and the maximal or ambient rate of the enzymaticreaction For the Mcr from Methanothermobacter marbur-gensis kinetic parameters have been determined to illustratethe reversibility of reaction (1) In themethanogenic reactionthe purified Mcr isoform I [55] catalyzes the production ofmethane with a 119881max of 30Umgminus1 and a 119870

119872of 5mM for

CH3-CoM The same (methanogenic) enzyme was able to

oxidize methane to CH3-CoM with a rate of 00114Umgminus1

and a 119870119872for methane of sim10 mM [56]

To answer if the observed AOM rates are in accordancewith the measured methane oxidation rate for the purifiedMcr enzyme from M marburgensis the Mcr activity duringAOM is needed Estimates for AOM rates in terms of activity(per cell dry mass) range between lt1 and 20mmol dayminus1 andg cell dry massminus1 [56ndash66] This equals an activity of 07 to

sim14 nmol min and mg cell dry massminus1 About half of the celldry mass is protein so the activity for the ANME archaeawould approximate 14 to 28 nmol min and mg proteinminus1 Toestimate the activity per mg of Mcr the proportion of Mcrto cellular protein is needed It was reported that 7 of theprotein of ANMEmicrobial mats from the Black Sea [67 68]and 104 of peptides fromHydrate Ridge mesocosms is Mcr[51] As these were no pure cultures the actual percentagesof Mcr in ANME cells may be higher Transcriptome data forANME-2d [43] showed that about 19 of the total transcriptswere derived from the mcr genes indicating (though notdemonstrating) a highMcr content in ANME-2d Estimatingthat 10 of the cellular protein would be Mcr the specificactivity of the enzymewould be between 14 and 280 nmolminand mg Mcr proteinminus1 which is up to 25 times higher thanthe measured reverse reaction rate of the M marburgensisenzyme (sim12 nmol min and mg Mcrminus1 [56]) However thereverse reaction rate of the M marburgensis Mcr was deter-mined under nonsaturating substrate conditions and wastherefore not possibly representing the true maximum rateNevertheless both reverse reaction rates are in the same orderof magnitude other than the forward reaction of 30000ndash100000 nmol min and mgMcrminus1 Thus it seems that the

10 Archaea

H2

CoM-SH

Mch

Mer

Mtd

Ftr

Fmd

Mcr

MPh

MPhH2

MPh

MPh

MPhH2

MtrVho

CoM-SH

CoB-S-S-CoM

CoB-SHHdrDE

Fpo

Fpo

Ech

CH3-CoM

2H+

H2

2H+

2H+

H+

MPhH2

CH4

CH3-H4MPTF420H2

F420

F420H2

F420

CH2=H4MPT

CHequivH4MPT

CHO-H4MPT

CHO-MFR

CO2

Fdred

Fdox

H2O

2Na+

CH3-OH

Figure 3 Methylotrophic methanogenesis in cytochrome containingMethanosarcina barkeri Black lines represent presence of conversionsand red lines indicate reversal of the hydrogenotrophic methanogenic pathway See Table 3 for nomenclature

Mcr in ANME may have similar catalytic properties as themethanogenic enzyme and that the high amount of Mcr permg total cell biomass in ANME may in part compensates forthe apparently relatively slow catalysis

Considering the thermodynamic constraints the Gibbsfree energy change of the Mcr forward reaction under stan-dard conditions is around minus30 kJmolminus1 [56] Therefore thereverse reaction is endergonic under standard conditions andwill not proceed However highmethane concentrations (105according to reaction (1) [69 70]) may lead to a favourablechange in the Gibbs free energy in the direction of AOMHigh methane partial pressure prevails at many habitatswhere AOM has been detected The solubility of methaneat atmospheric pressure is only 13mM [71] Consequentlyincreased AOM rates were reported upon pressurizing sam-ples of different geographical origin [59 60 72 73] The 119870

119872

of Mcr of M marburgensis for methane was determined ator above 10mM and reported 119870

119872values of S-AOM varied

from (at least) 11mM [74] a few mM [57] to even 37mM(equivalent to 3MPa CH

4) [58] Thus high pressure and

therefore high concentrations of methane in the natural habi-tat accelerate the oxidation rate of methane by Mcr Futureresearch to accurately determine119870

119872values and rates forMcr

at differentmethane partial pressures is however neededThismay seem difficult but microbial activity measurements at insitu methane partial pressure were shown to be successful inthe laboratory [75]

It was suggested that the Mcr reaction is the rate limitingstep in reverse methanogenesis [56] which is in line withthe above described challenges Supporting these findingsthere does not seem to be a major change in the aminoacid structure that determines whether the backwards or theforward reaction of Mcr is favoured Amino acid alignments[67] and the crystal structure of ANME-1 Mcr [76] indicatedhigh overall similarity of the methanogenic and methan-otrophic enzyme and unambiguously demonstrated that

Archaea 11

MHC

MHCS-layer

2H+

minuse

cyt b

Mch

Mer

Mtd

Ftr

Fmd

Mcr

MPh

HdrABC

MPh

MHC

MHC

MPh

CoB-S-S-CoM

CoB-SH

CoM-SH

HdrDE

Mtr

Fpo

Fpo

Rnf

MPhH2

MPhH2

MPhH2

MPhH2

CH4

CH3-CoM

CH3-H4MPT

F420H2

F420

F420H2

F420

CH2=H4MPT

CHequivH4MPT

CHO-H4MPT

CHO-MFR

CO2

Fdred

Fdox

H2O

2Na+

MPh

minuse

S-layer

MHC

SRB 2H+

2H+

2Na+

minuse

minuse

minuse

Figure 4 Methanotrophic pathway during S-AOM by ANME-2a [42] Red lines indicate reversal of the hydrogenotrophic methanogenicpathway See Table 3 for nomenclature

CoM-SH and CoB-SH are substrates of the methanotrophicenzyme However several posttranslational modifications ofamino acids were different betweenmethanogens andANMEarchaea and the cofactor F

430(the prosthetic group of Mcr)

is modified in ANME-1 but not in ANME-2 or ANME-3archaea [51 63 67 68 76 77] Furthermore ANME-1 seemsto lack the noncatalytic proteinDdomain of themcr gene thatis present in all other methanogens and methanotrophs butof which the function is unknown (IPR003901 Table 2) [51]A metabolically engineered Methanosarcina acetivorans wasable to convert methane and CO

2to acetate with a plasmid

containingMcr derived from ANME-1 [78] It is thus unclearif only thermodynamic constraints and the abundance ofMcrensureAOMactivity or if also specificmodifications canhavean effect on the reverse activity of Mcr

23 Methane Oxidation by Methanogens Pure cultures ofmethanogens were not able to oxidize methane under highmethane and low hydrogen concentrations (reviewed in[79 80]) Methanogens are only able to oxidize methaneduring net methane production [81] Labeled methane addi-tion (13C or 14C) to pure cultures of methanogens showedproduction of labeled CO

2during net methane production

This characteristic was confirmed with several pure culturesof methanogens [82ndash84] The process was called ldquotracemethane oxidationrdquo (TMO) since the CO

2was formed in

trace amounts relative to the methane produced [83] It isnot clear if TMO is due to the reported reversibility ofindividual enzymes [66] or if it is an active microbial processfrom which energy can be conserved TMO was speculatedto be an active metabolic process for three reasons (1)the amount of methane oxidized varied between differentspecies of methanogens grown on the same methanogenicsubstrate (2) the amount ofmethane oxidized varied betweendifferent methanogenic substrates and (3) TMO productsvaried between different methanogenic substrates [83 84]For instance when grown on acetate Methanosarcina ace-tivorans produced labeled acetate from labeled methaneWhen grown on carbon monoxide it produced both labeledacetate and methyl sulfides from labeled methane [84] Dur-ing hydrogenotrophic and methylotrophic methanogenesisTMO mainly produced CO

2from labeled methane [83]

However in contrast with AOM TMO rates never exceededmethanogenesis rates even during long-term incubationwith methane and sulfate [85] It seems that methanogensare not able to conserve energy from TMO even under

12 Archaea

Mch

Mer

Mtd

Ftr

Fmd

Mcr

MQ

MQ

EchHdrFrh

3MQ

HdrABC

MQ

cyt b Mtr

NrfH

cyt c

NrfA

CoB-S-S-CoM

CoB-SH

CoM-SH

HdrDE

HCOIIHCOIINapHOrf7

NarGH

S-layer

Fqo

Fqo

3H+

3H+

4H+

CH4

CH3-CoM

CH3-H4MPT

F420

F420H2

F420

F420H2

CH2=H4MPT

CHequivH4MPT

CHO-H4MPT

CHO-MFR

CO2

Fdred

Fdox

H2O

2Na+

NH4+

NO2minus

NO2minus

NO3minus

3MQH2

MQH2

MQH2

MQH2eminus

eminus

Rieske

Figure 5 Methanotrophic pathway during N-AOM by ldquoCaM nitroreducensrdquo MPEBLZ (ANME-2d) [43] Red lines indicate reversal of thehydrogenotrophic methanogenic pathway See Table 3 for nomenclature

thermodynamically favourable conditions TMOoccurs bothin absence and presence of an external electron acceptor andonly during net methanogenesis It is therefore most likelycaused by the reported back flux of individual enzymes of themethanogenic pathway [66]

TMO also occurred in granular sludge and in freshwaterand terrestrial samples These mixed communities showedhigher TMO rates than pure cultures reaching up to 90of the methane produced [27 85ndash87] TMO should thereforebe carefully considered in the experimental setup and inter-pretation of results when studying AOM in environmentalsamples especially since TMO rates were like AOM stim-ulated by a high methane partial pressure [72 86 88] Sulfatereduction was also stimulated by higher methane partialpressures [85]Thus a highmethane partial pressure can havea stimulating effect on methane oxidation (either throughAOM or TMO) and SR which could be unrelated to S-AOMMoreover addition of iron sulfate (FeSO

4) or manganese

oxide (MnO2) also increased TMO rates [86] Therefore

methane-dependent SR and sulfate- or metal-dependentmethane oxidation are not necessarily indications for AOMin mixed cultures In conclusion when studying complexldquoblack-boxrdquo communities only net methane oxidation isproof for AOM activity

24 Methane Production by ANME The process of S-AOMis at the energetic limit for sustaining life with estimates

of Gibbs free energy yields between minus18 and minus35 kJmolminus1[45 79 89ndash91] and doubling times between 11 and 75months [65 72 73 92 93] Since S-AOM operates close toits thermodynamic equilibrium the reversibility of individualenzymes leads to measurable back flux producing methane(3ndash7 of AOM) and sulfate (55ndash13 of SR) during S-AOM [66] This ldquotrace methane productionrdquo was observedin situ [11] and in sediment slurries with methanogenesisaround 10 [62 94] or even as high as 50 of AOM [34]When sulfate becomes depleted Gibbs free energy yieldsbecome even lower (less negative) and the enzymatic backflux becomes even more apparent up to 78 of net AOM[95] Previous measurements of 13C depletion below thesulfate-methane transition zone (SMTZ) ofmarine sedimentsthat were thought to be indicative for methanogenesis couldtherefore instead be attributed to the back flux of AOM [95]The occurrence of ANME-1 without a bacterial partner insediment layers where sulfate was depleted was previouslyinterpreted as evidence that ANME-1 perform methanogen-esis [24] but in light of the above it could also indicate AOMThere are indeed reports of AOM activity below the SMTZin the methanogenic zone [96ndash99] In contrast AOM withother electron acceptors than sulfate operates far from thethermodynamic equilibrium with Gibbs free energy changesbetween minus5172 and minus8414 kJmolmethaneminus1 (Table 1) Herethe reported anaerobic back flux [66] is expected to be lessapparent

Archaea 13

MetFMer

Mdh

FaeHps

SRB

MHC

Mch

Mtd

Ftr

Fmd

McrMQ

Hdr1

MQ

MHC

Hdr2

CoB-S-S-CoMCoB-SHCoM-SH

Mtr

Fqo

CH4

CH3-CoMCH3-OH

CH2O CH3-H4MPT

F420F420H2

CHO-H4MPT

CHO-MFR

CO2

FdredFdox

H2O

eminus

eminus

CHequivH4MPT

CH2=H4MPT

xH+

H2

MQH2

MQH2

+xNa

Figure 6 Methanotrophic pathway during S-AOM by ANME-1 [40 41] Red lines indicate reversal of the hydrogenotrophic methanogenicpathway grey lines represent absence of conversions and blue lines indicate a bypass of the hydrogenotrophic methanogenic pathway SeeTable 3 for nomenclature

In laboratory incubations researchers were not ableto stimulate net methanogenesis through addition ofmethanogenic substrates to AOM performing sediments[62 94] In two cases researchers were successful [23 100]In one of these cases sediment-free long-term AOM enrich-ments that were dominated by ANMESRB were incubatedwith methanogenic substrates The resulting methanogenicactivity most likely came from the enrichment of a minorpopulation of methanogens (up to 7permil of total archaealgene tag sequences) that was present in the inoculum[100] In the second study methanogenic substrates wereadded to ANME-1 and ANME-2 dominated microbialmat samples and methanogenesis also occurred [23]However no information was provided for the total archaealcommunity composition which makes it impossible toexclude methanogens as the responsible organisms

Genomic information of ANME also gives indication onpotential methanogenic routes Considering methylotrophicmethanogenesis no gene homologues catalyzing methyltransfer from methylated substrates to coenzyme M weredetected in ANME (Table 2) [40ndash43] Acetoclastic methano-genesis needs either the AMP- and ADP-forming acetyl-coenzyme A synthetase (Acs and Acd resp) or proceedsvia acetate kinase and phosphotransacetylase In ANME-1only the alpha subunit of a homologue of Acd was expressed

during AOM [41] but in an ANME-1 proteome of activeAOM biomass no Acd was detected [40] The Acd gene wasdetected in the single-aggregate genome and transcriptomeof ANME-2a [42] and in ANME-2d [43] However genedomains for Acd are also present in methanogens unableto use acetate as substrate (Table 2) and are probably usedfor lipid metabolism In hydrogenotrophic methanogenesishydrogenases are used to replenish reduced coenzyme B andto recycle oxidized F

420(discussed in Section 21) Both the

cytoplasmic Mvh complex and the membrane bound Vhowere not present in ANME-2d [43] and not expressed inANME-2a (which also lackedEch andF

420-dependent hydro-

genase (Frh)) [42] making hydrogenotrophic methanogen-esis unlikely In ANME-1 both the cytoplasmic HdrABCand MvhD are present as well as homologues of Frh andEch but these were lacking catalytic subunits [40 41] Aniron hydrogenase was found in both ANME-1 metagenomesbut not in any other methanotroph or methanogen [41](Table 2) This iron hydrogenase domain is part of a genethat is 70 identical to a [FeFe]-hydrogenase of Dehalococ-coides mccartyi [FeFe]-hydrogenases catalyze reversible H

2

production and uptake but these were presumed to have nokey function in AOM [41] However the gene is part of a genecluster of three genes containing a 51 kDaNADH ubiquinoneoxidoreductase subunit (Table S3) which could potentially

14 Archaea

form a complex that generates a proton motive force duringhydrogen oxidation Therefore hydrogenotrophic methano-genesis by ANME-1 cannot be excluded yet

3 Respiration during AnaerobicOxidation of Methane

For netAOMtooccur an external electron acceptor is neededwhich results in a favourable Gibbs free energy change(Table 1) A variety of terminal electron acceptors have beendiscovered for AOM which will be discussed in Sections 31ndash33

31 Sulfate-Dependent AOM During sulfate-dependentAOM electrons are transferred from ANME to the sulfate-reducing bacterial partner Previous work tried to uncoverhow electrons were transferred and most compoundsthat could act as interspecies electron carrier (IEC) wereexcluded to be involved in AOM such as methanolhydrogen methanethiol acetate and carbon monoxide[57 61 62 94 101] Indications that polysulfide could actas IEC were found and ANME-2a archaea were thoughtto perform both AOM and sulfate reduction (SR) [102]However in marine seeps hydrothermal vents and othernondiffusion based sediments AOM rates are high andANME form close associations with SRB in dense aggregates[1 5 103 104] In these aggregates the high AOM ratescould not be explained by diffusion of an IEC whichmade direct interspecies electron transfer (DIET) a moreplausible mechanism [89 105 106] Cellular activities wereindependent of aggregate type and distance between thesyntrophic partners within the aggregate which is bestexplained by DIET [107] DIET is normally achieved usingmultiheme cytochrome c proteins (MHCs) and conductivepili (ie nanowires) which are mainly found in bacteriathat donate electrons extracellularly such as Geobacter andShewanella species [108ndash114] Indeed ANME-2a from seep-sediment samples seem to transfer electrons directly usinglarge MHCs [107] which were found in the metagenome ofANME-2a [107 115] ANME-1 and the associated bacterialpartner also overexpressed genes for extracellular MHCsduring AOM [116] which complements previous findings oftranscription [41] and translation [40] of ANME-1 relatedMHC genes Domain based (meta)genome analysis showsthe high abundance of MHC domains in different ANMEas compared to methanogens (Table 2) A recently isolatedbacterial partner of ANME-1 (ldquoHotSeep-1rdquo) also producedcell-to-cell connections using pili-derived nanowires [116]which explain previously detected Deltaproteobacteria-related pili genes in an AOM sample dominated by ANME-1[40]

How ANME use MHCs to donate electrons to thebacterial partner is not yet clear For ANME-2a the electronsprobably flow from methanophenazine to membrane inte-grated di-heme cytochromes (cytochrome 119887119887

6) that transfer

the electrons through the S-layer via MHCS-layer fusionproteins to extracellular MHCs (Figure 4) (Figure 4 in[107]) Exosortases and archaea-specific archaeosortases are

involved in export of cell surface proteins such as the archaealS-layer proteins These transpeptidases recognize specificsignal peptides for protein- sorting that is archaeosor-tase A recognizes the protein-sorting signal PGF-CTERMand archaeosortase C recognizes the PEF-CTERM signal[117] Both ANME-2a and 2d show presence of di-hemecytochromes archaeosortase A (IPR014522) archaeosortaseC (IPR022504) and other exosortase gene domains (Table 2)Moreover some genes of both ANME-2a and 2d containedboth MHC and PGF or PEF-CTERM domains Lastly somegenes of both ANME-2a and 2d contained both MHC andS-layer domains [107] indicating that these could form theabove-stated MHCS-layer fusion proteins

ANME-1 do not seem to have di-heme cytochromes(Table 2) [115] PGF related domains (IPR026453 andIPR026371) were present in all ANME but PEF-CTERM(IPR017474) related domains were absent in ANME-1 (Table 2) Moreover ANME-1 lacked archaeosortaseA (IPR014522) and archaeosortase C gene domains(IPR022504) as well as some other exosortases (Table 2) Asearch in NCBIrsquos conserved domains database (CCD [118])and the EMBL InterPro database [119] of amino acidssequences of all genes from ANME metagenomes thatcontain MHC domains showed that ANME-1 did not haveany protein-sorting signal or S-layer domains within thesegenes In fact S-layer domains were completely absent inANME-1 (Table 2) These results imply that ANME-1 do notuse di-heme cytochromes for electron transfer to MHCsand do not produce an S-layer (Figure 6) This implies thatANME-1 use a different mechanism for DIET and couldexplain the need for less MHCs by ANME-1 (Table 2)and the observed pili-derived nanowires produced by thebacterial partner [116] The genome of the bacterial partnerof ANME-1 (ldquoHotSeep-1rdquo) encoded 24 c-type cytochromesof which 10 were similar to secreted MHCs of Geobactersulfurreducens [120] which also uses pili for DIET [121]

In the case of ANME-2a it is not clear if pili (ienanowires) were formed during AOM It was previouslythought that electrically conductive pili seemed to be aprerequisite for current production andDIET [122 123] evenwhen syntrophs were closely associated [124] such as withinANME-2SRB aggregates However conductive materialssuch as granular activated carbon were shown to be ableto substitute pili in DIET [124] Although in previous workconductive materials such as phenazines or humic acids didnot seem to stimulate AOM rates [61] in a recent study AOMwas decoupled from SR using artificial electron acceptors[125] This indicates that conductive materials can indeedreplace pili and that ANME-2ab could possibly couple AOMto metal oxide reduction or any other suitable electronacceptor (discussed in Section 33) However it needs to beproven if in ANME-2SRB aggregates no pili are formed andif the mechanism of DIET is fundamentally different fromANME-1

As for the polysulfide shuttling theory [102] canonicalgenes for dissimilatory sulfate reduction such as adenylyl-transferase (Sat) APS reductase (Apr) and dissimilatorysulfite reductase (Dsr) which are all present in the sulfate-reducing archeon A fulgidus (Table S2) were not found in

Archaea 15

metagenomes of ANME-1 [41] and ANME-2a (Table S1)The enzymes Sat and Dsr were also not detected in ANMEcells using fluorescent immunolabelling [126] ANME-1 werepreviously found to encode most proteins for assimilatorysulfate reduction [41] ANME-2d only harbor gene domainsthat encode Sat and assimilatoryATP sulfurylase APS kinaseand sodiumsulfate symporters which were not present inANME-2a (Table S1) It is therefore clear that at least ANME-2a cannot donate electrons to sulfate but need to donateelectrons to a sulfate-reducing partner

32 Nitrate-Dependent AOM Unlike during S-AOMANME-2d that perform N-AOM do not need a bacterialpartner but transfer electrons directly to a membrane boundnitrate reductase (Nar) [28 43] (Figure 5) The ANME-2dgenomes contain most MHCs found so far in archaea[107 115] (Table 2) Of the 87 proteins that contained aCxxCH binding motif of which 43 seemed to be true c-typecytochromes [115] 23 CxxCH motif-encoding transcriptswere expressed during N-AOM [43] The function of mostof these MHCs is not known but they are likely involvedin nitrate reduction since c-type cytochromes are capableof operating in the wide range of redox potentials thatcouple nitrate reduction (11986401015840 (NO

3

minusNO2

minus) = +433mV) andmethane oxidation (11986401015840 (CoM-S-S-CoBCoM-SH+CoB-SH)= minus143mV) [43] Nitrate as terminal electron acceptor inanaerobic respiration has been found in halophilic andthermophilic archaea [127] The nar gene cluster of ldquoCaM nitroreducensrdquo comprises several genes including thecatalytic alpha (NarG molybdopterin) and beta (NarHiron sulfur cluster) subunit of nitrate reductase [28 43] The(halo)archaeal nitrate reductase complex was reported to belocated at the extracellular side of the cytoplasmic membrane[128] and in most archaea associated with the cytoplasmicmembrane via NarM [129] The ldquoCa M nitroreducensrdquogenome does not encode NarM but encodes a TAT signalpeptide at the N-terminus of NarG for translocation acrossthe cytoplasmic membrane [28 43] Interestingly theNarG and NarH seem to have been acquired from theProteobacteria via lateral gene transfer [28]

It is not yet clear at which point in themetabolism ldquoCaMnitroreducensrdquo conserves energy During reverse methano-genesis N5-methyl-H

4MPTCoM methyltransferase (Mtr)

dissipates the sodium ion potential across the cytoplasmicmembrane so subsequent steps inN-AOMhave to be coupledto the build-up of a proton or sodium motive force to makethe overall process energetically favourable The analysis ofan environmental genome [43] indicated presence of severalprotein complexes involved in electron transport and energyconservation Electrons that enter the respiratory chain couldbe transported by membrane-integral electron carriers (iemenaquinones) to a Rieske-cytochrome b complex that mayuse cytochrome c as electron acceptor This in turn maybe the electron donor for the unusual nitrate reductasecomplex Energy conservation is thermodynamically andmechanistically feasible at the F

420H2dehydrogenase and the

Rieske-cytochrome b complex (Figure 5) (Figure 2 in [43])Further investigations are needed to determine whether

nitrate reductase is also involved in energy conservationbut this working hypothesis is strengthened by the presenceof cupredoxin multicopper oxidase domains and coppercenters related to the periplasmic domain of cytochrome coxidase subunit II (HCO II) in ANME-2d (Table S1)

BothANME-2d genomes discussed here are derived frombioreactors where ldquoCaM nitroreducensrdquo formed syntrophiccultures with nitrite scavenging bacteria either with ldquoCaKuenenia stuttgartiensisrdquo (anammox bacteria) [28] or ldquoCaMethylomirabilis oxyferardquo (NC10 bacteria) [31 43]This indi-cated that ANME-2d could be dependent on those bacteriafor nitrite removal However in addition to nitrite ldquoCa Mnitroreducensrdquo may also produce ammonium during AOMby a pentaheme c-type nitrite reductase (NrfAH) encodedin the genome [43] (Figure 5) In fact both ANME-2dgenomes contain domains for NrfA (IPR003321) and NrfH(IPR017571) (Table S1) implying that both ANME-2d speciesare not necessarily dependent on a nitrite scavenger duringAOM

33 Metal-Dependent AOM Evidence for metal-dependentAOM was found in marine sediments [130ndash132] In non-marine environments AOM was also hypothesized to becoupled to iron andor manganese oxide reduction [26 133ndash136] or even coupled to the reduction of humic acids [136137] However organisms responsible for metal-dependentAOM were not identified in these studies It was speculatedthat JS1 bacteria methanogenic archaea and Methanohalo-biumANME-3 could be responsible for iron-dependentAOM [138] Other researchers speculated that either ANME-1 or MethanococcoidesANME-3 together with a bacterialpartner were responsible for manganese-dependent AOM[139] In another study where AOM was decoupled from SRANME were not detected which leaves open the possibilitythat other archaeal clades besides ANME could performmetal-dependent AOM [131]

It was recently observed that cultures containing ANME-2a and ANME-2c could decouple AOM from SR in thepresence of artificial electron acceptors humic acids andsoluble iron [125] which confirmed previous findings ofAOM not connected to SR in ANME dominated samples[140] This suggests that ANME-2 could also use insolublemetal oxide minerals as electron acceptor during AOM TheMHCs of ANME-2ab and ANME-2d are larger than thosein Shewanella and Geobacter species [107] which are knownto be capable of extracellular electron conduction It wasspeculated that both ANME-2d and Ferroglobus placidus ofwhich the latter can perform solid iron reduction can foldCxxCHmotifs into extracellular conductive structures or pili[115] Many of the MHCs of ANME-2d were not expressedwhen grown with nitrate (discussed in section 32) implyingthat these are not needed for nitrate reduction [43] Thisstrengthens the hypothesis that also ANME-2d could coupleAOM to reduction of other extracellular electron acceptorsthan nitrate and even to insoluble metal oxides Indeedrecent work showed that ANME-2d could be involved inAOM coupled to chromium(VI) reduction [141] (Table 1reaction (5)) and in AOM coupled to the reduction of soluble

16 Archaea

iron and insoluble ferrihydrite and birnessite minerals [142](Table 1 reactions (3) and (4)) ANME-2d could even possiblydonate electrons to a bacterial partner besides nitrate-richenvironments ANME-2d archaea have been found inwells ofan aquifer where sulfate and methane concentrations overlap[143] Moreover ANME-2d was the only clade detected insediments of a freshwater lake where S-AOM occurred [144]Sulfate concentrations in these studies were low but above1mM and thus higher than the lowest reported concen-trations for S-AOM to occur [145 146] Lastly sequencesof ANME-2d were relatively more abundant in freshwatersediments fed with methane and sulfate than in sedimentsfed with onlymethane or only sulfate and noN-AOMactivitywas detected when fed with nitrate and methane [27] Theseindications hold promise that direct experimental evidencefor sulfate-dependent AOM by ANME-2d could be found inthe future

TheANME-1 genome contains fewerMHCgene domainsas compared to ANME-2a and ANME-2d and some otherarchaea such as somemethylotrophicmethanogens (Table 2)and some members of the Archaeoglobales [115] The MHCsof ANME-1 also have a smaller heme count as compared toother ANME and some other archaea with the largest beingan octaheme cytochrome [107] Each hemewithin aMHChasits own redox potential and therefore structurally differentMHCs represent a large range of redox potentials that canbe used for bioenergetic electron transfer (reviewed in [147])For instance metal oxide reduction in Shewanella oneidensisMR-1 is catalyzed by a chain of a tetraheme (CymA) twodecaheme (MtrA and MtrB) and eventually extracellulardecaheme cytochromes OmcAMtrC that reduce the ironminerals [121 148 149] In Geobacter sulfurreducens ironmineral reduction seems to be catalyzed by the tetrahemecytochrome OmcE and hexaheme cytochrome OmcS trans-ferring electrons from the outer membrane to type IV pilithat transmit the electrons to iron minerals [121 150 151]Since ANME-1 lack MHCs of the correct size and lack genedomains for pili production [116] they seem unable to reduceminerals via both mechanisms present in Shewanella andGeobacter It can therefore be speculated that ANME-1 areless versatile in electron acceptor use and are not able toreduce solid metal oxides However DIET mechanisms arestill not well understood and the true differences betweenMHCs of different ANME types need to be investigated usingbiochemical methods This would allow uncovering the truecapabilities concerning DIET

34 Menaquinones and Methanophenazines ANME-2a en-coded a protein with a domain specific for PhzF which is anenzyme involved in phenazine biosynthesis in Pseudomonasfluorescens [152 153] The respective gene is not present in allmethanophenazine containing methanogens (in our genomecomparison only inM acetivorans andM formicica Table 2)so it is unclear whether this enzyme is really involved inmethanophenazine biosynthesis It is however likely thatANME-2a use methanophenazines in their respiratory chainsince gene domains for menaquinone biosynthesis wereabsent (Table 2) ldquoCa M nitroreducensrdquo probably uses

menaquinones as membrane-integral electron carrier sinceenvironmental genomes [28 43] encoded the futalosine(mqn) biosynthesis pathway as reported for Archaeoglobusfulgidus [154] (Table 2) Moreover ldquoCa M nitroreducensrdquoenrichment cultures showed absence of methanophenazines[43] ANME-1 also contained gene domains formenaquinonebiosynthesis via the futalosine (mqn) biosynthesis pathway(Table 2) Indications for a quinone biosynthesis pathwayin ANME-1 were previously found to be weak since onlysome of the Ubi homologues of the oxic ubiquinone biosyn-thesis pathway were detected [41] but the futalosine (mqn)biosynthesis pathway was overlooked in that particular anal-ysis Additionally ANME-1 have Fqo homologues similarto Archaeoglobus fulgidus [44] and expressed the catalyticsubunit FqoF [41] However since the phenazine biosynthesisdomain PhzF was also present in the ANME-1 genomes(Table 2) and Fpo and Fqo are homologues we cannotconclude on genomic information alone which redox shuttleis used by ANME-1 during AOM If ANME-1 would usemenaquinones this would have implications for subsequentelectron transfer to MHCs since methanophenazine (1198640 =minus165mV) [155] and menaquinone (1198640 = minus80mV) [156] havedifferent redox potentials

35 Cell Adhesion Some gene domains involved in cel-lular adhesion were more abundant in ANME than inmethanogens (Table 2) especially in ANME-2a and ANME-1that are known to form syntrophic interactions for electrontransfer during respiration These domains include HYR(IPR003410) and CARDB domains (IPR011635) that bothhave a direct role in cellular adhesion [157] (Table 2) Interest-ingly also domains related to the cellulosome of Clostridiumspecies termed dockerin and cohesin were highly abundantin both ANME-1 and ANME-2a as compared to ANME-2dand methanogens together with many carbohydrate bindingdomains (Table 2) In Clostridium species dockerin andcohesin form an anchor to the bacterial cell wall that containsa scaffold with cellulose-degrading enzymes and a carbohy-drate bindingmodule that binds cellulose altogether formingthe cellulosome [158] These domains have been found in alldomains of life irrespective of cellulose utilization but thefunction of such proteins outside of the cellulosome is notknown [159]Therefore dockerin cohesin and carbohydratebinding domains in ANME could hypothetically form aconstruct that binds to carbohydrates and could possibly havea function in cell-to-cell contact or MHC adhesion but thisneeds further investigation

4 Future Challenges

Advances in (meta)genomics transcriptomics and pro-teomics have produced the valuable metabolic blueprints ofdifferent ANMEwith hypotheses on how centralmetabolismelectron transport and energy conservation may functionFuture experiments are needed to biochemically demonstratethat these hypotheses are correct

The bottleneck for biochemical studies of ANME isthe lack of pure cultures due to the slow and syntrophic

Archaea 17

growth However the recent milestone discovery of directelectron transfer provides opportunities to grow ANMEas stated previously on electron accepting electrodes (ieanodes) [160] In this way pure or highly enriched culturesof different ANME without their respective syntrophic part-ner could be obtained and MHCs responsible for electricconduction could be biochemically characterized It seemsthat ANME-1 are limited by the size and abundance ofMHCs which could relate to differences in behavior onan anode The partner bacteria of ANME-1 and ANME-2could be investigated on an electron donating electrode (iecathode) with specific focus on the ability to produce pili (ienanowires) Also worth investigating is if besides ANME-2d ANME-2ab could also use insoluble electron acceptorsand if ANME-2d could donate electrons to a bacterialpartner

Another future challenge is to isolate and characterizeMcr from different ANME clades It needs to be investi-gated if Mcr abundance in ANME cells compensates forthe slow reverse activity or if modifications in the Mcrof ANME-1 also contribute to a better reverse activity ofMcr Moreover the effect of methane partial pressure onreaction rates and enzyme kinetics needs to be determined insitu

ANME-1 are potentially able to perform hydrogeno-trophic methanogenesis due to the presence of a hydrogenasein the genome Genetic indications of menaquinones aselectron carrier in ANME-1 and the various cellulosome andcell adhesion related gene domains in all ANME are alsotopics that could be explored further Methanogenic archaeaare likely not able to perform AOM but additional studieson TMO and more genetic modifications to stimulate AOMin methanogens could help in understanding the param-eters needed for AOM to occur Ultimately physiologicalunderstanding of ANME will help to explain the observedecological niche separation of different ANME clades and theoccurrence of ANMEwithout a bacterial partnerThis wouldgreatly enhance our knowledge of themethane cycle in anoxicenvironments

Competing Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors thank Stefanie Berger (RU Nijmegen) for criticalreading of the manuscript This research is supported bythe Soehngen Institute of Anaerobic Microbiology (SIAM)Gravitation grant (024002002) of the Netherlands Ministryof Education Culture and Science and the NetherlandsOrganisation for Scientific Research (NWO) Mike S MJetten was further supported by ERC AG 339880 Eco-MoMand Alfons J M Stams was supported by ERC AG 323009Novel Anaerobes

References

[1] A Boetius K Ravenschlag C J Schubert et al ldquoA marinemicrobial consortium apparently mediating anaerobic oxida-tion of methanerdquo Nature vol 407 no 6804 pp 623ndash626 2000

[2] K-U Hinrichs J M Hayes S P Sylva P G Brewert andE F DeLong ldquoMethane-consuming archaebacteria in marinesedimentsrdquo Nature vol 398 no 6730 pp 802ndash805 1999

[3] V J Orphan C H House K-U Hinrichs K D McKeeganand E F DeLong ldquoMethane-consuming archaea revealed bydirectly coupled isotopic and phylogenetic analysisrdquo Sciencevol 293 no 5529 pp 484ndash487 2001

[4] K-U Hinrichs and A Boetius ldquoThe anaerobic oxidation ofmethane new insights in microbial ecology and biogeochem-istryrdquo inOceanMargin Systems GWefer D Billett D HebbelnB B Joslashrgensen M Schluter and T VanWeering Eds pp 457ndash477 Springer Berlin Germany 2002

[5] K Knittel T Losekann A Boetius R Kort and R AmannldquoDiversity and distribution of methanotrophic archaea at coldseepsrdquo Applied and Environmental Microbiology vol 71 no 1pp 467ndash479 2005

[6] K Knittel and A Boetius ldquoAnaerobic oxidation of methaneprogress with an unknown processrdquo Annual Review of Micro-biology vol 63 pp 311ndash334 2009

[7] V J Orphan K-U Hinrichs W Ussler III et al ldquoComparativeanalysis of methane-oxidizing archaea and sulfate-reducingbacteria in anoxic marine sedimentsrdquoApplied and Environmen-tal Microbiology vol 67 no 4 pp 1922ndash1934 2001

[8] T Losekann K Knittel T Nadalig et al ldquoDiversity andabundance of aerobic and anaerobic methane oxidizers atthe Haakon Mosby Mud Volcano Barents Seardquo Applied andEnvironmentalMicrobiology vol 73 no 10 pp 3348ndash3362 2007

[9] H Niemann T Losekann D De Beer et al ldquoNovel microbialcommunities of the Haakon Mosby mud volcano and their roleas amethane sinkrdquoNature vol 443 no 7113 pp 854ndash858 2006

[10] TNunouraHOida T Toki J Ashi K Takai andKHorikoshildquoQuantification of mcrA by quantitative fluorescent PCR insediments from methane seep of the Nankai Troughrdquo FEMSMicrobiology Ecology vol 57 no 1 pp 149ndash157 2006

[11] B Orcutt A Boetius M Elvert V Samarkin and S B JoyeldquoMolecular biogeochemistry of sulfate reduction methanogen-esis and the anaerobic oxidation of methane at Gulf of Mexicocold seepsrdquoGeochimica et Cosmochimica Acta vol 69 no 17 pp4267ndash4281 2005

[12] V J Orphan W Ussler III T H Naehr C H House K-U Hinrichs and C K Paull ldquoGeological geochemical andmicrobiological heterogeneity of the seafloor around methanevents in the Eel River Basin offshore Californiardquo ChemicalGeology vol 205 no 3-4 pp 265ndash289 2004

[13] M G Pachiadaki A Kallionaki A Dahlmann G J De Langeand K A Kormas ldquoDiversity and spatial distribution ofprokaryotic communities along a sediment vertical profile ofa deep-sea mud volcanordquo Microbial Ecology vol 62 no 3 pp655ndash668 2011

[14] I Roalkvam H Dahle Y Chen S L Joslashrgensen H Haflidasonand I H Steen ldquoFine-scale community structure analysis ofANME in Nyegga sediments with high and low methane fluxrdquoFrontiers in Microbiology vol 3 p 216 2012

[15] K Yanagawa M Sunamura M A Lever et al ldquoNiche separa-tion of methanotrophic archaea (ANME-1 and -2) in methane-seep sediments of the Eastern Japan Sea offshore JoetsurdquoGeomicrobiology Journal vol 28 no 2 pp 118ndash129 2011

18 Archaea

[16] A Pernthaler A E Dekas C T Brown S K Goffredi TEmbaye and V J Orphan ldquoDiverse syntrophic partnershipsfromdeep-seamethane vents revealed by direct cell capture andmetagenomicsrdquo Proceedings of the National Academy of Sciencesof the United States of America vol 105 no 19 pp 7052ndash70572008

[17] R Hatzenpichler S A Connon D Goudeau R R Malm-strom T Woyke and V J Orphan ldquoVisualizing in situtranslational activity for identifying and sorting slow-growingarchaealminusbacterial consortiardquo Proceedings of the NationalAcademy of Sciences vol 113 no 28 pp E4069ndashE4078 2016

[18] L Maignien R J Parkes B Cragg et al ldquoAnaerobic oxidationof methane in hypersaline cold seep sedimentsrdquo FEMS Micro-biology Ecology vol 83 no 1 pp 214ndash231 2013

[19] V J Orphan C H House K-U Hinrichs K D McKeeganand E F DeLong ldquoMultiple archaeal groups mediate methaneoxidation in anoxic cold seep sedimentsrdquo Proceedings of theNational Academy of Sciences of the United States of Americavol 99 no 11 pp 7663ndash7668 2002

[20] T TreudeM Kruger A Boetius and B B Joslashrgensen ldquoEnviron-mental control on anaerobic oxidation of methane in the gassysediments of Eckernforde Bay (German Baltic)rdquo Limnology andOceanography vol 50 no 6 pp 1771ndash1786 2005

[21] G C Jagersma R J W Meulepas I Heikamp-De Jong etal ldquoMicrobial diversity and community structure of a highlyactive anaerobic methane-oxidizing sulfate-reducing enrich-mentrdquo Environmental Microbiology vol 11 no 12 pp 3223ndash3232 2009

[22] M Blumenberg R Seifert J Reitner T Pape andWMichaelisldquoMembrane lipid patterns typify distinct anaerobic methan-otrophic consortiardquo Proceedings of the National Academy ofSciences of the United States of America vol 101 no 30 pp 11111ndash11116 2004

[23] S Bertram M Blumenberg W Michaelis M Siegert MKruger and R Seifert ldquoMethanogenic capabilities of ANME-archaea deduced from 13C-labelling approachesrdquo Environmen-tal Microbiology vol 15 no 8 pp 2384ndash2393 2013

[24] K G Lloyd M J Alperin and A Teske ldquoEnvironmental evi-dence for net methane production and oxidation in putativeANaerobic MEthanotrophic (ANME) archaeardquo EnvironmentalMicrobiology vol 13 no 9 pp 2548ndash2564 2011

[25] M Takeuchi H Yoshioka Y Seo et al ldquoA distinct freshwater-adapted subgroup of ANME-1 dominates active archaeal com-munities in terrestrial subsurfaces in Japanrdquo EnvironmentalMicrobiology vol 13 no 12 pp 3206ndash3218 2011

[26] R T Amos B A Bekins I M Cozzarelli et al ldquoEvidence foriron-mediated anaerobic methane oxidation in a crude oil-contaminated aquiferrdquo Geobiology vol 10 no 6 pp 506ndash5172012

[27] P H Timmers D A Suarez-Zuluaga M van Rossem MDiender A J Stams and C M Plugge ldquoAnaerobic oxidationof methane associated with sulfate reduction in a naturalfreshwater gas sourcerdquo ISME Journal vol 10 pp 1400ndash14122015

[28] M F Haroon S Hu Y Shi et al ldquoAnaerobic oxidation ofmethane coupled to nitrate reduction in a novel archaeallineagerdquo Nature vol 500 no 7468 pp 567ndash570 2013

[29] H J Mills C Hodges K Wilson I R MacDonald and PA Sobecky ldquoMicrobial diversity in sediments associated withsurface-breaching gas hydrate mounds in the Gulf of MexicordquoFEMS Microbiology Ecology vol 46 no 1 pp 39ndash52 2003

[30] K G Lloyd L Lapham and A Teske ldquoAn anaerobic methane-oxidizing community of ANME-1b archaea in hypersaline gulfofMexico sedimentsrdquoApplied and EnvironmentalMicrobiologyvol 72 no 11 pp 7218ndash7230 2006

[31] A A Raghoebarsing A Pol K T Van De Pas-Schoonen et alldquoA microbial consortium couples anaerobic methane oxidationto denitrificationrdquoNature vol 440 no 7086 pp 918ndash921 2006

[32] S Hu R J Zeng L C Burow P Lant J Keller and Z YuanldquoEnrichment of denitrifying anaerobic methane oxidizingmicroorganismsrdquo Environmental Microbiology Reports vol 1no 5 pp 377ndash384 2009

[33] Z-W Ding J Ding L Fu F Zhang and R J Zeng ldquoSimultane-ous enrichment of denitrifying methanotrophs and anammoxbacteriardquo Applied Microbiology and Biotechnology vol 98 no24 pp 10211ndash10221 2014

[34] R Seifert K Nauhaus M Blumenberg M Kruger and WMichaelis ldquoMethane dynamics in a microbial community ofthe Black Sea traced by stable carbon isotopes in vitrordquoOrganicGeochemistry vol 37 no 10 pp 1411ndash1419 2006

[35] J Ding Z-W Ding L Fu Y-Z Lu S H Cheng and R JZeng ldquoNew primers for detecting and quantifying denitrifyinganaerobic methane oxidation archaea in different ecologicalnichesrdquo Applied Microbiology and Biotechnology vol 99 no 22pp 9805ndash9812 2015

[36] A Vaksmaa C Luke T van Alen et al ldquoDistribution and activ-ity of the anaerobic methanotrophic community in a nitrogen-fertilized Italian paddy soilrdquo FEMS Microbiology Ecology vol92 no 12 2016

[37] P N Evans D H Parks G L Chadwick et al ldquoMethanemetabolism in the archaeal phylum Bathyarchaeota revealed bygenome-centric metagenomicsrdquo Science vol 350 no 6259 pp434ndash438 2015

[38] I Vanwonterghem P N Evans D H Parks et al ldquoMethy-lotrophic methanogenesis discovered in the archaeal phylumVerstraetearchaeotardquo Nature Microbiology vol 1 Article ID16170 2016

[39] P Worm J J Koehorst M Visser et al ldquoA genomic view onsyntrophic versus non-syntrophic lifestyle in anaerobic fattyacid degrading communitiesrdquo Biochimica et Biophysica ActamdashBioenergetics vol 1837 no 12 pp 2004ndash2016 2014

[40] R Stokke I Roalkvam A Lanzen H Haflidason and I HSteen ldquoIntegrated metagenomic and metaproteomic analysesof an ANME-1-dominated community in marine cold seepsedimentsrdquo Environmental Microbiology vol 14 no 5 pp 1333ndash1346 2012

[41] A Meyerdierks M Kube I Kostadinov et al ldquoMetagenomeand mRNA expression analyses of anaerobic methanotrophicarchaea of the ANME-1 grouprdquo Environmental Microbiologyvol 12 no 2 pp 422ndash439 2010

[42] F-P Wang Y Zhang Y Chen et al ldquoMethanotrophicarchaea possessing diverging methane-oxidizing and electron-transporting pathwaysrdquo ISME Journal vol 8 no 5 pp 1069ndash1078 2014

[43] A Arshad D R Speth R M de Graaf H J Op den Camp MS Jetten and C U Welte ldquoA metagenomics-based metabolicmodel of nitrate-dependent anaerobic oxidation of methane byMethanoperedens-like archaeardquo Frontiers inMicrobiology vol 6article1423 2015

[44] S J Hallam N Putnam CM Preston et al ldquoReversemethano-genesis testing the hypothesis with environmental genomicsrdquoScience vol 305 no 5689 pp 1457ndash1462 2004

Archaea 19

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Microbiology vol 14 no 3 pp 292ndash299 2011[46] U Deppenmeier V Muller and G Gottschalk ldquoPathways of

energy conservation in methanogenic archaeardquo Archives ofMicrobiology vol 165 no 3 pp 149ndash163 1996

[47] A-K Kaster J Moll K Parey and R K Thauer ldquoCoupling offerredoxin and heterodisulfide reduction via electron bifurca-tion in hydrogenotrophic methanogenic archaeardquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 108 no 7 pp 2981ndash2986 2011

[48] R K Thauer A-K Kaster H Seedorf W Buckel and RHedderich ldquoMethanogenic archaea ecologically relevant dif-ferences in energy conservationrdquo Nature Reviews Microbiologyvol 6 no 8 pp 579ndash591 2008

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[52] P V Welander and W W Metcalf ldquoLoss of the mtr operon inMethanosarcina blocks growth on methanol but not methano-genesis and reveals an unknown methanogenic pathwayrdquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 102 no 30 pp 10664ndash10669 2005

[53] P V Welander and W W Metcalf ldquoMutagenesis of the C1oxidation pathway inmethanosarcina barkeri new insights intothe MtrMer bypass pathwayrdquo Journal of Bacteriology vol 190no 6 pp 1928ndash1936 2008

[54] M Goenrich R K Thauer H Yurimoto and N KatoldquoFormaldehyde activating enzyme (Fae) and hexulose-6-phosphate synthase (Hps) inMethanosarcina barkeri a possiblefunction in ribose-5-phosphate biosynthesisrdquoArchives ofMicro-biology vol 184 no 1 pp 41ndash48 2005

[55] M Goenrich FMahlert E C Duin C Bauer B Jaun and R KThauer ldquoProbing the reactivity of Ni in the active site of methyl-coenzyme M reductase with substrate analoguesrdquo Journal ofBiological Inorganic Chemistry vol 9 no 6 pp 691ndash705 2004

[56] S Scheller M Goenrich R Boecher R K Thauer and BJaun ldquoThe key nickel enzyme of methanogenesis catalyses theanaerobic oxidation of methanerdquo Nature vol 465 no 7298 pp606ndash608 2010

[57] K Nauhaus A Boetius M Kruger and F Widdel ldquoIn vitrodemonstration of anaerobic oxidation of methane coupled tosulphate reduction in sediment from amarine gas hydrate areardquoEnvironmental Microbiology vol 4 no 5 pp 296ndash305 2002

[58] Y Zhang J-P Henriet J Bursens and N Boon ldquoStimulationof in vitro anaerobic oxidation of methane rate in a continuoushigh-pressure bioreactorrdquo Bioresource Technology vol 101 no9 pp 3132ndash3138 2010

[59] M Kruger T Treude H Wolters K Nauhaus and A BoetiusldquoMicrobial methane turnover in different marine habitatsrdquoPalaeogeography Palaeoclimatology Palaeoecology vol 227 no1ndash3 pp 6ndash17 2005

[60] C Deusner V Meyer and T G Ferdelman ldquoHigh-pressuresystems for gas-phase free continuous incubation of enrichedmarinemicrobial communities performing anaerobic oxidationof methanerdquo Biotechnology and Bioengineering vol 105 no 3pp 524ndash533 2010

[61] K Nauhaus T Treude A Boetius and M Kruger ldquoEnviron-mental regulation of the anaerobic oxidation of methane acomparison of ANME-I and ANME-II communitiesrdquo Environ-mental Microbiology vol 7 no 1 pp 98ndash106 2005

[62] T Treude V Orphan K Knittel A Gieseke C H House andA Boetius ldquoConsumption of methane and CO

2by methan-

otrophicmicrobial mats from gas seeps of the anoxic Black SeardquoApplied and EnvironmentalMicrobiology vol 73 no 7 pp 2271ndash2283 2007

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[64] M Kruger M Blumenberg S Kasten et al ldquoA novel multi-layered methanotrophic microbial mat system growing on thesediment of the Black Seardquo Environmental Microbiology vol 10no 8 pp 1934ndash1947 2008

[65] R J WMeulepas C G Jagersma J Gieteling C J N BuismanA J M Stams and P N L Lens ldquoEnrichment of anaerobicmethanotrophs in sulfate-reducing membrane bioreactorsrdquoBiotechnology and Bioengineering vol 104 no 3 pp 458ndash4702009

[66] T Holler G Wegener H Niemann et al ldquoCarbon and sulfurback flux during anaerobic microbial oxidation of methane andcoupled sulfate reductionrdquo Proceedings of the National Academyof Sciences of the United States of America vol 108 no 52 ppE1484ndashE1490 2011

[67] M Kruger AMeyerdierks F O Glockner et al ldquoA conspicuousnickel protein in microbial mats that oxidize methane anaero-bicallyrdquo Nature vol 426 no 6968 pp 878ndash881 2003

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variant from archaea associated with anaerobic oxidation ofmethanerdquo Journal of the American Chemical Society vol 130 no32 pp 10758ndash10767 2008

[69] S Shima and R K Thauer ldquoMethyl-coenzyme M reductaseand the anaerobic oxidation of methane in methanotrophicArchaeardquo Current Opinion in Microbiology vol 8 no 6 pp643ndash648 2005

[70] R K Thauer and S Shima ldquoMethane as fuel for anaerobicmicroorganismsrdquo Annals of the New York Academy of Sciencesvol 1125 pp 158ndash170 2008

[71] S Yamamoto J B Alcauskas and T E Crozier ldquoSolubility ofmethane in distilled water and seawaterrdquo Journal of Chemicaland Engineering Data vol 21 no 1 pp 78ndash80 1976

[72] P H A Timmers J Gieteling H C A Widjaja-Greefkeset al ldquoGrowth of anaerobic methane-oxidizing archaea andsulfate-reducing bacteria in a high-pressure membrane capsulebioreactorrdquoApplied and EnvironmentalMicrobiology vol 81 no4 pp 1286ndash1296 2015

[73] MKruger HWoltersMGehre S B Joye andH-H RichnowldquoTracing the slow growth of anaerobic methane-oxidizingcommunities by 15N-labelling techniquesrdquo FEMS MicrobiologyEcology vol 63 no 3 pp 401ndash411 2008

[74] R J W Meulepas C G Jagersma A F Khadem C J N Buis-man A J M Stams and P N L Lens ldquoEffect of environmentalconditions on sulfate reduction withmethane as electron donorby an Eckernforde Bay enrichmentrdquo Environmental Science andTechnology vol 43 no 17 pp 6553ndash6559 2009

20 Archaea

[75] M W Bowles V A Samarkin and S B Joye ldquoImprovedmeasurement of microbial activity in deep-sea sediments atin situ pressure and methane concentrationrdquo Limnology andOceanography Methods vol 9 pp 499ndash506 2011

[76] S Shima M Krueger T Weinert et al ldquoStructure of a methyl-coenzyme M reductase from Black Sea mats that oxidizemethane anaerobicallyrdquo Nature vol 481 no 7379 pp 98ndash1012012

[77] K D Allen G Wegener and R H White ldquoDiscovery of multi-ple modified F-430 coenzymes in methanogens and anaerobicmethanotrophic archaea suggests possible new roles for F-430in naturerdquoApplied and Environmental Microbiology vol 80 no20 pp 6403ndash6412 2014

[78] V W Soo M J McAnulty A Tripathi et al ldquoReversingmethanogenesis to capture methane for liquid biofuel precur-sorsrdquoMicrobial Cell Factories vol 15 article 11 2016

[79] D L Valentine and W S Reeburgh ldquoNew perspectives onanaerobicmethane oxidationrdquoEnvironmentalMicrobiology vol2 no 5 pp 477ndash484 2000

[80] D L Valentine ldquoBiogeochemistry and microbial ecology ofmethane oxidation in anoxic environments a reviewrdquo Antonievan Leeuwenhoek International Journal of General and Molecu-lar Microbiology vol 81 no 1-4 pp 271ndash282 2002

[81] A J B Zehnder and T D Brock ldquoMethane formation andmethane oxidation by methanogenic bacteriardquo Journal of Bac-teriology vol 137 no 1 pp 420ndash432 1979

[82] J Harder ldquoAnaerobic methane oxidation by bacteria employ-ing 14C-methane uncontaminated with 14C-carbon monoxiderdquoMarine Geology vol 137 no 1-2 pp 13ndash23 1997

[83] J J Moran C H House K H Freeman and J G FerryldquoTrace methane oxidation studied in several Euryarchaeotaunder diverse conditionsrdquo Archaea vol 1 no 5 pp 303ndash3092005

[84] J J Moran C H House B Thomas and K H FreemanldquoProducts of tracemethane oxidation during nonmethyltrophicgrowth by Methanosarcinardquo Journal of Geophysical ResearchBiogeosciences vol 112 no 2 2007

[85] R J W Meulepas C G Jagersma Y Zhang et al ldquoTracemethane oxidation and the methane dependency of sulfatereduction in anaerobic granular sludgerdquo FEMS MicrobiologyEcology vol 72 no 2 pp 261ndash271 2010

[86] A J B Zehnder andTD Brock ldquoAnaerobicmethane oxidationoccurrence and ecologyrdquoApplied and Environmental Microbiol-ogy vol 39 no 1 pp 194ndash204 1980

[87] S J Blazewicz D G Petersen M P Waldrop and M K Fire-stone ldquoAnaerobic oxidation of methane in tropical and borealsoils ecological significance in terrestrial methane cyclingrdquoJournal of Geophysical Research Biogeosciences vol 117 no 2Article ID G02033 2012

[88] K A Smemo and J B Yavitt ldquoEvidence for anaerobic CH4

oxidation in freshwater peatlandsrdquo Geomicrobiology Journalvol 24 no 7-8 pp 583ndash597 2007

[89] M J Alperin and T M Hoehler ldquoAnaerobic methane oxidationby archaeasulfate-reducing bacteria aggregates 1 Thermody-namic and physical constraintsrdquo American Journal of Sciencevol 309 no 10 pp 869ndash957 2009

[90] S L Caldwell J R Laidler E A Brewer J O Eberly S CSandborgh and F S Colwell ldquoAnaerobic oxidation of methanemechanisms bioenergetics and the ecology of associatedmicroorganismsrdquo Environmental Science and Technology vol42 no 18 pp 6791ndash6799 2008

[91] GWang A J Spivack and S DrsquoHondt ldquoGibbs energies of reac-tion and microbial mutualism in anaerobic deep subseafloorsediments of ODP Site 1226rdquoGeochimica et Cosmochimica Actavol 74 no 14 pp 3938ndash3947 2010

[92] P R Girguis A E Cozen and E F DeLong ldquoGrowth andpopulation dynamics of anaerobic methane-oxidizing archaeaand sulfate-reducing bacteria in a continuous-flow bioreactorrdquoApplied and EnvironmentalMicrobiology vol 71 no 7 pp 3725ndash3733 2005

[93] K Nauhaus M Albrecht M Elvert A Boetius and F WiddelldquoIn vitro cell growth ofmarine archaeal-bacterial consortia dur-ing anaerobic oxidation ofmethanewith sulfaterdquoEnvironmentalMicrobiology vol 9 no 1 pp 187ndash196 2007

[94] B Orcutt V Samarkin A Boetius and S Joye ldquoOn the relation-ship between methane production and oxidation by anaerobicmethanotrophic communities from cold seeps of the Gulf ofMexicordquo Environmental Microbiology vol 10 no 5 pp 1108ndash1117 2008

[95] M Y Yoshinaga T Holler T Goldhammer et al ldquoCarbon iso-tope equilibration during sulphate-limited anaerobic oxidationof methanerdquo Nature Geoscience vol 7 no 3 pp 190ndash194 2014

[96] T Treude J Niggemann J Kallmeyer et al ldquoAnaerobic oxi-dation of methane and sulfate reduction along the Chileancontinental marginrdquo Geochimica et Cosmochimica Acta vol 69no 11 pp 2767ndash2779 2005

[97] R J Parkes B A Cragg N Banning et al ldquoBiogeochemistryand biodiversity of methane cycling in subsurface marinesediments (SkagerrakDenmark)rdquoEnvironmentalMicrobiologyvol 9 no 5 pp 1146ndash1161 2007

[98] N J Knab B A Cragg E R C Hornibrook et al ldquoRegulationof anaerobic methane oxidation in sediments of the Black SeardquoBiogeosciences vol 6 no 8 pp 1505ndash1518 2009

[99] H Yoshioka A Maruyama T Nakamura et al ldquoActivities anddistribution of methanogenic and methane-oxidizing microbesin marine sediments from the Cascadia Marginrdquo Geobiologyvol 8 no 3 pp 223ndash233 2010

[100] G Wegener V Krukenberg S E Ruff M Y Kellermann andK Knittel ldquoMetabolic capabilities of microorganisms involvedin and associated with the anaerobic oxidation of methanerdquoFrontiers in Microbiology vol 7 article 46 2016

[101] R J W Meulepas C G Jagersma A F Khadem A J MStams and P N L Lens ldquoEffect of methanogenic substrateson anaerobic oxidation of methane and sulfate reduction by ananaerobic methanotrophic enrichmentrdquo Applied Microbiologyand Biotechnology vol 87 no 4 pp 1499ndash1506 2010

[102] J Milucka T G Ferdelman L Polerecky et al ldquoZero-valentsulphur is a key intermediate in marine methane oxidationrdquoNature vol 491 no 7425 pp 541ndash546 2012

[103] W Michaelis R Seifert K Nauhaus et al ldquoMicrobial reefs inthe black sea fueled by anaerobic oxidation ofmethanerdquo Sciencevol 297 no 5583 pp 1013ndash1015 2002

[104] A Vigneron P Cruaud P Pignet et al ldquoArchaeal and anaerobicmethane oxidizer communities in the Sonora Margin coldseeps Guaymas Basin (Gulf of California)rdquo ISME Journal vol7 no 8 pp 1595ndash1608 2013

[105] M Alperin and T Hoehler ldquoThe ongoing mystery of sea-floormethanerdquo Science vol 329 no 5989 pp 288ndash289 2010

[106] B Orcutt and C Meile ldquoConstraints on mechanisms and ratesof anaerobic oxidation of methane by microbial consortiaprocess-basedmodeling of ANME-2 archaea and sulfate reduc-ing bacteria interactionsrdquo Biogeosciences vol 5 no 6 pp 1587ndash1599 2008

Archaea 21

[107] S E McGlynn G L Chadwick C P Kempes and V J OrphanldquoSingle cell activity reveals direct electron transfer in methan-otrophic consortiardquoNature vol 526 no 7574 pp 531ndash535 2015

[108] D R Lovley ldquoElectromicrobiologyrdquo Annual Review of Microbi-ology vol 66 pp 391ndash409 2012

[109] S M Strycharz-Glaven R M Snider A Guiseppi-Elie andL M Tender ldquoOn the electrical conductivity of microbialnanowires and biofilmsrdquoEnergy and Environmental Science vol4 no 11 pp 4366ndash4379 2011

[110] D J Richardson J N Butt J K Fredrickson et al ldquoThe lsquoporinndashcytochromersquo model for microbe-to-mineral electron transferrdquoMolecular Microbiology vol 85 no 2 pp 201ndash212 2012

[111] A Okamoto K Hashimoto and R Nakamura ldquoLong-rangeelectron conduction of Shewanella biofilms mediated by outermembrane C-type cytochromesrdquo Bioelectrochemistry vol 85pp 61ndash65 2012

[112] M Y El-Naggar G Wanger K M Leung et al ldquoElectricaltransport along bacterial nanowires from Shewanella oneidensisMR-1rdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 107 no 42 pp 18127ndash18131 2010

[113] G Reguera K D McCarthy T Mehta J S Nicoll M TTuominen and D R Lovley ldquoExtracellular electron transfer viamicrobial nanowiresrdquo Nature vol 435 no 7045 pp 1098ndash11012005

[114] Z M Summers H E Fogarty C Leang A E Franks N SMalvankar and D R Lovley ldquoDirect exchange of electronswithin aggregates of an evolved syntrophic coculture of anaer-obic bacteriardquo Science vol 330 no 6009 pp 1413ndash1415 2010

[115] A Kletzin T Heimerl J Flechsler L V Niftrik R Rachel andA Klingl ldquoCytochromes c in archaea distribution maturationcell architecture and the special case of Ignicoccus hospitalisrdquoFrontiers in Microbiology vol 6 article 439 2015

[116] GWegener V Krukenberg D Riedel H E Tegetmeyer and ABoetius ldquoIntercellular wiring enables electron transfer betweenmethanotrophic archaea and bacteriardquo Nature vol 526 no7574 pp 587ndash590 2015

[117] D HHaft S H Payne and J D Selengut ldquoArchaeosortases andexosortases are widely distributed systems linking membranetransit with posttranslational modificationrdquo Journal of Bacteri-ology vol 194 no 1 pp 36ndash48 2012

[118] A Marchler-Bauer M K Derbyshire N R Gonzales et alldquoCDD NCBIrsquos conserved domain databaserdquo Nucleic AcidsResearch vol 43 no 1 pp D222ndashD226 2015

[119] A Mitchell H-Y Chang L Daugherty et al ldquoThe InterProprotein families database the classification resource after 15yearsrdquo Nucleic Acids Research vol 43 no 1 pp D213ndashD2212015

[120] V Krukenberg K Harding M Richter et al ldquoCandidatusdesulfofervidus auxilii a hydrogenotrophic sulfate-reducingbacterium involved in the thermophilic anaerobic oxidation ofmethanerdquo Environmental Microbiology vol 18 pp 3073ndash30912016

[121] L Shi T C Squier J M Zachara and J K Fredrickson ldquoRes-piration of metal (hydr)oxides by Shewanella and Geobactera key role for multihaem c-type cytochromesrdquo MolecularMicrobiology vol 65 no 1 pp 12ndash20 2007

[122] N S Malvankar and D R Lovley ldquoMicrobial nanowires forbioenergy applicationsrdquo Current Opinion in Biotechnology vol27 pp 88ndash95 2014

[123] A-E Rotaru T LWoodard K PNevin andDR Lovley ldquoLinkbetween capacity for current production and syntrophic growth

in Geobacter speciesrdquo Frontiers in Microbiology vol 6 article744 2015

[124] A-E Rotaru P M Shrestha F Liu et al ldquoDirect interspecieselectron transfer between Geobacter metallireducens andMethanosarcina barkerirdquo Applied and Environmental Microbi-ology vol 80 no 15 pp 4599ndash4605 2014

[125] S Scheller H Yu G L Chadwick S E McGlynn and VJ Orphan ldquoArtificial electron acceptors decouple archaealmethane oxidation from sulfate reductionrdquo Science vol 351 no6274 pp 703ndash707 2016

[126] J Milucka F Widdel and S Shima ldquoImmunological detec-tion of enzymes for sulfate reduction in anaerobic methane-oxidizing consortiardquo Environmental Microbiology vol 15 no 5pp 1561ndash1571 2013

[127] P Cabello M D Roldan and C Moreno-Vivian ldquoNitratereduction and the nitrogen cycle in archaeardquoMicrobiology vol150 no 11 pp 3527ndash3546 2004

[128] R MMartinez-Espinosa E J Dridge M J Bonete et al ldquoLookon the positive sideThe orientation identification and bioener-getics of lsquoArchaealrsquomembrane-boundnitrate reductasesrdquoFEMSMicrobiology Letters vol 276 no 2 pp 129ndash139 2007

[129] S de VriesMMomcilovicM J F Strampraad J PWhiteleggeA Baghai and I Schroder ldquoAdaptation to a high-tungsten envi-ronment pyrobaculum aerophilum contains an active tungstennitrate reductaserdquo Biochemistry vol 49 no 45 pp 9911ndash99212010

[130] M Egger O Rasigraf C J Sapart et al ldquoIron-mediated anaer-obic oxidation of methane in brackish coastal sedimentsrdquoEnvironmental Science and Technology vol 49 no 1 pp 277ndash283 2015

[131] T Treude S Krause J Maltby A W Dale R Coffin and LJ Hamdan ldquoSulfate reduction and methane oxidation activitybelow the sulfate-methane transition zone in Alaskan BeaufortSea continental margin sediments implications for deep sulfurcyclingrdquo Geochimica et Cosmochimica Acta vol 144 pp 217ndash237 2014

[132] N Riedinger M J Formolo T W Lyons S Henkel A Beckand S Kasten ldquoAn inorganic geochemical argument for coupledanaerobic oxidation of methane and iron reduction in marinesedimentsrdquo Geobiology vol 12 no 2 pp 172ndash181 2014

[133] Y-H Chang T-W Cheng W-J Lai et al ldquoMicrobial methanecycling in a terrestrialmud volcano in eastern Taiwanrdquo Environ-mental Microbiology vol 14 no 4 pp 895ndash908 2012

[134] S A Crowe S Katsev K Leslie et al ldquoThe methane cycle inferruginous Lake Matanordquo Geobiology vol 9 no 1 pp 61ndash782011

[135] O Sivan M Adler A Pearson et al ldquoGeochemical evidence foriron-mediated anaerobic oxidation of methanerdquo Limnology andOceanography vol 56 no 4 pp 1536ndash1544 2011

[136] K E A Segarra C Comerford J Slaughter and S B JoyeldquoImpact of electron acceptor availability on the anaerobic oxi-dation of methane in coastal freshwater and brackish wetlandsedimentsrdquo Geochimica et Cosmochimica Acta vol 115 pp 15ndash30 2013

[137] V Gupta K A Smemo J B Yavitt D Fowle B Branfireunand N Basiliko ldquoStable isotopes reveal widespread anaerobicmethane oxidation across latitude and peatland typerdquo Environ-mental Science and Technology vol 47 no 15 pp 8273ndash82792013

[138] O Oni T Miyatake S Kasten et al ldquoDistinct microbialpopulations are tightly linked to the profile of dissolved iron in

22 Archaea

the methanic sediments of the Helgolandmud area North SeardquoFrontiers in Microbiology vol 6 2015

[139] E J Beal C H House and V J Orphan ldquoManganese- andiron-dependent marine methane oxidationrdquo Science vol 325no 5937 pp 184ndash187 2009

[140] M W Bowles V A Samarkin K M Bowles and S B JoyeldquoWeak coupling between sulfate reduction and the anaerobicoxidation of methane in methane-rich seafloor sedimentsduring ex situ incubationrdquo Geochimica et Cosmochimica Actavol 75 no 2 pp 500ndash519 2011

[141] Y Z Lu L Fu J Ding Z Ding N Li and R J Zeng ldquoCr(VI)reduction coupled with anaerobic oxidation of methane in alaboratory reactorrdquoWater Research vol 102 pp 445ndash452 2016

[142] K F Ettwig B Zhu D Speth J T Keltjens M S Jetten and BKartal ldquoArchaea catalyze iron-dependent anaerobic oxidationof methanerdquo Proceedings of the National Academy of Sciences ofthe United States of America vol 113 no 45 pp 12792ndash127962016

[143] T M Flynn R A Sanford H Ryu et al ldquoFunctional microbialdiversity explains groundwater chemistry in a pristine aquiferrdquoBMCMicrobiology vol 13 no 1 article no 146 2013

[144] C J Schubert F Vazquez T Losekann-Behrens K KnittelM Tonolla and A Boetius ldquoEvidence for anaerobic oxidationof methane in sediments of a freshwater system (Lago diCadagno)rdquo FEMS Microbiology Ecology vol 76 no 1 pp 26ndash38 2011

[145] K E A Segarra F Schubotz V Samarkin M Y Yoshinaga K-U Hinrichs and S B Joye ldquoHigh rates of anaerobic methaneoxidation in freshwater wetlands reduce potential atmosphericmethane emissionsrdquo Nature Communications vol 6 article7477 2015

[146] E J Beal M W Claire and C H House ldquoHigh rates ofanaerobic methanotrophy at low sulfate concentrations withimplications for past and present methane levelsrdquo Geobiologyvol 9 no 2 pp 131ndash139 2011

[147] F Kracke I Vassilev and J O Kromer ldquoMicrobial electrontransport and energy conservationmdashthe foundation for opti-mizing bioelectrochemical systemsrdquo Frontiers in Microbiologyvol 6 article 575 2015

[148] C L Reardon A C Dohnalkova P Nachimuthu et al ldquoRoleof outer-membrane cytochromes MtrC and OmcA in thebiomineralization of ferrihydrite by Shewanella oneidensisMR-1rdquo Geobiology vol 8 no 1 pp 56ndash68 2010

[149] L Shi B Chen Z Wang et al ldquoIsolation of a high-affinityfunctional protein complex between OmcA and MtrC twoouter membrane decaheme c-type cytochromes of Shewanellaoneidensis MR-1rdquo Journal of Bacteriology vol 188 no 13 pp4705ndash4714 2006

[150] X Qian T Mester L Morgado et al ldquoBiochemical charac-terization of purified OmcS a c-type cytochrome requiredfor insoluble Fe(III) reduction in Geobacter sulfurreducensrdquoBiochimica et BiophysicaActamdashBioenergetics vol 1807 no 4 pp404ndash412 2011

[151] T Mehta M V Coppi S E Childers and D R Lovley ldquoOutermembrane c-type cytochromes required for Fe(III) andMn(IV)oxide reduction in Geobacter sulfurreducensrdquo Applied andEnvironmentalMicrobiology vol 71 no 12 pp 8634ndash8641 2005

[152] W Blankenfeldt A P Kuzin T Skarina et al ldquoStructure andfunction of the phenazine biosynthetic protein PhzF fromPseudomonas fluorescensrdquoProceedings of theNational Academyof Sciences of the United States of America vol 101 no 47 pp16431ndash16436 2004

[153] J F Parsons F Song L Parsons K Calabrese E Eisensteinand J E Ladner ldquoStructure and function of the phenazinebiosynthesis protein PhzF fromPseudomonas fluorescens 2-79rdquoBiochemistry vol 43 no 39 pp 12427ndash12435 2004

[154] T Hiratsuka K Furihata J Ishikawa et al ldquoAn alternativemenaquinone biosynthetic pathway operating in microorgan-ismsrdquo Science vol 321 no 5896 pp 1670ndash1673 2008

[155] M Tietze A Beuchle I Lamla et al ldquoRedox potentials ofmethanophenazine and CoB-S-S-CoM factors involved inelectron transport in methanogenic archaeardquo ChemBioChemvol 4 no 4 pp 333ndash335 2003

[156] Q H Tran and G Unden ldquoChanges in the proton potentialand the cellular energetics of Escherichia coli during growth byaerobic and anaerobic respiration or by fermentationrdquoEuropeanJournal of Biochemistry vol 251 no 1-2 pp 538ndash543 1998

[157] I Callebaut D Gilges I Vigon and J-P Mornon ldquoHYR anextracellular module involved in cellular adhesion and relatedto the immunoglobulin-like foldrdquo Protein Science vol 9 no 7pp 1382ndash1390 2000

[158] H J Gilbert ldquoCellulosomes microbial nanomachines that dis-play plasticity in quaternary structurerdquoMolecular Microbiologyvol 63 no 6 pp 1568ndash1576 2007

[159] A Peer S P Smith E A Bayer R Lamed and I BorovokldquoNoncellulosomal cohesin- and dockerin-like modules in thethree domains of liferdquo FEMS Microbiology Letters vol 291 no1 pp 1ndash16 2009

[160] M Wagner ldquoMicrobiology conductive consortiardquo Nature vol526 no 7574 pp 513ndash514 2015

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

10 Archaea

H2

CoM-SH

Mch

Mer

Mtd

Ftr

Fmd

Mcr

MPh

MPhH2

MPh

MPh

MPhH2

MtrVho

CoM-SH

CoB-S-S-CoM

CoB-SHHdrDE

Fpo

Fpo

Ech

CH3-CoM

2H+

H2

2H+

2H+

H+

MPhH2

CH4

CH3-H4MPTF420H2

F420

F420H2

F420

CH2=H4MPT

CHequivH4MPT

CHO-H4MPT

CHO-MFR

CO2

Fdred

Fdox

H2O

2Na+

CH3-OH

Figure 3 Methylotrophic methanogenesis in cytochrome containingMethanosarcina barkeri Black lines represent presence of conversionsand red lines indicate reversal of the hydrogenotrophic methanogenic pathway See Table 3 for nomenclature

Mcr in ANME may have similar catalytic properties as themethanogenic enzyme and that the high amount of Mcr permg total cell biomass in ANME may in part compensates forthe apparently relatively slow catalysis

Considering the thermodynamic constraints the Gibbsfree energy change of the Mcr forward reaction under stan-dard conditions is around minus30 kJmolminus1 [56] Therefore thereverse reaction is endergonic under standard conditions andwill not proceed However highmethane concentrations (105according to reaction (1) [69 70]) may lead to a favourablechange in the Gibbs free energy in the direction of AOMHigh methane partial pressure prevails at many habitatswhere AOM has been detected The solubility of methaneat atmospheric pressure is only 13mM [71] Consequentlyincreased AOM rates were reported upon pressurizing sam-ples of different geographical origin [59 60 72 73] The 119870

119872

of Mcr of M marburgensis for methane was determined ator above 10mM and reported 119870

119872values of S-AOM varied

from (at least) 11mM [74] a few mM [57] to even 37mM(equivalent to 3MPa CH

4) [58] Thus high pressure and

therefore high concentrations of methane in the natural habi-tat accelerate the oxidation rate of methane by Mcr Futureresearch to accurately determine119870

119872values and rates forMcr

at differentmethane partial pressures is however neededThismay seem difficult but microbial activity measurements at insitu methane partial pressure were shown to be successful inthe laboratory [75]

It was suggested that the Mcr reaction is the rate limitingstep in reverse methanogenesis [56] which is in line withthe above described challenges Supporting these findingsthere does not seem to be a major change in the aminoacid structure that determines whether the backwards or theforward reaction of Mcr is favoured Amino acid alignments[67] and the crystal structure of ANME-1 Mcr [76] indicatedhigh overall similarity of the methanogenic and methan-otrophic enzyme and unambiguously demonstrated that

Archaea 11

MHC

MHCS-layer

2H+

minuse

cyt b

Mch

Mer

Mtd

Ftr

Fmd

Mcr

MPh

HdrABC

MPh

MHC

MHC

MPh

CoB-S-S-CoM

CoB-SH

CoM-SH

HdrDE

Mtr

Fpo

Fpo

Rnf

MPhH2

MPhH2

MPhH2

MPhH2

CH4

CH3-CoM

CH3-H4MPT

F420H2

F420

F420H2

F420

CH2=H4MPT

CHequivH4MPT

CHO-H4MPT

CHO-MFR

CO2

Fdred

Fdox

H2O

2Na+

MPh

minuse

S-layer

MHC

SRB 2H+

2H+

2Na+

minuse

minuse

minuse

Figure 4 Methanotrophic pathway during S-AOM by ANME-2a [42] Red lines indicate reversal of the hydrogenotrophic methanogenicpathway See Table 3 for nomenclature

CoM-SH and CoB-SH are substrates of the methanotrophicenzyme However several posttranslational modifications ofamino acids were different betweenmethanogens andANMEarchaea and the cofactor F

430(the prosthetic group of Mcr)

is modified in ANME-1 but not in ANME-2 or ANME-3archaea [51 63 67 68 76 77] Furthermore ANME-1 seemsto lack the noncatalytic proteinDdomain of themcr gene thatis present in all other methanogens and methanotrophs butof which the function is unknown (IPR003901 Table 2) [51]A metabolically engineered Methanosarcina acetivorans wasable to convert methane and CO

2to acetate with a plasmid

containingMcr derived from ANME-1 [78] It is thus unclearif only thermodynamic constraints and the abundance ofMcrensureAOMactivity or if also specificmodifications canhavean effect on the reverse activity of Mcr

23 Methane Oxidation by Methanogens Pure cultures ofmethanogens were not able to oxidize methane under highmethane and low hydrogen concentrations (reviewed in[79 80]) Methanogens are only able to oxidize methaneduring net methane production [81] Labeled methane addi-tion (13C or 14C) to pure cultures of methanogens showedproduction of labeled CO

2during net methane production

This characteristic was confirmed with several pure culturesof methanogens [82ndash84] The process was called ldquotracemethane oxidationrdquo (TMO) since the CO

2was formed in

trace amounts relative to the methane produced [83] It isnot clear if TMO is due to the reported reversibility ofindividual enzymes [66] or if it is an active microbial processfrom which energy can be conserved TMO was speculatedto be an active metabolic process for three reasons (1)the amount of methane oxidized varied between differentspecies of methanogens grown on the same methanogenicsubstrate (2) the amount ofmethane oxidized varied betweendifferent methanogenic substrates and (3) TMO productsvaried between different methanogenic substrates [83 84]For instance when grown on acetate Methanosarcina ace-tivorans produced labeled acetate from labeled methaneWhen grown on carbon monoxide it produced both labeledacetate and methyl sulfides from labeled methane [84] Dur-ing hydrogenotrophic and methylotrophic methanogenesisTMO mainly produced CO

2from labeled methane [83]

However in contrast with AOM TMO rates never exceededmethanogenesis rates even during long-term incubationwith methane and sulfate [85] It seems that methanogensare not able to conserve energy from TMO even under

12 Archaea

Mch

Mer

Mtd

Ftr

Fmd

Mcr

MQ

MQ

EchHdrFrh

3MQ

HdrABC

MQ

cyt b Mtr

NrfH

cyt c

NrfA

CoB-S-S-CoM

CoB-SH

CoM-SH

HdrDE

HCOIIHCOIINapHOrf7

NarGH

S-layer

Fqo

Fqo

3H+

3H+

4H+

CH4

CH3-CoM

CH3-H4MPT

F420

F420H2

F420

F420H2

CH2=H4MPT

CHequivH4MPT

CHO-H4MPT

CHO-MFR

CO2

Fdred

Fdox

H2O

2Na+

NH4+

NO2minus

NO2minus

NO3minus

3MQH2

MQH2

MQH2

MQH2eminus

eminus

Rieske

Figure 5 Methanotrophic pathway during N-AOM by ldquoCaM nitroreducensrdquo MPEBLZ (ANME-2d) [43] Red lines indicate reversal of thehydrogenotrophic methanogenic pathway See Table 3 for nomenclature

thermodynamically favourable conditions TMOoccurs bothin absence and presence of an external electron acceptor andonly during net methanogenesis It is therefore most likelycaused by the reported back flux of individual enzymes of themethanogenic pathway [66]

TMO also occurred in granular sludge and in freshwaterand terrestrial samples These mixed communities showedhigher TMO rates than pure cultures reaching up to 90of the methane produced [27 85ndash87] TMO should thereforebe carefully considered in the experimental setup and inter-pretation of results when studying AOM in environmentalsamples especially since TMO rates were like AOM stim-ulated by a high methane partial pressure [72 86 88] Sulfatereduction was also stimulated by higher methane partialpressures [85]Thus a highmethane partial pressure can havea stimulating effect on methane oxidation (either throughAOM or TMO) and SR which could be unrelated to S-AOMMoreover addition of iron sulfate (FeSO

4) or manganese

oxide (MnO2) also increased TMO rates [86] Therefore

methane-dependent SR and sulfate- or metal-dependentmethane oxidation are not necessarily indications for AOMin mixed cultures In conclusion when studying complexldquoblack-boxrdquo communities only net methane oxidation isproof for AOM activity

24 Methane Production by ANME The process of S-AOMis at the energetic limit for sustaining life with estimates

of Gibbs free energy yields between minus18 and minus35 kJmolminus1[45 79 89ndash91] and doubling times between 11 and 75months [65 72 73 92 93] Since S-AOM operates close toits thermodynamic equilibrium the reversibility of individualenzymes leads to measurable back flux producing methane(3ndash7 of AOM) and sulfate (55ndash13 of SR) during S-AOM [66] This ldquotrace methane productionrdquo was observedin situ [11] and in sediment slurries with methanogenesisaround 10 [62 94] or even as high as 50 of AOM [34]When sulfate becomes depleted Gibbs free energy yieldsbecome even lower (less negative) and the enzymatic backflux becomes even more apparent up to 78 of net AOM[95] Previous measurements of 13C depletion below thesulfate-methane transition zone (SMTZ) ofmarine sedimentsthat were thought to be indicative for methanogenesis couldtherefore instead be attributed to the back flux of AOM [95]The occurrence of ANME-1 without a bacterial partner insediment layers where sulfate was depleted was previouslyinterpreted as evidence that ANME-1 perform methanogen-esis [24] but in light of the above it could also indicate AOMThere are indeed reports of AOM activity below the SMTZin the methanogenic zone [96ndash99] In contrast AOM withother electron acceptors than sulfate operates far from thethermodynamic equilibrium with Gibbs free energy changesbetween minus5172 and minus8414 kJmolmethaneminus1 (Table 1) Herethe reported anaerobic back flux [66] is expected to be lessapparent

Archaea 13

MetFMer

Mdh

FaeHps

SRB

MHC

Mch

Mtd

Ftr

Fmd

McrMQ

Hdr1

MQ

MHC

Hdr2

CoB-S-S-CoMCoB-SHCoM-SH

Mtr

Fqo

CH4

CH3-CoMCH3-OH

CH2O CH3-H4MPT

F420F420H2

CHO-H4MPT

CHO-MFR

CO2

FdredFdox

H2O

eminus

eminus

CHequivH4MPT

CH2=H4MPT

xH+

H2

MQH2

MQH2

+xNa

Figure 6 Methanotrophic pathway during S-AOM by ANME-1 [40 41] Red lines indicate reversal of the hydrogenotrophic methanogenicpathway grey lines represent absence of conversions and blue lines indicate a bypass of the hydrogenotrophic methanogenic pathway SeeTable 3 for nomenclature

In laboratory incubations researchers were not ableto stimulate net methanogenesis through addition ofmethanogenic substrates to AOM performing sediments[62 94] In two cases researchers were successful [23 100]In one of these cases sediment-free long-term AOM enrich-ments that were dominated by ANMESRB were incubatedwith methanogenic substrates The resulting methanogenicactivity most likely came from the enrichment of a minorpopulation of methanogens (up to 7permil of total archaealgene tag sequences) that was present in the inoculum[100] In the second study methanogenic substrates wereadded to ANME-1 and ANME-2 dominated microbialmat samples and methanogenesis also occurred [23]However no information was provided for the total archaealcommunity composition which makes it impossible toexclude methanogens as the responsible organisms

Genomic information of ANME also gives indication onpotential methanogenic routes Considering methylotrophicmethanogenesis no gene homologues catalyzing methyltransfer from methylated substrates to coenzyme M weredetected in ANME (Table 2) [40ndash43] Acetoclastic methano-genesis needs either the AMP- and ADP-forming acetyl-coenzyme A synthetase (Acs and Acd resp) or proceedsvia acetate kinase and phosphotransacetylase In ANME-1only the alpha subunit of a homologue of Acd was expressed

during AOM [41] but in an ANME-1 proteome of activeAOM biomass no Acd was detected [40] The Acd gene wasdetected in the single-aggregate genome and transcriptomeof ANME-2a [42] and in ANME-2d [43] However genedomains for Acd are also present in methanogens unableto use acetate as substrate (Table 2) and are probably usedfor lipid metabolism In hydrogenotrophic methanogenesishydrogenases are used to replenish reduced coenzyme B andto recycle oxidized F

420(discussed in Section 21) Both the

cytoplasmic Mvh complex and the membrane bound Vhowere not present in ANME-2d [43] and not expressed inANME-2a (which also lackedEch andF

420-dependent hydro-

genase (Frh)) [42] making hydrogenotrophic methanogen-esis unlikely In ANME-1 both the cytoplasmic HdrABCand MvhD are present as well as homologues of Frh andEch but these were lacking catalytic subunits [40 41] Aniron hydrogenase was found in both ANME-1 metagenomesbut not in any other methanotroph or methanogen [41](Table 2) This iron hydrogenase domain is part of a genethat is 70 identical to a [FeFe]-hydrogenase of Dehalococ-coides mccartyi [FeFe]-hydrogenases catalyze reversible H

2

production and uptake but these were presumed to have nokey function in AOM [41] However the gene is part of a genecluster of three genes containing a 51 kDaNADH ubiquinoneoxidoreductase subunit (Table S3) which could potentially

14 Archaea

form a complex that generates a proton motive force duringhydrogen oxidation Therefore hydrogenotrophic methano-genesis by ANME-1 cannot be excluded yet

3 Respiration during AnaerobicOxidation of Methane

For netAOMtooccur an external electron acceptor is neededwhich results in a favourable Gibbs free energy change(Table 1) A variety of terminal electron acceptors have beendiscovered for AOM which will be discussed in Sections 31ndash33

31 Sulfate-Dependent AOM During sulfate-dependentAOM electrons are transferred from ANME to the sulfate-reducing bacterial partner Previous work tried to uncoverhow electrons were transferred and most compoundsthat could act as interspecies electron carrier (IEC) wereexcluded to be involved in AOM such as methanolhydrogen methanethiol acetate and carbon monoxide[57 61 62 94 101] Indications that polysulfide could actas IEC were found and ANME-2a archaea were thoughtto perform both AOM and sulfate reduction (SR) [102]However in marine seeps hydrothermal vents and othernondiffusion based sediments AOM rates are high andANME form close associations with SRB in dense aggregates[1 5 103 104] In these aggregates the high AOM ratescould not be explained by diffusion of an IEC whichmade direct interspecies electron transfer (DIET) a moreplausible mechanism [89 105 106] Cellular activities wereindependent of aggregate type and distance between thesyntrophic partners within the aggregate which is bestexplained by DIET [107] DIET is normally achieved usingmultiheme cytochrome c proteins (MHCs) and conductivepili (ie nanowires) which are mainly found in bacteriathat donate electrons extracellularly such as Geobacter andShewanella species [108ndash114] Indeed ANME-2a from seep-sediment samples seem to transfer electrons directly usinglarge MHCs [107] which were found in the metagenome ofANME-2a [107 115] ANME-1 and the associated bacterialpartner also overexpressed genes for extracellular MHCsduring AOM [116] which complements previous findings oftranscription [41] and translation [40] of ANME-1 relatedMHC genes Domain based (meta)genome analysis showsthe high abundance of MHC domains in different ANMEas compared to methanogens (Table 2) A recently isolatedbacterial partner of ANME-1 (ldquoHotSeep-1rdquo) also producedcell-to-cell connections using pili-derived nanowires [116]which explain previously detected Deltaproteobacteria-related pili genes in an AOM sample dominated by ANME-1[40]

How ANME use MHCs to donate electrons to thebacterial partner is not yet clear For ANME-2a the electronsprobably flow from methanophenazine to membrane inte-grated di-heme cytochromes (cytochrome 119887119887

6) that transfer

the electrons through the S-layer via MHCS-layer fusionproteins to extracellular MHCs (Figure 4) (Figure 4 in[107]) Exosortases and archaea-specific archaeosortases are

involved in export of cell surface proteins such as the archaealS-layer proteins These transpeptidases recognize specificsignal peptides for protein- sorting that is archaeosor-tase A recognizes the protein-sorting signal PGF-CTERMand archaeosortase C recognizes the PEF-CTERM signal[117] Both ANME-2a and 2d show presence of di-hemecytochromes archaeosortase A (IPR014522) archaeosortaseC (IPR022504) and other exosortase gene domains (Table 2)Moreover some genes of both ANME-2a and 2d containedboth MHC and PGF or PEF-CTERM domains Lastly somegenes of both ANME-2a and 2d contained both MHC andS-layer domains [107] indicating that these could form theabove-stated MHCS-layer fusion proteins

ANME-1 do not seem to have di-heme cytochromes(Table 2) [115] PGF related domains (IPR026453 andIPR026371) were present in all ANME but PEF-CTERM(IPR017474) related domains were absent in ANME-1 (Table 2) Moreover ANME-1 lacked archaeosortaseA (IPR014522) and archaeosortase C gene domains(IPR022504) as well as some other exosortases (Table 2) Asearch in NCBIrsquos conserved domains database (CCD [118])and the EMBL InterPro database [119] of amino acidssequences of all genes from ANME metagenomes thatcontain MHC domains showed that ANME-1 did not haveany protein-sorting signal or S-layer domains within thesegenes In fact S-layer domains were completely absent inANME-1 (Table 2) These results imply that ANME-1 do notuse di-heme cytochromes for electron transfer to MHCsand do not produce an S-layer (Figure 6) This implies thatANME-1 use a different mechanism for DIET and couldexplain the need for less MHCs by ANME-1 (Table 2)and the observed pili-derived nanowires produced by thebacterial partner [116] The genome of the bacterial partnerof ANME-1 (ldquoHotSeep-1rdquo) encoded 24 c-type cytochromesof which 10 were similar to secreted MHCs of Geobactersulfurreducens [120] which also uses pili for DIET [121]

In the case of ANME-2a it is not clear if pili (ienanowires) were formed during AOM It was previouslythought that electrically conductive pili seemed to be aprerequisite for current production andDIET [122 123] evenwhen syntrophs were closely associated [124] such as withinANME-2SRB aggregates However conductive materialssuch as granular activated carbon were shown to be ableto substitute pili in DIET [124] Although in previous workconductive materials such as phenazines or humic acids didnot seem to stimulate AOM rates [61] in a recent study AOMwas decoupled from SR using artificial electron acceptors[125] This indicates that conductive materials can indeedreplace pili and that ANME-2ab could possibly couple AOMto metal oxide reduction or any other suitable electronacceptor (discussed in Section 33) However it needs to beproven if in ANME-2SRB aggregates no pili are formed andif the mechanism of DIET is fundamentally different fromANME-1

As for the polysulfide shuttling theory [102] canonicalgenes for dissimilatory sulfate reduction such as adenylyl-transferase (Sat) APS reductase (Apr) and dissimilatorysulfite reductase (Dsr) which are all present in the sulfate-reducing archeon A fulgidus (Table S2) were not found in

Archaea 15

metagenomes of ANME-1 [41] and ANME-2a (Table S1)The enzymes Sat and Dsr were also not detected in ANMEcells using fluorescent immunolabelling [126] ANME-1 werepreviously found to encode most proteins for assimilatorysulfate reduction [41] ANME-2d only harbor gene domainsthat encode Sat and assimilatoryATP sulfurylase APS kinaseand sodiumsulfate symporters which were not present inANME-2a (Table S1) It is therefore clear that at least ANME-2a cannot donate electrons to sulfate but need to donateelectrons to a sulfate-reducing partner

32 Nitrate-Dependent AOM Unlike during S-AOMANME-2d that perform N-AOM do not need a bacterialpartner but transfer electrons directly to a membrane boundnitrate reductase (Nar) [28 43] (Figure 5) The ANME-2dgenomes contain most MHCs found so far in archaea[107 115] (Table 2) Of the 87 proteins that contained aCxxCH binding motif of which 43 seemed to be true c-typecytochromes [115] 23 CxxCH motif-encoding transcriptswere expressed during N-AOM [43] The function of mostof these MHCs is not known but they are likely involvedin nitrate reduction since c-type cytochromes are capableof operating in the wide range of redox potentials thatcouple nitrate reduction (11986401015840 (NO

3

minusNO2

minus) = +433mV) andmethane oxidation (11986401015840 (CoM-S-S-CoBCoM-SH+CoB-SH)= minus143mV) [43] Nitrate as terminal electron acceptor inanaerobic respiration has been found in halophilic andthermophilic archaea [127] The nar gene cluster of ldquoCaM nitroreducensrdquo comprises several genes including thecatalytic alpha (NarG molybdopterin) and beta (NarHiron sulfur cluster) subunit of nitrate reductase [28 43] The(halo)archaeal nitrate reductase complex was reported to belocated at the extracellular side of the cytoplasmic membrane[128] and in most archaea associated with the cytoplasmicmembrane via NarM [129] The ldquoCa M nitroreducensrdquogenome does not encode NarM but encodes a TAT signalpeptide at the N-terminus of NarG for translocation acrossthe cytoplasmic membrane [28 43] Interestingly theNarG and NarH seem to have been acquired from theProteobacteria via lateral gene transfer [28]

It is not yet clear at which point in themetabolism ldquoCaMnitroreducensrdquo conserves energy During reverse methano-genesis N5-methyl-H

4MPTCoM methyltransferase (Mtr)

dissipates the sodium ion potential across the cytoplasmicmembrane so subsequent steps inN-AOMhave to be coupledto the build-up of a proton or sodium motive force to makethe overall process energetically favourable The analysis ofan environmental genome [43] indicated presence of severalprotein complexes involved in electron transport and energyconservation Electrons that enter the respiratory chain couldbe transported by membrane-integral electron carriers (iemenaquinones) to a Rieske-cytochrome b complex that mayuse cytochrome c as electron acceptor This in turn maybe the electron donor for the unusual nitrate reductasecomplex Energy conservation is thermodynamically andmechanistically feasible at the F

420H2dehydrogenase and the

Rieske-cytochrome b complex (Figure 5) (Figure 2 in [43])Further investigations are needed to determine whether

nitrate reductase is also involved in energy conservationbut this working hypothesis is strengthened by the presenceof cupredoxin multicopper oxidase domains and coppercenters related to the periplasmic domain of cytochrome coxidase subunit II (HCO II) in ANME-2d (Table S1)

BothANME-2d genomes discussed here are derived frombioreactors where ldquoCaM nitroreducensrdquo formed syntrophiccultures with nitrite scavenging bacteria either with ldquoCaKuenenia stuttgartiensisrdquo (anammox bacteria) [28] or ldquoCaMethylomirabilis oxyferardquo (NC10 bacteria) [31 43]This indi-cated that ANME-2d could be dependent on those bacteriafor nitrite removal However in addition to nitrite ldquoCa Mnitroreducensrdquo may also produce ammonium during AOMby a pentaheme c-type nitrite reductase (NrfAH) encodedin the genome [43] (Figure 5) In fact both ANME-2dgenomes contain domains for NrfA (IPR003321) and NrfH(IPR017571) (Table S1) implying that both ANME-2d speciesare not necessarily dependent on a nitrite scavenger duringAOM

33 Metal-Dependent AOM Evidence for metal-dependentAOM was found in marine sediments [130ndash132] In non-marine environments AOM was also hypothesized to becoupled to iron andor manganese oxide reduction [26 133ndash136] or even coupled to the reduction of humic acids [136137] However organisms responsible for metal-dependentAOM were not identified in these studies It was speculatedthat JS1 bacteria methanogenic archaea and Methanohalo-biumANME-3 could be responsible for iron-dependentAOM [138] Other researchers speculated that either ANME-1 or MethanococcoidesANME-3 together with a bacterialpartner were responsible for manganese-dependent AOM[139] In another study where AOM was decoupled from SRANME were not detected which leaves open the possibilitythat other archaeal clades besides ANME could performmetal-dependent AOM [131]

It was recently observed that cultures containing ANME-2a and ANME-2c could decouple AOM from SR in thepresence of artificial electron acceptors humic acids andsoluble iron [125] which confirmed previous findings ofAOM not connected to SR in ANME dominated samples[140] This suggests that ANME-2 could also use insolublemetal oxide minerals as electron acceptor during AOM TheMHCs of ANME-2ab and ANME-2d are larger than thosein Shewanella and Geobacter species [107] which are knownto be capable of extracellular electron conduction It wasspeculated that both ANME-2d and Ferroglobus placidus ofwhich the latter can perform solid iron reduction can foldCxxCHmotifs into extracellular conductive structures or pili[115] Many of the MHCs of ANME-2d were not expressedwhen grown with nitrate (discussed in section 32) implyingthat these are not needed for nitrate reduction [43] Thisstrengthens the hypothesis that also ANME-2d could coupleAOM to reduction of other extracellular electron acceptorsthan nitrate and even to insoluble metal oxides Indeedrecent work showed that ANME-2d could be involved inAOM coupled to chromium(VI) reduction [141] (Table 1reaction (5)) and in AOM coupled to the reduction of soluble

16 Archaea

iron and insoluble ferrihydrite and birnessite minerals [142](Table 1 reactions (3) and (4)) ANME-2d could even possiblydonate electrons to a bacterial partner besides nitrate-richenvironments ANME-2d archaea have been found inwells ofan aquifer where sulfate and methane concentrations overlap[143] Moreover ANME-2d was the only clade detected insediments of a freshwater lake where S-AOM occurred [144]Sulfate concentrations in these studies were low but above1mM and thus higher than the lowest reported concen-trations for S-AOM to occur [145 146] Lastly sequencesof ANME-2d were relatively more abundant in freshwatersediments fed with methane and sulfate than in sedimentsfed with onlymethane or only sulfate and noN-AOMactivitywas detected when fed with nitrate and methane [27] Theseindications hold promise that direct experimental evidencefor sulfate-dependent AOM by ANME-2d could be found inthe future

TheANME-1 genome contains fewerMHCgene domainsas compared to ANME-2a and ANME-2d and some otherarchaea such as somemethylotrophicmethanogens (Table 2)and some members of the Archaeoglobales [115] The MHCsof ANME-1 also have a smaller heme count as compared toother ANME and some other archaea with the largest beingan octaheme cytochrome [107] Each hemewithin aMHChasits own redox potential and therefore structurally differentMHCs represent a large range of redox potentials that canbe used for bioenergetic electron transfer (reviewed in [147])For instance metal oxide reduction in Shewanella oneidensisMR-1 is catalyzed by a chain of a tetraheme (CymA) twodecaheme (MtrA and MtrB) and eventually extracellulardecaheme cytochromes OmcAMtrC that reduce the ironminerals [121 148 149] In Geobacter sulfurreducens ironmineral reduction seems to be catalyzed by the tetrahemecytochrome OmcE and hexaheme cytochrome OmcS trans-ferring electrons from the outer membrane to type IV pilithat transmit the electrons to iron minerals [121 150 151]Since ANME-1 lack MHCs of the correct size and lack genedomains for pili production [116] they seem unable to reduceminerals via both mechanisms present in Shewanella andGeobacter It can therefore be speculated that ANME-1 areless versatile in electron acceptor use and are not able toreduce solid metal oxides However DIET mechanisms arestill not well understood and the true differences betweenMHCs of different ANME types need to be investigated usingbiochemical methods This would allow uncovering the truecapabilities concerning DIET

34 Menaquinones and Methanophenazines ANME-2a en-coded a protein with a domain specific for PhzF which is anenzyme involved in phenazine biosynthesis in Pseudomonasfluorescens [152 153] The respective gene is not present in allmethanophenazine containing methanogens (in our genomecomparison only inM acetivorans andM formicica Table 2)so it is unclear whether this enzyme is really involved inmethanophenazine biosynthesis It is however likely thatANME-2a use methanophenazines in their respiratory chainsince gene domains for menaquinone biosynthesis wereabsent (Table 2) ldquoCa M nitroreducensrdquo probably uses

menaquinones as membrane-integral electron carrier sinceenvironmental genomes [28 43] encoded the futalosine(mqn) biosynthesis pathway as reported for Archaeoglobusfulgidus [154] (Table 2) Moreover ldquoCa M nitroreducensrdquoenrichment cultures showed absence of methanophenazines[43] ANME-1 also contained gene domains formenaquinonebiosynthesis via the futalosine (mqn) biosynthesis pathway(Table 2) Indications for a quinone biosynthesis pathwayin ANME-1 were previously found to be weak since onlysome of the Ubi homologues of the oxic ubiquinone biosyn-thesis pathway were detected [41] but the futalosine (mqn)biosynthesis pathway was overlooked in that particular anal-ysis Additionally ANME-1 have Fqo homologues similarto Archaeoglobus fulgidus [44] and expressed the catalyticsubunit FqoF [41] However since the phenazine biosynthesisdomain PhzF was also present in the ANME-1 genomes(Table 2) and Fpo and Fqo are homologues we cannotconclude on genomic information alone which redox shuttleis used by ANME-1 during AOM If ANME-1 would usemenaquinones this would have implications for subsequentelectron transfer to MHCs since methanophenazine (1198640 =minus165mV) [155] and menaquinone (1198640 = minus80mV) [156] havedifferent redox potentials

35 Cell Adhesion Some gene domains involved in cel-lular adhesion were more abundant in ANME than inmethanogens (Table 2) especially in ANME-2a and ANME-1that are known to form syntrophic interactions for electrontransfer during respiration These domains include HYR(IPR003410) and CARDB domains (IPR011635) that bothhave a direct role in cellular adhesion [157] (Table 2) Interest-ingly also domains related to the cellulosome of Clostridiumspecies termed dockerin and cohesin were highly abundantin both ANME-1 and ANME-2a as compared to ANME-2dand methanogens together with many carbohydrate bindingdomains (Table 2) In Clostridium species dockerin andcohesin form an anchor to the bacterial cell wall that containsa scaffold with cellulose-degrading enzymes and a carbohy-drate bindingmodule that binds cellulose altogether formingthe cellulosome [158] These domains have been found in alldomains of life irrespective of cellulose utilization but thefunction of such proteins outside of the cellulosome is notknown [159]Therefore dockerin cohesin and carbohydratebinding domains in ANME could hypothetically form aconstruct that binds to carbohydrates and could possibly havea function in cell-to-cell contact or MHC adhesion but thisneeds further investigation

4 Future Challenges

Advances in (meta)genomics transcriptomics and pro-teomics have produced the valuable metabolic blueprints ofdifferent ANMEwith hypotheses on how centralmetabolismelectron transport and energy conservation may functionFuture experiments are needed to biochemically demonstratethat these hypotheses are correct

The bottleneck for biochemical studies of ANME isthe lack of pure cultures due to the slow and syntrophic

Archaea 17

growth However the recent milestone discovery of directelectron transfer provides opportunities to grow ANMEas stated previously on electron accepting electrodes (ieanodes) [160] In this way pure or highly enriched culturesof different ANME without their respective syntrophic part-ner could be obtained and MHCs responsible for electricconduction could be biochemically characterized It seemsthat ANME-1 are limited by the size and abundance ofMHCs which could relate to differences in behavior onan anode The partner bacteria of ANME-1 and ANME-2could be investigated on an electron donating electrode (iecathode) with specific focus on the ability to produce pili (ienanowires) Also worth investigating is if besides ANME-2d ANME-2ab could also use insoluble electron acceptorsand if ANME-2d could donate electrons to a bacterialpartner

Another future challenge is to isolate and characterizeMcr from different ANME clades It needs to be investi-gated if Mcr abundance in ANME cells compensates forthe slow reverse activity or if modifications in the Mcrof ANME-1 also contribute to a better reverse activity ofMcr Moreover the effect of methane partial pressure onreaction rates and enzyme kinetics needs to be determined insitu

ANME-1 are potentially able to perform hydrogeno-trophic methanogenesis due to the presence of a hydrogenasein the genome Genetic indications of menaquinones aselectron carrier in ANME-1 and the various cellulosome andcell adhesion related gene domains in all ANME are alsotopics that could be explored further Methanogenic archaeaare likely not able to perform AOM but additional studieson TMO and more genetic modifications to stimulate AOMin methanogens could help in understanding the param-eters needed for AOM to occur Ultimately physiologicalunderstanding of ANME will help to explain the observedecological niche separation of different ANME clades and theoccurrence of ANMEwithout a bacterial partnerThis wouldgreatly enhance our knowledge of themethane cycle in anoxicenvironments

Competing Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors thank Stefanie Berger (RU Nijmegen) for criticalreading of the manuscript This research is supported bythe Soehngen Institute of Anaerobic Microbiology (SIAM)Gravitation grant (024002002) of the Netherlands Ministryof Education Culture and Science and the NetherlandsOrganisation for Scientific Research (NWO) Mike S MJetten was further supported by ERC AG 339880 Eco-MoMand Alfons J M Stams was supported by ERC AG 323009Novel Anaerobes

References

[1] A Boetius K Ravenschlag C J Schubert et al ldquoA marinemicrobial consortium apparently mediating anaerobic oxida-tion of methanerdquo Nature vol 407 no 6804 pp 623ndash626 2000

[2] K-U Hinrichs J M Hayes S P Sylva P G Brewert andE F DeLong ldquoMethane-consuming archaebacteria in marinesedimentsrdquo Nature vol 398 no 6730 pp 802ndash805 1999

[3] V J Orphan C H House K-U Hinrichs K D McKeeganand E F DeLong ldquoMethane-consuming archaea revealed bydirectly coupled isotopic and phylogenetic analysisrdquo Sciencevol 293 no 5529 pp 484ndash487 2001

[4] K-U Hinrichs and A Boetius ldquoThe anaerobic oxidation ofmethane new insights in microbial ecology and biogeochem-istryrdquo inOceanMargin Systems GWefer D Billett D HebbelnB B Joslashrgensen M Schluter and T VanWeering Eds pp 457ndash477 Springer Berlin Germany 2002

[5] K Knittel T Losekann A Boetius R Kort and R AmannldquoDiversity and distribution of methanotrophic archaea at coldseepsrdquo Applied and Environmental Microbiology vol 71 no 1pp 467ndash479 2005

[6] K Knittel and A Boetius ldquoAnaerobic oxidation of methaneprogress with an unknown processrdquo Annual Review of Micro-biology vol 63 pp 311ndash334 2009

[7] V J Orphan K-U Hinrichs W Ussler III et al ldquoComparativeanalysis of methane-oxidizing archaea and sulfate-reducingbacteria in anoxic marine sedimentsrdquoApplied and Environmen-tal Microbiology vol 67 no 4 pp 1922ndash1934 2001

[8] T Losekann K Knittel T Nadalig et al ldquoDiversity andabundance of aerobic and anaerobic methane oxidizers atthe Haakon Mosby Mud Volcano Barents Seardquo Applied andEnvironmentalMicrobiology vol 73 no 10 pp 3348ndash3362 2007

[9] H Niemann T Losekann D De Beer et al ldquoNovel microbialcommunities of the Haakon Mosby mud volcano and their roleas amethane sinkrdquoNature vol 443 no 7113 pp 854ndash858 2006

[10] TNunouraHOida T Toki J Ashi K Takai andKHorikoshildquoQuantification of mcrA by quantitative fluorescent PCR insediments from methane seep of the Nankai Troughrdquo FEMSMicrobiology Ecology vol 57 no 1 pp 149ndash157 2006

[11] B Orcutt A Boetius M Elvert V Samarkin and S B JoyeldquoMolecular biogeochemistry of sulfate reduction methanogen-esis and the anaerobic oxidation of methane at Gulf of Mexicocold seepsrdquoGeochimica et Cosmochimica Acta vol 69 no 17 pp4267ndash4281 2005

[12] V J Orphan W Ussler III T H Naehr C H House K-U Hinrichs and C K Paull ldquoGeological geochemical andmicrobiological heterogeneity of the seafloor around methanevents in the Eel River Basin offshore Californiardquo ChemicalGeology vol 205 no 3-4 pp 265ndash289 2004

[13] M G Pachiadaki A Kallionaki A Dahlmann G J De Langeand K A Kormas ldquoDiversity and spatial distribution ofprokaryotic communities along a sediment vertical profile ofa deep-sea mud volcanordquo Microbial Ecology vol 62 no 3 pp655ndash668 2011

[14] I Roalkvam H Dahle Y Chen S L Joslashrgensen H Haflidasonand I H Steen ldquoFine-scale community structure analysis ofANME in Nyegga sediments with high and low methane fluxrdquoFrontiers in Microbiology vol 3 p 216 2012

[15] K Yanagawa M Sunamura M A Lever et al ldquoNiche separa-tion of methanotrophic archaea (ANME-1 and -2) in methane-seep sediments of the Eastern Japan Sea offshore JoetsurdquoGeomicrobiology Journal vol 28 no 2 pp 118ndash129 2011

18 Archaea

[16] A Pernthaler A E Dekas C T Brown S K Goffredi TEmbaye and V J Orphan ldquoDiverse syntrophic partnershipsfromdeep-seamethane vents revealed by direct cell capture andmetagenomicsrdquo Proceedings of the National Academy of Sciencesof the United States of America vol 105 no 19 pp 7052ndash70572008

[17] R Hatzenpichler S A Connon D Goudeau R R Malm-strom T Woyke and V J Orphan ldquoVisualizing in situtranslational activity for identifying and sorting slow-growingarchaealminusbacterial consortiardquo Proceedings of the NationalAcademy of Sciences vol 113 no 28 pp E4069ndashE4078 2016

[18] L Maignien R J Parkes B Cragg et al ldquoAnaerobic oxidationof methane in hypersaline cold seep sedimentsrdquo FEMS Micro-biology Ecology vol 83 no 1 pp 214ndash231 2013

[19] V J Orphan C H House K-U Hinrichs K D McKeeganand E F DeLong ldquoMultiple archaeal groups mediate methaneoxidation in anoxic cold seep sedimentsrdquo Proceedings of theNational Academy of Sciences of the United States of Americavol 99 no 11 pp 7663ndash7668 2002

[20] T TreudeM Kruger A Boetius and B B Joslashrgensen ldquoEnviron-mental control on anaerobic oxidation of methane in the gassysediments of Eckernforde Bay (German Baltic)rdquo Limnology andOceanography vol 50 no 6 pp 1771ndash1786 2005

[21] G C Jagersma R J W Meulepas I Heikamp-De Jong etal ldquoMicrobial diversity and community structure of a highlyactive anaerobic methane-oxidizing sulfate-reducing enrich-mentrdquo Environmental Microbiology vol 11 no 12 pp 3223ndash3232 2009

[22] M Blumenberg R Seifert J Reitner T Pape andWMichaelisldquoMembrane lipid patterns typify distinct anaerobic methan-otrophic consortiardquo Proceedings of the National Academy ofSciences of the United States of America vol 101 no 30 pp 11111ndash11116 2004

[23] S Bertram M Blumenberg W Michaelis M Siegert MKruger and R Seifert ldquoMethanogenic capabilities of ANME-archaea deduced from 13C-labelling approachesrdquo Environmen-tal Microbiology vol 15 no 8 pp 2384ndash2393 2013

[24] K G Lloyd M J Alperin and A Teske ldquoEnvironmental evi-dence for net methane production and oxidation in putativeANaerobic MEthanotrophic (ANME) archaeardquo EnvironmentalMicrobiology vol 13 no 9 pp 2548ndash2564 2011

[25] M Takeuchi H Yoshioka Y Seo et al ldquoA distinct freshwater-adapted subgroup of ANME-1 dominates active archaeal com-munities in terrestrial subsurfaces in Japanrdquo EnvironmentalMicrobiology vol 13 no 12 pp 3206ndash3218 2011

[26] R T Amos B A Bekins I M Cozzarelli et al ldquoEvidence foriron-mediated anaerobic methane oxidation in a crude oil-contaminated aquiferrdquo Geobiology vol 10 no 6 pp 506ndash5172012

[27] P H Timmers D A Suarez-Zuluaga M van Rossem MDiender A J Stams and C M Plugge ldquoAnaerobic oxidationof methane associated with sulfate reduction in a naturalfreshwater gas sourcerdquo ISME Journal vol 10 pp 1400ndash14122015

[28] M F Haroon S Hu Y Shi et al ldquoAnaerobic oxidation ofmethane coupled to nitrate reduction in a novel archaeallineagerdquo Nature vol 500 no 7468 pp 567ndash570 2013

[29] H J Mills C Hodges K Wilson I R MacDonald and PA Sobecky ldquoMicrobial diversity in sediments associated withsurface-breaching gas hydrate mounds in the Gulf of MexicordquoFEMS Microbiology Ecology vol 46 no 1 pp 39ndash52 2003

[30] K G Lloyd L Lapham and A Teske ldquoAn anaerobic methane-oxidizing community of ANME-1b archaea in hypersaline gulfofMexico sedimentsrdquoApplied and EnvironmentalMicrobiologyvol 72 no 11 pp 7218ndash7230 2006

[31] A A Raghoebarsing A Pol K T Van De Pas-Schoonen et alldquoA microbial consortium couples anaerobic methane oxidationto denitrificationrdquoNature vol 440 no 7086 pp 918ndash921 2006

[32] S Hu R J Zeng L C Burow P Lant J Keller and Z YuanldquoEnrichment of denitrifying anaerobic methane oxidizingmicroorganismsrdquo Environmental Microbiology Reports vol 1no 5 pp 377ndash384 2009

[33] Z-W Ding J Ding L Fu F Zhang and R J Zeng ldquoSimultane-ous enrichment of denitrifying methanotrophs and anammoxbacteriardquo Applied Microbiology and Biotechnology vol 98 no24 pp 10211ndash10221 2014

[34] R Seifert K Nauhaus M Blumenberg M Kruger and WMichaelis ldquoMethane dynamics in a microbial community ofthe Black Sea traced by stable carbon isotopes in vitrordquoOrganicGeochemistry vol 37 no 10 pp 1411ndash1419 2006

[35] J Ding Z-W Ding L Fu Y-Z Lu S H Cheng and R JZeng ldquoNew primers for detecting and quantifying denitrifyinganaerobic methane oxidation archaea in different ecologicalnichesrdquo Applied Microbiology and Biotechnology vol 99 no 22pp 9805ndash9812 2015

[36] A Vaksmaa C Luke T van Alen et al ldquoDistribution and activ-ity of the anaerobic methanotrophic community in a nitrogen-fertilized Italian paddy soilrdquo FEMS Microbiology Ecology vol92 no 12 2016

[37] P N Evans D H Parks G L Chadwick et al ldquoMethanemetabolism in the archaeal phylum Bathyarchaeota revealed bygenome-centric metagenomicsrdquo Science vol 350 no 6259 pp434ndash438 2015

[38] I Vanwonterghem P N Evans D H Parks et al ldquoMethy-lotrophic methanogenesis discovered in the archaeal phylumVerstraetearchaeotardquo Nature Microbiology vol 1 Article ID16170 2016

[39] P Worm J J Koehorst M Visser et al ldquoA genomic view onsyntrophic versus non-syntrophic lifestyle in anaerobic fattyacid degrading communitiesrdquo Biochimica et Biophysica ActamdashBioenergetics vol 1837 no 12 pp 2004ndash2016 2014

[40] R Stokke I Roalkvam A Lanzen H Haflidason and I HSteen ldquoIntegrated metagenomic and metaproteomic analysesof an ANME-1-dominated community in marine cold seepsedimentsrdquo Environmental Microbiology vol 14 no 5 pp 1333ndash1346 2012

[41] A Meyerdierks M Kube I Kostadinov et al ldquoMetagenomeand mRNA expression analyses of anaerobic methanotrophicarchaea of the ANME-1 grouprdquo Environmental Microbiologyvol 12 no 2 pp 422ndash439 2010

[42] F-P Wang Y Zhang Y Chen et al ldquoMethanotrophicarchaea possessing diverging methane-oxidizing and electron-transporting pathwaysrdquo ISME Journal vol 8 no 5 pp 1069ndash1078 2014

[43] A Arshad D R Speth R M de Graaf H J Op den Camp MS Jetten and C U Welte ldquoA metagenomics-based metabolicmodel of nitrate-dependent anaerobic oxidation of methane byMethanoperedens-like archaeardquo Frontiers inMicrobiology vol 6article1423 2015

[44] S J Hallam N Putnam CM Preston et al ldquoReversemethano-genesis testing the hypothesis with environmental genomicsrdquoScience vol 305 no 5689 pp 1457ndash1462 2004

Archaea 19

[45] R K Thauer ldquoAnaerobic oxidation of methane with sulfate onthe reversibility of the reactions that are catalyzed by enzymesalso involved inmethanogenesis fromCO

2rdquoCurrent Opinion in

Microbiology vol 14 no 3 pp 292ndash299 2011[46] U Deppenmeier V Muller and G Gottschalk ldquoPathways of

energy conservation in methanogenic archaeardquo Archives ofMicrobiology vol 165 no 3 pp 149ndash163 1996

[47] A-K Kaster J Moll K Parey and R K Thauer ldquoCoupling offerredoxin and heterodisulfide reduction via electron bifurca-tion in hydrogenotrophic methanogenic archaeardquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 108 no 7 pp 2981ndash2986 2011

[48] R K Thauer A-K Kaster H Seedorf W Buckel and RHedderich ldquoMethanogenic archaea ecologically relevant dif-ferences in energy conservationrdquo Nature Reviews Microbiologyvol 6 no 8 pp 579ndash591 2008

[49] W Ludwig O Strunk R Westram et al ldquoARB a softwareenvironment for sequence datardquoNucleic Acids Research vol 32no 4 pp 1363ndash1371 2004

[50] E Pruesse C Quast K Knittel et al ldquoSILVA a comprehensiveonline resource for quality checked and aligned ribosomal RNAsequence data compatible with ARBrdquo Nucleic Acids Researchvol 35 no 21 pp 7188ndash7196 2007

[51] J J Marlow C T Skennerton Z Li et al ldquoProteomic stableisotope probing reveals biosynthesis dynamics of slow growingmethane based microbial communitiesrdquo Frontiers in Microbiol-ogy vol 7 article 386 2016

[52] P V Welander and W W Metcalf ldquoLoss of the mtr operon inMethanosarcina blocks growth on methanol but not methano-genesis and reveals an unknown methanogenic pathwayrdquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 102 no 30 pp 10664ndash10669 2005

[53] P V Welander and W W Metcalf ldquoMutagenesis of the C1oxidation pathway inmethanosarcina barkeri new insights intothe MtrMer bypass pathwayrdquo Journal of Bacteriology vol 190no 6 pp 1928ndash1936 2008

[54] M Goenrich R K Thauer H Yurimoto and N KatoldquoFormaldehyde activating enzyme (Fae) and hexulose-6-phosphate synthase (Hps) inMethanosarcina barkeri a possiblefunction in ribose-5-phosphate biosynthesisrdquoArchives ofMicro-biology vol 184 no 1 pp 41ndash48 2005

[55] M Goenrich FMahlert E C Duin C Bauer B Jaun and R KThauer ldquoProbing the reactivity of Ni in the active site of methyl-coenzyme M reductase with substrate analoguesrdquo Journal ofBiological Inorganic Chemistry vol 9 no 6 pp 691ndash705 2004

[56] S Scheller M Goenrich R Boecher R K Thauer and BJaun ldquoThe key nickel enzyme of methanogenesis catalyses theanaerobic oxidation of methanerdquo Nature vol 465 no 7298 pp606ndash608 2010

[57] K Nauhaus A Boetius M Kruger and F Widdel ldquoIn vitrodemonstration of anaerobic oxidation of methane coupled tosulphate reduction in sediment from amarine gas hydrate areardquoEnvironmental Microbiology vol 4 no 5 pp 296ndash305 2002

[58] Y Zhang J-P Henriet J Bursens and N Boon ldquoStimulationof in vitro anaerobic oxidation of methane rate in a continuoushigh-pressure bioreactorrdquo Bioresource Technology vol 101 no9 pp 3132ndash3138 2010

[59] M Kruger T Treude H Wolters K Nauhaus and A BoetiusldquoMicrobial methane turnover in different marine habitatsrdquoPalaeogeography Palaeoclimatology Palaeoecology vol 227 no1ndash3 pp 6ndash17 2005

[60] C Deusner V Meyer and T G Ferdelman ldquoHigh-pressuresystems for gas-phase free continuous incubation of enrichedmarinemicrobial communities performing anaerobic oxidationof methanerdquo Biotechnology and Bioengineering vol 105 no 3pp 524ndash533 2010

[61] K Nauhaus T Treude A Boetius and M Kruger ldquoEnviron-mental regulation of the anaerobic oxidation of methane acomparison of ANME-I and ANME-II communitiesrdquo Environ-mental Microbiology vol 7 no 1 pp 98ndash106 2005

[62] T Treude V Orphan K Knittel A Gieseke C H House andA Boetius ldquoConsumption of methane and CO

2by methan-

otrophicmicrobial mats from gas seeps of the anoxic Black SeardquoApplied and EnvironmentalMicrobiology vol 73 no 7 pp 2271ndash2283 2007

[63] T Holler F Widdel K Knittel et al ldquoThermophilic anaerobicoxidation of methane by marine microbial consortiardquo ISMEJournal vol 5 no 12 pp 1946ndash1956 2011

[64] M Kruger M Blumenberg S Kasten et al ldquoA novel multi-layered methanotrophic microbial mat system growing on thesediment of the Black Seardquo Environmental Microbiology vol 10no 8 pp 1934ndash1947 2008

[65] R J WMeulepas C G Jagersma J Gieteling C J N BuismanA J M Stams and P N L Lens ldquoEnrichment of anaerobicmethanotrophs in sulfate-reducing membrane bioreactorsrdquoBiotechnology and Bioengineering vol 104 no 3 pp 458ndash4702009

[66] T Holler G Wegener H Niemann et al ldquoCarbon and sulfurback flux during anaerobic microbial oxidation of methane andcoupled sulfate reductionrdquo Proceedings of the National Academyof Sciences of the United States of America vol 108 no 52 ppE1484ndashE1490 2011

[67] M Kruger AMeyerdierks F O Glockner et al ldquoA conspicuousnickel protein in microbial mats that oxidize methane anaero-bicallyrdquo Nature vol 426 no 6968 pp 878ndash881 2003

[68] S Mayr C Latkoczy M Kruger et al ldquoStructure of an F430

variant from archaea associated with anaerobic oxidation ofmethanerdquo Journal of the American Chemical Society vol 130 no32 pp 10758ndash10767 2008

[69] S Shima and R K Thauer ldquoMethyl-coenzyme M reductaseand the anaerobic oxidation of methane in methanotrophicArchaeardquo Current Opinion in Microbiology vol 8 no 6 pp643ndash648 2005

[70] R K Thauer and S Shima ldquoMethane as fuel for anaerobicmicroorganismsrdquo Annals of the New York Academy of Sciencesvol 1125 pp 158ndash170 2008

[71] S Yamamoto J B Alcauskas and T E Crozier ldquoSolubility ofmethane in distilled water and seawaterrdquo Journal of Chemicaland Engineering Data vol 21 no 1 pp 78ndash80 1976

[72] P H A Timmers J Gieteling H C A Widjaja-Greefkeset al ldquoGrowth of anaerobic methane-oxidizing archaea andsulfate-reducing bacteria in a high-pressure membrane capsulebioreactorrdquoApplied and EnvironmentalMicrobiology vol 81 no4 pp 1286ndash1296 2015

[73] MKruger HWoltersMGehre S B Joye andH-H RichnowldquoTracing the slow growth of anaerobic methane-oxidizingcommunities by 15N-labelling techniquesrdquo FEMS MicrobiologyEcology vol 63 no 3 pp 401ndash411 2008

[74] R J W Meulepas C G Jagersma A F Khadem C J N Buis-man A J M Stams and P N L Lens ldquoEffect of environmentalconditions on sulfate reduction withmethane as electron donorby an Eckernforde Bay enrichmentrdquo Environmental Science andTechnology vol 43 no 17 pp 6553ndash6559 2009

20 Archaea

[75] M W Bowles V A Samarkin and S B Joye ldquoImprovedmeasurement of microbial activity in deep-sea sediments atin situ pressure and methane concentrationrdquo Limnology andOceanography Methods vol 9 pp 499ndash506 2011

[76] S Shima M Krueger T Weinert et al ldquoStructure of a methyl-coenzyme M reductase from Black Sea mats that oxidizemethane anaerobicallyrdquo Nature vol 481 no 7379 pp 98ndash1012012

[77] K D Allen G Wegener and R H White ldquoDiscovery of multi-ple modified F-430 coenzymes in methanogens and anaerobicmethanotrophic archaea suggests possible new roles for F-430in naturerdquoApplied and Environmental Microbiology vol 80 no20 pp 6403ndash6412 2014

[78] V W Soo M J McAnulty A Tripathi et al ldquoReversingmethanogenesis to capture methane for liquid biofuel precur-sorsrdquoMicrobial Cell Factories vol 15 article 11 2016

[79] D L Valentine and W S Reeburgh ldquoNew perspectives onanaerobicmethane oxidationrdquoEnvironmentalMicrobiology vol2 no 5 pp 477ndash484 2000

[80] D L Valentine ldquoBiogeochemistry and microbial ecology ofmethane oxidation in anoxic environments a reviewrdquo Antonievan Leeuwenhoek International Journal of General and Molecu-lar Microbiology vol 81 no 1-4 pp 271ndash282 2002

[81] A J B Zehnder and T D Brock ldquoMethane formation andmethane oxidation by methanogenic bacteriardquo Journal of Bac-teriology vol 137 no 1 pp 420ndash432 1979

[82] J Harder ldquoAnaerobic methane oxidation by bacteria employ-ing 14C-methane uncontaminated with 14C-carbon monoxiderdquoMarine Geology vol 137 no 1-2 pp 13ndash23 1997

[83] J J Moran C H House K H Freeman and J G FerryldquoTrace methane oxidation studied in several Euryarchaeotaunder diverse conditionsrdquo Archaea vol 1 no 5 pp 303ndash3092005

[84] J J Moran C H House B Thomas and K H FreemanldquoProducts of tracemethane oxidation during nonmethyltrophicgrowth by Methanosarcinardquo Journal of Geophysical ResearchBiogeosciences vol 112 no 2 2007

[85] R J W Meulepas C G Jagersma Y Zhang et al ldquoTracemethane oxidation and the methane dependency of sulfatereduction in anaerobic granular sludgerdquo FEMS MicrobiologyEcology vol 72 no 2 pp 261ndash271 2010

[86] A J B Zehnder andTD Brock ldquoAnaerobicmethane oxidationoccurrence and ecologyrdquoApplied and Environmental Microbiol-ogy vol 39 no 1 pp 194ndash204 1980

[87] S J Blazewicz D G Petersen M P Waldrop and M K Fire-stone ldquoAnaerobic oxidation of methane in tropical and borealsoils ecological significance in terrestrial methane cyclingrdquoJournal of Geophysical Research Biogeosciences vol 117 no 2Article ID G02033 2012

[88] K A Smemo and J B Yavitt ldquoEvidence for anaerobic CH4

oxidation in freshwater peatlandsrdquo Geomicrobiology Journalvol 24 no 7-8 pp 583ndash597 2007

[89] M J Alperin and T M Hoehler ldquoAnaerobic methane oxidationby archaeasulfate-reducing bacteria aggregates 1 Thermody-namic and physical constraintsrdquo American Journal of Sciencevol 309 no 10 pp 869ndash957 2009

[90] S L Caldwell J R Laidler E A Brewer J O Eberly S CSandborgh and F S Colwell ldquoAnaerobic oxidation of methanemechanisms bioenergetics and the ecology of associatedmicroorganismsrdquo Environmental Science and Technology vol42 no 18 pp 6791ndash6799 2008

[91] GWang A J Spivack and S DrsquoHondt ldquoGibbs energies of reac-tion and microbial mutualism in anaerobic deep subseafloorsediments of ODP Site 1226rdquoGeochimica et Cosmochimica Actavol 74 no 14 pp 3938ndash3947 2010

[92] P R Girguis A E Cozen and E F DeLong ldquoGrowth andpopulation dynamics of anaerobic methane-oxidizing archaeaand sulfate-reducing bacteria in a continuous-flow bioreactorrdquoApplied and EnvironmentalMicrobiology vol 71 no 7 pp 3725ndash3733 2005

[93] K Nauhaus M Albrecht M Elvert A Boetius and F WiddelldquoIn vitro cell growth ofmarine archaeal-bacterial consortia dur-ing anaerobic oxidation ofmethanewith sulfaterdquoEnvironmentalMicrobiology vol 9 no 1 pp 187ndash196 2007

[94] B Orcutt V Samarkin A Boetius and S Joye ldquoOn the relation-ship between methane production and oxidation by anaerobicmethanotrophic communities from cold seeps of the Gulf ofMexicordquo Environmental Microbiology vol 10 no 5 pp 1108ndash1117 2008

[95] M Y Yoshinaga T Holler T Goldhammer et al ldquoCarbon iso-tope equilibration during sulphate-limited anaerobic oxidationof methanerdquo Nature Geoscience vol 7 no 3 pp 190ndash194 2014

[96] T Treude J Niggemann J Kallmeyer et al ldquoAnaerobic oxi-dation of methane and sulfate reduction along the Chileancontinental marginrdquo Geochimica et Cosmochimica Acta vol 69no 11 pp 2767ndash2779 2005

[97] R J Parkes B A Cragg N Banning et al ldquoBiogeochemistryand biodiversity of methane cycling in subsurface marinesediments (SkagerrakDenmark)rdquoEnvironmentalMicrobiologyvol 9 no 5 pp 1146ndash1161 2007

[98] N J Knab B A Cragg E R C Hornibrook et al ldquoRegulationof anaerobic methane oxidation in sediments of the Black SeardquoBiogeosciences vol 6 no 8 pp 1505ndash1518 2009

[99] H Yoshioka A Maruyama T Nakamura et al ldquoActivities anddistribution of methanogenic and methane-oxidizing microbesin marine sediments from the Cascadia Marginrdquo Geobiologyvol 8 no 3 pp 223ndash233 2010

[100] G Wegener V Krukenberg S E Ruff M Y Kellermann andK Knittel ldquoMetabolic capabilities of microorganisms involvedin and associated with the anaerobic oxidation of methanerdquoFrontiers in Microbiology vol 7 article 46 2016

[101] R J W Meulepas C G Jagersma A F Khadem A J MStams and P N L Lens ldquoEffect of methanogenic substrateson anaerobic oxidation of methane and sulfate reduction by ananaerobic methanotrophic enrichmentrdquo Applied Microbiologyand Biotechnology vol 87 no 4 pp 1499ndash1506 2010

[102] J Milucka T G Ferdelman L Polerecky et al ldquoZero-valentsulphur is a key intermediate in marine methane oxidationrdquoNature vol 491 no 7425 pp 541ndash546 2012

[103] W Michaelis R Seifert K Nauhaus et al ldquoMicrobial reefs inthe black sea fueled by anaerobic oxidation ofmethanerdquo Sciencevol 297 no 5583 pp 1013ndash1015 2002

[104] A Vigneron P Cruaud P Pignet et al ldquoArchaeal and anaerobicmethane oxidizer communities in the Sonora Margin coldseeps Guaymas Basin (Gulf of California)rdquo ISME Journal vol7 no 8 pp 1595ndash1608 2013

[105] M Alperin and T Hoehler ldquoThe ongoing mystery of sea-floormethanerdquo Science vol 329 no 5989 pp 288ndash289 2010

[106] B Orcutt and C Meile ldquoConstraints on mechanisms and ratesof anaerobic oxidation of methane by microbial consortiaprocess-basedmodeling of ANME-2 archaea and sulfate reduc-ing bacteria interactionsrdquo Biogeosciences vol 5 no 6 pp 1587ndash1599 2008

Archaea 21

[107] S E McGlynn G L Chadwick C P Kempes and V J OrphanldquoSingle cell activity reveals direct electron transfer in methan-otrophic consortiardquoNature vol 526 no 7574 pp 531ndash535 2015

[108] D R Lovley ldquoElectromicrobiologyrdquo Annual Review of Microbi-ology vol 66 pp 391ndash409 2012

[109] S M Strycharz-Glaven R M Snider A Guiseppi-Elie andL M Tender ldquoOn the electrical conductivity of microbialnanowires and biofilmsrdquoEnergy and Environmental Science vol4 no 11 pp 4366ndash4379 2011

[110] D J Richardson J N Butt J K Fredrickson et al ldquoThe lsquoporinndashcytochromersquo model for microbe-to-mineral electron transferrdquoMolecular Microbiology vol 85 no 2 pp 201ndash212 2012

[111] A Okamoto K Hashimoto and R Nakamura ldquoLong-rangeelectron conduction of Shewanella biofilms mediated by outermembrane C-type cytochromesrdquo Bioelectrochemistry vol 85pp 61ndash65 2012

[112] M Y El-Naggar G Wanger K M Leung et al ldquoElectricaltransport along bacterial nanowires from Shewanella oneidensisMR-1rdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 107 no 42 pp 18127ndash18131 2010

[113] G Reguera K D McCarthy T Mehta J S Nicoll M TTuominen and D R Lovley ldquoExtracellular electron transfer viamicrobial nanowiresrdquo Nature vol 435 no 7045 pp 1098ndash11012005

[114] Z M Summers H E Fogarty C Leang A E Franks N SMalvankar and D R Lovley ldquoDirect exchange of electronswithin aggregates of an evolved syntrophic coculture of anaer-obic bacteriardquo Science vol 330 no 6009 pp 1413ndash1415 2010

[115] A Kletzin T Heimerl J Flechsler L V Niftrik R Rachel andA Klingl ldquoCytochromes c in archaea distribution maturationcell architecture and the special case of Ignicoccus hospitalisrdquoFrontiers in Microbiology vol 6 article 439 2015

[116] GWegener V Krukenberg D Riedel H E Tegetmeyer and ABoetius ldquoIntercellular wiring enables electron transfer betweenmethanotrophic archaea and bacteriardquo Nature vol 526 no7574 pp 587ndash590 2015

[117] D HHaft S H Payne and J D Selengut ldquoArchaeosortases andexosortases are widely distributed systems linking membranetransit with posttranslational modificationrdquo Journal of Bacteri-ology vol 194 no 1 pp 36ndash48 2012

[118] A Marchler-Bauer M K Derbyshire N R Gonzales et alldquoCDD NCBIrsquos conserved domain databaserdquo Nucleic AcidsResearch vol 43 no 1 pp D222ndashD226 2015

[119] A Mitchell H-Y Chang L Daugherty et al ldquoThe InterProprotein families database the classification resource after 15yearsrdquo Nucleic Acids Research vol 43 no 1 pp D213ndashD2212015

[120] V Krukenberg K Harding M Richter et al ldquoCandidatusdesulfofervidus auxilii a hydrogenotrophic sulfate-reducingbacterium involved in the thermophilic anaerobic oxidation ofmethanerdquo Environmental Microbiology vol 18 pp 3073ndash30912016

[121] L Shi T C Squier J M Zachara and J K Fredrickson ldquoRes-piration of metal (hydr)oxides by Shewanella and Geobactera key role for multihaem c-type cytochromesrdquo MolecularMicrobiology vol 65 no 1 pp 12ndash20 2007

[122] N S Malvankar and D R Lovley ldquoMicrobial nanowires forbioenergy applicationsrdquo Current Opinion in Biotechnology vol27 pp 88ndash95 2014

[123] A-E Rotaru T LWoodard K PNevin andDR Lovley ldquoLinkbetween capacity for current production and syntrophic growth

in Geobacter speciesrdquo Frontiers in Microbiology vol 6 article744 2015

[124] A-E Rotaru P M Shrestha F Liu et al ldquoDirect interspecieselectron transfer between Geobacter metallireducens andMethanosarcina barkerirdquo Applied and Environmental Microbi-ology vol 80 no 15 pp 4599ndash4605 2014

[125] S Scheller H Yu G L Chadwick S E McGlynn and VJ Orphan ldquoArtificial electron acceptors decouple archaealmethane oxidation from sulfate reductionrdquo Science vol 351 no6274 pp 703ndash707 2016

[126] J Milucka F Widdel and S Shima ldquoImmunological detec-tion of enzymes for sulfate reduction in anaerobic methane-oxidizing consortiardquo Environmental Microbiology vol 15 no 5pp 1561ndash1571 2013

[127] P Cabello M D Roldan and C Moreno-Vivian ldquoNitratereduction and the nitrogen cycle in archaeardquoMicrobiology vol150 no 11 pp 3527ndash3546 2004

[128] R MMartinez-Espinosa E J Dridge M J Bonete et al ldquoLookon the positive sideThe orientation identification and bioener-getics of lsquoArchaealrsquomembrane-boundnitrate reductasesrdquoFEMSMicrobiology Letters vol 276 no 2 pp 129ndash139 2007

[129] S de VriesMMomcilovicM J F Strampraad J PWhiteleggeA Baghai and I Schroder ldquoAdaptation to a high-tungsten envi-ronment pyrobaculum aerophilum contains an active tungstennitrate reductaserdquo Biochemistry vol 49 no 45 pp 9911ndash99212010

[130] M Egger O Rasigraf C J Sapart et al ldquoIron-mediated anaer-obic oxidation of methane in brackish coastal sedimentsrdquoEnvironmental Science and Technology vol 49 no 1 pp 277ndash283 2015

[131] T Treude S Krause J Maltby A W Dale R Coffin and LJ Hamdan ldquoSulfate reduction and methane oxidation activitybelow the sulfate-methane transition zone in Alaskan BeaufortSea continental margin sediments implications for deep sulfurcyclingrdquo Geochimica et Cosmochimica Acta vol 144 pp 217ndash237 2014

[132] N Riedinger M J Formolo T W Lyons S Henkel A Beckand S Kasten ldquoAn inorganic geochemical argument for coupledanaerobic oxidation of methane and iron reduction in marinesedimentsrdquo Geobiology vol 12 no 2 pp 172ndash181 2014

[133] Y-H Chang T-W Cheng W-J Lai et al ldquoMicrobial methanecycling in a terrestrialmud volcano in eastern Taiwanrdquo Environ-mental Microbiology vol 14 no 4 pp 895ndash908 2012

[134] S A Crowe S Katsev K Leslie et al ldquoThe methane cycle inferruginous Lake Matanordquo Geobiology vol 9 no 1 pp 61ndash782011

[135] O Sivan M Adler A Pearson et al ldquoGeochemical evidence foriron-mediated anaerobic oxidation of methanerdquo Limnology andOceanography vol 56 no 4 pp 1536ndash1544 2011

[136] K E A Segarra C Comerford J Slaughter and S B JoyeldquoImpact of electron acceptor availability on the anaerobic oxi-dation of methane in coastal freshwater and brackish wetlandsedimentsrdquo Geochimica et Cosmochimica Acta vol 115 pp 15ndash30 2013

[137] V Gupta K A Smemo J B Yavitt D Fowle B Branfireunand N Basiliko ldquoStable isotopes reveal widespread anaerobicmethane oxidation across latitude and peatland typerdquo Environ-mental Science and Technology vol 47 no 15 pp 8273ndash82792013

[138] O Oni T Miyatake S Kasten et al ldquoDistinct microbialpopulations are tightly linked to the profile of dissolved iron in

22 Archaea

the methanic sediments of the Helgolandmud area North SeardquoFrontiers in Microbiology vol 6 2015

[139] E J Beal C H House and V J Orphan ldquoManganese- andiron-dependent marine methane oxidationrdquo Science vol 325no 5937 pp 184ndash187 2009

[140] M W Bowles V A Samarkin K M Bowles and S B JoyeldquoWeak coupling between sulfate reduction and the anaerobicoxidation of methane in methane-rich seafloor sedimentsduring ex situ incubationrdquo Geochimica et Cosmochimica Actavol 75 no 2 pp 500ndash519 2011

[141] Y Z Lu L Fu J Ding Z Ding N Li and R J Zeng ldquoCr(VI)reduction coupled with anaerobic oxidation of methane in alaboratory reactorrdquoWater Research vol 102 pp 445ndash452 2016

[142] K F Ettwig B Zhu D Speth J T Keltjens M S Jetten and BKartal ldquoArchaea catalyze iron-dependent anaerobic oxidationof methanerdquo Proceedings of the National Academy of Sciences ofthe United States of America vol 113 no 45 pp 12792ndash127962016

[143] T M Flynn R A Sanford H Ryu et al ldquoFunctional microbialdiversity explains groundwater chemistry in a pristine aquiferrdquoBMCMicrobiology vol 13 no 1 article no 146 2013

[144] C J Schubert F Vazquez T Losekann-Behrens K KnittelM Tonolla and A Boetius ldquoEvidence for anaerobic oxidationof methane in sediments of a freshwater system (Lago diCadagno)rdquo FEMS Microbiology Ecology vol 76 no 1 pp 26ndash38 2011

[145] K E A Segarra F Schubotz V Samarkin M Y Yoshinaga K-U Hinrichs and S B Joye ldquoHigh rates of anaerobic methaneoxidation in freshwater wetlands reduce potential atmosphericmethane emissionsrdquo Nature Communications vol 6 article7477 2015

[146] E J Beal M W Claire and C H House ldquoHigh rates ofanaerobic methanotrophy at low sulfate concentrations withimplications for past and present methane levelsrdquo Geobiologyvol 9 no 2 pp 131ndash139 2011

[147] F Kracke I Vassilev and J O Kromer ldquoMicrobial electrontransport and energy conservationmdashthe foundation for opti-mizing bioelectrochemical systemsrdquo Frontiers in Microbiologyvol 6 article 575 2015

[148] C L Reardon A C Dohnalkova P Nachimuthu et al ldquoRoleof outer-membrane cytochromes MtrC and OmcA in thebiomineralization of ferrihydrite by Shewanella oneidensisMR-1rdquo Geobiology vol 8 no 1 pp 56ndash68 2010

[149] L Shi B Chen Z Wang et al ldquoIsolation of a high-affinityfunctional protein complex between OmcA and MtrC twoouter membrane decaheme c-type cytochromes of Shewanellaoneidensis MR-1rdquo Journal of Bacteriology vol 188 no 13 pp4705ndash4714 2006

[150] X Qian T Mester L Morgado et al ldquoBiochemical charac-terization of purified OmcS a c-type cytochrome requiredfor insoluble Fe(III) reduction in Geobacter sulfurreducensrdquoBiochimica et BiophysicaActamdashBioenergetics vol 1807 no 4 pp404ndash412 2011

[151] T Mehta M V Coppi S E Childers and D R Lovley ldquoOutermembrane c-type cytochromes required for Fe(III) andMn(IV)oxide reduction in Geobacter sulfurreducensrdquo Applied andEnvironmentalMicrobiology vol 71 no 12 pp 8634ndash8641 2005

[152] W Blankenfeldt A P Kuzin T Skarina et al ldquoStructure andfunction of the phenazine biosynthetic protein PhzF fromPseudomonas fluorescensrdquoProceedings of theNational Academyof Sciences of the United States of America vol 101 no 47 pp16431ndash16436 2004

[153] J F Parsons F Song L Parsons K Calabrese E Eisensteinand J E Ladner ldquoStructure and function of the phenazinebiosynthesis protein PhzF fromPseudomonas fluorescens 2-79rdquoBiochemistry vol 43 no 39 pp 12427ndash12435 2004

[154] T Hiratsuka K Furihata J Ishikawa et al ldquoAn alternativemenaquinone biosynthetic pathway operating in microorgan-ismsrdquo Science vol 321 no 5896 pp 1670ndash1673 2008

[155] M Tietze A Beuchle I Lamla et al ldquoRedox potentials ofmethanophenazine and CoB-S-S-CoM factors involved inelectron transport in methanogenic archaeardquo ChemBioChemvol 4 no 4 pp 333ndash335 2003

[156] Q H Tran and G Unden ldquoChanges in the proton potentialand the cellular energetics of Escherichia coli during growth byaerobic and anaerobic respiration or by fermentationrdquoEuropeanJournal of Biochemistry vol 251 no 1-2 pp 538ndash543 1998

[157] I Callebaut D Gilges I Vigon and J-P Mornon ldquoHYR anextracellular module involved in cellular adhesion and relatedto the immunoglobulin-like foldrdquo Protein Science vol 9 no 7pp 1382ndash1390 2000

[158] H J Gilbert ldquoCellulosomes microbial nanomachines that dis-play plasticity in quaternary structurerdquoMolecular Microbiologyvol 63 no 6 pp 1568ndash1576 2007

[159] A Peer S P Smith E A Bayer R Lamed and I BorovokldquoNoncellulosomal cohesin- and dockerin-like modules in thethree domains of liferdquo FEMS Microbiology Letters vol 291 no1 pp 1ndash16 2009

[160] M Wagner ldquoMicrobiology conductive consortiardquo Nature vol526 no 7574 pp 513ndash514 2015

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

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The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

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Signal TransductionJournal of

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Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Enzyme Research

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International Journal of

Microbiology

Archaea 11

MHC

MHCS-layer

2H+

minuse

cyt b

Mch

Mer

Mtd

Ftr

Fmd

Mcr

MPh

HdrABC

MPh

MHC

MHC

MPh

CoB-S-S-CoM

CoB-SH

CoM-SH

HdrDE

Mtr

Fpo

Fpo

Rnf

MPhH2

MPhH2

MPhH2

MPhH2

CH4

CH3-CoM

CH3-H4MPT

F420H2

F420

F420H2

F420

CH2=H4MPT

CHequivH4MPT

CHO-H4MPT

CHO-MFR

CO2

Fdred

Fdox

H2O

2Na+

MPh

minuse

S-layer

MHC

SRB 2H+

2H+

2Na+

minuse

minuse

minuse

Figure 4 Methanotrophic pathway during S-AOM by ANME-2a [42] Red lines indicate reversal of the hydrogenotrophic methanogenicpathway See Table 3 for nomenclature

CoM-SH and CoB-SH are substrates of the methanotrophicenzyme However several posttranslational modifications ofamino acids were different betweenmethanogens andANMEarchaea and the cofactor F

430(the prosthetic group of Mcr)

is modified in ANME-1 but not in ANME-2 or ANME-3archaea [51 63 67 68 76 77] Furthermore ANME-1 seemsto lack the noncatalytic proteinDdomain of themcr gene thatis present in all other methanogens and methanotrophs butof which the function is unknown (IPR003901 Table 2) [51]A metabolically engineered Methanosarcina acetivorans wasable to convert methane and CO

2to acetate with a plasmid

containingMcr derived from ANME-1 [78] It is thus unclearif only thermodynamic constraints and the abundance ofMcrensureAOMactivity or if also specificmodifications canhavean effect on the reverse activity of Mcr

23 Methane Oxidation by Methanogens Pure cultures ofmethanogens were not able to oxidize methane under highmethane and low hydrogen concentrations (reviewed in[79 80]) Methanogens are only able to oxidize methaneduring net methane production [81] Labeled methane addi-tion (13C or 14C) to pure cultures of methanogens showedproduction of labeled CO

2during net methane production

This characteristic was confirmed with several pure culturesof methanogens [82ndash84] The process was called ldquotracemethane oxidationrdquo (TMO) since the CO

2was formed in

trace amounts relative to the methane produced [83] It isnot clear if TMO is due to the reported reversibility ofindividual enzymes [66] or if it is an active microbial processfrom which energy can be conserved TMO was speculatedto be an active metabolic process for three reasons (1)the amount of methane oxidized varied between differentspecies of methanogens grown on the same methanogenicsubstrate (2) the amount ofmethane oxidized varied betweendifferent methanogenic substrates and (3) TMO productsvaried between different methanogenic substrates [83 84]For instance when grown on acetate Methanosarcina ace-tivorans produced labeled acetate from labeled methaneWhen grown on carbon monoxide it produced both labeledacetate and methyl sulfides from labeled methane [84] Dur-ing hydrogenotrophic and methylotrophic methanogenesisTMO mainly produced CO

2from labeled methane [83]

However in contrast with AOM TMO rates never exceededmethanogenesis rates even during long-term incubationwith methane and sulfate [85] It seems that methanogensare not able to conserve energy from TMO even under

12 Archaea

Mch

Mer

Mtd

Ftr

Fmd

Mcr

MQ

MQ

EchHdrFrh

3MQ

HdrABC

MQ

cyt b Mtr

NrfH

cyt c

NrfA

CoB-S-S-CoM

CoB-SH

CoM-SH

HdrDE

HCOIIHCOIINapHOrf7

NarGH

S-layer

Fqo

Fqo

3H+

3H+

4H+

CH4

CH3-CoM

CH3-H4MPT

F420

F420H2

F420

F420H2

CH2=H4MPT

CHequivH4MPT

CHO-H4MPT

CHO-MFR

CO2

Fdred

Fdox

H2O

2Na+

NH4+

NO2minus

NO2minus

NO3minus

3MQH2

MQH2

MQH2

MQH2eminus

eminus

Rieske

Figure 5 Methanotrophic pathway during N-AOM by ldquoCaM nitroreducensrdquo MPEBLZ (ANME-2d) [43] Red lines indicate reversal of thehydrogenotrophic methanogenic pathway See Table 3 for nomenclature

thermodynamically favourable conditions TMOoccurs bothin absence and presence of an external electron acceptor andonly during net methanogenesis It is therefore most likelycaused by the reported back flux of individual enzymes of themethanogenic pathway [66]

TMO also occurred in granular sludge and in freshwaterand terrestrial samples These mixed communities showedhigher TMO rates than pure cultures reaching up to 90of the methane produced [27 85ndash87] TMO should thereforebe carefully considered in the experimental setup and inter-pretation of results when studying AOM in environmentalsamples especially since TMO rates were like AOM stim-ulated by a high methane partial pressure [72 86 88] Sulfatereduction was also stimulated by higher methane partialpressures [85]Thus a highmethane partial pressure can havea stimulating effect on methane oxidation (either throughAOM or TMO) and SR which could be unrelated to S-AOMMoreover addition of iron sulfate (FeSO

4) or manganese

oxide (MnO2) also increased TMO rates [86] Therefore

methane-dependent SR and sulfate- or metal-dependentmethane oxidation are not necessarily indications for AOMin mixed cultures In conclusion when studying complexldquoblack-boxrdquo communities only net methane oxidation isproof for AOM activity

24 Methane Production by ANME The process of S-AOMis at the energetic limit for sustaining life with estimates

of Gibbs free energy yields between minus18 and minus35 kJmolminus1[45 79 89ndash91] and doubling times between 11 and 75months [65 72 73 92 93] Since S-AOM operates close toits thermodynamic equilibrium the reversibility of individualenzymes leads to measurable back flux producing methane(3ndash7 of AOM) and sulfate (55ndash13 of SR) during S-AOM [66] This ldquotrace methane productionrdquo was observedin situ [11] and in sediment slurries with methanogenesisaround 10 [62 94] or even as high as 50 of AOM [34]When sulfate becomes depleted Gibbs free energy yieldsbecome even lower (less negative) and the enzymatic backflux becomes even more apparent up to 78 of net AOM[95] Previous measurements of 13C depletion below thesulfate-methane transition zone (SMTZ) ofmarine sedimentsthat were thought to be indicative for methanogenesis couldtherefore instead be attributed to the back flux of AOM [95]The occurrence of ANME-1 without a bacterial partner insediment layers where sulfate was depleted was previouslyinterpreted as evidence that ANME-1 perform methanogen-esis [24] but in light of the above it could also indicate AOMThere are indeed reports of AOM activity below the SMTZin the methanogenic zone [96ndash99] In contrast AOM withother electron acceptors than sulfate operates far from thethermodynamic equilibrium with Gibbs free energy changesbetween minus5172 and minus8414 kJmolmethaneminus1 (Table 1) Herethe reported anaerobic back flux [66] is expected to be lessapparent

Archaea 13

MetFMer

Mdh

FaeHps

SRB

MHC

Mch

Mtd

Ftr

Fmd

McrMQ

Hdr1

MQ

MHC

Hdr2

CoB-S-S-CoMCoB-SHCoM-SH

Mtr

Fqo

CH4

CH3-CoMCH3-OH

CH2O CH3-H4MPT

F420F420H2

CHO-H4MPT

CHO-MFR

CO2

FdredFdox

H2O

eminus

eminus

CHequivH4MPT

CH2=H4MPT

xH+

H2

MQH2

MQH2

+xNa

Figure 6 Methanotrophic pathway during S-AOM by ANME-1 [40 41] Red lines indicate reversal of the hydrogenotrophic methanogenicpathway grey lines represent absence of conversions and blue lines indicate a bypass of the hydrogenotrophic methanogenic pathway SeeTable 3 for nomenclature

In laboratory incubations researchers were not ableto stimulate net methanogenesis through addition ofmethanogenic substrates to AOM performing sediments[62 94] In two cases researchers were successful [23 100]In one of these cases sediment-free long-term AOM enrich-ments that were dominated by ANMESRB were incubatedwith methanogenic substrates The resulting methanogenicactivity most likely came from the enrichment of a minorpopulation of methanogens (up to 7permil of total archaealgene tag sequences) that was present in the inoculum[100] In the second study methanogenic substrates wereadded to ANME-1 and ANME-2 dominated microbialmat samples and methanogenesis also occurred [23]However no information was provided for the total archaealcommunity composition which makes it impossible toexclude methanogens as the responsible organisms

Genomic information of ANME also gives indication onpotential methanogenic routes Considering methylotrophicmethanogenesis no gene homologues catalyzing methyltransfer from methylated substrates to coenzyme M weredetected in ANME (Table 2) [40ndash43] Acetoclastic methano-genesis needs either the AMP- and ADP-forming acetyl-coenzyme A synthetase (Acs and Acd resp) or proceedsvia acetate kinase and phosphotransacetylase In ANME-1only the alpha subunit of a homologue of Acd was expressed

during AOM [41] but in an ANME-1 proteome of activeAOM biomass no Acd was detected [40] The Acd gene wasdetected in the single-aggregate genome and transcriptomeof ANME-2a [42] and in ANME-2d [43] However genedomains for Acd are also present in methanogens unableto use acetate as substrate (Table 2) and are probably usedfor lipid metabolism In hydrogenotrophic methanogenesishydrogenases are used to replenish reduced coenzyme B andto recycle oxidized F

420(discussed in Section 21) Both the

cytoplasmic Mvh complex and the membrane bound Vhowere not present in ANME-2d [43] and not expressed inANME-2a (which also lackedEch andF

420-dependent hydro-

genase (Frh)) [42] making hydrogenotrophic methanogen-esis unlikely In ANME-1 both the cytoplasmic HdrABCand MvhD are present as well as homologues of Frh andEch but these were lacking catalytic subunits [40 41] Aniron hydrogenase was found in both ANME-1 metagenomesbut not in any other methanotroph or methanogen [41](Table 2) This iron hydrogenase domain is part of a genethat is 70 identical to a [FeFe]-hydrogenase of Dehalococ-coides mccartyi [FeFe]-hydrogenases catalyze reversible H

2

production and uptake but these were presumed to have nokey function in AOM [41] However the gene is part of a genecluster of three genes containing a 51 kDaNADH ubiquinoneoxidoreductase subunit (Table S3) which could potentially

14 Archaea

form a complex that generates a proton motive force duringhydrogen oxidation Therefore hydrogenotrophic methano-genesis by ANME-1 cannot be excluded yet

3 Respiration during AnaerobicOxidation of Methane

For netAOMtooccur an external electron acceptor is neededwhich results in a favourable Gibbs free energy change(Table 1) A variety of terminal electron acceptors have beendiscovered for AOM which will be discussed in Sections 31ndash33

31 Sulfate-Dependent AOM During sulfate-dependentAOM electrons are transferred from ANME to the sulfate-reducing bacterial partner Previous work tried to uncoverhow electrons were transferred and most compoundsthat could act as interspecies electron carrier (IEC) wereexcluded to be involved in AOM such as methanolhydrogen methanethiol acetate and carbon monoxide[57 61 62 94 101] Indications that polysulfide could actas IEC were found and ANME-2a archaea were thoughtto perform both AOM and sulfate reduction (SR) [102]However in marine seeps hydrothermal vents and othernondiffusion based sediments AOM rates are high andANME form close associations with SRB in dense aggregates[1 5 103 104] In these aggregates the high AOM ratescould not be explained by diffusion of an IEC whichmade direct interspecies electron transfer (DIET) a moreplausible mechanism [89 105 106] Cellular activities wereindependent of aggregate type and distance between thesyntrophic partners within the aggregate which is bestexplained by DIET [107] DIET is normally achieved usingmultiheme cytochrome c proteins (MHCs) and conductivepili (ie nanowires) which are mainly found in bacteriathat donate electrons extracellularly such as Geobacter andShewanella species [108ndash114] Indeed ANME-2a from seep-sediment samples seem to transfer electrons directly usinglarge MHCs [107] which were found in the metagenome ofANME-2a [107 115] ANME-1 and the associated bacterialpartner also overexpressed genes for extracellular MHCsduring AOM [116] which complements previous findings oftranscription [41] and translation [40] of ANME-1 relatedMHC genes Domain based (meta)genome analysis showsthe high abundance of MHC domains in different ANMEas compared to methanogens (Table 2) A recently isolatedbacterial partner of ANME-1 (ldquoHotSeep-1rdquo) also producedcell-to-cell connections using pili-derived nanowires [116]which explain previously detected Deltaproteobacteria-related pili genes in an AOM sample dominated by ANME-1[40]

How ANME use MHCs to donate electrons to thebacterial partner is not yet clear For ANME-2a the electronsprobably flow from methanophenazine to membrane inte-grated di-heme cytochromes (cytochrome 119887119887

6) that transfer

the electrons through the S-layer via MHCS-layer fusionproteins to extracellular MHCs (Figure 4) (Figure 4 in[107]) Exosortases and archaea-specific archaeosortases are

involved in export of cell surface proteins such as the archaealS-layer proteins These transpeptidases recognize specificsignal peptides for protein- sorting that is archaeosor-tase A recognizes the protein-sorting signal PGF-CTERMand archaeosortase C recognizes the PEF-CTERM signal[117] Both ANME-2a and 2d show presence of di-hemecytochromes archaeosortase A (IPR014522) archaeosortaseC (IPR022504) and other exosortase gene domains (Table 2)Moreover some genes of both ANME-2a and 2d containedboth MHC and PGF or PEF-CTERM domains Lastly somegenes of both ANME-2a and 2d contained both MHC andS-layer domains [107] indicating that these could form theabove-stated MHCS-layer fusion proteins

ANME-1 do not seem to have di-heme cytochromes(Table 2) [115] PGF related domains (IPR026453 andIPR026371) were present in all ANME but PEF-CTERM(IPR017474) related domains were absent in ANME-1 (Table 2) Moreover ANME-1 lacked archaeosortaseA (IPR014522) and archaeosortase C gene domains(IPR022504) as well as some other exosortases (Table 2) Asearch in NCBIrsquos conserved domains database (CCD [118])and the EMBL InterPro database [119] of amino acidssequences of all genes from ANME metagenomes thatcontain MHC domains showed that ANME-1 did not haveany protein-sorting signal or S-layer domains within thesegenes In fact S-layer domains were completely absent inANME-1 (Table 2) These results imply that ANME-1 do notuse di-heme cytochromes for electron transfer to MHCsand do not produce an S-layer (Figure 6) This implies thatANME-1 use a different mechanism for DIET and couldexplain the need for less MHCs by ANME-1 (Table 2)and the observed pili-derived nanowires produced by thebacterial partner [116] The genome of the bacterial partnerof ANME-1 (ldquoHotSeep-1rdquo) encoded 24 c-type cytochromesof which 10 were similar to secreted MHCs of Geobactersulfurreducens [120] which also uses pili for DIET [121]

In the case of ANME-2a it is not clear if pili (ienanowires) were formed during AOM It was previouslythought that electrically conductive pili seemed to be aprerequisite for current production andDIET [122 123] evenwhen syntrophs were closely associated [124] such as withinANME-2SRB aggregates However conductive materialssuch as granular activated carbon were shown to be ableto substitute pili in DIET [124] Although in previous workconductive materials such as phenazines or humic acids didnot seem to stimulate AOM rates [61] in a recent study AOMwas decoupled from SR using artificial electron acceptors[125] This indicates that conductive materials can indeedreplace pili and that ANME-2ab could possibly couple AOMto metal oxide reduction or any other suitable electronacceptor (discussed in Section 33) However it needs to beproven if in ANME-2SRB aggregates no pili are formed andif the mechanism of DIET is fundamentally different fromANME-1

As for the polysulfide shuttling theory [102] canonicalgenes for dissimilatory sulfate reduction such as adenylyl-transferase (Sat) APS reductase (Apr) and dissimilatorysulfite reductase (Dsr) which are all present in the sulfate-reducing archeon A fulgidus (Table S2) were not found in

Archaea 15

metagenomes of ANME-1 [41] and ANME-2a (Table S1)The enzymes Sat and Dsr were also not detected in ANMEcells using fluorescent immunolabelling [126] ANME-1 werepreviously found to encode most proteins for assimilatorysulfate reduction [41] ANME-2d only harbor gene domainsthat encode Sat and assimilatoryATP sulfurylase APS kinaseand sodiumsulfate symporters which were not present inANME-2a (Table S1) It is therefore clear that at least ANME-2a cannot donate electrons to sulfate but need to donateelectrons to a sulfate-reducing partner

32 Nitrate-Dependent AOM Unlike during S-AOMANME-2d that perform N-AOM do not need a bacterialpartner but transfer electrons directly to a membrane boundnitrate reductase (Nar) [28 43] (Figure 5) The ANME-2dgenomes contain most MHCs found so far in archaea[107 115] (Table 2) Of the 87 proteins that contained aCxxCH binding motif of which 43 seemed to be true c-typecytochromes [115] 23 CxxCH motif-encoding transcriptswere expressed during N-AOM [43] The function of mostof these MHCs is not known but they are likely involvedin nitrate reduction since c-type cytochromes are capableof operating in the wide range of redox potentials thatcouple nitrate reduction (11986401015840 (NO

3

minusNO2

minus) = +433mV) andmethane oxidation (11986401015840 (CoM-S-S-CoBCoM-SH+CoB-SH)= minus143mV) [43] Nitrate as terminal electron acceptor inanaerobic respiration has been found in halophilic andthermophilic archaea [127] The nar gene cluster of ldquoCaM nitroreducensrdquo comprises several genes including thecatalytic alpha (NarG molybdopterin) and beta (NarHiron sulfur cluster) subunit of nitrate reductase [28 43] The(halo)archaeal nitrate reductase complex was reported to belocated at the extracellular side of the cytoplasmic membrane[128] and in most archaea associated with the cytoplasmicmembrane via NarM [129] The ldquoCa M nitroreducensrdquogenome does not encode NarM but encodes a TAT signalpeptide at the N-terminus of NarG for translocation acrossthe cytoplasmic membrane [28 43] Interestingly theNarG and NarH seem to have been acquired from theProteobacteria via lateral gene transfer [28]

It is not yet clear at which point in themetabolism ldquoCaMnitroreducensrdquo conserves energy During reverse methano-genesis N5-methyl-H

4MPTCoM methyltransferase (Mtr)

dissipates the sodium ion potential across the cytoplasmicmembrane so subsequent steps inN-AOMhave to be coupledto the build-up of a proton or sodium motive force to makethe overall process energetically favourable The analysis ofan environmental genome [43] indicated presence of severalprotein complexes involved in electron transport and energyconservation Electrons that enter the respiratory chain couldbe transported by membrane-integral electron carriers (iemenaquinones) to a Rieske-cytochrome b complex that mayuse cytochrome c as electron acceptor This in turn maybe the electron donor for the unusual nitrate reductasecomplex Energy conservation is thermodynamically andmechanistically feasible at the F

420H2dehydrogenase and the

Rieske-cytochrome b complex (Figure 5) (Figure 2 in [43])Further investigations are needed to determine whether

nitrate reductase is also involved in energy conservationbut this working hypothesis is strengthened by the presenceof cupredoxin multicopper oxidase domains and coppercenters related to the periplasmic domain of cytochrome coxidase subunit II (HCO II) in ANME-2d (Table S1)

BothANME-2d genomes discussed here are derived frombioreactors where ldquoCaM nitroreducensrdquo formed syntrophiccultures with nitrite scavenging bacteria either with ldquoCaKuenenia stuttgartiensisrdquo (anammox bacteria) [28] or ldquoCaMethylomirabilis oxyferardquo (NC10 bacteria) [31 43]This indi-cated that ANME-2d could be dependent on those bacteriafor nitrite removal However in addition to nitrite ldquoCa Mnitroreducensrdquo may also produce ammonium during AOMby a pentaheme c-type nitrite reductase (NrfAH) encodedin the genome [43] (Figure 5) In fact both ANME-2dgenomes contain domains for NrfA (IPR003321) and NrfH(IPR017571) (Table S1) implying that both ANME-2d speciesare not necessarily dependent on a nitrite scavenger duringAOM

33 Metal-Dependent AOM Evidence for metal-dependentAOM was found in marine sediments [130ndash132] In non-marine environments AOM was also hypothesized to becoupled to iron andor manganese oxide reduction [26 133ndash136] or even coupled to the reduction of humic acids [136137] However organisms responsible for metal-dependentAOM were not identified in these studies It was speculatedthat JS1 bacteria methanogenic archaea and Methanohalo-biumANME-3 could be responsible for iron-dependentAOM [138] Other researchers speculated that either ANME-1 or MethanococcoidesANME-3 together with a bacterialpartner were responsible for manganese-dependent AOM[139] In another study where AOM was decoupled from SRANME were not detected which leaves open the possibilitythat other archaeal clades besides ANME could performmetal-dependent AOM [131]

It was recently observed that cultures containing ANME-2a and ANME-2c could decouple AOM from SR in thepresence of artificial electron acceptors humic acids andsoluble iron [125] which confirmed previous findings ofAOM not connected to SR in ANME dominated samples[140] This suggests that ANME-2 could also use insolublemetal oxide minerals as electron acceptor during AOM TheMHCs of ANME-2ab and ANME-2d are larger than thosein Shewanella and Geobacter species [107] which are knownto be capable of extracellular electron conduction It wasspeculated that both ANME-2d and Ferroglobus placidus ofwhich the latter can perform solid iron reduction can foldCxxCHmotifs into extracellular conductive structures or pili[115] Many of the MHCs of ANME-2d were not expressedwhen grown with nitrate (discussed in section 32) implyingthat these are not needed for nitrate reduction [43] Thisstrengthens the hypothesis that also ANME-2d could coupleAOM to reduction of other extracellular electron acceptorsthan nitrate and even to insoluble metal oxides Indeedrecent work showed that ANME-2d could be involved inAOM coupled to chromium(VI) reduction [141] (Table 1reaction (5)) and in AOM coupled to the reduction of soluble

16 Archaea

iron and insoluble ferrihydrite and birnessite minerals [142](Table 1 reactions (3) and (4)) ANME-2d could even possiblydonate electrons to a bacterial partner besides nitrate-richenvironments ANME-2d archaea have been found inwells ofan aquifer where sulfate and methane concentrations overlap[143] Moreover ANME-2d was the only clade detected insediments of a freshwater lake where S-AOM occurred [144]Sulfate concentrations in these studies were low but above1mM and thus higher than the lowest reported concen-trations for S-AOM to occur [145 146] Lastly sequencesof ANME-2d were relatively more abundant in freshwatersediments fed with methane and sulfate than in sedimentsfed with onlymethane or only sulfate and noN-AOMactivitywas detected when fed with nitrate and methane [27] Theseindications hold promise that direct experimental evidencefor sulfate-dependent AOM by ANME-2d could be found inthe future

TheANME-1 genome contains fewerMHCgene domainsas compared to ANME-2a and ANME-2d and some otherarchaea such as somemethylotrophicmethanogens (Table 2)and some members of the Archaeoglobales [115] The MHCsof ANME-1 also have a smaller heme count as compared toother ANME and some other archaea with the largest beingan octaheme cytochrome [107] Each hemewithin aMHChasits own redox potential and therefore structurally differentMHCs represent a large range of redox potentials that canbe used for bioenergetic electron transfer (reviewed in [147])For instance metal oxide reduction in Shewanella oneidensisMR-1 is catalyzed by a chain of a tetraheme (CymA) twodecaheme (MtrA and MtrB) and eventually extracellulardecaheme cytochromes OmcAMtrC that reduce the ironminerals [121 148 149] In Geobacter sulfurreducens ironmineral reduction seems to be catalyzed by the tetrahemecytochrome OmcE and hexaheme cytochrome OmcS trans-ferring electrons from the outer membrane to type IV pilithat transmit the electrons to iron minerals [121 150 151]Since ANME-1 lack MHCs of the correct size and lack genedomains for pili production [116] they seem unable to reduceminerals via both mechanisms present in Shewanella andGeobacter It can therefore be speculated that ANME-1 areless versatile in electron acceptor use and are not able toreduce solid metal oxides However DIET mechanisms arestill not well understood and the true differences betweenMHCs of different ANME types need to be investigated usingbiochemical methods This would allow uncovering the truecapabilities concerning DIET

34 Menaquinones and Methanophenazines ANME-2a en-coded a protein with a domain specific for PhzF which is anenzyme involved in phenazine biosynthesis in Pseudomonasfluorescens [152 153] The respective gene is not present in allmethanophenazine containing methanogens (in our genomecomparison only inM acetivorans andM formicica Table 2)so it is unclear whether this enzyme is really involved inmethanophenazine biosynthesis It is however likely thatANME-2a use methanophenazines in their respiratory chainsince gene domains for menaquinone biosynthesis wereabsent (Table 2) ldquoCa M nitroreducensrdquo probably uses

menaquinones as membrane-integral electron carrier sinceenvironmental genomes [28 43] encoded the futalosine(mqn) biosynthesis pathway as reported for Archaeoglobusfulgidus [154] (Table 2) Moreover ldquoCa M nitroreducensrdquoenrichment cultures showed absence of methanophenazines[43] ANME-1 also contained gene domains formenaquinonebiosynthesis via the futalosine (mqn) biosynthesis pathway(Table 2) Indications for a quinone biosynthesis pathwayin ANME-1 were previously found to be weak since onlysome of the Ubi homologues of the oxic ubiquinone biosyn-thesis pathway were detected [41] but the futalosine (mqn)biosynthesis pathway was overlooked in that particular anal-ysis Additionally ANME-1 have Fqo homologues similarto Archaeoglobus fulgidus [44] and expressed the catalyticsubunit FqoF [41] However since the phenazine biosynthesisdomain PhzF was also present in the ANME-1 genomes(Table 2) and Fpo and Fqo are homologues we cannotconclude on genomic information alone which redox shuttleis used by ANME-1 during AOM If ANME-1 would usemenaquinones this would have implications for subsequentelectron transfer to MHCs since methanophenazine (1198640 =minus165mV) [155] and menaquinone (1198640 = minus80mV) [156] havedifferent redox potentials

35 Cell Adhesion Some gene domains involved in cel-lular adhesion were more abundant in ANME than inmethanogens (Table 2) especially in ANME-2a and ANME-1that are known to form syntrophic interactions for electrontransfer during respiration These domains include HYR(IPR003410) and CARDB domains (IPR011635) that bothhave a direct role in cellular adhesion [157] (Table 2) Interest-ingly also domains related to the cellulosome of Clostridiumspecies termed dockerin and cohesin were highly abundantin both ANME-1 and ANME-2a as compared to ANME-2dand methanogens together with many carbohydrate bindingdomains (Table 2) In Clostridium species dockerin andcohesin form an anchor to the bacterial cell wall that containsa scaffold with cellulose-degrading enzymes and a carbohy-drate bindingmodule that binds cellulose altogether formingthe cellulosome [158] These domains have been found in alldomains of life irrespective of cellulose utilization but thefunction of such proteins outside of the cellulosome is notknown [159]Therefore dockerin cohesin and carbohydratebinding domains in ANME could hypothetically form aconstruct that binds to carbohydrates and could possibly havea function in cell-to-cell contact or MHC adhesion but thisneeds further investigation

4 Future Challenges

Advances in (meta)genomics transcriptomics and pro-teomics have produced the valuable metabolic blueprints ofdifferent ANMEwith hypotheses on how centralmetabolismelectron transport and energy conservation may functionFuture experiments are needed to biochemically demonstratethat these hypotheses are correct

The bottleneck for biochemical studies of ANME isthe lack of pure cultures due to the slow and syntrophic

Archaea 17

growth However the recent milestone discovery of directelectron transfer provides opportunities to grow ANMEas stated previously on electron accepting electrodes (ieanodes) [160] In this way pure or highly enriched culturesof different ANME without their respective syntrophic part-ner could be obtained and MHCs responsible for electricconduction could be biochemically characterized It seemsthat ANME-1 are limited by the size and abundance ofMHCs which could relate to differences in behavior onan anode The partner bacteria of ANME-1 and ANME-2could be investigated on an electron donating electrode (iecathode) with specific focus on the ability to produce pili (ienanowires) Also worth investigating is if besides ANME-2d ANME-2ab could also use insoluble electron acceptorsand if ANME-2d could donate electrons to a bacterialpartner

Another future challenge is to isolate and characterizeMcr from different ANME clades It needs to be investi-gated if Mcr abundance in ANME cells compensates forthe slow reverse activity or if modifications in the Mcrof ANME-1 also contribute to a better reverse activity ofMcr Moreover the effect of methane partial pressure onreaction rates and enzyme kinetics needs to be determined insitu

ANME-1 are potentially able to perform hydrogeno-trophic methanogenesis due to the presence of a hydrogenasein the genome Genetic indications of menaquinones aselectron carrier in ANME-1 and the various cellulosome andcell adhesion related gene domains in all ANME are alsotopics that could be explored further Methanogenic archaeaare likely not able to perform AOM but additional studieson TMO and more genetic modifications to stimulate AOMin methanogens could help in understanding the param-eters needed for AOM to occur Ultimately physiologicalunderstanding of ANME will help to explain the observedecological niche separation of different ANME clades and theoccurrence of ANMEwithout a bacterial partnerThis wouldgreatly enhance our knowledge of themethane cycle in anoxicenvironments

Competing Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors thank Stefanie Berger (RU Nijmegen) for criticalreading of the manuscript This research is supported bythe Soehngen Institute of Anaerobic Microbiology (SIAM)Gravitation grant (024002002) of the Netherlands Ministryof Education Culture and Science and the NetherlandsOrganisation for Scientific Research (NWO) Mike S MJetten was further supported by ERC AG 339880 Eco-MoMand Alfons J M Stams was supported by ERC AG 323009Novel Anaerobes

References

[1] A Boetius K Ravenschlag C J Schubert et al ldquoA marinemicrobial consortium apparently mediating anaerobic oxida-tion of methanerdquo Nature vol 407 no 6804 pp 623ndash626 2000

[2] K-U Hinrichs J M Hayes S P Sylva P G Brewert andE F DeLong ldquoMethane-consuming archaebacteria in marinesedimentsrdquo Nature vol 398 no 6730 pp 802ndash805 1999

[3] V J Orphan C H House K-U Hinrichs K D McKeeganand E F DeLong ldquoMethane-consuming archaea revealed bydirectly coupled isotopic and phylogenetic analysisrdquo Sciencevol 293 no 5529 pp 484ndash487 2001

[4] K-U Hinrichs and A Boetius ldquoThe anaerobic oxidation ofmethane new insights in microbial ecology and biogeochem-istryrdquo inOceanMargin Systems GWefer D Billett D HebbelnB B Joslashrgensen M Schluter and T VanWeering Eds pp 457ndash477 Springer Berlin Germany 2002

[5] K Knittel T Losekann A Boetius R Kort and R AmannldquoDiversity and distribution of methanotrophic archaea at coldseepsrdquo Applied and Environmental Microbiology vol 71 no 1pp 467ndash479 2005

[6] K Knittel and A Boetius ldquoAnaerobic oxidation of methaneprogress with an unknown processrdquo Annual Review of Micro-biology vol 63 pp 311ndash334 2009

[7] V J Orphan K-U Hinrichs W Ussler III et al ldquoComparativeanalysis of methane-oxidizing archaea and sulfate-reducingbacteria in anoxic marine sedimentsrdquoApplied and Environmen-tal Microbiology vol 67 no 4 pp 1922ndash1934 2001

[8] T Losekann K Knittel T Nadalig et al ldquoDiversity andabundance of aerobic and anaerobic methane oxidizers atthe Haakon Mosby Mud Volcano Barents Seardquo Applied andEnvironmentalMicrobiology vol 73 no 10 pp 3348ndash3362 2007

[9] H Niemann T Losekann D De Beer et al ldquoNovel microbialcommunities of the Haakon Mosby mud volcano and their roleas amethane sinkrdquoNature vol 443 no 7113 pp 854ndash858 2006

[10] TNunouraHOida T Toki J Ashi K Takai andKHorikoshildquoQuantification of mcrA by quantitative fluorescent PCR insediments from methane seep of the Nankai Troughrdquo FEMSMicrobiology Ecology vol 57 no 1 pp 149ndash157 2006

[11] B Orcutt A Boetius M Elvert V Samarkin and S B JoyeldquoMolecular biogeochemistry of sulfate reduction methanogen-esis and the anaerobic oxidation of methane at Gulf of Mexicocold seepsrdquoGeochimica et Cosmochimica Acta vol 69 no 17 pp4267ndash4281 2005

[12] V J Orphan W Ussler III T H Naehr C H House K-U Hinrichs and C K Paull ldquoGeological geochemical andmicrobiological heterogeneity of the seafloor around methanevents in the Eel River Basin offshore Californiardquo ChemicalGeology vol 205 no 3-4 pp 265ndash289 2004

[13] M G Pachiadaki A Kallionaki A Dahlmann G J De Langeand K A Kormas ldquoDiversity and spatial distribution ofprokaryotic communities along a sediment vertical profile ofa deep-sea mud volcanordquo Microbial Ecology vol 62 no 3 pp655ndash668 2011

[14] I Roalkvam H Dahle Y Chen S L Joslashrgensen H Haflidasonand I H Steen ldquoFine-scale community structure analysis ofANME in Nyegga sediments with high and low methane fluxrdquoFrontiers in Microbiology vol 3 p 216 2012

[15] K Yanagawa M Sunamura M A Lever et al ldquoNiche separa-tion of methanotrophic archaea (ANME-1 and -2) in methane-seep sediments of the Eastern Japan Sea offshore JoetsurdquoGeomicrobiology Journal vol 28 no 2 pp 118ndash129 2011

18 Archaea

[16] A Pernthaler A E Dekas C T Brown S K Goffredi TEmbaye and V J Orphan ldquoDiverse syntrophic partnershipsfromdeep-seamethane vents revealed by direct cell capture andmetagenomicsrdquo Proceedings of the National Academy of Sciencesof the United States of America vol 105 no 19 pp 7052ndash70572008

[17] R Hatzenpichler S A Connon D Goudeau R R Malm-strom T Woyke and V J Orphan ldquoVisualizing in situtranslational activity for identifying and sorting slow-growingarchaealminusbacterial consortiardquo Proceedings of the NationalAcademy of Sciences vol 113 no 28 pp E4069ndashE4078 2016

[18] L Maignien R J Parkes B Cragg et al ldquoAnaerobic oxidationof methane in hypersaline cold seep sedimentsrdquo FEMS Micro-biology Ecology vol 83 no 1 pp 214ndash231 2013

[19] V J Orphan C H House K-U Hinrichs K D McKeeganand E F DeLong ldquoMultiple archaeal groups mediate methaneoxidation in anoxic cold seep sedimentsrdquo Proceedings of theNational Academy of Sciences of the United States of Americavol 99 no 11 pp 7663ndash7668 2002

[20] T TreudeM Kruger A Boetius and B B Joslashrgensen ldquoEnviron-mental control on anaerobic oxidation of methane in the gassysediments of Eckernforde Bay (German Baltic)rdquo Limnology andOceanography vol 50 no 6 pp 1771ndash1786 2005

[21] G C Jagersma R J W Meulepas I Heikamp-De Jong etal ldquoMicrobial diversity and community structure of a highlyactive anaerobic methane-oxidizing sulfate-reducing enrich-mentrdquo Environmental Microbiology vol 11 no 12 pp 3223ndash3232 2009

[22] M Blumenberg R Seifert J Reitner T Pape andWMichaelisldquoMembrane lipid patterns typify distinct anaerobic methan-otrophic consortiardquo Proceedings of the National Academy ofSciences of the United States of America vol 101 no 30 pp 11111ndash11116 2004

[23] S Bertram M Blumenberg W Michaelis M Siegert MKruger and R Seifert ldquoMethanogenic capabilities of ANME-archaea deduced from 13C-labelling approachesrdquo Environmen-tal Microbiology vol 15 no 8 pp 2384ndash2393 2013

[24] K G Lloyd M J Alperin and A Teske ldquoEnvironmental evi-dence for net methane production and oxidation in putativeANaerobic MEthanotrophic (ANME) archaeardquo EnvironmentalMicrobiology vol 13 no 9 pp 2548ndash2564 2011

[25] M Takeuchi H Yoshioka Y Seo et al ldquoA distinct freshwater-adapted subgroup of ANME-1 dominates active archaeal com-munities in terrestrial subsurfaces in Japanrdquo EnvironmentalMicrobiology vol 13 no 12 pp 3206ndash3218 2011

[26] R T Amos B A Bekins I M Cozzarelli et al ldquoEvidence foriron-mediated anaerobic methane oxidation in a crude oil-contaminated aquiferrdquo Geobiology vol 10 no 6 pp 506ndash5172012

[27] P H Timmers D A Suarez-Zuluaga M van Rossem MDiender A J Stams and C M Plugge ldquoAnaerobic oxidationof methane associated with sulfate reduction in a naturalfreshwater gas sourcerdquo ISME Journal vol 10 pp 1400ndash14122015

[28] M F Haroon S Hu Y Shi et al ldquoAnaerobic oxidation ofmethane coupled to nitrate reduction in a novel archaeallineagerdquo Nature vol 500 no 7468 pp 567ndash570 2013

[29] H J Mills C Hodges K Wilson I R MacDonald and PA Sobecky ldquoMicrobial diversity in sediments associated withsurface-breaching gas hydrate mounds in the Gulf of MexicordquoFEMS Microbiology Ecology vol 46 no 1 pp 39ndash52 2003

[30] K G Lloyd L Lapham and A Teske ldquoAn anaerobic methane-oxidizing community of ANME-1b archaea in hypersaline gulfofMexico sedimentsrdquoApplied and EnvironmentalMicrobiologyvol 72 no 11 pp 7218ndash7230 2006

[31] A A Raghoebarsing A Pol K T Van De Pas-Schoonen et alldquoA microbial consortium couples anaerobic methane oxidationto denitrificationrdquoNature vol 440 no 7086 pp 918ndash921 2006

[32] S Hu R J Zeng L C Burow P Lant J Keller and Z YuanldquoEnrichment of denitrifying anaerobic methane oxidizingmicroorganismsrdquo Environmental Microbiology Reports vol 1no 5 pp 377ndash384 2009

[33] Z-W Ding J Ding L Fu F Zhang and R J Zeng ldquoSimultane-ous enrichment of denitrifying methanotrophs and anammoxbacteriardquo Applied Microbiology and Biotechnology vol 98 no24 pp 10211ndash10221 2014

[34] R Seifert K Nauhaus M Blumenberg M Kruger and WMichaelis ldquoMethane dynamics in a microbial community ofthe Black Sea traced by stable carbon isotopes in vitrordquoOrganicGeochemistry vol 37 no 10 pp 1411ndash1419 2006

[35] J Ding Z-W Ding L Fu Y-Z Lu S H Cheng and R JZeng ldquoNew primers for detecting and quantifying denitrifyinganaerobic methane oxidation archaea in different ecologicalnichesrdquo Applied Microbiology and Biotechnology vol 99 no 22pp 9805ndash9812 2015

[36] A Vaksmaa C Luke T van Alen et al ldquoDistribution and activ-ity of the anaerobic methanotrophic community in a nitrogen-fertilized Italian paddy soilrdquo FEMS Microbiology Ecology vol92 no 12 2016

[37] P N Evans D H Parks G L Chadwick et al ldquoMethanemetabolism in the archaeal phylum Bathyarchaeota revealed bygenome-centric metagenomicsrdquo Science vol 350 no 6259 pp434ndash438 2015

[38] I Vanwonterghem P N Evans D H Parks et al ldquoMethy-lotrophic methanogenesis discovered in the archaeal phylumVerstraetearchaeotardquo Nature Microbiology vol 1 Article ID16170 2016

[39] P Worm J J Koehorst M Visser et al ldquoA genomic view onsyntrophic versus non-syntrophic lifestyle in anaerobic fattyacid degrading communitiesrdquo Biochimica et Biophysica ActamdashBioenergetics vol 1837 no 12 pp 2004ndash2016 2014

[40] R Stokke I Roalkvam A Lanzen H Haflidason and I HSteen ldquoIntegrated metagenomic and metaproteomic analysesof an ANME-1-dominated community in marine cold seepsedimentsrdquo Environmental Microbiology vol 14 no 5 pp 1333ndash1346 2012

[41] A Meyerdierks M Kube I Kostadinov et al ldquoMetagenomeand mRNA expression analyses of anaerobic methanotrophicarchaea of the ANME-1 grouprdquo Environmental Microbiologyvol 12 no 2 pp 422ndash439 2010

[42] F-P Wang Y Zhang Y Chen et al ldquoMethanotrophicarchaea possessing diverging methane-oxidizing and electron-transporting pathwaysrdquo ISME Journal vol 8 no 5 pp 1069ndash1078 2014

[43] A Arshad D R Speth R M de Graaf H J Op den Camp MS Jetten and C U Welte ldquoA metagenomics-based metabolicmodel of nitrate-dependent anaerobic oxidation of methane byMethanoperedens-like archaeardquo Frontiers inMicrobiology vol 6article1423 2015

[44] S J Hallam N Putnam CM Preston et al ldquoReversemethano-genesis testing the hypothesis with environmental genomicsrdquoScience vol 305 no 5689 pp 1457ndash1462 2004

Archaea 19

[45] R K Thauer ldquoAnaerobic oxidation of methane with sulfate onthe reversibility of the reactions that are catalyzed by enzymesalso involved inmethanogenesis fromCO

2rdquoCurrent Opinion in

Microbiology vol 14 no 3 pp 292ndash299 2011[46] U Deppenmeier V Muller and G Gottschalk ldquoPathways of

energy conservation in methanogenic archaeardquo Archives ofMicrobiology vol 165 no 3 pp 149ndash163 1996

[47] A-K Kaster J Moll K Parey and R K Thauer ldquoCoupling offerredoxin and heterodisulfide reduction via electron bifurca-tion in hydrogenotrophic methanogenic archaeardquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 108 no 7 pp 2981ndash2986 2011

[48] R K Thauer A-K Kaster H Seedorf W Buckel and RHedderich ldquoMethanogenic archaea ecologically relevant dif-ferences in energy conservationrdquo Nature Reviews Microbiologyvol 6 no 8 pp 579ndash591 2008

[49] W Ludwig O Strunk R Westram et al ldquoARB a softwareenvironment for sequence datardquoNucleic Acids Research vol 32no 4 pp 1363ndash1371 2004

[50] E Pruesse C Quast K Knittel et al ldquoSILVA a comprehensiveonline resource for quality checked and aligned ribosomal RNAsequence data compatible with ARBrdquo Nucleic Acids Researchvol 35 no 21 pp 7188ndash7196 2007

[51] J J Marlow C T Skennerton Z Li et al ldquoProteomic stableisotope probing reveals biosynthesis dynamics of slow growingmethane based microbial communitiesrdquo Frontiers in Microbiol-ogy vol 7 article 386 2016

[52] P V Welander and W W Metcalf ldquoLoss of the mtr operon inMethanosarcina blocks growth on methanol but not methano-genesis and reveals an unknown methanogenic pathwayrdquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 102 no 30 pp 10664ndash10669 2005

[53] P V Welander and W W Metcalf ldquoMutagenesis of the C1oxidation pathway inmethanosarcina barkeri new insights intothe MtrMer bypass pathwayrdquo Journal of Bacteriology vol 190no 6 pp 1928ndash1936 2008

[54] M Goenrich R K Thauer H Yurimoto and N KatoldquoFormaldehyde activating enzyme (Fae) and hexulose-6-phosphate synthase (Hps) inMethanosarcina barkeri a possiblefunction in ribose-5-phosphate biosynthesisrdquoArchives ofMicro-biology vol 184 no 1 pp 41ndash48 2005

[55] M Goenrich FMahlert E C Duin C Bauer B Jaun and R KThauer ldquoProbing the reactivity of Ni in the active site of methyl-coenzyme M reductase with substrate analoguesrdquo Journal ofBiological Inorganic Chemistry vol 9 no 6 pp 691ndash705 2004

[56] S Scheller M Goenrich R Boecher R K Thauer and BJaun ldquoThe key nickel enzyme of methanogenesis catalyses theanaerobic oxidation of methanerdquo Nature vol 465 no 7298 pp606ndash608 2010

[57] K Nauhaus A Boetius M Kruger and F Widdel ldquoIn vitrodemonstration of anaerobic oxidation of methane coupled tosulphate reduction in sediment from amarine gas hydrate areardquoEnvironmental Microbiology vol 4 no 5 pp 296ndash305 2002

[58] Y Zhang J-P Henriet J Bursens and N Boon ldquoStimulationof in vitro anaerobic oxidation of methane rate in a continuoushigh-pressure bioreactorrdquo Bioresource Technology vol 101 no9 pp 3132ndash3138 2010

[59] M Kruger T Treude H Wolters K Nauhaus and A BoetiusldquoMicrobial methane turnover in different marine habitatsrdquoPalaeogeography Palaeoclimatology Palaeoecology vol 227 no1ndash3 pp 6ndash17 2005

[60] C Deusner V Meyer and T G Ferdelman ldquoHigh-pressuresystems for gas-phase free continuous incubation of enrichedmarinemicrobial communities performing anaerobic oxidationof methanerdquo Biotechnology and Bioengineering vol 105 no 3pp 524ndash533 2010

[61] K Nauhaus T Treude A Boetius and M Kruger ldquoEnviron-mental regulation of the anaerobic oxidation of methane acomparison of ANME-I and ANME-II communitiesrdquo Environ-mental Microbiology vol 7 no 1 pp 98ndash106 2005

[62] T Treude V Orphan K Knittel A Gieseke C H House andA Boetius ldquoConsumption of methane and CO

2by methan-

otrophicmicrobial mats from gas seeps of the anoxic Black SeardquoApplied and EnvironmentalMicrobiology vol 73 no 7 pp 2271ndash2283 2007

[63] T Holler F Widdel K Knittel et al ldquoThermophilic anaerobicoxidation of methane by marine microbial consortiardquo ISMEJournal vol 5 no 12 pp 1946ndash1956 2011

[64] M Kruger M Blumenberg S Kasten et al ldquoA novel multi-layered methanotrophic microbial mat system growing on thesediment of the Black Seardquo Environmental Microbiology vol 10no 8 pp 1934ndash1947 2008

[65] R J WMeulepas C G Jagersma J Gieteling C J N BuismanA J M Stams and P N L Lens ldquoEnrichment of anaerobicmethanotrophs in sulfate-reducing membrane bioreactorsrdquoBiotechnology and Bioengineering vol 104 no 3 pp 458ndash4702009

[66] T Holler G Wegener H Niemann et al ldquoCarbon and sulfurback flux during anaerobic microbial oxidation of methane andcoupled sulfate reductionrdquo Proceedings of the National Academyof Sciences of the United States of America vol 108 no 52 ppE1484ndashE1490 2011

[67] M Kruger AMeyerdierks F O Glockner et al ldquoA conspicuousnickel protein in microbial mats that oxidize methane anaero-bicallyrdquo Nature vol 426 no 6968 pp 878ndash881 2003

[68] S Mayr C Latkoczy M Kruger et al ldquoStructure of an F430

variant from archaea associated with anaerobic oxidation ofmethanerdquo Journal of the American Chemical Society vol 130 no32 pp 10758ndash10767 2008

[69] S Shima and R K Thauer ldquoMethyl-coenzyme M reductaseand the anaerobic oxidation of methane in methanotrophicArchaeardquo Current Opinion in Microbiology vol 8 no 6 pp643ndash648 2005

[70] R K Thauer and S Shima ldquoMethane as fuel for anaerobicmicroorganismsrdquo Annals of the New York Academy of Sciencesvol 1125 pp 158ndash170 2008

[71] S Yamamoto J B Alcauskas and T E Crozier ldquoSolubility ofmethane in distilled water and seawaterrdquo Journal of Chemicaland Engineering Data vol 21 no 1 pp 78ndash80 1976

[72] P H A Timmers J Gieteling H C A Widjaja-Greefkeset al ldquoGrowth of anaerobic methane-oxidizing archaea andsulfate-reducing bacteria in a high-pressure membrane capsulebioreactorrdquoApplied and EnvironmentalMicrobiology vol 81 no4 pp 1286ndash1296 2015

[73] MKruger HWoltersMGehre S B Joye andH-H RichnowldquoTracing the slow growth of anaerobic methane-oxidizingcommunities by 15N-labelling techniquesrdquo FEMS MicrobiologyEcology vol 63 no 3 pp 401ndash411 2008

[74] R J W Meulepas C G Jagersma A F Khadem C J N Buis-man A J M Stams and P N L Lens ldquoEffect of environmentalconditions on sulfate reduction withmethane as electron donorby an Eckernforde Bay enrichmentrdquo Environmental Science andTechnology vol 43 no 17 pp 6553ndash6559 2009

20 Archaea

[75] M W Bowles V A Samarkin and S B Joye ldquoImprovedmeasurement of microbial activity in deep-sea sediments atin situ pressure and methane concentrationrdquo Limnology andOceanography Methods vol 9 pp 499ndash506 2011

[76] S Shima M Krueger T Weinert et al ldquoStructure of a methyl-coenzyme M reductase from Black Sea mats that oxidizemethane anaerobicallyrdquo Nature vol 481 no 7379 pp 98ndash1012012

[77] K D Allen G Wegener and R H White ldquoDiscovery of multi-ple modified F-430 coenzymes in methanogens and anaerobicmethanotrophic archaea suggests possible new roles for F-430in naturerdquoApplied and Environmental Microbiology vol 80 no20 pp 6403ndash6412 2014

[78] V W Soo M J McAnulty A Tripathi et al ldquoReversingmethanogenesis to capture methane for liquid biofuel precur-sorsrdquoMicrobial Cell Factories vol 15 article 11 2016

[79] D L Valentine and W S Reeburgh ldquoNew perspectives onanaerobicmethane oxidationrdquoEnvironmentalMicrobiology vol2 no 5 pp 477ndash484 2000

[80] D L Valentine ldquoBiogeochemistry and microbial ecology ofmethane oxidation in anoxic environments a reviewrdquo Antonievan Leeuwenhoek International Journal of General and Molecu-lar Microbiology vol 81 no 1-4 pp 271ndash282 2002

[81] A J B Zehnder and T D Brock ldquoMethane formation andmethane oxidation by methanogenic bacteriardquo Journal of Bac-teriology vol 137 no 1 pp 420ndash432 1979

[82] J Harder ldquoAnaerobic methane oxidation by bacteria employ-ing 14C-methane uncontaminated with 14C-carbon monoxiderdquoMarine Geology vol 137 no 1-2 pp 13ndash23 1997

[83] J J Moran C H House K H Freeman and J G FerryldquoTrace methane oxidation studied in several Euryarchaeotaunder diverse conditionsrdquo Archaea vol 1 no 5 pp 303ndash3092005

[84] J J Moran C H House B Thomas and K H FreemanldquoProducts of tracemethane oxidation during nonmethyltrophicgrowth by Methanosarcinardquo Journal of Geophysical ResearchBiogeosciences vol 112 no 2 2007

[85] R J W Meulepas C G Jagersma Y Zhang et al ldquoTracemethane oxidation and the methane dependency of sulfatereduction in anaerobic granular sludgerdquo FEMS MicrobiologyEcology vol 72 no 2 pp 261ndash271 2010

[86] A J B Zehnder andTD Brock ldquoAnaerobicmethane oxidationoccurrence and ecologyrdquoApplied and Environmental Microbiol-ogy vol 39 no 1 pp 194ndash204 1980

[87] S J Blazewicz D G Petersen M P Waldrop and M K Fire-stone ldquoAnaerobic oxidation of methane in tropical and borealsoils ecological significance in terrestrial methane cyclingrdquoJournal of Geophysical Research Biogeosciences vol 117 no 2Article ID G02033 2012

[88] K A Smemo and J B Yavitt ldquoEvidence for anaerobic CH4

oxidation in freshwater peatlandsrdquo Geomicrobiology Journalvol 24 no 7-8 pp 583ndash597 2007

[89] M J Alperin and T M Hoehler ldquoAnaerobic methane oxidationby archaeasulfate-reducing bacteria aggregates 1 Thermody-namic and physical constraintsrdquo American Journal of Sciencevol 309 no 10 pp 869ndash957 2009

[90] S L Caldwell J R Laidler E A Brewer J O Eberly S CSandborgh and F S Colwell ldquoAnaerobic oxidation of methanemechanisms bioenergetics and the ecology of associatedmicroorganismsrdquo Environmental Science and Technology vol42 no 18 pp 6791ndash6799 2008

[91] GWang A J Spivack and S DrsquoHondt ldquoGibbs energies of reac-tion and microbial mutualism in anaerobic deep subseafloorsediments of ODP Site 1226rdquoGeochimica et Cosmochimica Actavol 74 no 14 pp 3938ndash3947 2010

[92] P R Girguis A E Cozen and E F DeLong ldquoGrowth andpopulation dynamics of anaerobic methane-oxidizing archaeaand sulfate-reducing bacteria in a continuous-flow bioreactorrdquoApplied and EnvironmentalMicrobiology vol 71 no 7 pp 3725ndash3733 2005

[93] K Nauhaus M Albrecht M Elvert A Boetius and F WiddelldquoIn vitro cell growth ofmarine archaeal-bacterial consortia dur-ing anaerobic oxidation ofmethanewith sulfaterdquoEnvironmentalMicrobiology vol 9 no 1 pp 187ndash196 2007

[94] B Orcutt V Samarkin A Boetius and S Joye ldquoOn the relation-ship between methane production and oxidation by anaerobicmethanotrophic communities from cold seeps of the Gulf ofMexicordquo Environmental Microbiology vol 10 no 5 pp 1108ndash1117 2008

[95] M Y Yoshinaga T Holler T Goldhammer et al ldquoCarbon iso-tope equilibration during sulphate-limited anaerobic oxidationof methanerdquo Nature Geoscience vol 7 no 3 pp 190ndash194 2014

[96] T Treude J Niggemann J Kallmeyer et al ldquoAnaerobic oxi-dation of methane and sulfate reduction along the Chileancontinental marginrdquo Geochimica et Cosmochimica Acta vol 69no 11 pp 2767ndash2779 2005

[97] R J Parkes B A Cragg N Banning et al ldquoBiogeochemistryand biodiversity of methane cycling in subsurface marinesediments (SkagerrakDenmark)rdquoEnvironmentalMicrobiologyvol 9 no 5 pp 1146ndash1161 2007

[98] N J Knab B A Cragg E R C Hornibrook et al ldquoRegulationof anaerobic methane oxidation in sediments of the Black SeardquoBiogeosciences vol 6 no 8 pp 1505ndash1518 2009

[99] H Yoshioka A Maruyama T Nakamura et al ldquoActivities anddistribution of methanogenic and methane-oxidizing microbesin marine sediments from the Cascadia Marginrdquo Geobiologyvol 8 no 3 pp 223ndash233 2010

[100] G Wegener V Krukenberg S E Ruff M Y Kellermann andK Knittel ldquoMetabolic capabilities of microorganisms involvedin and associated with the anaerobic oxidation of methanerdquoFrontiers in Microbiology vol 7 article 46 2016

[101] R J W Meulepas C G Jagersma A F Khadem A J MStams and P N L Lens ldquoEffect of methanogenic substrateson anaerobic oxidation of methane and sulfate reduction by ananaerobic methanotrophic enrichmentrdquo Applied Microbiologyand Biotechnology vol 87 no 4 pp 1499ndash1506 2010

[102] J Milucka T G Ferdelman L Polerecky et al ldquoZero-valentsulphur is a key intermediate in marine methane oxidationrdquoNature vol 491 no 7425 pp 541ndash546 2012

[103] W Michaelis R Seifert K Nauhaus et al ldquoMicrobial reefs inthe black sea fueled by anaerobic oxidation ofmethanerdquo Sciencevol 297 no 5583 pp 1013ndash1015 2002

[104] A Vigneron P Cruaud P Pignet et al ldquoArchaeal and anaerobicmethane oxidizer communities in the Sonora Margin coldseeps Guaymas Basin (Gulf of California)rdquo ISME Journal vol7 no 8 pp 1595ndash1608 2013

[105] M Alperin and T Hoehler ldquoThe ongoing mystery of sea-floormethanerdquo Science vol 329 no 5989 pp 288ndash289 2010

[106] B Orcutt and C Meile ldquoConstraints on mechanisms and ratesof anaerobic oxidation of methane by microbial consortiaprocess-basedmodeling of ANME-2 archaea and sulfate reduc-ing bacteria interactionsrdquo Biogeosciences vol 5 no 6 pp 1587ndash1599 2008

Archaea 21

[107] S E McGlynn G L Chadwick C P Kempes and V J OrphanldquoSingle cell activity reveals direct electron transfer in methan-otrophic consortiardquoNature vol 526 no 7574 pp 531ndash535 2015

[108] D R Lovley ldquoElectromicrobiologyrdquo Annual Review of Microbi-ology vol 66 pp 391ndash409 2012

[109] S M Strycharz-Glaven R M Snider A Guiseppi-Elie andL M Tender ldquoOn the electrical conductivity of microbialnanowires and biofilmsrdquoEnergy and Environmental Science vol4 no 11 pp 4366ndash4379 2011

[110] D J Richardson J N Butt J K Fredrickson et al ldquoThe lsquoporinndashcytochromersquo model for microbe-to-mineral electron transferrdquoMolecular Microbiology vol 85 no 2 pp 201ndash212 2012

[111] A Okamoto K Hashimoto and R Nakamura ldquoLong-rangeelectron conduction of Shewanella biofilms mediated by outermembrane C-type cytochromesrdquo Bioelectrochemistry vol 85pp 61ndash65 2012

[112] M Y El-Naggar G Wanger K M Leung et al ldquoElectricaltransport along bacterial nanowires from Shewanella oneidensisMR-1rdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 107 no 42 pp 18127ndash18131 2010

[113] G Reguera K D McCarthy T Mehta J S Nicoll M TTuominen and D R Lovley ldquoExtracellular electron transfer viamicrobial nanowiresrdquo Nature vol 435 no 7045 pp 1098ndash11012005

[114] Z M Summers H E Fogarty C Leang A E Franks N SMalvankar and D R Lovley ldquoDirect exchange of electronswithin aggregates of an evolved syntrophic coculture of anaer-obic bacteriardquo Science vol 330 no 6009 pp 1413ndash1415 2010

[115] A Kletzin T Heimerl J Flechsler L V Niftrik R Rachel andA Klingl ldquoCytochromes c in archaea distribution maturationcell architecture and the special case of Ignicoccus hospitalisrdquoFrontiers in Microbiology vol 6 article 439 2015

[116] GWegener V Krukenberg D Riedel H E Tegetmeyer and ABoetius ldquoIntercellular wiring enables electron transfer betweenmethanotrophic archaea and bacteriardquo Nature vol 526 no7574 pp 587ndash590 2015

[117] D HHaft S H Payne and J D Selengut ldquoArchaeosortases andexosortases are widely distributed systems linking membranetransit with posttranslational modificationrdquo Journal of Bacteri-ology vol 194 no 1 pp 36ndash48 2012

[118] A Marchler-Bauer M K Derbyshire N R Gonzales et alldquoCDD NCBIrsquos conserved domain databaserdquo Nucleic AcidsResearch vol 43 no 1 pp D222ndashD226 2015

[119] A Mitchell H-Y Chang L Daugherty et al ldquoThe InterProprotein families database the classification resource after 15yearsrdquo Nucleic Acids Research vol 43 no 1 pp D213ndashD2212015

[120] V Krukenberg K Harding M Richter et al ldquoCandidatusdesulfofervidus auxilii a hydrogenotrophic sulfate-reducingbacterium involved in the thermophilic anaerobic oxidation ofmethanerdquo Environmental Microbiology vol 18 pp 3073ndash30912016

[121] L Shi T C Squier J M Zachara and J K Fredrickson ldquoRes-piration of metal (hydr)oxides by Shewanella and Geobactera key role for multihaem c-type cytochromesrdquo MolecularMicrobiology vol 65 no 1 pp 12ndash20 2007

[122] N S Malvankar and D R Lovley ldquoMicrobial nanowires forbioenergy applicationsrdquo Current Opinion in Biotechnology vol27 pp 88ndash95 2014

[123] A-E Rotaru T LWoodard K PNevin andDR Lovley ldquoLinkbetween capacity for current production and syntrophic growth

in Geobacter speciesrdquo Frontiers in Microbiology vol 6 article744 2015

[124] A-E Rotaru P M Shrestha F Liu et al ldquoDirect interspecieselectron transfer between Geobacter metallireducens andMethanosarcina barkerirdquo Applied and Environmental Microbi-ology vol 80 no 15 pp 4599ndash4605 2014

[125] S Scheller H Yu G L Chadwick S E McGlynn and VJ Orphan ldquoArtificial electron acceptors decouple archaealmethane oxidation from sulfate reductionrdquo Science vol 351 no6274 pp 703ndash707 2016

[126] J Milucka F Widdel and S Shima ldquoImmunological detec-tion of enzymes for sulfate reduction in anaerobic methane-oxidizing consortiardquo Environmental Microbiology vol 15 no 5pp 1561ndash1571 2013

[127] P Cabello M D Roldan and C Moreno-Vivian ldquoNitratereduction and the nitrogen cycle in archaeardquoMicrobiology vol150 no 11 pp 3527ndash3546 2004

[128] R MMartinez-Espinosa E J Dridge M J Bonete et al ldquoLookon the positive sideThe orientation identification and bioener-getics of lsquoArchaealrsquomembrane-boundnitrate reductasesrdquoFEMSMicrobiology Letters vol 276 no 2 pp 129ndash139 2007

[129] S de VriesMMomcilovicM J F Strampraad J PWhiteleggeA Baghai and I Schroder ldquoAdaptation to a high-tungsten envi-ronment pyrobaculum aerophilum contains an active tungstennitrate reductaserdquo Biochemistry vol 49 no 45 pp 9911ndash99212010

[130] M Egger O Rasigraf C J Sapart et al ldquoIron-mediated anaer-obic oxidation of methane in brackish coastal sedimentsrdquoEnvironmental Science and Technology vol 49 no 1 pp 277ndash283 2015

[131] T Treude S Krause J Maltby A W Dale R Coffin and LJ Hamdan ldquoSulfate reduction and methane oxidation activitybelow the sulfate-methane transition zone in Alaskan BeaufortSea continental margin sediments implications for deep sulfurcyclingrdquo Geochimica et Cosmochimica Acta vol 144 pp 217ndash237 2014

[132] N Riedinger M J Formolo T W Lyons S Henkel A Beckand S Kasten ldquoAn inorganic geochemical argument for coupledanaerobic oxidation of methane and iron reduction in marinesedimentsrdquo Geobiology vol 12 no 2 pp 172ndash181 2014

[133] Y-H Chang T-W Cheng W-J Lai et al ldquoMicrobial methanecycling in a terrestrialmud volcano in eastern Taiwanrdquo Environ-mental Microbiology vol 14 no 4 pp 895ndash908 2012

[134] S A Crowe S Katsev K Leslie et al ldquoThe methane cycle inferruginous Lake Matanordquo Geobiology vol 9 no 1 pp 61ndash782011

[135] O Sivan M Adler A Pearson et al ldquoGeochemical evidence foriron-mediated anaerobic oxidation of methanerdquo Limnology andOceanography vol 56 no 4 pp 1536ndash1544 2011

[136] K E A Segarra C Comerford J Slaughter and S B JoyeldquoImpact of electron acceptor availability on the anaerobic oxi-dation of methane in coastal freshwater and brackish wetlandsedimentsrdquo Geochimica et Cosmochimica Acta vol 115 pp 15ndash30 2013

[137] V Gupta K A Smemo J B Yavitt D Fowle B Branfireunand N Basiliko ldquoStable isotopes reveal widespread anaerobicmethane oxidation across latitude and peatland typerdquo Environ-mental Science and Technology vol 47 no 15 pp 8273ndash82792013

[138] O Oni T Miyatake S Kasten et al ldquoDistinct microbialpopulations are tightly linked to the profile of dissolved iron in

22 Archaea

the methanic sediments of the Helgolandmud area North SeardquoFrontiers in Microbiology vol 6 2015

[139] E J Beal C H House and V J Orphan ldquoManganese- andiron-dependent marine methane oxidationrdquo Science vol 325no 5937 pp 184ndash187 2009

[140] M W Bowles V A Samarkin K M Bowles and S B JoyeldquoWeak coupling between sulfate reduction and the anaerobicoxidation of methane in methane-rich seafloor sedimentsduring ex situ incubationrdquo Geochimica et Cosmochimica Actavol 75 no 2 pp 500ndash519 2011

[141] Y Z Lu L Fu J Ding Z Ding N Li and R J Zeng ldquoCr(VI)reduction coupled with anaerobic oxidation of methane in alaboratory reactorrdquoWater Research vol 102 pp 445ndash452 2016

[142] K F Ettwig B Zhu D Speth J T Keltjens M S Jetten and BKartal ldquoArchaea catalyze iron-dependent anaerobic oxidationof methanerdquo Proceedings of the National Academy of Sciences ofthe United States of America vol 113 no 45 pp 12792ndash127962016

[143] T M Flynn R A Sanford H Ryu et al ldquoFunctional microbialdiversity explains groundwater chemistry in a pristine aquiferrdquoBMCMicrobiology vol 13 no 1 article no 146 2013

[144] C J Schubert F Vazquez T Losekann-Behrens K KnittelM Tonolla and A Boetius ldquoEvidence for anaerobic oxidationof methane in sediments of a freshwater system (Lago diCadagno)rdquo FEMS Microbiology Ecology vol 76 no 1 pp 26ndash38 2011

[145] K E A Segarra F Schubotz V Samarkin M Y Yoshinaga K-U Hinrichs and S B Joye ldquoHigh rates of anaerobic methaneoxidation in freshwater wetlands reduce potential atmosphericmethane emissionsrdquo Nature Communications vol 6 article7477 2015

[146] E J Beal M W Claire and C H House ldquoHigh rates ofanaerobic methanotrophy at low sulfate concentrations withimplications for past and present methane levelsrdquo Geobiologyvol 9 no 2 pp 131ndash139 2011

[147] F Kracke I Vassilev and J O Kromer ldquoMicrobial electrontransport and energy conservationmdashthe foundation for opti-mizing bioelectrochemical systemsrdquo Frontiers in Microbiologyvol 6 article 575 2015

[148] C L Reardon A C Dohnalkova P Nachimuthu et al ldquoRoleof outer-membrane cytochromes MtrC and OmcA in thebiomineralization of ferrihydrite by Shewanella oneidensisMR-1rdquo Geobiology vol 8 no 1 pp 56ndash68 2010

[149] L Shi B Chen Z Wang et al ldquoIsolation of a high-affinityfunctional protein complex between OmcA and MtrC twoouter membrane decaheme c-type cytochromes of Shewanellaoneidensis MR-1rdquo Journal of Bacteriology vol 188 no 13 pp4705ndash4714 2006

[150] X Qian T Mester L Morgado et al ldquoBiochemical charac-terization of purified OmcS a c-type cytochrome requiredfor insoluble Fe(III) reduction in Geobacter sulfurreducensrdquoBiochimica et BiophysicaActamdashBioenergetics vol 1807 no 4 pp404ndash412 2011

[151] T Mehta M V Coppi S E Childers and D R Lovley ldquoOutermembrane c-type cytochromes required for Fe(III) andMn(IV)oxide reduction in Geobacter sulfurreducensrdquo Applied andEnvironmentalMicrobiology vol 71 no 12 pp 8634ndash8641 2005

[152] W Blankenfeldt A P Kuzin T Skarina et al ldquoStructure andfunction of the phenazine biosynthetic protein PhzF fromPseudomonas fluorescensrdquoProceedings of theNational Academyof Sciences of the United States of America vol 101 no 47 pp16431ndash16436 2004

[153] J F Parsons F Song L Parsons K Calabrese E Eisensteinand J E Ladner ldquoStructure and function of the phenazinebiosynthesis protein PhzF fromPseudomonas fluorescens 2-79rdquoBiochemistry vol 43 no 39 pp 12427ndash12435 2004

[154] T Hiratsuka K Furihata J Ishikawa et al ldquoAn alternativemenaquinone biosynthetic pathway operating in microorgan-ismsrdquo Science vol 321 no 5896 pp 1670ndash1673 2008

[155] M Tietze A Beuchle I Lamla et al ldquoRedox potentials ofmethanophenazine and CoB-S-S-CoM factors involved inelectron transport in methanogenic archaeardquo ChemBioChemvol 4 no 4 pp 333ndash335 2003

[156] Q H Tran and G Unden ldquoChanges in the proton potentialand the cellular energetics of Escherichia coli during growth byaerobic and anaerobic respiration or by fermentationrdquoEuropeanJournal of Biochemistry vol 251 no 1-2 pp 538ndash543 1998

[157] I Callebaut D Gilges I Vigon and J-P Mornon ldquoHYR anextracellular module involved in cellular adhesion and relatedto the immunoglobulin-like foldrdquo Protein Science vol 9 no 7pp 1382ndash1390 2000

[158] H J Gilbert ldquoCellulosomes microbial nanomachines that dis-play plasticity in quaternary structurerdquoMolecular Microbiologyvol 63 no 6 pp 1568ndash1576 2007

[159] A Peer S P Smith E A Bayer R Lamed and I BorovokldquoNoncellulosomal cohesin- and dockerin-like modules in thethree domains of liferdquo FEMS Microbiology Letters vol 291 no1 pp 1ndash16 2009

[160] M Wagner ldquoMicrobiology conductive consortiardquo Nature vol526 no 7574 pp 513ndash514 2015

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

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The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

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Signal TransductionJournal of

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BioMed Research International

Evolutionary BiologyInternational Journal of

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

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Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

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Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

12 Archaea

Mch

Mer

Mtd

Ftr

Fmd

Mcr

MQ

MQ

EchHdrFrh

3MQ

HdrABC

MQ

cyt b Mtr

NrfH

cyt c

NrfA

CoB-S-S-CoM

CoB-SH

CoM-SH

HdrDE

HCOIIHCOIINapHOrf7

NarGH

S-layer

Fqo

Fqo

3H+

3H+

4H+

CH4

CH3-CoM

CH3-H4MPT

F420

F420H2

F420

F420H2

CH2=H4MPT

CHequivH4MPT

CHO-H4MPT

CHO-MFR

CO2

Fdred

Fdox

H2O

2Na+

NH4+

NO2minus

NO2minus

NO3minus

3MQH2

MQH2

MQH2

MQH2eminus

eminus

Rieske

Figure 5 Methanotrophic pathway during N-AOM by ldquoCaM nitroreducensrdquo MPEBLZ (ANME-2d) [43] Red lines indicate reversal of thehydrogenotrophic methanogenic pathway See Table 3 for nomenclature

thermodynamically favourable conditions TMOoccurs bothin absence and presence of an external electron acceptor andonly during net methanogenesis It is therefore most likelycaused by the reported back flux of individual enzymes of themethanogenic pathway [66]

TMO also occurred in granular sludge and in freshwaterand terrestrial samples These mixed communities showedhigher TMO rates than pure cultures reaching up to 90of the methane produced [27 85ndash87] TMO should thereforebe carefully considered in the experimental setup and inter-pretation of results when studying AOM in environmentalsamples especially since TMO rates were like AOM stim-ulated by a high methane partial pressure [72 86 88] Sulfatereduction was also stimulated by higher methane partialpressures [85]Thus a highmethane partial pressure can havea stimulating effect on methane oxidation (either throughAOM or TMO) and SR which could be unrelated to S-AOMMoreover addition of iron sulfate (FeSO

4) or manganese

oxide (MnO2) also increased TMO rates [86] Therefore

methane-dependent SR and sulfate- or metal-dependentmethane oxidation are not necessarily indications for AOMin mixed cultures In conclusion when studying complexldquoblack-boxrdquo communities only net methane oxidation isproof for AOM activity

24 Methane Production by ANME The process of S-AOMis at the energetic limit for sustaining life with estimates

of Gibbs free energy yields between minus18 and minus35 kJmolminus1[45 79 89ndash91] and doubling times between 11 and 75months [65 72 73 92 93] Since S-AOM operates close toits thermodynamic equilibrium the reversibility of individualenzymes leads to measurable back flux producing methane(3ndash7 of AOM) and sulfate (55ndash13 of SR) during S-AOM [66] This ldquotrace methane productionrdquo was observedin situ [11] and in sediment slurries with methanogenesisaround 10 [62 94] or even as high as 50 of AOM [34]When sulfate becomes depleted Gibbs free energy yieldsbecome even lower (less negative) and the enzymatic backflux becomes even more apparent up to 78 of net AOM[95] Previous measurements of 13C depletion below thesulfate-methane transition zone (SMTZ) ofmarine sedimentsthat were thought to be indicative for methanogenesis couldtherefore instead be attributed to the back flux of AOM [95]The occurrence of ANME-1 without a bacterial partner insediment layers where sulfate was depleted was previouslyinterpreted as evidence that ANME-1 perform methanogen-esis [24] but in light of the above it could also indicate AOMThere are indeed reports of AOM activity below the SMTZin the methanogenic zone [96ndash99] In contrast AOM withother electron acceptors than sulfate operates far from thethermodynamic equilibrium with Gibbs free energy changesbetween minus5172 and minus8414 kJmolmethaneminus1 (Table 1) Herethe reported anaerobic back flux [66] is expected to be lessapparent

Archaea 13

MetFMer

Mdh

FaeHps

SRB

MHC

Mch

Mtd

Ftr

Fmd

McrMQ

Hdr1

MQ

MHC

Hdr2

CoB-S-S-CoMCoB-SHCoM-SH

Mtr

Fqo

CH4

CH3-CoMCH3-OH

CH2O CH3-H4MPT

F420F420H2

CHO-H4MPT

CHO-MFR

CO2

FdredFdox

H2O

eminus

eminus

CHequivH4MPT

CH2=H4MPT

xH+

H2

MQH2

MQH2

+xNa

Figure 6 Methanotrophic pathway during S-AOM by ANME-1 [40 41] Red lines indicate reversal of the hydrogenotrophic methanogenicpathway grey lines represent absence of conversions and blue lines indicate a bypass of the hydrogenotrophic methanogenic pathway SeeTable 3 for nomenclature

In laboratory incubations researchers were not ableto stimulate net methanogenesis through addition ofmethanogenic substrates to AOM performing sediments[62 94] In two cases researchers were successful [23 100]In one of these cases sediment-free long-term AOM enrich-ments that were dominated by ANMESRB were incubatedwith methanogenic substrates The resulting methanogenicactivity most likely came from the enrichment of a minorpopulation of methanogens (up to 7permil of total archaealgene tag sequences) that was present in the inoculum[100] In the second study methanogenic substrates wereadded to ANME-1 and ANME-2 dominated microbialmat samples and methanogenesis also occurred [23]However no information was provided for the total archaealcommunity composition which makes it impossible toexclude methanogens as the responsible organisms

Genomic information of ANME also gives indication onpotential methanogenic routes Considering methylotrophicmethanogenesis no gene homologues catalyzing methyltransfer from methylated substrates to coenzyme M weredetected in ANME (Table 2) [40ndash43] Acetoclastic methano-genesis needs either the AMP- and ADP-forming acetyl-coenzyme A synthetase (Acs and Acd resp) or proceedsvia acetate kinase and phosphotransacetylase In ANME-1only the alpha subunit of a homologue of Acd was expressed

during AOM [41] but in an ANME-1 proteome of activeAOM biomass no Acd was detected [40] The Acd gene wasdetected in the single-aggregate genome and transcriptomeof ANME-2a [42] and in ANME-2d [43] However genedomains for Acd are also present in methanogens unableto use acetate as substrate (Table 2) and are probably usedfor lipid metabolism In hydrogenotrophic methanogenesishydrogenases are used to replenish reduced coenzyme B andto recycle oxidized F

420(discussed in Section 21) Both the

cytoplasmic Mvh complex and the membrane bound Vhowere not present in ANME-2d [43] and not expressed inANME-2a (which also lackedEch andF

420-dependent hydro-

genase (Frh)) [42] making hydrogenotrophic methanogen-esis unlikely In ANME-1 both the cytoplasmic HdrABCand MvhD are present as well as homologues of Frh andEch but these were lacking catalytic subunits [40 41] Aniron hydrogenase was found in both ANME-1 metagenomesbut not in any other methanotroph or methanogen [41](Table 2) This iron hydrogenase domain is part of a genethat is 70 identical to a [FeFe]-hydrogenase of Dehalococ-coides mccartyi [FeFe]-hydrogenases catalyze reversible H

2

production and uptake but these were presumed to have nokey function in AOM [41] However the gene is part of a genecluster of three genes containing a 51 kDaNADH ubiquinoneoxidoreductase subunit (Table S3) which could potentially

14 Archaea

form a complex that generates a proton motive force duringhydrogen oxidation Therefore hydrogenotrophic methano-genesis by ANME-1 cannot be excluded yet

3 Respiration during AnaerobicOxidation of Methane

For netAOMtooccur an external electron acceptor is neededwhich results in a favourable Gibbs free energy change(Table 1) A variety of terminal electron acceptors have beendiscovered for AOM which will be discussed in Sections 31ndash33

31 Sulfate-Dependent AOM During sulfate-dependentAOM electrons are transferred from ANME to the sulfate-reducing bacterial partner Previous work tried to uncoverhow electrons were transferred and most compoundsthat could act as interspecies electron carrier (IEC) wereexcluded to be involved in AOM such as methanolhydrogen methanethiol acetate and carbon monoxide[57 61 62 94 101] Indications that polysulfide could actas IEC were found and ANME-2a archaea were thoughtto perform both AOM and sulfate reduction (SR) [102]However in marine seeps hydrothermal vents and othernondiffusion based sediments AOM rates are high andANME form close associations with SRB in dense aggregates[1 5 103 104] In these aggregates the high AOM ratescould not be explained by diffusion of an IEC whichmade direct interspecies electron transfer (DIET) a moreplausible mechanism [89 105 106] Cellular activities wereindependent of aggregate type and distance between thesyntrophic partners within the aggregate which is bestexplained by DIET [107] DIET is normally achieved usingmultiheme cytochrome c proteins (MHCs) and conductivepili (ie nanowires) which are mainly found in bacteriathat donate electrons extracellularly such as Geobacter andShewanella species [108ndash114] Indeed ANME-2a from seep-sediment samples seem to transfer electrons directly usinglarge MHCs [107] which were found in the metagenome ofANME-2a [107 115] ANME-1 and the associated bacterialpartner also overexpressed genes for extracellular MHCsduring AOM [116] which complements previous findings oftranscription [41] and translation [40] of ANME-1 relatedMHC genes Domain based (meta)genome analysis showsthe high abundance of MHC domains in different ANMEas compared to methanogens (Table 2) A recently isolatedbacterial partner of ANME-1 (ldquoHotSeep-1rdquo) also producedcell-to-cell connections using pili-derived nanowires [116]which explain previously detected Deltaproteobacteria-related pili genes in an AOM sample dominated by ANME-1[40]

How ANME use MHCs to donate electrons to thebacterial partner is not yet clear For ANME-2a the electronsprobably flow from methanophenazine to membrane inte-grated di-heme cytochromes (cytochrome 119887119887

6) that transfer

the electrons through the S-layer via MHCS-layer fusionproteins to extracellular MHCs (Figure 4) (Figure 4 in[107]) Exosortases and archaea-specific archaeosortases are

involved in export of cell surface proteins such as the archaealS-layer proteins These transpeptidases recognize specificsignal peptides for protein- sorting that is archaeosor-tase A recognizes the protein-sorting signal PGF-CTERMand archaeosortase C recognizes the PEF-CTERM signal[117] Both ANME-2a and 2d show presence of di-hemecytochromes archaeosortase A (IPR014522) archaeosortaseC (IPR022504) and other exosortase gene domains (Table 2)Moreover some genes of both ANME-2a and 2d containedboth MHC and PGF or PEF-CTERM domains Lastly somegenes of both ANME-2a and 2d contained both MHC andS-layer domains [107] indicating that these could form theabove-stated MHCS-layer fusion proteins

ANME-1 do not seem to have di-heme cytochromes(Table 2) [115] PGF related domains (IPR026453 andIPR026371) were present in all ANME but PEF-CTERM(IPR017474) related domains were absent in ANME-1 (Table 2) Moreover ANME-1 lacked archaeosortaseA (IPR014522) and archaeosortase C gene domains(IPR022504) as well as some other exosortases (Table 2) Asearch in NCBIrsquos conserved domains database (CCD [118])and the EMBL InterPro database [119] of amino acidssequences of all genes from ANME metagenomes thatcontain MHC domains showed that ANME-1 did not haveany protein-sorting signal or S-layer domains within thesegenes In fact S-layer domains were completely absent inANME-1 (Table 2) These results imply that ANME-1 do notuse di-heme cytochromes for electron transfer to MHCsand do not produce an S-layer (Figure 6) This implies thatANME-1 use a different mechanism for DIET and couldexplain the need for less MHCs by ANME-1 (Table 2)and the observed pili-derived nanowires produced by thebacterial partner [116] The genome of the bacterial partnerof ANME-1 (ldquoHotSeep-1rdquo) encoded 24 c-type cytochromesof which 10 were similar to secreted MHCs of Geobactersulfurreducens [120] which also uses pili for DIET [121]

In the case of ANME-2a it is not clear if pili (ienanowires) were formed during AOM It was previouslythought that electrically conductive pili seemed to be aprerequisite for current production andDIET [122 123] evenwhen syntrophs were closely associated [124] such as withinANME-2SRB aggregates However conductive materialssuch as granular activated carbon were shown to be ableto substitute pili in DIET [124] Although in previous workconductive materials such as phenazines or humic acids didnot seem to stimulate AOM rates [61] in a recent study AOMwas decoupled from SR using artificial electron acceptors[125] This indicates that conductive materials can indeedreplace pili and that ANME-2ab could possibly couple AOMto metal oxide reduction or any other suitable electronacceptor (discussed in Section 33) However it needs to beproven if in ANME-2SRB aggregates no pili are formed andif the mechanism of DIET is fundamentally different fromANME-1

As for the polysulfide shuttling theory [102] canonicalgenes for dissimilatory sulfate reduction such as adenylyl-transferase (Sat) APS reductase (Apr) and dissimilatorysulfite reductase (Dsr) which are all present in the sulfate-reducing archeon A fulgidus (Table S2) were not found in

Archaea 15

metagenomes of ANME-1 [41] and ANME-2a (Table S1)The enzymes Sat and Dsr were also not detected in ANMEcells using fluorescent immunolabelling [126] ANME-1 werepreviously found to encode most proteins for assimilatorysulfate reduction [41] ANME-2d only harbor gene domainsthat encode Sat and assimilatoryATP sulfurylase APS kinaseand sodiumsulfate symporters which were not present inANME-2a (Table S1) It is therefore clear that at least ANME-2a cannot donate electrons to sulfate but need to donateelectrons to a sulfate-reducing partner

32 Nitrate-Dependent AOM Unlike during S-AOMANME-2d that perform N-AOM do not need a bacterialpartner but transfer electrons directly to a membrane boundnitrate reductase (Nar) [28 43] (Figure 5) The ANME-2dgenomes contain most MHCs found so far in archaea[107 115] (Table 2) Of the 87 proteins that contained aCxxCH binding motif of which 43 seemed to be true c-typecytochromes [115] 23 CxxCH motif-encoding transcriptswere expressed during N-AOM [43] The function of mostof these MHCs is not known but they are likely involvedin nitrate reduction since c-type cytochromes are capableof operating in the wide range of redox potentials thatcouple nitrate reduction (11986401015840 (NO

3

minusNO2

minus) = +433mV) andmethane oxidation (11986401015840 (CoM-S-S-CoBCoM-SH+CoB-SH)= minus143mV) [43] Nitrate as terminal electron acceptor inanaerobic respiration has been found in halophilic andthermophilic archaea [127] The nar gene cluster of ldquoCaM nitroreducensrdquo comprises several genes including thecatalytic alpha (NarG molybdopterin) and beta (NarHiron sulfur cluster) subunit of nitrate reductase [28 43] The(halo)archaeal nitrate reductase complex was reported to belocated at the extracellular side of the cytoplasmic membrane[128] and in most archaea associated with the cytoplasmicmembrane via NarM [129] The ldquoCa M nitroreducensrdquogenome does not encode NarM but encodes a TAT signalpeptide at the N-terminus of NarG for translocation acrossthe cytoplasmic membrane [28 43] Interestingly theNarG and NarH seem to have been acquired from theProteobacteria via lateral gene transfer [28]

It is not yet clear at which point in themetabolism ldquoCaMnitroreducensrdquo conserves energy During reverse methano-genesis N5-methyl-H

4MPTCoM methyltransferase (Mtr)

dissipates the sodium ion potential across the cytoplasmicmembrane so subsequent steps inN-AOMhave to be coupledto the build-up of a proton or sodium motive force to makethe overall process energetically favourable The analysis ofan environmental genome [43] indicated presence of severalprotein complexes involved in electron transport and energyconservation Electrons that enter the respiratory chain couldbe transported by membrane-integral electron carriers (iemenaquinones) to a Rieske-cytochrome b complex that mayuse cytochrome c as electron acceptor This in turn maybe the electron donor for the unusual nitrate reductasecomplex Energy conservation is thermodynamically andmechanistically feasible at the F

420H2dehydrogenase and the

Rieske-cytochrome b complex (Figure 5) (Figure 2 in [43])Further investigations are needed to determine whether

nitrate reductase is also involved in energy conservationbut this working hypothesis is strengthened by the presenceof cupredoxin multicopper oxidase domains and coppercenters related to the periplasmic domain of cytochrome coxidase subunit II (HCO II) in ANME-2d (Table S1)

BothANME-2d genomes discussed here are derived frombioreactors where ldquoCaM nitroreducensrdquo formed syntrophiccultures with nitrite scavenging bacteria either with ldquoCaKuenenia stuttgartiensisrdquo (anammox bacteria) [28] or ldquoCaMethylomirabilis oxyferardquo (NC10 bacteria) [31 43]This indi-cated that ANME-2d could be dependent on those bacteriafor nitrite removal However in addition to nitrite ldquoCa Mnitroreducensrdquo may also produce ammonium during AOMby a pentaheme c-type nitrite reductase (NrfAH) encodedin the genome [43] (Figure 5) In fact both ANME-2dgenomes contain domains for NrfA (IPR003321) and NrfH(IPR017571) (Table S1) implying that both ANME-2d speciesare not necessarily dependent on a nitrite scavenger duringAOM

33 Metal-Dependent AOM Evidence for metal-dependentAOM was found in marine sediments [130ndash132] In non-marine environments AOM was also hypothesized to becoupled to iron andor manganese oxide reduction [26 133ndash136] or even coupled to the reduction of humic acids [136137] However organisms responsible for metal-dependentAOM were not identified in these studies It was speculatedthat JS1 bacteria methanogenic archaea and Methanohalo-biumANME-3 could be responsible for iron-dependentAOM [138] Other researchers speculated that either ANME-1 or MethanococcoidesANME-3 together with a bacterialpartner were responsible for manganese-dependent AOM[139] In another study where AOM was decoupled from SRANME were not detected which leaves open the possibilitythat other archaeal clades besides ANME could performmetal-dependent AOM [131]

It was recently observed that cultures containing ANME-2a and ANME-2c could decouple AOM from SR in thepresence of artificial electron acceptors humic acids andsoluble iron [125] which confirmed previous findings ofAOM not connected to SR in ANME dominated samples[140] This suggests that ANME-2 could also use insolublemetal oxide minerals as electron acceptor during AOM TheMHCs of ANME-2ab and ANME-2d are larger than thosein Shewanella and Geobacter species [107] which are knownto be capable of extracellular electron conduction It wasspeculated that both ANME-2d and Ferroglobus placidus ofwhich the latter can perform solid iron reduction can foldCxxCHmotifs into extracellular conductive structures or pili[115] Many of the MHCs of ANME-2d were not expressedwhen grown with nitrate (discussed in section 32) implyingthat these are not needed for nitrate reduction [43] Thisstrengthens the hypothesis that also ANME-2d could coupleAOM to reduction of other extracellular electron acceptorsthan nitrate and even to insoluble metal oxides Indeedrecent work showed that ANME-2d could be involved inAOM coupled to chromium(VI) reduction [141] (Table 1reaction (5)) and in AOM coupled to the reduction of soluble

16 Archaea

iron and insoluble ferrihydrite and birnessite minerals [142](Table 1 reactions (3) and (4)) ANME-2d could even possiblydonate electrons to a bacterial partner besides nitrate-richenvironments ANME-2d archaea have been found inwells ofan aquifer where sulfate and methane concentrations overlap[143] Moreover ANME-2d was the only clade detected insediments of a freshwater lake where S-AOM occurred [144]Sulfate concentrations in these studies were low but above1mM and thus higher than the lowest reported concen-trations for S-AOM to occur [145 146] Lastly sequencesof ANME-2d were relatively more abundant in freshwatersediments fed with methane and sulfate than in sedimentsfed with onlymethane or only sulfate and noN-AOMactivitywas detected when fed with nitrate and methane [27] Theseindications hold promise that direct experimental evidencefor sulfate-dependent AOM by ANME-2d could be found inthe future

TheANME-1 genome contains fewerMHCgene domainsas compared to ANME-2a and ANME-2d and some otherarchaea such as somemethylotrophicmethanogens (Table 2)and some members of the Archaeoglobales [115] The MHCsof ANME-1 also have a smaller heme count as compared toother ANME and some other archaea with the largest beingan octaheme cytochrome [107] Each hemewithin aMHChasits own redox potential and therefore structurally differentMHCs represent a large range of redox potentials that canbe used for bioenergetic electron transfer (reviewed in [147])For instance metal oxide reduction in Shewanella oneidensisMR-1 is catalyzed by a chain of a tetraheme (CymA) twodecaheme (MtrA and MtrB) and eventually extracellulardecaheme cytochromes OmcAMtrC that reduce the ironminerals [121 148 149] In Geobacter sulfurreducens ironmineral reduction seems to be catalyzed by the tetrahemecytochrome OmcE and hexaheme cytochrome OmcS trans-ferring electrons from the outer membrane to type IV pilithat transmit the electrons to iron minerals [121 150 151]Since ANME-1 lack MHCs of the correct size and lack genedomains for pili production [116] they seem unable to reduceminerals via both mechanisms present in Shewanella andGeobacter It can therefore be speculated that ANME-1 areless versatile in electron acceptor use and are not able toreduce solid metal oxides However DIET mechanisms arestill not well understood and the true differences betweenMHCs of different ANME types need to be investigated usingbiochemical methods This would allow uncovering the truecapabilities concerning DIET

34 Menaquinones and Methanophenazines ANME-2a en-coded a protein with a domain specific for PhzF which is anenzyme involved in phenazine biosynthesis in Pseudomonasfluorescens [152 153] The respective gene is not present in allmethanophenazine containing methanogens (in our genomecomparison only inM acetivorans andM formicica Table 2)so it is unclear whether this enzyme is really involved inmethanophenazine biosynthesis It is however likely thatANME-2a use methanophenazines in their respiratory chainsince gene domains for menaquinone biosynthesis wereabsent (Table 2) ldquoCa M nitroreducensrdquo probably uses

menaquinones as membrane-integral electron carrier sinceenvironmental genomes [28 43] encoded the futalosine(mqn) biosynthesis pathway as reported for Archaeoglobusfulgidus [154] (Table 2) Moreover ldquoCa M nitroreducensrdquoenrichment cultures showed absence of methanophenazines[43] ANME-1 also contained gene domains formenaquinonebiosynthesis via the futalosine (mqn) biosynthesis pathway(Table 2) Indications for a quinone biosynthesis pathwayin ANME-1 were previously found to be weak since onlysome of the Ubi homologues of the oxic ubiquinone biosyn-thesis pathway were detected [41] but the futalosine (mqn)biosynthesis pathway was overlooked in that particular anal-ysis Additionally ANME-1 have Fqo homologues similarto Archaeoglobus fulgidus [44] and expressed the catalyticsubunit FqoF [41] However since the phenazine biosynthesisdomain PhzF was also present in the ANME-1 genomes(Table 2) and Fpo and Fqo are homologues we cannotconclude on genomic information alone which redox shuttleis used by ANME-1 during AOM If ANME-1 would usemenaquinones this would have implications for subsequentelectron transfer to MHCs since methanophenazine (1198640 =minus165mV) [155] and menaquinone (1198640 = minus80mV) [156] havedifferent redox potentials

35 Cell Adhesion Some gene domains involved in cel-lular adhesion were more abundant in ANME than inmethanogens (Table 2) especially in ANME-2a and ANME-1that are known to form syntrophic interactions for electrontransfer during respiration These domains include HYR(IPR003410) and CARDB domains (IPR011635) that bothhave a direct role in cellular adhesion [157] (Table 2) Interest-ingly also domains related to the cellulosome of Clostridiumspecies termed dockerin and cohesin were highly abundantin both ANME-1 and ANME-2a as compared to ANME-2dand methanogens together with many carbohydrate bindingdomains (Table 2) In Clostridium species dockerin andcohesin form an anchor to the bacterial cell wall that containsa scaffold with cellulose-degrading enzymes and a carbohy-drate bindingmodule that binds cellulose altogether formingthe cellulosome [158] These domains have been found in alldomains of life irrespective of cellulose utilization but thefunction of such proteins outside of the cellulosome is notknown [159]Therefore dockerin cohesin and carbohydratebinding domains in ANME could hypothetically form aconstruct that binds to carbohydrates and could possibly havea function in cell-to-cell contact or MHC adhesion but thisneeds further investigation

4 Future Challenges

Advances in (meta)genomics transcriptomics and pro-teomics have produced the valuable metabolic blueprints ofdifferent ANMEwith hypotheses on how centralmetabolismelectron transport and energy conservation may functionFuture experiments are needed to biochemically demonstratethat these hypotheses are correct

The bottleneck for biochemical studies of ANME isthe lack of pure cultures due to the slow and syntrophic

Archaea 17

growth However the recent milestone discovery of directelectron transfer provides opportunities to grow ANMEas stated previously on electron accepting electrodes (ieanodes) [160] In this way pure or highly enriched culturesof different ANME without their respective syntrophic part-ner could be obtained and MHCs responsible for electricconduction could be biochemically characterized It seemsthat ANME-1 are limited by the size and abundance ofMHCs which could relate to differences in behavior onan anode The partner bacteria of ANME-1 and ANME-2could be investigated on an electron donating electrode (iecathode) with specific focus on the ability to produce pili (ienanowires) Also worth investigating is if besides ANME-2d ANME-2ab could also use insoluble electron acceptorsand if ANME-2d could donate electrons to a bacterialpartner

Another future challenge is to isolate and characterizeMcr from different ANME clades It needs to be investi-gated if Mcr abundance in ANME cells compensates forthe slow reverse activity or if modifications in the Mcrof ANME-1 also contribute to a better reverse activity ofMcr Moreover the effect of methane partial pressure onreaction rates and enzyme kinetics needs to be determined insitu

ANME-1 are potentially able to perform hydrogeno-trophic methanogenesis due to the presence of a hydrogenasein the genome Genetic indications of menaquinones aselectron carrier in ANME-1 and the various cellulosome andcell adhesion related gene domains in all ANME are alsotopics that could be explored further Methanogenic archaeaare likely not able to perform AOM but additional studieson TMO and more genetic modifications to stimulate AOMin methanogens could help in understanding the param-eters needed for AOM to occur Ultimately physiologicalunderstanding of ANME will help to explain the observedecological niche separation of different ANME clades and theoccurrence of ANMEwithout a bacterial partnerThis wouldgreatly enhance our knowledge of themethane cycle in anoxicenvironments

Competing Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors thank Stefanie Berger (RU Nijmegen) for criticalreading of the manuscript This research is supported bythe Soehngen Institute of Anaerobic Microbiology (SIAM)Gravitation grant (024002002) of the Netherlands Ministryof Education Culture and Science and the NetherlandsOrganisation for Scientific Research (NWO) Mike S MJetten was further supported by ERC AG 339880 Eco-MoMand Alfons J M Stams was supported by ERC AG 323009Novel Anaerobes

References

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[2] K-U Hinrichs J M Hayes S P Sylva P G Brewert andE F DeLong ldquoMethane-consuming archaebacteria in marinesedimentsrdquo Nature vol 398 no 6730 pp 802ndash805 1999

[3] V J Orphan C H House K-U Hinrichs K D McKeeganand E F DeLong ldquoMethane-consuming archaea revealed bydirectly coupled isotopic and phylogenetic analysisrdquo Sciencevol 293 no 5529 pp 484ndash487 2001

[4] K-U Hinrichs and A Boetius ldquoThe anaerobic oxidation ofmethane new insights in microbial ecology and biogeochem-istryrdquo inOceanMargin Systems GWefer D Billett D HebbelnB B Joslashrgensen M Schluter and T VanWeering Eds pp 457ndash477 Springer Berlin Germany 2002

[5] K Knittel T Losekann A Boetius R Kort and R AmannldquoDiversity and distribution of methanotrophic archaea at coldseepsrdquo Applied and Environmental Microbiology vol 71 no 1pp 467ndash479 2005

[6] K Knittel and A Boetius ldquoAnaerobic oxidation of methaneprogress with an unknown processrdquo Annual Review of Micro-biology vol 63 pp 311ndash334 2009

[7] V J Orphan K-U Hinrichs W Ussler III et al ldquoComparativeanalysis of methane-oxidizing archaea and sulfate-reducingbacteria in anoxic marine sedimentsrdquoApplied and Environmen-tal Microbiology vol 67 no 4 pp 1922ndash1934 2001

[8] T Losekann K Knittel T Nadalig et al ldquoDiversity andabundance of aerobic and anaerobic methane oxidizers atthe Haakon Mosby Mud Volcano Barents Seardquo Applied andEnvironmentalMicrobiology vol 73 no 10 pp 3348ndash3362 2007

[9] H Niemann T Losekann D De Beer et al ldquoNovel microbialcommunities of the Haakon Mosby mud volcano and their roleas amethane sinkrdquoNature vol 443 no 7113 pp 854ndash858 2006

[10] TNunouraHOida T Toki J Ashi K Takai andKHorikoshildquoQuantification of mcrA by quantitative fluorescent PCR insediments from methane seep of the Nankai Troughrdquo FEMSMicrobiology Ecology vol 57 no 1 pp 149ndash157 2006

[11] B Orcutt A Boetius M Elvert V Samarkin and S B JoyeldquoMolecular biogeochemistry of sulfate reduction methanogen-esis and the anaerobic oxidation of methane at Gulf of Mexicocold seepsrdquoGeochimica et Cosmochimica Acta vol 69 no 17 pp4267ndash4281 2005

[12] V J Orphan W Ussler III T H Naehr C H House K-U Hinrichs and C K Paull ldquoGeological geochemical andmicrobiological heterogeneity of the seafloor around methanevents in the Eel River Basin offshore Californiardquo ChemicalGeology vol 205 no 3-4 pp 265ndash289 2004

[13] M G Pachiadaki A Kallionaki A Dahlmann G J De Langeand K A Kormas ldquoDiversity and spatial distribution ofprokaryotic communities along a sediment vertical profile ofa deep-sea mud volcanordquo Microbial Ecology vol 62 no 3 pp655ndash668 2011

[14] I Roalkvam H Dahle Y Chen S L Joslashrgensen H Haflidasonand I H Steen ldquoFine-scale community structure analysis ofANME in Nyegga sediments with high and low methane fluxrdquoFrontiers in Microbiology vol 3 p 216 2012

[15] K Yanagawa M Sunamura M A Lever et al ldquoNiche separa-tion of methanotrophic archaea (ANME-1 and -2) in methane-seep sediments of the Eastern Japan Sea offshore JoetsurdquoGeomicrobiology Journal vol 28 no 2 pp 118ndash129 2011

18 Archaea

[16] A Pernthaler A E Dekas C T Brown S K Goffredi TEmbaye and V J Orphan ldquoDiverse syntrophic partnershipsfromdeep-seamethane vents revealed by direct cell capture andmetagenomicsrdquo Proceedings of the National Academy of Sciencesof the United States of America vol 105 no 19 pp 7052ndash70572008

[17] R Hatzenpichler S A Connon D Goudeau R R Malm-strom T Woyke and V J Orphan ldquoVisualizing in situtranslational activity for identifying and sorting slow-growingarchaealminusbacterial consortiardquo Proceedings of the NationalAcademy of Sciences vol 113 no 28 pp E4069ndashE4078 2016

[18] L Maignien R J Parkes B Cragg et al ldquoAnaerobic oxidationof methane in hypersaline cold seep sedimentsrdquo FEMS Micro-biology Ecology vol 83 no 1 pp 214ndash231 2013

[19] V J Orphan C H House K-U Hinrichs K D McKeeganand E F DeLong ldquoMultiple archaeal groups mediate methaneoxidation in anoxic cold seep sedimentsrdquo Proceedings of theNational Academy of Sciences of the United States of Americavol 99 no 11 pp 7663ndash7668 2002

[20] T TreudeM Kruger A Boetius and B B Joslashrgensen ldquoEnviron-mental control on anaerobic oxidation of methane in the gassysediments of Eckernforde Bay (German Baltic)rdquo Limnology andOceanography vol 50 no 6 pp 1771ndash1786 2005

[21] G C Jagersma R J W Meulepas I Heikamp-De Jong etal ldquoMicrobial diversity and community structure of a highlyactive anaerobic methane-oxidizing sulfate-reducing enrich-mentrdquo Environmental Microbiology vol 11 no 12 pp 3223ndash3232 2009

[22] M Blumenberg R Seifert J Reitner T Pape andWMichaelisldquoMembrane lipid patterns typify distinct anaerobic methan-otrophic consortiardquo Proceedings of the National Academy ofSciences of the United States of America vol 101 no 30 pp 11111ndash11116 2004

[23] S Bertram M Blumenberg W Michaelis M Siegert MKruger and R Seifert ldquoMethanogenic capabilities of ANME-archaea deduced from 13C-labelling approachesrdquo Environmen-tal Microbiology vol 15 no 8 pp 2384ndash2393 2013

[24] K G Lloyd M J Alperin and A Teske ldquoEnvironmental evi-dence for net methane production and oxidation in putativeANaerobic MEthanotrophic (ANME) archaeardquo EnvironmentalMicrobiology vol 13 no 9 pp 2548ndash2564 2011

[25] M Takeuchi H Yoshioka Y Seo et al ldquoA distinct freshwater-adapted subgroup of ANME-1 dominates active archaeal com-munities in terrestrial subsurfaces in Japanrdquo EnvironmentalMicrobiology vol 13 no 12 pp 3206ndash3218 2011

[26] R T Amos B A Bekins I M Cozzarelli et al ldquoEvidence foriron-mediated anaerobic methane oxidation in a crude oil-contaminated aquiferrdquo Geobiology vol 10 no 6 pp 506ndash5172012

[27] P H Timmers D A Suarez-Zuluaga M van Rossem MDiender A J Stams and C M Plugge ldquoAnaerobic oxidationof methane associated with sulfate reduction in a naturalfreshwater gas sourcerdquo ISME Journal vol 10 pp 1400ndash14122015

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[29] H J Mills C Hodges K Wilson I R MacDonald and PA Sobecky ldquoMicrobial diversity in sediments associated withsurface-breaching gas hydrate mounds in the Gulf of MexicordquoFEMS Microbiology Ecology vol 46 no 1 pp 39ndash52 2003

[30] K G Lloyd L Lapham and A Teske ldquoAn anaerobic methane-oxidizing community of ANME-1b archaea in hypersaline gulfofMexico sedimentsrdquoApplied and EnvironmentalMicrobiologyvol 72 no 11 pp 7218ndash7230 2006

[31] A A Raghoebarsing A Pol K T Van De Pas-Schoonen et alldquoA microbial consortium couples anaerobic methane oxidationto denitrificationrdquoNature vol 440 no 7086 pp 918ndash921 2006

[32] S Hu R J Zeng L C Burow P Lant J Keller and Z YuanldquoEnrichment of denitrifying anaerobic methane oxidizingmicroorganismsrdquo Environmental Microbiology Reports vol 1no 5 pp 377ndash384 2009

[33] Z-W Ding J Ding L Fu F Zhang and R J Zeng ldquoSimultane-ous enrichment of denitrifying methanotrophs and anammoxbacteriardquo Applied Microbiology and Biotechnology vol 98 no24 pp 10211ndash10221 2014

[34] R Seifert K Nauhaus M Blumenberg M Kruger and WMichaelis ldquoMethane dynamics in a microbial community ofthe Black Sea traced by stable carbon isotopes in vitrordquoOrganicGeochemistry vol 37 no 10 pp 1411ndash1419 2006

[35] J Ding Z-W Ding L Fu Y-Z Lu S H Cheng and R JZeng ldquoNew primers for detecting and quantifying denitrifyinganaerobic methane oxidation archaea in different ecologicalnichesrdquo Applied Microbiology and Biotechnology vol 99 no 22pp 9805ndash9812 2015

[36] A Vaksmaa C Luke T van Alen et al ldquoDistribution and activ-ity of the anaerobic methanotrophic community in a nitrogen-fertilized Italian paddy soilrdquo FEMS Microbiology Ecology vol92 no 12 2016

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[40] R Stokke I Roalkvam A Lanzen H Haflidason and I HSteen ldquoIntegrated metagenomic and metaproteomic analysesof an ANME-1-dominated community in marine cold seepsedimentsrdquo Environmental Microbiology vol 14 no 5 pp 1333ndash1346 2012

[41] A Meyerdierks M Kube I Kostadinov et al ldquoMetagenomeand mRNA expression analyses of anaerobic methanotrophicarchaea of the ANME-1 grouprdquo Environmental Microbiologyvol 12 no 2 pp 422ndash439 2010

[42] F-P Wang Y Zhang Y Chen et al ldquoMethanotrophicarchaea possessing diverging methane-oxidizing and electron-transporting pathwaysrdquo ISME Journal vol 8 no 5 pp 1069ndash1078 2014

[43] A Arshad D R Speth R M de Graaf H J Op den Camp MS Jetten and C U Welte ldquoA metagenomics-based metabolicmodel of nitrate-dependent anaerobic oxidation of methane byMethanoperedens-like archaeardquo Frontiers inMicrobiology vol 6article1423 2015

[44] S J Hallam N Putnam CM Preston et al ldquoReversemethano-genesis testing the hypothesis with environmental genomicsrdquoScience vol 305 no 5689 pp 1457ndash1462 2004

Archaea 19

[45] R K Thauer ldquoAnaerobic oxidation of methane with sulfate onthe reversibility of the reactions that are catalyzed by enzymesalso involved inmethanogenesis fromCO

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energy conservation in methanogenic archaeardquo Archives ofMicrobiology vol 165 no 3 pp 149ndash163 1996

[47] A-K Kaster J Moll K Parey and R K Thauer ldquoCoupling offerredoxin and heterodisulfide reduction via electron bifurca-tion in hydrogenotrophic methanogenic archaeardquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 108 no 7 pp 2981ndash2986 2011

[48] R K Thauer A-K Kaster H Seedorf W Buckel and RHedderich ldquoMethanogenic archaea ecologically relevant dif-ferences in energy conservationrdquo Nature Reviews Microbiologyvol 6 no 8 pp 579ndash591 2008

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[52] P V Welander and W W Metcalf ldquoLoss of the mtr operon inMethanosarcina blocks growth on methanol but not methano-genesis and reveals an unknown methanogenic pathwayrdquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 102 no 30 pp 10664ndash10669 2005

[53] P V Welander and W W Metcalf ldquoMutagenesis of the C1oxidation pathway inmethanosarcina barkeri new insights intothe MtrMer bypass pathwayrdquo Journal of Bacteriology vol 190no 6 pp 1928ndash1936 2008

[54] M Goenrich R K Thauer H Yurimoto and N KatoldquoFormaldehyde activating enzyme (Fae) and hexulose-6-phosphate synthase (Hps) inMethanosarcina barkeri a possiblefunction in ribose-5-phosphate biosynthesisrdquoArchives ofMicro-biology vol 184 no 1 pp 41ndash48 2005

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2by methan-

otrophicmicrobial mats from gas seeps of the anoxic Black SeardquoApplied and EnvironmentalMicrobiology vol 73 no 7 pp 2271ndash2283 2007

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[65] R J WMeulepas C G Jagersma J Gieteling C J N BuismanA J M Stams and P N L Lens ldquoEnrichment of anaerobicmethanotrophs in sulfate-reducing membrane bioreactorsrdquoBiotechnology and Bioengineering vol 104 no 3 pp 458ndash4702009

[66] T Holler G Wegener H Niemann et al ldquoCarbon and sulfurback flux during anaerobic microbial oxidation of methane andcoupled sulfate reductionrdquo Proceedings of the National Academyof Sciences of the United States of America vol 108 no 52 ppE1484ndashE1490 2011

[67] M Kruger AMeyerdierks F O Glockner et al ldquoA conspicuousnickel protein in microbial mats that oxidize methane anaero-bicallyrdquo Nature vol 426 no 6968 pp 878ndash881 2003

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variant from archaea associated with anaerobic oxidation ofmethanerdquo Journal of the American Chemical Society vol 130 no32 pp 10758ndash10767 2008

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[70] R K Thauer and S Shima ldquoMethane as fuel for anaerobicmicroorganismsrdquo Annals of the New York Academy of Sciencesvol 1125 pp 158ndash170 2008

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[72] P H A Timmers J Gieteling H C A Widjaja-Greefkeset al ldquoGrowth of anaerobic methane-oxidizing archaea andsulfate-reducing bacteria in a high-pressure membrane capsulebioreactorrdquoApplied and EnvironmentalMicrobiology vol 81 no4 pp 1286ndash1296 2015

[73] MKruger HWoltersMGehre S B Joye andH-H RichnowldquoTracing the slow growth of anaerobic methane-oxidizingcommunities by 15N-labelling techniquesrdquo FEMS MicrobiologyEcology vol 63 no 3 pp 401ndash411 2008

[74] R J W Meulepas C G Jagersma A F Khadem C J N Buis-man A J M Stams and P N L Lens ldquoEffect of environmentalconditions on sulfate reduction withmethane as electron donorby an Eckernforde Bay enrichmentrdquo Environmental Science andTechnology vol 43 no 17 pp 6553ndash6559 2009

20 Archaea

[75] M W Bowles V A Samarkin and S B Joye ldquoImprovedmeasurement of microbial activity in deep-sea sediments atin situ pressure and methane concentrationrdquo Limnology andOceanography Methods vol 9 pp 499ndash506 2011

[76] S Shima M Krueger T Weinert et al ldquoStructure of a methyl-coenzyme M reductase from Black Sea mats that oxidizemethane anaerobicallyrdquo Nature vol 481 no 7379 pp 98ndash1012012

[77] K D Allen G Wegener and R H White ldquoDiscovery of multi-ple modified F-430 coenzymes in methanogens and anaerobicmethanotrophic archaea suggests possible new roles for F-430in naturerdquoApplied and Environmental Microbiology vol 80 no20 pp 6403ndash6412 2014

[78] V W Soo M J McAnulty A Tripathi et al ldquoReversingmethanogenesis to capture methane for liquid biofuel precur-sorsrdquoMicrobial Cell Factories vol 15 article 11 2016

[79] D L Valentine and W S Reeburgh ldquoNew perspectives onanaerobicmethane oxidationrdquoEnvironmentalMicrobiology vol2 no 5 pp 477ndash484 2000

[80] D L Valentine ldquoBiogeochemistry and microbial ecology ofmethane oxidation in anoxic environments a reviewrdquo Antonievan Leeuwenhoek International Journal of General and Molecu-lar Microbiology vol 81 no 1-4 pp 271ndash282 2002

[81] A J B Zehnder and T D Brock ldquoMethane formation andmethane oxidation by methanogenic bacteriardquo Journal of Bac-teriology vol 137 no 1 pp 420ndash432 1979

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[83] J J Moran C H House K H Freeman and J G FerryldquoTrace methane oxidation studied in several Euryarchaeotaunder diverse conditionsrdquo Archaea vol 1 no 5 pp 303ndash3092005

[84] J J Moran C H House B Thomas and K H FreemanldquoProducts of tracemethane oxidation during nonmethyltrophicgrowth by Methanosarcinardquo Journal of Geophysical ResearchBiogeosciences vol 112 no 2 2007

[85] R J W Meulepas C G Jagersma Y Zhang et al ldquoTracemethane oxidation and the methane dependency of sulfatereduction in anaerobic granular sludgerdquo FEMS MicrobiologyEcology vol 72 no 2 pp 261ndash271 2010

[86] A J B Zehnder andTD Brock ldquoAnaerobicmethane oxidationoccurrence and ecologyrdquoApplied and Environmental Microbiol-ogy vol 39 no 1 pp 194ndash204 1980

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oxidation in freshwater peatlandsrdquo Geomicrobiology Journalvol 24 no 7-8 pp 583ndash597 2007

[89] M J Alperin and T M Hoehler ldquoAnaerobic methane oxidationby archaeasulfate-reducing bacteria aggregates 1 Thermody-namic and physical constraintsrdquo American Journal of Sciencevol 309 no 10 pp 869ndash957 2009

[90] S L Caldwell J R Laidler E A Brewer J O Eberly S CSandborgh and F S Colwell ldquoAnaerobic oxidation of methanemechanisms bioenergetics and the ecology of associatedmicroorganismsrdquo Environmental Science and Technology vol42 no 18 pp 6791ndash6799 2008

[91] GWang A J Spivack and S DrsquoHondt ldquoGibbs energies of reac-tion and microbial mutualism in anaerobic deep subseafloorsediments of ODP Site 1226rdquoGeochimica et Cosmochimica Actavol 74 no 14 pp 3938ndash3947 2010

[92] P R Girguis A E Cozen and E F DeLong ldquoGrowth andpopulation dynamics of anaerobic methane-oxidizing archaeaand sulfate-reducing bacteria in a continuous-flow bioreactorrdquoApplied and EnvironmentalMicrobiology vol 71 no 7 pp 3725ndash3733 2005

[93] K Nauhaus M Albrecht M Elvert A Boetius and F WiddelldquoIn vitro cell growth ofmarine archaeal-bacterial consortia dur-ing anaerobic oxidation ofmethanewith sulfaterdquoEnvironmentalMicrobiology vol 9 no 1 pp 187ndash196 2007

[94] B Orcutt V Samarkin A Boetius and S Joye ldquoOn the relation-ship between methane production and oxidation by anaerobicmethanotrophic communities from cold seeps of the Gulf ofMexicordquo Environmental Microbiology vol 10 no 5 pp 1108ndash1117 2008

[95] M Y Yoshinaga T Holler T Goldhammer et al ldquoCarbon iso-tope equilibration during sulphate-limited anaerobic oxidationof methanerdquo Nature Geoscience vol 7 no 3 pp 190ndash194 2014

[96] T Treude J Niggemann J Kallmeyer et al ldquoAnaerobic oxi-dation of methane and sulfate reduction along the Chileancontinental marginrdquo Geochimica et Cosmochimica Acta vol 69no 11 pp 2767ndash2779 2005

[97] R J Parkes B A Cragg N Banning et al ldquoBiogeochemistryand biodiversity of methane cycling in subsurface marinesediments (SkagerrakDenmark)rdquoEnvironmentalMicrobiologyvol 9 no 5 pp 1146ndash1161 2007

[98] N J Knab B A Cragg E R C Hornibrook et al ldquoRegulationof anaerobic methane oxidation in sediments of the Black SeardquoBiogeosciences vol 6 no 8 pp 1505ndash1518 2009

[99] H Yoshioka A Maruyama T Nakamura et al ldquoActivities anddistribution of methanogenic and methane-oxidizing microbesin marine sediments from the Cascadia Marginrdquo Geobiologyvol 8 no 3 pp 223ndash233 2010

[100] G Wegener V Krukenberg S E Ruff M Y Kellermann andK Knittel ldquoMetabolic capabilities of microorganisms involvedin and associated with the anaerobic oxidation of methanerdquoFrontiers in Microbiology vol 7 article 46 2016

[101] R J W Meulepas C G Jagersma A F Khadem A J MStams and P N L Lens ldquoEffect of methanogenic substrateson anaerobic oxidation of methane and sulfate reduction by ananaerobic methanotrophic enrichmentrdquo Applied Microbiologyand Biotechnology vol 87 no 4 pp 1499ndash1506 2010

[102] J Milucka T G Ferdelman L Polerecky et al ldquoZero-valentsulphur is a key intermediate in marine methane oxidationrdquoNature vol 491 no 7425 pp 541ndash546 2012

[103] W Michaelis R Seifert K Nauhaus et al ldquoMicrobial reefs inthe black sea fueled by anaerobic oxidation ofmethanerdquo Sciencevol 297 no 5583 pp 1013ndash1015 2002

[104] A Vigneron P Cruaud P Pignet et al ldquoArchaeal and anaerobicmethane oxidizer communities in the Sonora Margin coldseeps Guaymas Basin (Gulf of California)rdquo ISME Journal vol7 no 8 pp 1595ndash1608 2013

[105] M Alperin and T Hoehler ldquoThe ongoing mystery of sea-floormethanerdquo Science vol 329 no 5989 pp 288ndash289 2010

[106] B Orcutt and C Meile ldquoConstraints on mechanisms and ratesof anaerobic oxidation of methane by microbial consortiaprocess-basedmodeling of ANME-2 archaea and sulfate reduc-ing bacteria interactionsrdquo Biogeosciences vol 5 no 6 pp 1587ndash1599 2008

Archaea 21

[107] S E McGlynn G L Chadwick C P Kempes and V J OrphanldquoSingle cell activity reveals direct electron transfer in methan-otrophic consortiardquoNature vol 526 no 7574 pp 531ndash535 2015

[108] D R Lovley ldquoElectromicrobiologyrdquo Annual Review of Microbi-ology vol 66 pp 391ndash409 2012

[109] S M Strycharz-Glaven R M Snider A Guiseppi-Elie andL M Tender ldquoOn the electrical conductivity of microbialnanowires and biofilmsrdquoEnergy and Environmental Science vol4 no 11 pp 4366ndash4379 2011

[110] D J Richardson J N Butt J K Fredrickson et al ldquoThe lsquoporinndashcytochromersquo model for microbe-to-mineral electron transferrdquoMolecular Microbiology vol 85 no 2 pp 201ndash212 2012

[111] A Okamoto K Hashimoto and R Nakamura ldquoLong-rangeelectron conduction of Shewanella biofilms mediated by outermembrane C-type cytochromesrdquo Bioelectrochemistry vol 85pp 61ndash65 2012

[112] M Y El-Naggar G Wanger K M Leung et al ldquoElectricaltransport along bacterial nanowires from Shewanella oneidensisMR-1rdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 107 no 42 pp 18127ndash18131 2010

[113] G Reguera K D McCarthy T Mehta J S Nicoll M TTuominen and D R Lovley ldquoExtracellular electron transfer viamicrobial nanowiresrdquo Nature vol 435 no 7045 pp 1098ndash11012005

[114] Z M Summers H E Fogarty C Leang A E Franks N SMalvankar and D R Lovley ldquoDirect exchange of electronswithin aggregates of an evolved syntrophic coculture of anaer-obic bacteriardquo Science vol 330 no 6009 pp 1413ndash1415 2010

[115] A Kletzin T Heimerl J Flechsler L V Niftrik R Rachel andA Klingl ldquoCytochromes c in archaea distribution maturationcell architecture and the special case of Ignicoccus hospitalisrdquoFrontiers in Microbiology vol 6 article 439 2015

[116] GWegener V Krukenberg D Riedel H E Tegetmeyer and ABoetius ldquoIntercellular wiring enables electron transfer betweenmethanotrophic archaea and bacteriardquo Nature vol 526 no7574 pp 587ndash590 2015

[117] D HHaft S H Payne and J D Selengut ldquoArchaeosortases andexosortases are widely distributed systems linking membranetransit with posttranslational modificationrdquo Journal of Bacteri-ology vol 194 no 1 pp 36ndash48 2012

[118] A Marchler-Bauer M K Derbyshire N R Gonzales et alldquoCDD NCBIrsquos conserved domain databaserdquo Nucleic AcidsResearch vol 43 no 1 pp D222ndashD226 2015

[119] A Mitchell H-Y Chang L Daugherty et al ldquoThe InterProprotein families database the classification resource after 15yearsrdquo Nucleic Acids Research vol 43 no 1 pp D213ndashD2212015

[120] V Krukenberg K Harding M Richter et al ldquoCandidatusdesulfofervidus auxilii a hydrogenotrophic sulfate-reducingbacterium involved in the thermophilic anaerobic oxidation ofmethanerdquo Environmental Microbiology vol 18 pp 3073ndash30912016

[121] L Shi T C Squier J M Zachara and J K Fredrickson ldquoRes-piration of metal (hydr)oxides by Shewanella and Geobactera key role for multihaem c-type cytochromesrdquo MolecularMicrobiology vol 65 no 1 pp 12ndash20 2007

[122] N S Malvankar and D R Lovley ldquoMicrobial nanowires forbioenergy applicationsrdquo Current Opinion in Biotechnology vol27 pp 88ndash95 2014

[123] A-E Rotaru T LWoodard K PNevin andDR Lovley ldquoLinkbetween capacity for current production and syntrophic growth

in Geobacter speciesrdquo Frontiers in Microbiology vol 6 article744 2015

[124] A-E Rotaru P M Shrestha F Liu et al ldquoDirect interspecieselectron transfer between Geobacter metallireducens andMethanosarcina barkerirdquo Applied and Environmental Microbi-ology vol 80 no 15 pp 4599ndash4605 2014

[125] S Scheller H Yu G L Chadwick S E McGlynn and VJ Orphan ldquoArtificial electron acceptors decouple archaealmethane oxidation from sulfate reductionrdquo Science vol 351 no6274 pp 703ndash707 2016

[126] J Milucka F Widdel and S Shima ldquoImmunological detec-tion of enzymes for sulfate reduction in anaerobic methane-oxidizing consortiardquo Environmental Microbiology vol 15 no 5pp 1561ndash1571 2013

[127] P Cabello M D Roldan and C Moreno-Vivian ldquoNitratereduction and the nitrogen cycle in archaeardquoMicrobiology vol150 no 11 pp 3527ndash3546 2004

[128] R MMartinez-Espinosa E J Dridge M J Bonete et al ldquoLookon the positive sideThe orientation identification and bioener-getics of lsquoArchaealrsquomembrane-boundnitrate reductasesrdquoFEMSMicrobiology Letters vol 276 no 2 pp 129ndash139 2007

[129] S de VriesMMomcilovicM J F Strampraad J PWhiteleggeA Baghai and I Schroder ldquoAdaptation to a high-tungsten envi-ronment pyrobaculum aerophilum contains an active tungstennitrate reductaserdquo Biochemistry vol 49 no 45 pp 9911ndash99212010

[130] M Egger O Rasigraf C J Sapart et al ldquoIron-mediated anaer-obic oxidation of methane in brackish coastal sedimentsrdquoEnvironmental Science and Technology vol 49 no 1 pp 277ndash283 2015

[131] T Treude S Krause J Maltby A W Dale R Coffin and LJ Hamdan ldquoSulfate reduction and methane oxidation activitybelow the sulfate-methane transition zone in Alaskan BeaufortSea continental margin sediments implications for deep sulfurcyclingrdquo Geochimica et Cosmochimica Acta vol 144 pp 217ndash237 2014

[132] N Riedinger M J Formolo T W Lyons S Henkel A Beckand S Kasten ldquoAn inorganic geochemical argument for coupledanaerobic oxidation of methane and iron reduction in marinesedimentsrdquo Geobiology vol 12 no 2 pp 172ndash181 2014

[133] Y-H Chang T-W Cheng W-J Lai et al ldquoMicrobial methanecycling in a terrestrialmud volcano in eastern Taiwanrdquo Environ-mental Microbiology vol 14 no 4 pp 895ndash908 2012

[134] S A Crowe S Katsev K Leslie et al ldquoThe methane cycle inferruginous Lake Matanordquo Geobiology vol 9 no 1 pp 61ndash782011

[135] O Sivan M Adler A Pearson et al ldquoGeochemical evidence foriron-mediated anaerobic oxidation of methanerdquo Limnology andOceanography vol 56 no 4 pp 1536ndash1544 2011

[136] K E A Segarra C Comerford J Slaughter and S B JoyeldquoImpact of electron acceptor availability on the anaerobic oxi-dation of methane in coastal freshwater and brackish wetlandsedimentsrdquo Geochimica et Cosmochimica Acta vol 115 pp 15ndash30 2013

[137] V Gupta K A Smemo J B Yavitt D Fowle B Branfireunand N Basiliko ldquoStable isotopes reveal widespread anaerobicmethane oxidation across latitude and peatland typerdquo Environ-mental Science and Technology vol 47 no 15 pp 8273ndash82792013

[138] O Oni T Miyatake S Kasten et al ldquoDistinct microbialpopulations are tightly linked to the profile of dissolved iron in

22 Archaea

the methanic sediments of the Helgolandmud area North SeardquoFrontiers in Microbiology vol 6 2015

[139] E J Beal C H House and V J Orphan ldquoManganese- andiron-dependent marine methane oxidationrdquo Science vol 325no 5937 pp 184ndash187 2009

[140] M W Bowles V A Samarkin K M Bowles and S B JoyeldquoWeak coupling between sulfate reduction and the anaerobicoxidation of methane in methane-rich seafloor sedimentsduring ex situ incubationrdquo Geochimica et Cosmochimica Actavol 75 no 2 pp 500ndash519 2011

[141] Y Z Lu L Fu J Ding Z Ding N Li and R J Zeng ldquoCr(VI)reduction coupled with anaerobic oxidation of methane in alaboratory reactorrdquoWater Research vol 102 pp 445ndash452 2016

[142] K F Ettwig B Zhu D Speth J T Keltjens M S Jetten and BKartal ldquoArchaea catalyze iron-dependent anaerobic oxidationof methanerdquo Proceedings of the National Academy of Sciences ofthe United States of America vol 113 no 45 pp 12792ndash127962016

[143] T M Flynn R A Sanford H Ryu et al ldquoFunctional microbialdiversity explains groundwater chemistry in a pristine aquiferrdquoBMCMicrobiology vol 13 no 1 article no 146 2013

[144] C J Schubert F Vazquez T Losekann-Behrens K KnittelM Tonolla and A Boetius ldquoEvidence for anaerobic oxidationof methane in sediments of a freshwater system (Lago diCadagno)rdquo FEMS Microbiology Ecology vol 76 no 1 pp 26ndash38 2011

[145] K E A Segarra F Schubotz V Samarkin M Y Yoshinaga K-U Hinrichs and S B Joye ldquoHigh rates of anaerobic methaneoxidation in freshwater wetlands reduce potential atmosphericmethane emissionsrdquo Nature Communications vol 6 article7477 2015

[146] E J Beal M W Claire and C H House ldquoHigh rates ofanaerobic methanotrophy at low sulfate concentrations withimplications for past and present methane levelsrdquo Geobiologyvol 9 no 2 pp 131ndash139 2011

[147] F Kracke I Vassilev and J O Kromer ldquoMicrobial electrontransport and energy conservationmdashthe foundation for opti-mizing bioelectrochemical systemsrdquo Frontiers in Microbiologyvol 6 article 575 2015

[148] C L Reardon A C Dohnalkova P Nachimuthu et al ldquoRoleof outer-membrane cytochromes MtrC and OmcA in thebiomineralization of ferrihydrite by Shewanella oneidensisMR-1rdquo Geobiology vol 8 no 1 pp 56ndash68 2010

[149] L Shi B Chen Z Wang et al ldquoIsolation of a high-affinityfunctional protein complex between OmcA and MtrC twoouter membrane decaheme c-type cytochromes of Shewanellaoneidensis MR-1rdquo Journal of Bacteriology vol 188 no 13 pp4705ndash4714 2006

[150] X Qian T Mester L Morgado et al ldquoBiochemical charac-terization of purified OmcS a c-type cytochrome requiredfor insoluble Fe(III) reduction in Geobacter sulfurreducensrdquoBiochimica et BiophysicaActamdashBioenergetics vol 1807 no 4 pp404ndash412 2011

[151] T Mehta M V Coppi S E Childers and D R Lovley ldquoOutermembrane c-type cytochromes required for Fe(III) andMn(IV)oxide reduction in Geobacter sulfurreducensrdquo Applied andEnvironmentalMicrobiology vol 71 no 12 pp 8634ndash8641 2005

[152] W Blankenfeldt A P Kuzin T Skarina et al ldquoStructure andfunction of the phenazine biosynthetic protein PhzF fromPseudomonas fluorescensrdquoProceedings of theNational Academyof Sciences of the United States of America vol 101 no 47 pp16431ndash16436 2004

[153] J F Parsons F Song L Parsons K Calabrese E Eisensteinand J E Ladner ldquoStructure and function of the phenazinebiosynthesis protein PhzF fromPseudomonas fluorescens 2-79rdquoBiochemistry vol 43 no 39 pp 12427ndash12435 2004

[154] T Hiratsuka K Furihata J Ishikawa et al ldquoAn alternativemenaquinone biosynthetic pathway operating in microorgan-ismsrdquo Science vol 321 no 5896 pp 1670ndash1673 2008

[155] M Tietze A Beuchle I Lamla et al ldquoRedox potentials ofmethanophenazine and CoB-S-S-CoM factors involved inelectron transport in methanogenic archaeardquo ChemBioChemvol 4 no 4 pp 333ndash335 2003

[156] Q H Tran and G Unden ldquoChanges in the proton potentialand the cellular energetics of Escherichia coli during growth byaerobic and anaerobic respiration or by fermentationrdquoEuropeanJournal of Biochemistry vol 251 no 1-2 pp 538ndash543 1998

[157] I Callebaut D Gilges I Vigon and J-P Mornon ldquoHYR anextracellular module involved in cellular adhesion and relatedto the immunoglobulin-like foldrdquo Protein Science vol 9 no 7pp 1382ndash1390 2000

[158] H J Gilbert ldquoCellulosomes microbial nanomachines that dis-play plasticity in quaternary structurerdquoMolecular Microbiologyvol 63 no 6 pp 1568ndash1576 2007

[159] A Peer S P Smith E A Bayer R Lamed and I BorovokldquoNoncellulosomal cohesin- and dockerin-like modules in thethree domains of liferdquo FEMS Microbiology Letters vol 291 no1 pp 1ndash16 2009

[160] M Wagner ldquoMicrobiology conductive consortiardquo Nature vol526 no 7574 pp 513ndash514 2015

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Archaea 13

MetFMer

Mdh

FaeHps

SRB

MHC

Mch

Mtd

Ftr

Fmd

McrMQ

Hdr1

MQ

MHC

Hdr2

CoB-S-S-CoMCoB-SHCoM-SH

Mtr

Fqo

CH4

CH3-CoMCH3-OH

CH2O CH3-H4MPT

F420F420H2

CHO-H4MPT

CHO-MFR

CO2

FdredFdox

H2O

eminus

eminus

CHequivH4MPT

CH2=H4MPT

xH+

H2

MQH2

MQH2

+xNa

Figure 6 Methanotrophic pathway during S-AOM by ANME-1 [40 41] Red lines indicate reversal of the hydrogenotrophic methanogenicpathway grey lines represent absence of conversions and blue lines indicate a bypass of the hydrogenotrophic methanogenic pathway SeeTable 3 for nomenclature

In laboratory incubations researchers were not ableto stimulate net methanogenesis through addition ofmethanogenic substrates to AOM performing sediments[62 94] In two cases researchers were successful [23 100]In one of these cases sediment-free long-term AOM enrich-ments that were dominated by ANMESRB were incubatedwith methanogenic substrates The resulting methanogenicactivity most likely came from the enrichment of a minorpopulation of methanogens (up to 7permil of total archaealgene tag sequences) that was present in the inoculum[100] In the second study methanogenic substrates wereadded to ANME-1 and ANME-2 dominated microbialmat samples and methanogenesis also occurred [23]However no information was provided for the total archaealcommunity composition which makes it impossible toexclude methanogens as the responsible organisms

Genomic information of ANME also gives indication onpotential methanogenic routes Considering methylotrophicmethanogenesis no gene homologues catalyzing methyltransfer from methylated substrates to coenzyme M weredetected in ANME (Table 2) [40ndash43] Acetoclastic methano-genesis needs either the AMP- and ADP-forming acetyl-coenzyme A synthetase (Acs and Acd resp) or proceedsvia acetate kinase and phosphotransacetylase In ANME-1only the alpha subunit of a homologue of Acd was expressed

during AOM [41] but in an ANME-1 proteome of activeAOM biomass no Acd was detected [40] The Acd gene wasdetected in the single-aggregate genome and transcriptomeof ANME-2a [42] and in ANME-2d [43] However genedomains for Acd are also present in methanogens unableto use acetate as substrate (Table 2) and are probably usedfor lipid metabolism In hydrogenotrophic methanogenesishydrogenases are used to replenish reduced coenzyme B andto recycle oxidized F

420(discussed in Section 21) Both the

cytoplasmic Mvh complex and the membrane bound Vhowere not present in ANME-2d [43] and not expressed inANME-2a (which also lackedEch andF

420-dependent hydro-

genase (Frh)) [42] making hydrogenotrophic methanogen-esis unlikely In ANME-1 both the cytoplasmic HdrABCand MvhD are present as well as homologues of Frh andEch but these were lacking catalytic subunits [40 41] Aniron hydrogenase was found in both ANME-1 metagenomesbut not in any other methanotroph or methanogen [41](Table 2) This iron hydrogenase domain is part of a genethat is 70 identical to a [FeFe]-hydrogenase of Dehalococ-coides mccartyi [FeFe]-hydrogenases catalyze reversible H

2

production and uptake but these were presumed to have nokey function in AOM [41] However the gene is part of a genecluster of three genes containing a 51 kDaNADH ubiquinoneoxidoreductase subunit (Table S3) which could potentially

14 Archaea

form a complex that generates a proton motive force duringhydrogen oxidation Therefore hydrogenotrophic methano-genesis by ANME-1 cannot be excluded yet

3 Respiration during AnaerobicOxidation of Methane

For netAOMtooccur an external electron acceptor is neededwhich results in a favourable Gibbs free energy change(Table 1) A variety of terminal electron acceptors have beendiscovered for AOM which will be discussed in Sections 31ndash33

31 Sulfate-Dependent AOM During sulfate-dependentAOM electrons are transferred from ANME to the sulfate-reducing bacterial partner Previous work tried to uncoverhow electrons were transferred and most compoundsthat could act as interspecies electron carrier (IEC) wereexcluded to be involved in AOM such as methanolhydrogen methanethiol acetate and carbon monoxide[57 61 62 94 101] Indications that polysulfide could actas IEC were found and ANME-2a archaea were thoughtto perform both AOM and sulfate reduction (SR) [102]However in marine seeps hydrothermal vents and othernondiffusion based sediments AOM rates are high andANME form close associations with SRB in dense aggregates[1 5 103 104] In these aggregates the high AOM ratescould not be explained by diffusion of an IEC whichmade direct interspecies electron transfer (DIET) a moreplausible mechanism [89 105 106] Cellular activities wereindependent of aggregate type and distance between thesyntrophic partners within the aggregate which is bestexplained by DIET [107] DIET is normally achieved usingmultiheme cytochrome c proteins (MHCs) and conductivepili (ie nanowires) which are mainly found in bacteriathat donate electrons extracellularly such as Geobacter andShewanella species [108ndash114] Indeed ANME-2a from seep-sediment samples seem to transfer electrons directly usinglarge MHCs [107] which were found in the metagenome ofANME-2a [107 115] ANME-1 and the associated bacterialpartner also overexpressed genes for extracellular MHCsduring AOM [116] which complements previous findings oftranscription [41] and translation [40] of ANME-1 relatedMHC genes Domain based (meta)genome analysis showsthe high abundance of MHC domains in different ANMEas compared to methanogens (Table 2) A recently isolatedbacterial partner of ANME-1 (ldquoHotSeep-1rdquo) also producedcell-to-cell connections using pili-derived nanowires [116]which explain previously detected Deltaproteobacteria-related pili genes in an AOM sample dominated by ANME-1[40]

How ANME use MHCs to donate electrons to thebacterial partner is not yet clear For ANME-2a the electronsprobably flow from methanophenazine to membrane inte-grated di-heme cytochromes (cytochrome 119887119887

6) that transfer

the electrons through the S-layer via MHCS-layer fusionproteins to extracellular MHCs (Figure 4) (Figure 4 in[107]) Exosortases and archaea-specific archaeosortases are

involved in export of cell surface proteins such as the archaealS-layer proteins These transpeptidases recognize specificsignal peptides for protein- sorting that is archaeosor-tase A recognizes the protein-sorting signal PGF-CTERMand archaeosortase C recognizes the PEF-CTERM signal[117] Both ANME-2a and 2d show presence of di-hemecytochromes archaeosortase A (IPR014522) archaeosortaseC (IPR022504) and other exosortase gene domains (Table 2)Moreover some genes of both ANME-2a and 2d containedboth MHC and PGF or PEF-CTERM domains Lastly somegenes of both ANME-2a and 2d contained both MHC andS-layer domains [107] indicating that these could form theabove-stated MHCS-layer fusion proteins

ANME-1 do not seem to have di-heme cytochromes(Table 2) [115] PGF related domains (IPR026453 andIPR026371) were present in all ANME but PEF-CTERM(IPR017474) related domains were absent in ANME-1 (Table 2) Moreover ANME-1 lacked archaeosortaseA (IPR014522) and archaeosortase C gene domains(IPR022504) as well as some other exosortases (Table 2) Asearch in NCBIrsquos conserved domains database (CCD [118])and the EMBL InterPro database [119] of amino acidssequences of all genes from ANME metagenomes thatcontain MHC domains showed that ANME-1 did not haveany protein-sorting signal or S-layer domains within thesegenes In fact S-layer domains were completely absent inANME-1 (Table 2) These results imply that ANME-1 do notuse di-heme cytochromes for electron transfer to MHCsand do not produce an S-layer (Figure 6) This implies thatANME-1 use a different mechanism for DIET and couldexplain the need for less MHCs by ANME-1 (Table 2)and the observed pili-derived nanowires produced by thebacterial partner [116] The genome of the bacterial partnerof ANME-1 (ldquoHotSeep-1rdquo) encoded 24 c-type cytochromesof which 10 were similar to secreted MHCs of Geobactersulfurreducens [120] which also uses pili for DIET [121]

In the case of ANME-2a it is not clear if pili (ienanowires) were formed during AOM It was previouslythought that electrically conductive pili seemed to be aprerequisite for current production andDIET [122 123] evenwhen syntrophs were closely associated [124] such as withinANME-2SRB aggregates However conductive materialssuch as granular activated carbon were shown to be ableto substitute pili in DIET [124] Although in previous workconductive materials such as phenazines or humic acids didnot seem to stimulate AOM rates [61] in a recent study AOMwas decoupled from SR using artificial electron acceptors[125] This indicates that conductive materials can indeedreplace pili and that ANME-2ab could possibly couple AOMto metal oxide reduction or any other suitable electronacceptor (discussed in Section 33) However it needs to beproven if in ANME-2SRB aggregates no pili are formed andif the mechanism of DIET is fundamentally different fromANME-1

As for the polysulfide shuttling theory [102] canonicalgenes for dissimilatory sulfate reduction such as adenylyl-transferase (Sat) APS reductase (Apr) and dissimilatorysulfite reductase (Dsr) which are all present in the sulfate-reducing archeon A fulgidus (Table S2) were not found in

Archaea 15

metagenomes of ANME-1 [41] and ANME-2a (Table S1)The enzymes Sat and Dsr were also not detected in ANMEcells using fluorescent immunolabelling [126] ANME-1 werepreviously found to encode most proteins for assimilatorysulfate reduction [41] ANME-2d only harbor gene domainsthat encode Sat and assimilatoryATP sulfurylase APS kinaseand sodiumsulfate symporters which were not present inANME-2a (Table S1) It is therefore clear that at least ANME-2a cannot donate electrons to sulfate but need to donateelectrons to a sulfate-reducing partner

32 Nitrate-Dependent AOM Unlike during S-AOMANME-2d that perform N-AOM do not need a bacterialpartner but transfer electrons directly to a membrane boundnitrate reductase (Nar) [28 43] (Figure 5) The ANME-2dgenomes contain most MHCs found so far in archaea[107 115] (Table 2) Of the 87 proteins that contained aCxxCH binding motif of which 43 seemed to be true c-typecytochromes [115] 23 CxxCH motif-encoding transcriptswere expressed during N-AOM [43] The function of mostof these MHCs is not known but they are likely involvedin nitrate reduction since c-type cytochromes are capableof operating in the wide range of redox potentials thatcouple nitrate reduction (11986401015840 (NO

3

minusNO2

minus) = +433mV) andmethane oxidation (11986401015840 (CoM-S-S-CoBCoM-SH+CoB-SH)= minus143mV) [43] Nitrate as terminal electron acceptor inanaerobic respiration has been found in halophilic andthermophilic archaea [127] The nar gene cluster of ldquoCaM nitroreducensrdquo comprises several genes including thecatalytic alpha (NarG molybdopterin) and beta (NarHiron sulfur cluster) subunit of nitrate reductase [28 43] The(halo)archaeal nitrate reductase complex was reported to belocated at the extracellular side of the cytoplasmic membrane[128] and in most archaea associated with the cytoplasmicmembrane via NarM [129] The ldquoCa M nitroreducensrdquogenome does not encode NarM but encodes a TAT signalpeptide at the N-terminus of NarG for translocation acrossthe cytoplasmic membrane [28 43] Interestingly theNarG and NarH seem to have been acquired from theProteobacteria via lateral gene transfer [28]

It is not yet clear at which point in themetabolism ldquoCaMnitroreducensrdquo conserves energy During reverse methano-genesis N5-methyl-H

4MPTCoM methyltransferase (Mtr)

dissipates the sodium ion potential across the cytoplasmicmembrane so subsequent steps inN-AOMhave to be coupledto the build-up of a proton or sodium motive force to makethe overall process energetically favourable The analysis ofan environmental genome [43] indicated presence of severalprotein complexes involved in electron transport and energyconservation Electrons that enter the respiratory chain couldbe transported by membrane-integral electron carriers (iemenaquinones) to a Rieske-cytochrome b complex that mayuse cytochrome c as electron acceptor This in turn maybe the electron donor for the unusual nitrate reductasecomplex Energy conservation is thermodynamically andmechanistically feasible at the F

420H2dehydrogenase and the

Rieske-cytochrome b complex (Figure 5) (Figure 2 in [43])Further investigations are needed to determine whether

nitrate reductase is also involved in energy conservationbut this working hypothesis is strengthened by the presenceof cupredoxin multicopper oxidase domains and coppercenters related to the periplasmic domain of cytochrome coxidase subunit II (HCO II) in ANME-2d (Table S1)

BothANME-2d genomes discussed here are derived frombioreactors where ldquoCaM nitroreducensrdquo formed syntrophiccultures with nitrite scavenging bacteria either with ldquoCaKuenenia stuttgartiensisrdquo (anammox bacteria) [28] or ldquoCaMethylomirabilis oxyferardquo (NC10 bacteria) [31 43]This indi-cated that ANME-2d could be dependent on those bacteriafor nitrite removal However in addition to nitrite ldquoCa Mnitroreducensrdquo may also produce ammonium during AOMby a pentaheme c-type nitrite reductase (NrfAH) encodedin the genome [43] (Figure 5) In fact both ANME-2dgenomes contain domains for NrfA (IPR003321) and NrfH(IPR017571) (Table S1) implying that both ANME-2d speciesare not necessarily dependent on a nitrite scavenger duringAOM

33 Metal-Dependent AOM Evidence for metal-dependentAOM was found in marine sediments [130ndash132] In non-marine environments AOM was also hypothesized to becoupled to iron andor manganese oxide reduction [26 133ndash136] or even coupled to the reduction of humic acids [136137] However organisms responsible for metal-dependentAOM were not identified in these studies It was speculatedthat JS1 bacteria methanogenic archaea and Methanohalo-biumANME-3 could be responsible for iron-dependentAOM [138] Other researchers speculated that either ANME-1 or MethanococcoidesANME-3 together with a bacterialpartner were responsible for manganese-dependent AOM[139] In another study where AOM was decoupled from SRANME were not detected which leaves open the possibilitythat other archaeal clades besides ANME could performmetal-dependent AOM [131]

It was recently observed that cultures containing ANME-2a and ANME-2c could decouple AOM from SR in thepresence of artificial electron acceptors humic acids andsoluble iron [125] which confirmed previous findings ofAOM not connected to SR in ANME dominated samples[140] This suggests that ANME-2 could also use insolublemetal oxide minerals as electron acceptor during AOM TheMHCs of ANME-2ab and ANME-2d are larger than thosein Shewanella and Geobacter species [107] which are knownto be capable of extracellular electron conduction It wasspeculated that both ANME-2d and Ferroglobus placidus ofwhich the latter can perform solid iron reduction can foldCxxCHmotifs into extracellular conductive structures or pili[115] Many of the MHCs of ANME-2d were not expressedwhen grown with nitrate (discussed in section 32) implyingthat these are not needed for nitrate reduction [43] Thisstrengthens the hypothesis that also ANME-2d could coupleAOM to reduction of other extracellular electron acceptorsthan nitrate and even to insoluble metal oxides Indeedrecent work showed that ANME-2d could be involved inAOM coupled to chromium(VI) reduction [141] (Table 1reaction (5)) and in AOM coupled to the reduction of soluble

16 Archaea

iron and insoluble ferrihydrite and birnessite minerals [142](Table 1 reactions (3) and (4)) ANME-2d could even possiblydonate electrons to a bacterial partner besides nitrate-richenvironments ANME-2d archaea have been found inwells ofan aquifer where sulfate and methane concentrations overlap[143] Moreover ANME-2d was the only clade detected insediments of a freshwater lake where S-AOM occurred [144]Sulfate concentrations in these studies were low but above1mM and thus higher than the lowest reported concen-trations for S-AOM to occur [145 146] Lastly sequencesof ANME-2d were relatively more abundant in freshwatersediments fed with methane and sulfate than in sedimentsfed with onlymethane or only sulfate and noN-AOMactivitywas detected when fed with nitrate and methane [27] Theseindications hold promise that direct experimental evidencefor sulfate-dependent AOM by ANME-2d could be found inthe future

TheANME-1 genome contains fewerMHCgene domainsas compared to ANME-2a and ANME-2d and some otherarchaea such as somemethylotrophicmethanogens (Table 2)and some members of the Archaeoglobales [115] The MHCsof ANME-1 also have a smaller heme count as compared toother ANME and some other archaea with the largest beingan octaheme cytochrome [107] Each hemewithin aMHChasits own redox potential and therefore structurally differentMHCs represent a large range of redox potentials that canbe used for bioenergetic electron transfer (reviewed in [147])For instance metal oxide reduction in Shewanella oneidensisMR-1 is catalyzed by a chain of a tetraheme (CymA) twodecaheme (MtrA and MtrB) and eventually extracellulardecaheme cytochromes OmcAMtrC that reduce the ironminerals [121 148 149] In Geobacter sulfurreducens ironmineral reduction seems to be catalyzed by the tetrahemecytochrome OmcE and hexaheme cytochrome OmcS trans-ferring electrons from the outer membrane to type IV pilithat transmit the electrons to iron minerals [121 150 151]Since ANME-1 lack MHCs of the correct size and lack genedomains for pili production [116] they seem unable to reduceminerals via both mechanisms present in Shewanella andGeobacter It can therefore be speculated that ANME-1 areless versatile in electron acceptor use and are not able toreduce solid metal oxides However DIET mechanisms arestill not well understood and the true differences betweenMHCs of different ANME types need to be investigated usingbiochemical methods This would allow uncovering the truecapabilities concerning DIET

34 Menaquinones and Methanophenazines ANME-2a en-coded a protein with a domain specific for PhzF which is anenzyme involved in phenazine biosynthesis in Pseudomonasfluorescens [152 153] The respective gene is not present in allmethanophenazine containing methanogens (in our genomecomparison only inM acetivorans andM formicica Table 2)so it is unclear whether this enzyme is really involved inmethanophenazine biosynthesis It is however likely thatANME-2a use methanophenazines in their respiratory chainsince gene domains for menaquinone biosynthesis wereabsent (Table 2) ldquoCa M nitroreducensrdquo probably uses

menaquinones as membrane-integral electron carrier sinceenvironmental genomes [28 43] encoded the futalosine(mqn) biosynthesis pathway as reported for Archaeoglobusfulgidus [154] (Table 2) Moreover ldquoCa M nitroreducensrdquoenrichment cultures showed absence of methanophenazines[43] ANME-1 also contained gene domains formenaquinonebiosynthesis via the futalosine (mqn) biosynthesis pathway(Table 2) Indications for a quinone biosynthesis pathwayin ANME-1 were previously found to be weak since onlysome of the Ubi homologues of the oxic ubiquinone biosyn-thesis pathway were detected [41] but the futalosine (mqn)biosynthesis pathway was overlooked in that particular anal-ysis Additionally ANME-1 have Fqo homologues similarto Archaeoglobus fulgidus [44] and expressed the catalyticsubunit FqoF [41] However since the phenazine biosynthesisdomain PhzF was also present in the ANME-1 genomes(Table 2) and Fpo and Fqo are homologues we cannotconclude on genomic information alone which redox shuttleis used by ANME-1 during AOM If ANME-1 would usemenaquinones this would have implications for subsequentelectron transfer to MHCs since methanophenazine (1198640 =minus165mV) [155] and menaquinone (1198640 = minus80mV) [156] havedifferent redox potentials

35 Cell Adhesion Some gene domains involved in cel-lular adhesion were more abundant in ANME than inmethanogens (Table 2) especially in ANME-2a and ANME-1that are known to form syntrophic interactions for electrontransfer during respiration These domains include HYR(IPR003410) and CARDB domains (IPR011635) that bothhave a direct role in cellular adhesion [157] (Table 2) Interest-ingly also domains related to the cellulosome of Clostridiumspecies termed dockerin and cohesin were highly abundantin both ANME-1 and ANME-2a as compared to ANME-2dand methanogens together with many carbohydrate bindingdomains (Table 2) In Clostridium species dockerin andcohesin form an anchor to the bacterial cell wall that containsa scaffold with cellulose-degrading enzymes and a carbohy-drate bindingmodule that binds cellulose altogether formingthe cellulosome [158] These domains have been found in alldomains of life irrespective of cellulose utilization but thefunction of such proteins outside of the cellulosome is notknown [159]Therefore dockerin cohesin and carbohydratebinding domains in ANME could hypothetically form aconstruct that binds to carbohydrates and could possibly havea function in cell-to-cell contact or MHC adhesion but thisneeds further investigation

4 Future Challenges

Advances in (meta)genomics transcriptomics and pro-teomics have produced the valuable metabolic blueprints ofdifferent ANMEwith hypotheses on how centralmetabolismelectron transport and energy conservation may functionFuture experiments are needed to biochemically demonstratethat these hypotheses are correct

The bottleneck for biochemical studies of ANME isthe lack of pure cultures due to the slow and syntrophic

Archaea 17

growth However the recent milestone discovery of directelectron transfer provides opportunities to grow ANMEas stated previously on electron accepting electrodes (ieanodes) [160] In this way pure or highly enriched culturesof different ANME without their respective syntrophic part-ner could be obtained and MHCs responsible for electricconduction could be biochemically characterized It seemsthat ANME-1 are limited by the size and abundance ofMHCs which could relate to differences in behavior onan anode The partner bacteria of ANME-1 and ANME-2could be investigated on an electron donating electrode (iecathode) with specific focus on the ability to produce pili (ienanowires) Also worth investigating is if besides ANME-2d ANME-2ab could also use insoluble electron acceptorsand if ANME-2d could donate electrons to a bacterialpartner

Another future challenge is to isolate and characterizeMcr from different ANME clades It needs to be investi-gated if Mcr abundance in ANME cells compensates forthe slow reverse activity or if modifications in the Mcrof ANME-1 also contribute to a better reverse activity ofMcr Moreover the effect of methane partial pressure onreaction rates and enzyme kinetics needs to be determined insitu

ANME-1 are potentially able to perform hydrogeno-trophic methanogenesis due to the presence of a hydrogenasein the genome Genetic indications of menaquinones aselectron carrier in ANME-1 and the various cellulosome andcell adhesion related gene domains in all ANME are alsotopics that could be explored further Methanogenic archaeaare likely not able to perform AOM but additional studieson TMO and more genetic modifications to stimulate AOMin methanogens could help in understanding the param-eters needed for AOM to occur Ultimately physiologicalunderstanding of ANME will help to explain the observedecological niche separation of different ANME clades and theoccurrence of ANMEwithout a bacterial partnerThis wouldgreatly enhance our knowledge of themethane cycle in anoxicenvironments

Competing Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors thank Stefanie Berger (RU Nijmegen) for criticalreading of the manuscript This research is supported bythe Soehngen Institute of Anaerobic Microbiology (SIAM)Gravitation grant (024002002) of the Netherlands Ministryof Education Culture and Science and the NetherlandsOrganisation for Scientific Research (NWO) Mike S MJetten was further supported by ERC AG 339880 Eco-MoMand Alfons J M Stams was supported by ERC AG 323009Novel Anaerobes

References

[1] A Boetius K Ravenschlag C J Schubert et al ldquoA marinemicrobial consortium apparently mediating anaerobic oxida-tion of methanerdquo Nature vol 407 no 6804 pp 623ndash626 2000

[2] K-U Hinrichs J M Hayes S P Sylva P G Brewert andE F DeLong ldquoMethane-consuming archaebacteria in marinesedimentsrdquo Nature vol 398 no 6730 pp 802ndash805 1999

[3] V J Orphan C H House K-U Hinrichs K D McKeeganand E F DeLong ldquoMethane-consuming archaea revealed bydirectly coupled isotopic and phylogenetic analysisrdquo Sciencevol 293 no 5529 pp 484ndash487 2001

[4] K-U Hinrichs and A Boetius ldquoThe anaerobic oxidation ofmethane new insights in microbial ecology and biogeochem-istryrdquo inOceanMargin Systems GWefer D Billett D HebbelnB B Joslashrgensen M Schluter and T VanWeering Eds pp 457ndash477 Springer Berlin Germany 2002

[5] K Knittel T Losekann A Boetius R Kort and R AmannldquoDiversity and distribution of methanotrophic archaea at coldseepsrdquo Applied and Environmental Microbiology vol 71 no 1pp 467ndash479 2005

[6] K Knittel and A Boetius ldquoAnaerobic oxidation of methaneprogress with an unknown processrdquo Annual Review of Micro-biology vol 63 pp 311ndash334 2009

[7] V J Orphan K-U Hinrichs W Ussler III et al ldquoComparativeanalysis of methane-oxidizing archaea and sulfate-reducingbacteria in anoxic marine sedimentsrdquoApplied and Environmen-tal Microbiology vol 67 no 4 pp 1922ndash1934 2001

[8] T Losekann K Knittel T Nadalig et al ldquoDiversity andabundance of aerobic and anaerobic methane oxidizers atthe Haakon Mosby Mud Volcano Barents Seardquo Applied andEnvironmentalMicrobiology vol 73 no 10 pp 3348ndash3362 2007

[9] H Niemann T Losekann D De Beer et al ldquoNovel microbialcommunities of the Haakon Mosby mud volcano and their roleas amethane sinkrdquoNature vol 443 no 7113 pp 854ndash858 2006

[10] TNunouraHOida T Toki J Ashi K Takai andKHorikoshildquoQuantification of mcrA by quantitative fluorescent PCR insediments from methane seep of the Nankai Troughrdquo FEMSMicrobiology Ecology vol 57 no 1 pp 149ndash157 2006

[11] B Orcutt A Boetius M Elvert V Samarkin and S B JoyeldquoMolecular biogeochemistry of sulfate reduction methanogen-esis and the anaerobic oxidation of methane at Gulf of Mexicocold seepsrdquoGeochimica et Cosmochimica Acta vol 69 no 17 pp4267ndash4281 2005

[12] V J Orphan W Ussler III T H Naehr C H House K-U Hinrichs and C K Paull ldquoGeological geochemical andmicrobiological heterogeneity of the seafloor around methanevents in the Eel River Basin offshore Californiardquo ChemicalGeology vol 205 no 3-4 pp 265ndash289 2004

[13] M G Pachiadaki A Kallionaki A Dahlmann G J De Langeand K A Kormas ldquoDiversity and spatial distribution ofprokaryotic communities along a sediment vertical profile ofa deep-sea mud volcanordquo Microbial Ecology vol 62 no 3 pp655ndash668 2011

[14] I Roalkvam H Dahle Y Chen S L Joslashrgensen H Haflidasonand I H Steen ldquoFine-scale community structure analysis ofANME in Nyegga sediments with high and low methane fluxrdquoFrontiers in Microbiology vol 3 p 216 2012

[15] K Yanagawa M Sunamura M A Lever et al ldquoNiche separa-tion of methanotrophic archaea (ANME-1 and -2) in methane-seep sediments of the Eastern Japan Sea offshore JoetsurdquoGeomicrobiology Journal vol 28 no 2 pp 118ndash129 2011

18 Archaea

[16] A Pernthaler A E Dekas C T Brown S K Goffredi TEmbaye and V J Orphan ldquoDiverse syntrophic partnershipsfromdeep-seamethane vents revealed by direct cell capture andmetagenomicsrdquo Proceedings of the National Academy of Sciencesof the United States of America vol 105 no 19 pp 7052ndash70572008

[17] R Hatzenpichler S A Connon D Goudeau R R Malm-strom T Woyke and V J Orphan ldquoVisualizing in situtranslational activity for identifying and sorting slow-growingarchaealminusbacterial consortiardquo Proceedings of the NationalAcademy of Sciences vol 113 no 28 pp E4069ndashE4078 2016

[18] L Maignien R J Parkes B Cragg et al ldquoAnaerobic oxidationof methane in hypersaline cold seep sedimentsrdquo FEMS Micro-biology Ecology vol 83 no 1 pp 214ndash231 2013

[19] V J Orphan C H House K-U Hinrichs K D McKeeganand E F DeLong ldquoMultiple archaeal groups mediate methaneoxidation in anoxic cold seep sedimentsrdquo Proceedings of theNational Academy of Sciences of the United States of Americavol 99 no 11 pp 7663ndash7668 2002

[20] T TreudeM Kruger A Boetius and B B Joslashrgensen ldquoEnviron-mental control on anaerobic oxidation of methane in the gassysediments of Eckernforde Bay (German Baltic)rdquo Limnology andOceanography vol 50 no 6 pp 1771ndash1786 2005

[21] G C Jagersma R J W Meulepas I Heikamp-De Jong etal ldquoMicrobial diversity and community structure of a highlyactive anaerobic methane-oxidizing sulfate-reducing enrich-mentrdquo Environmental Microbiology vol 11 no 12 pp 3223ndash3232 2009

[22] M Blumenberg R Seifert J Reitner T Pape andWMichaelisldquoMembrane lipid patterns typify distinct anaerobic methan-otrophic consortiardquo Proceedings of the National Academy ofSciences of the United States of America vol 101 no 30 pp 11111ndash11116 2004

[23] S Bertram M Blumenberg W Michaelis M Siegert MKruger and R Seifert ldquoMethanogenic capabilities of ANME-archaea deduced from 13C-labelling approachesrdquo Environmen-tal Microbiology vol 15 no 8 pp 2384ndash2393 2013

[24] K G Lloyd M J Alperin and A Teske ldquoEnvironmental evi-dence for net methane production and oxidation in putativeANaerobic MEthanotrophic (ANME) archaeardquo EnvironmentalMicrobiology vol 13 no 9 pp 2548ndash2564 2011

[25] M Takeuchi H Yoshioka Y Seo et al ldquoA distinct freshwater-adapted subgroup of ANME-1 dominates active archaeal com-munities in terrestrial subsurfaces in Japanrdquo EnvironmentalMicrobiology vol 13 no 12 pp 3206ndash3218 2011

[26] R T Amos B A Bekins I M Cozzarelli et al ldquoEvidence foriron-mediated anaerobic methane oxidation in a crude oil-contaminated aquiferrdquo Geobiology vol 10 no 6 pp 506ndash5172012

[27] P H Timmers D A Suarez-Zuluaga M van Rossem MDiender A J Stams and C M Plugge ldquoAnaerobic oxidationof methane associated with sulfate reduction in a naturalfreshwater gas sourcerdquo ISME Journal vol 10 pp 1400ndash14122015

[28] M F Haroon S Hu Y Shi et al ldquoAnaerobic oxidation ofmethane coupled to nitrate reduction in a novel archaeallineagerdquo Nature vol 500 no 7468 pp 567ndash570 2013

[29] H J Mills C Hodges K Wilson I R MacDonald and PA Sobecky ldquoMicrobial diversity in sediments associated withsurface-breaching gas hydrate mounds in the Gulf of MexicordquoFEMS Microbiology Ecology vol 46 no 1 pp 39ndash52 2003

[30] K G Lloyd L Lapham and A Teske ldquoAn anaerobic methane-oxidizing community of ANME-1b archaea in hypersaline gulfofMexico sedimentsrdquoApplied and EnvironmentalMicrobiologyvol 72 no 11 pp 7218ndash7230 2006

[31] A A Raghoebarsing A Pol K T Van De Pas-Schoonen et alldquoA microbial consortium couples anaerobic methane oxidationto denitrificationrdquoNature vol 440 no 7086 pp 918ndash921 2006

[32] S Hu R J Zeng L C Burow P Lant J Keller and Z YuanldquoEnrichment of denitrifying anaerobic methane oxidizingmicroorganismsrdquo Environmental Microbiology Reports vol 1no 5 pp 377ndash384 2009

[33] Z-W Ding J Ding L Fu F Zhang and R J Zeng ldquoSimultane-ous enrichment of denitrifying methanotrophs and anammoxbacteriardquo Applied Microbiology and Biotechnology vol 98 no24 pp 10211ndash10221 2014

[34] R Seifert K Nauhaus M Blumenberg M Kruger and WMichaelis ldquoMethane dynamics in a microbial community ofthe Black Sea traced by stable carbon isotopes in vitrordquoOrganicGeochemistry vol 37 no 10 pp 1411ndash1419 2006

[35] J Ding Z-W Ding L Fu Y-Z Lu S H Cheng and R JZeng ldquoNew primers for detecting and quantifying denitrifyinganaerobic methane oxidation archaea in different ecologicalnichesrdquo Applied Microbiology and Biotechnology vol 99 no 22pp 9805ndash9812 2015

[36] A Vaksmaa C Luke T van Alen et al ldquoDistribution and activ-ity of the anaerobic methanotrophic community in a nitrogen-fertilized Italian paddy soilrdquo FEMS Microbiology Ecology vol92 no 12 2016

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[40] R Stokke I Roalkvam A Lanzen H Haflidason and I HSteen ldquoIntegrated metagenomic and metaproteomic analysesof an ANME-1-dominated community in marine cold seepsedimentsrdquo Environmental Microbiology vol 14 no 5 pp 1333ndash1346 2012

[41] A Meyerdierks M Kube I Kostadinov et al ldquoMetagenomeand mRNA expression analyses of anaerobic methanotrophicarchaea of the ANME-1 grouprdquo Environmental Microbiologyvol 12 no 2 pp 422ndash439 2010

[42] F-P Wang Y Zhang Y Chen et al ldquoMethanotrophicarchaea possessing diverging methane-oxidizing and electron-transporting pathwaysrdquo ISME Journal vol 8 no 5 pp 1069ndash1078 2014

[43] A Arshad D R Speth R M de Graaf H J Op den Camp MS Jetten and C U Welte ldquoA metagenomics-based metabolicmodel of nitrate-dependent anaerobic oxidation of methane byMethanoperedens-like archaeardquo Frontiers inMicrobiology vol 6article1423 2015

[44] S J Hallam N Putnam CM Preston et al ldquoReversemethano-genesis testing the hypothesis with environmental genomicsrdquoScience vol 305 no 5689 pp 1457ndash1462 2004

Archaea 19

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energy conservation in methanogenic archaeardquo Archives ofMicrobiology vol 165 no 3 pp 149ndash163 1996

[47] A-K Kaster J Moll K Parey and R K Thauer ldquoCoupling offerredoxin and heterodisulfide reduction via electron bifurca-tion in hydrogenotrophic methanogenic archaeardquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 108 no 7 pp 2981ndash2986 2011

[48] R K Thauer A-K Kaster H Seedorf W Buckel and RHedderich ldquoMethanogenic archaea ecologically relevant dif-ferences in energy conservationrdquo Nature Reviews Microbiologyvol 6 no 8 pp 579ndash591 2008

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[52] P V Welander and W W Metcalf ldquoLoss of the mtr operon inMethanosarcina blocks growth on methanol but not methano-genesis and reveals an unknown methanogenic pathwayrdquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 102 no 30 pp 10664ndash10669 2005

[53] P V Welander and W W Metcalf ldquoMutagenesis of the C1oxidation pathway inmethanosarcina barkeri new insights intothe MtrMer bypass pathwayrdquo Journal of Bacteriology vol 190no 6 pp 1928ndash1936 2008

[54] M Goenrich R K Thauer H Yurimoto and N KatoldquoFormaldehyde activating enzyme (Fae) and hexulose-6-phosphate synthase (Hps) inMethanosarcina barkeri a possiblefunction in ribose-5-phosphate biosynthesisrdquoArchives ofMicro-biology vol 184 no 1 pp 41ndash48 2005

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[57] K Nauhaus A Boetius M Kruger and F Widdel ldquoIn vitrodemonstration of anaerobic oxidation of methane coupled tosulphate reduction in sediment from amarine gas hydrate areardquoEnvironmental Microbiology vol 4 no 5 pp 296ndash305 2002

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[59] M Kruger T Treude H Wolters K Nauhaus and A BoetiusldquoMicrobial methane turnover in different marine habitatsrdquoPalaeogeography Palaeoclimatology Palaeoecology vol 227 no1ndash3 pp 6ndash17 2005

[60] C Deusner V Meyer and T G Ferdelman ldquoHigh-pressuresystems for gas-phase free continuous incubation of enrichedmarinemicrobial communities performing anaerobic oxidationof methanerdquo Biotechnology and Bioengineering vol 105 no 3pp 524ndash533 2010

[61] K Nauhaus T Treude A Boetius and M Kruger ldquoEnviron-mental regulation of the anaerobic oxidation of methane acomparison of ANME-I and ANME-II communitiesrdquo Environ-mental Microbiology vol 7 no 1 pp 98ndash106 2005

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2by methan-

otrophicmicrobial mats from gas seeps of the anoxic Black SeardquoApplied and EnvironmentalMicrobiology vol 73 no 7 pp 2271ndash2283 2007

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[65] R J WMeulepas C G Jagersma J Gieteling C J N BuismanA J M Stams and P N L Lens ldquoEnrichment of anaerobicmethanotrophs in sulfate-reducing membrane bioreactorsrdquoBiotechnology and Bioengineering vol 104 no 3 pp 458ndash4702009

[66] T Holler G Wegener H Niemann et al ldquoCarbon and sulfurback flux during anaerobic microbial oxidation of methane andcoupled sulfate reductionrdquo Proceedings of the National Academyof Sciences of the United States of America vol 108 no 52 ppE1484ndashE1490 2011

[67] M Kruger AMeyerdierks F O Glockner et al ldquoA conspicuousnickel protein in microbial mats that oxidize methane anaero-bicallyrdquo Nature vol 426 no 6968 pp 878ndash881 2003

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variant from archaea associated with anaerobic oxidation ofmethanerdquo Journal of the American Chemical Society vol 130 no32 pp 10758ndash10767 2008

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[70] R K Thauer and S Shima ldquoMethane as fuel for anaerobicmicroorganismsrdquo Annals of the New York Academy of Sciencesvol 1125 pp 158ndash170 2008

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[72] P H A Timmers J Gieteling H C A Widjaja-Greefkeset al ldquoGrowth of anaerobic methane-oxidizing archaea andsulfate-reducing bacteria in a high-pressure membrane capsulebioreactorrdquoApplied and EnvironmentalMicrobiology vol 81 no4 pp 1286ndash1296 2015

[73] MKruger HWoltersMGehre S B Joye andH-H RichnowldquoTracing the slow growth of anaerobic methane-oxidizingcommunities by 15N-labelling techniquesrdquo FEMS MicrobiologyEcology vol 63 no 3 pp 401ndash411 2008

[74] R J W Meulepas C G Jagersma A F Khadem C J N Buis-man A J M Stams and P N L Lens ldquoEffect of environmentalconditions on sulfate reduction withmethane as electron donorby an Eckernforde Bay enrichmentrdquo Environmental Science andTechnology vol 43 no 17 pp 6553ndash6559 2009

20 Archaea

[75] M W Bowles V A Samarkin and S B Joye ldquoImprovedmeasurement of microbial activity in deep-sea sediments atin situ pressure and methane concentrationrdquo Limnology andOceanography Methods vol 9 pp 499ndash506 2011

[76] S Shima M Krueger T Weinert et al ldquoStructure of a methyl-coenzyme M reductase from Black Sea mats that oxidizemethane anaerobicallyrdquo Nature vol 481 no 7379 pp 98ndash1012012

[77] K D Allen G Wegener and R H White ldquoDiscovery of multi-ple modified F-430 coenzymes in methanogens and anaerobicmethanotrophic archaea suggests possible new roles for F-430in naturerdquoApplied and Environmental Microbiology vol 80 no20 pp 6403ndash6412 2014

[78] V W Soo M J McAnulty A Tripathi et al ldquoReversingmethanogenesis to capture methane for liquid biofuel precur-sorsrdquoMicrobial Cell Factories vol 15 article 11 2016

[79] D L Valentine and W S Reeburgh ldquoNew perspectives onanaerobicmethane oxidationrdquoEnvironmentalMicrobiology vol2 no 5 pp 477ndash484 2000

[80] D L Valentine ldquoBiogeochemistry and microbial ecology ofmethane oxidation in anoxic environments a reviewrdquo Antonievan Leeuwenhoek International Journal of General and Molecu-lar Microbiology vol 81 no 1-4 pp 271ndash282 2002

[81] A J B Zehnder and T D Brock ldquoMethane formation andmethane oxidation by methanogenic bacteriardquo Journal of Bac-teriology vol 137 no 1 pp 420ndash432 1979

[82] J Harder ldquoAnaerobic methane oxidation by bacteria employ-ing 14C-methane uncontaminated with 14C-carbon monoxiderdquoMarine Geology vol 137 no 1-2 pp 13ndash23 1997

[83] J J Moran C H House K H Freeman and J G FerryldquoTrace methane oxidation studied in several Euryarchaeotaunder diverse conditionsrdquo Archaea vol 1 no 5 pp 303ndash3092005

[84] J J Moran C H House B Thomas and K H FreemanldquoProducts of tracemethane oxidation during nonmethyltrophicgrowth by Methanosarcinardquo Journal of Geophysical ResearchBiogeosciences vol 112 no 2 2007

[85] R J W Meulepas C G Jagersma Y Zhang et al ldquoTracemethane oxidation and the methane dependency of sulfatereduction in anaerobic granular sludgerdquo FEMS MicrobiologyEcology vol 72 no 2 pp 261ndash271 2010

[86] A J B Zehnder andTD Brock ldquoAnaerobicmethane oxidationoccurrence and ecologyrdquoApplied and Environmental Microbiol-ogy vol 39 no 1 pp 194ndash204 1980

[87] S J Blazewicz D G Petersen M P Waldrop and M K Fire-stone ldquoAnaerobic oxidation of methane in tropical and borealsoils ecological significance in terrestrial methane cyclingrdquoJournal of Geophysical Research Biogeosciences vol 117 no 2Article ID G02033 2012

[88] K A Smemo and J B Yavitt ldquoEvidence for anaerobic CH4

oxidation in freshwater peatlandsrdquo Geomicrobiology Journalvol 24 no 7-8 pp 583ndash597 2007

[89] M J Alperin and T M Hoehler ldquoAnaerobic methane oxidationby archaeasulfate-reducing bacteria aggregates 1 Thermody-namic and physical constraintsrdquo American Journal of Sciencevol 309 no 10 pp 869ndash957 2009

[90] S L Caldwell J R Laidler E A Brewer J O Eberly S CSandborgh and F S Colwell ldquoAnaerobic oxidation of methanemechanisms bioenergetics and the ecology of associatedmicroorganismsrdquo Environmental Science and Technology vol42 no 18 pp 6791ndash6799 2008

[91] GWang A J Spivack and S DrsquoHondt ldquoGibbs energies of reac-tion and microbial mutualism in anaerobic deep subseafloorsediments of ODP Site 1226rdquoGeochimica et Cosmochimica Actavol 74 no 14 pp 3938ndash3947 2010

[92] P R Girguis A E Cozen and E F DeLong ldquoGrowth andpopulation dynamics of anaerobic methane-oxidizing archaeaand sulfate-reducing bacteria in a continuous-flow bioreactorrdquoApplied and EnvironmentalMicrobiology vol 71 no 7 pp 3725ndash3733 2005

[93] K Nauhaus M Albrecht M Elvert A Boetius and F WiddelldquoIn vitro cell growth ofmarine archaeal-bacterial consortia dur-ing anaerobic oxidation ofmethanewith sulfaterdquoEnvironmentalMicrobiology vol 9 no 1 pp 187ndash196 2007

[94] B Orcutt V Samarkin A Boetius and S Joye ldquoOn the relation-ship between methane production and oxidation by anaerobicmethanotrophic communities from cold seeps of the Gulf ofMexicordquo Environmental Microbiology vol 10 no 5 pp 1108ndash1117 2008

[95] M Y Yoshinaga T Holler T Goldhammer et al ldquoCarbon iso-tope equilibration during sulphate-limited anaerobic oxidationof methanerdquo Nature Geoscience vol 7 no 3 pp 190ndash194 2014

[96] T Treude J Niggemann J Kallmeyer et al ldquoAnaerobic oxi-dation of methane and sulfate reduction along the Chileancontinental marginrdquo Geochimica et Cosmochimica Acta vol 69no 11 pp 2767ndash2779 2005

[97] R J Parkes B A Cragg N Banning et al ldquoBiogeochemistryand biodiversity of methane cycling in subsurface marinesediments (SkagerrakDenmark)rdquoEnvironmentalMicrobiologyvol 9 no 5 pp 1146ndash1161 2007

[98] N J Knab B A Cragg E R C Hornibrook et al ldquoRegulationof anaerobic methane oxidation in sediments of the Black SeardquoBiogeosciences vol 6 no 8 pp 1505ndash1518 2009

[99] H Yoshioka A Maruyama T Nakamura et al ldquoActivities anddistribution of methanogenic and methane-oxidizing microbesin marine sediments from the Cascadia Marginrdquo Geobiologyvol 8 no 3 pp 223ndash233 2010

[100] G Wegener V Krukenberg S E Ruff M Y Kellermann andK Knittel ldquoMetabolic capabilities of microorganisms involvedin and associated with the anaerobic oxidation of methanerdquoFrontiers in Microbiology vol 7 article 46 2016

[101] R J W Meulepas C G Jagersma A F Khadem A J MStams and P N L Lens ldquoEffect of methanogenic substrateson anaerobic oxidation of methane and sulfate reduction by ananaerobic methanotrophic enrichmentrdquo Applied Microbiologyand Biotechnology vol 87 no 4 pp 1499ndash1506 2010

[102] J Milucka T G Ferdelman L Polerecky et al ldquoZero-valentsulphur is a key intermediate in marine methane oxidationrdquoNature vol 491 no 7425 pp 541ndash546 2012

[103] W Michaelis R Seifert K Nauhaus et al ldquoMicrobial reefs inthe black sea fueled by anaerobic oxidation ofmethanerdquo Sciencevol 297 no 5583 pp 1013ndash1015 2002

[104] A Vigneron P Cruaud P Pignet et al ldquoArchaeal and anaerobicmethane oxidizer communities in the Sonora Margin coldseeps Guaymas Basin (Gulf of California)rdquo ISME Journal vol7 no 8 pp 1595ndash1608 2013

[105] M Alperin and T Hoehler ldquoThe ongoing mystery of sea-floormethanerdquo Science vol 329 no 5989 pp 288ndash289 2010

[106] B Orcutt and C Meile ldquoConstraints on mechanisms and ratesof anaerobic oxidation of methane by microbial consortiaprocess-basedmodeling of ANME-2 archaea and sulfate reduc-ing bacteria interactionsrdquo Biogeosciences vol 5 no 6 pp 1587ndash1599 2008

Archaea 21

[107] S E McGlynn G L Chadwick C P Kempes and V J OrphanldquoSingle cell activity reveals direct electron transfer in methan-otrophic consortiardquoNature vol 526 no 7574 pp 531ndash535 2015

[108] D R Lovley ldquoElectromicrobiologyrdquo Annual Review of Microbi-ology vol 66 pp 391ndash409 2012

[109] S M Strycharz-Glaven R M Snider A Guiseppi-Elie andL M Tender ldquoOn the electrical conductivity of microbialnanowires and biofilmsrdquoEnergy and Environmental Science vol4 no 11 pp 4366ndash4379 2011

[110] D J Richardson J N Butt J K Fredrickson et al ldquoThe lsquoporinndashcytochromersquo model for microbe-to-mineral electron transferrdquoMolecular Microbiology vol 85 no 2 pp 201ndash212 2012

[111] A Okamoto K Hashimoto and R Nakamura ldquoLong-rangeelectron conduction of Shewanella biofilms mediated by outermembrane C-type cytochromesrdquo Bioelectrochemistry vol 85pp 61ndash65 2012

[112] M Y El-Naggar G Wanger K M Leung et al ldquoElectricaltransport along bacterial nanowires from Shewanella oneidensisMR-1rdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 107 no 42 pp 18127ndash18131 2010

[113] G Reguera K D McCarthy T Mehta J S Nicoll M TTuominen and D R Lovley ldquoExtracellular electron transfer viamicrobial nanowiresrdquo Nature vol 435 no 7045 pp 1098ndash11012005

[114] Z M Summers H E Fogarty C Leang A E Franks N SMalvankar and D R Lovley ldquoDirect exchange of electronswithin aggregates of an evolved syntrophic coculture of anaer-obic bacteriardquo Science vol 330 no 6009 pp 1413ndash1415 2010

[115] A Kletzin T Heimerl J Flechsler L V Niftrik R Rachel andA Klingl ldquoCytochromes c in archaea distribution maturationcell architecture and the special case of Ignicoccus hospitalisrdquoFrontiers in Microbiology vol 6 article 439 2015

[116] GWegener V Krukenberg D Riedel H E Tegetmeyer and ABoetius ldquoIntercellular wiring enables electron transfer betweenmethanotrophic archaea and bacteriardquo Nature vol 526 no7574 pp 587ndash590 2015

[117] D HHaft S H Payne and J D Selengut ldquoArchaeosortases andexosortases are widely distributed systems linking membranetransit with posttranslational modificationrdquo Journal of Bacteri-ology vol 194 no 1 pp 36ndash48 2012

[118] A Marchler-Bauer M K Derbyshire N R Gonzales et alldquoCDD NCBIrsquos conserved domain databaserdquo Nucleic AcidsResearch vol 43 no 1 pp D222ndashD226 2015

[119] A Mitchell H-Y Chang L Daugherty et al ldquoThe InterProprotein families database the classification resource after 15yearsrdquo Nucleic Acids Research vol 43 no 1 pp D213ndashD2212015

[120] V Krukenberg K Harding M Richter et al ldquoCandidatusdesulfofervidus auxilii a hydrogenotrophic sulfate-reducingbacterium involved in the thermophilic anaerobic oxidation ofmethanerdquo Environmental Microbiology vol 18 pp 3073ndash30912016

[121] L Shi T C Squier J M Zachara and J K Fredrickson ldquoRes-piration of metal (hydr)oxides by Shewanella and Geobactera key role for multihaem c-type cytochromesrdquo MolecularMicrobiology vol 65 no 1 pp 12ndash20 2007

[122] N S Malvankar and D R Lovley ldquoMicrobial nanowires forbioenergy applicationsrdquo Current Opinion in Biotechnology vol27 pp 88ndash95 2014

[123] A-E Rotaru T LWoodard K PNevin andDR Lovley ldquoLinkbetween capacity for current production and syntrophic growth

in Geobacter speciesrdquo Frontiers in Microbiology vol 6 article744 2015

[124] A-E Rotaru P M Shrestha F Liu et al ldquoDirect interspecieselectron transfer between Geobacter metallireducens andMethanosarcina barkerirdquo Applied and Environmental Microbi-ology vol 80 no 15 pp 4599ndash4605 2014

[125] S Scheller H Yu G L Chadwick S E McGlynn and VJ Orphan ldquoArtificial electron acceptors decouple archaealmethane oxidation from sulfate reductionrdquo Science vol 351 no6274 pp 703ndash707 2016

[126] J Milucka F Widdel and S Shima ldquoImmunological detec-tion of enzymes for sulfate reduction in anaerobic methane-oxidizing consortiardquo Environmental Microbiology vol 15 no 5pp 1561ndash1571 2013

[127] P Cabello M D Roldan and C Moreno-Vivian ldquoNitratereduction and the nitrogen cycle in archaeardquoMicrobiology vol150 no 11 pp 3527ndash3546 2004

[128] R MMartinez-Espinosa E J Dridge M J Bonete et al ldquoLookon the positive sideThe orientation identification and bioener-getics of lsquoArchaealrsquomembrane-boundnitrate reductasesrdquoFEMSMicrobiology Letters vol 276 no 2 pp 129ndash139 2007

[129] S de VriesMMomcilovicM J F Strampraad J PWhiteleggeA Baghai and I Schroder ldquoAdaptation to a high-tungsten envi-ronment pyrobaculum aerophilum contains an active tungstennitrate reductaserdquo Biochemistry vol 49 no 45 pp 9911ndash99212010

[130] M Egger O Rasigraf C J Sapart et al ldquoIron-mediated anaer-obic oxidation of methane in brackish coastal sedimentsrdquoEnvironmental Science and Technology vol 49 no 1 pp 277ndash283 2015

[131] T Treude S Krause J Maltby A W Dale R Coffin and LJ Hamdan ldquoSulfate reduction and methane oxidation activitybelow the sulfate-methane transition zone in Alaskan BeaufortSea continental margin sediments implications for deep sulfurcyclingrdquo Geochimica et Cosmochimica Acta vol 144 pp 217ndash237 2014

[132] N Riedinger M J Formolo T W Lyons S Henkel A Beckand S Kasten ldquoAn inorganic geochemical argument for coupledanaerobic oxidation of methane and iron reduction in marinesedimentsrdquo Geobiology vol 12 no 2 pp 172ndash181 2014

[133] Y-H Chang T-W Cheng W-J Lai et al ldquoMicrobial methanecycling in a terrestrialmud volcano in eastern Taiwanrdquo Environ-mental Microbiology vol 14 no 4 pp 895ndash908 2012

[134] S A Crowe S Katsev K Leslie et al ldquoThe methane cycle inferruginous Lake Matanordquo Geobiology vol 9 no 1 pp 61ndash782011

[135] O Sivan M Adler A Pearson et al ldquoGeochemical evidence foriron-mediated anaerobic oxidation of methanerdquo Limnology andOceanography vol 56 no 4 pp 1536ndash1544 2011

[136] K E A Segarra C Comerford J Slaughter and S B JoyeldquoImpact of electron acceptor availability on the anaerobic oxi-dation of methane in coastal freshwater and brackish wetlandsedimentsrdquo Geochimica et Cosmochimica Acta vol 115 pp 15ndash30 2013

[137] V Gupta K A Smemo J B Yavitt D Fowle B Branfireunand N Basiliko ldquoStable isotopes reveal widespread anaerobicmethane oxidation across latitude and peatland typerdquo Environ-mental Science and Technology vol 47 no 15 pp 8273ndash82792013

[138] O Oni T Miyatake S Kasten et al ldquoDistinct microbialpopulations are tightly linked to the profile of dissolved iron in

22 Archaea

the methanic sediments of the Helgolandmud area North SeardquoFrontiers in Microbiology vol 6 2015

[139] E J Beal C H House and V J Orphan ldquoManganese- andiron-dependent marine methane oxidationrdquo Science vol 325no 5937 pp 184ndash187 2009

[140] M W Bowles V A Samarkin K M Bowles and S B JoyeldquoWeak coupling between sulfate reduction and the anaerobicoxidation of methane in methane-rich seafloor sedimentsduring ex situ incubationrdquo Geochimica et Cosmochimica Actavol 75 no 2 pp 500ndash519 2011

[141] Y Z Lu L Fu J Ding Z Ding N Li and R J Zeng ldquoCr(VI)reduction coupled with anaerobic oxidation of methane in alaboratory reactorrdquoWater Research vol 102 pp 445ndash452 2016

[142] K F Ettwig B Zhu D Speth J T Keltjens M S Jetten and BKartal ldquoArchaea catalyze iron-dependent anaerobic oxidationof methanerdquo Proceedings of the National Academy of Sciences ofthe United States of America vol 113 no 45 pp 12792ndash127962016

[143] T M Flynn R A Sanford H Ryu et al ldquoFunctional microbialdiversity explains groundwater chemistry in a pristine aquiferrdquoBMCMicrobiology vol 13 no 1 article no 146 2013

[144] C J Schubert F Vazquez T Losekann-Behrens K KnittelM Tonolla and A Boetius ldquoEvidence for anaerobic oxidationof methane in sediments of a freshwater system (Lago diCadagno)rdquo FEMS Microbiology Ecology vol 76 no 1 pp 26ndash38 2011

[145] K E A Segarra F Schubotz V Samarkin M Y Yoshinaga K-U Hinrichs and S B Joye ldquoHigh rates of anaerobic methaneoxidation in freshwater wetlands reduce potential atmosphericmethane emissionsrdquo Nature Communications vol 6 article7477 2015

[146] E J Beal M W Claire and C H House ldquoHigh rates ofanaerobic methanotrophy at low sulfate concentrations withimplications for past and present methane levelsrdquo Geobiologyvol 9 no 2 pp 131ndash139 2011

[147] F Kracke I Vassilev and J O Kromer ldquoMicrobial electrontransport and energy conservationmdashthe foundation for opti-mizing bioelectrochemical systemsrdquo Frontiers in Microbiologyvol 6 article 575 2015

[148] C L Reardon A C Dohnalkova P Nachimuthu et al ldquoRoleof outer-membrane cytochromes MtrC and OmcA in thebiomineralization of ferrihydrite by Shewanella oneidensisMR-1rdquo Geobiology vol 8 no 1 pp 56ndash68 2010

[149] L Shi B Chen Z Wang et al ldquoIsolation of a high-affinityfunctional protein complex between OmcA and MtrC twoouter membrane decaheme c-type cytochromes of Shewanellaoneidensis MR-1rdquo Journal of Bacteriology vol 188 no 13 pp4705ndash4714 2006

[150] X Qian T Mester L Morgado et al ldquoBiochemical charac-terization of purified OmcS a c-type cytochrome requiredfor insoluble Fe(III) reduction in Geobacter sulfurreducensrdquoBiochimica et BiophysicaActamdashBioenergetics vol 1807 no 4 pp404ndash412 2011

[151] T Mehta M V Coppi S E Childers and D R Lovley ldquoOutermembrane c-type cytochromes required for Fe(III) andMn(IV)oxide reduction in Geobacter sulfurreducensrdquo Applied andEnvironmentalMicrobiology vol 71 no 12 pp 8634ndash8641 2005

[152] W Blankenfeldt A P Kuzin T Skarina et al ldquoStructure andfunction of the phenazine biosynthetic protein PhzF fromPseudomonas fluorescensrdquoProceedings of theNational Academyof Sciences of the United States of America vol 101 no 47 pp16431ndash16436 2004

[153] J F Parsons F Song L Parsons K Calabrese E Eisensteinand J E Ladner ldquoStructure and function of the phenazinebiosynthesis protein PhzF fromPseudomonas fluorescens 2-79rdquoBiochemistry vol 43 no 39 pp 12427ndash12435 2004

[154] T Hiratsuka K Furihata J Ishikawa et al ldquoAn alternativemenaquinone biosynthetic pathway operating in microorgan-ismsrdquo Science vol 321 no 5896 pp 1670ndash1673 2008

[155] M Tietze A Beuchle I Lamla et al ldquoRedox potentials ofmethanophenazine and CoB-S-S-CoM factors involved inelectron transport in methanogenic archaeardquo ChemBioChemvol 4 no 4 pp 333ndash335 2003

[156] Q H Tran and G Unden ldquoChanges in the proton potentialand the cellular energetics of Escherichia coli during growth byaerobic and anaerobic respiration or by fermentationrdquoEuropeanJournal of Biochemistry vol 251 no 1-2 pp 538ndash543 1998

[157] I Callebaut D Gilges I Vigon and J-P Mornon ldquoHYR anextracellular module involved in cellular adhesion and relatedto the immunoglobulin-like foldrdquo Protein Science vol 9 no 7pp 1382ndash1390 2000

[158] H J Gilbert ldquoCellulosomes microbial nanomachines that dis-play plasticity in quaternary structurerdquoMolecular Microbiologyvol 63 no 6 pp 1568ndash1576 2007

[159] A Peer S P Smith E A Bayer R Lamed and I BorovokldquoNoncellulosomal cohesin- and dockerin-like modules in thethree domains of liferdquo FEMS Microbiology Letters vol 291 no1 pp 1ndash16 2009

[160] M Wagner ldquoMicrobiology conductive consortiardquo Nature vol526 no 7574 pp 513ndash514 2015

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

14 Archaea

form a complex that generates a proton motive force duringhydrogen oxidation Therefore hydrogenotrophic methano-genesis by ANME-1 cannot be excluded yet

3 Respiration during AnaerobicOxidation of Methane

For netAOMtooccur an external electron acceptor is neededwhich results in a favourable Gibbs free energy change(Table 1) A variety of terminal electron acceptors have beendiscovered for AOM which will be discussed in Sections 31ndash33

31 Sulfate-Dependent AOM During sulfate-dependentAOM electrons are transferred from ANME to the sulfate-reducing bacterial partner Previous work tried to uncoverhow electrons were transferred and most compoundsthat could act as interspecies electron carrier (IEC) wereexcluded to be involved in AOM such as methanolhydrogen methanethiol acetate and carbon monoxide[57 61 62 94 101] Indications that polysulfide could actas IEC were found and ANME-2a archaea were thoughtto perform both AOM and sulfate reduction (SR) [102]However in marine seeps hydrothermal vents and othernondiffusion based sediments AOM rates are high andANME form close associations with SRB in dense aggregates[1 5 103 104] In these aggregates the high AOM ratescould not be explained by diffusion of an IEC whichmade direct interspecies electron transfer (DIET) a moreplausible mechanism [89 105 106] Cellular activities wereindependent of aggregate type and distance between thesyntrophic partners within the aggregate which is bestexplained by DIET [107] DIET is normally achieved usingmultiheme cytochrome c proteins (MHCs) and conductivepili (ie nanowires) which are mainly found in bacteriathat donate electrons extracellularly such as Geobacter andShewanella species [108ndash114] Indeed ANME-2a from seep-sediment samples seem to transfer electrons directly usinglarge MHCs [107] which were found in the metagenome ofANME-2a [107 115] ANME-1 and the associated bacterialpartner also overexpressed genes for extracellular MHCsduring AOM [116] which complements previous findings oftranscription [41] and translation [40] of ANME-1 relatedMHC genes Domain based (meta)genome analysis showsthe high abundance of MHC domains in different ANMEas compared to methanogens (Table 2) A recently isolatedbacterial partner of ANME-1 (ldquoHotSeep-1rdquo) also producedcell-to-cell connections using pili-derived nanowires [116]which explain previously detected Deltaproteobacteria-related pili genes in an AOM sample dominated by ANME-1[40]

How ANME use MHCs to donate electrons to thebacterial partner is not yet clear For ANME-2a the electronsprobably flow from methanophenazine to membrane inte-grated di-heme cytochromes (cytochrome 119887119887

6) that transfer

the electrons through the S-layer via MHCS-layer fusionproteins to extracellular MHCs (Figure 4) (Figure 4 in[107]) Exosortases and archaea-specific archaeosortases are

involved in export of cell surface proteins such as the archaealS-layer proteins These transpeptidases recognize specificsignal peptides for protein- sorting that is archaeosor-tase A recognizes the protein-sorting signal PGF-CTERMand archaeosortase C recognizes the PEF-CTERM signal[117] Both ANME-2a and 2d show presence of di-hemecytochromes archaeosortase A (IPR014522) archaeosortaseC (IPR022504) and other exosortase gene domains (Table 2)Moreover some genes of both ANME-2a and 2d containedboth MHC and PGF or PEF-CTERM domains Lastly somegenes of both ANME-2a and 2d contained both MHC andS-layer domains [107] indicating that these could form theabove-stated MHCS-layer fusion proteins

ANME-1 do not seem to have di-heme cytochromes(Table 2) [115] PGF related domains (IPR026453 andIPR026371) were present in all ANME but PEF-CTERM(IPR017474) related domains were absent in ANME-1 (Table 2) Moreover ANME-1 lacked archaeosortaseA (IPR014522) and archaeosortase C gene domains(IPR022504) as well as some other exosortases (Table 2) Asearch in NCBIrsquos conserved domains database (CCD [118])and the EMBL InterPro database [119] of amino acidssequences of all genes from ANME metagenomes thatcontain MHC domains showed that ANME-1 did not haveany protein-sorting signal or S-layer domains within thesegenes In fact S-layer domains were completely absent inANME-1 (Table 2) These results imply that ANME-1 do notuse di-heme cytochromes for electron transfer to MHCsand do not produce an S-layer (Figure 6) This implies thatANME-1 use a different mechanism for DIET and couldexplain the need for less MHCs by ANME-1 (Table 2)and the observed pili-derived nanowires produced by thebacterial partner [116] The genome of the bacterial partnerof ANME-1 (ldquoHotSeep-1rdquo) encoded 24 c-type cytochromesof which 10 were similar to secreted MHCs of Geobactersulfurreducens [120] which also uses pili for DIET [121]

In the case of ANME-2a it is not clear if pili (ienanowires) were formed during AOM It was previouslythought that electrically conductive pili seemed to be aprerequisite for current production andDIET [122 123] evenwhen syntrophs were closely associated [124] such as withinANME-2SRB aggregates However conductive materialssuch as granular activated carbon were shown to be ableto substitute pili in DIET [124] Although in previous workconductive materials such as phenazines or humic acids didnot seem to stimulate AOM rates [61] in a recent study AOMwas decoupled from SR using artificial electron acceptors[125] This indicates that conductive materials can indeedreplace pili and that ANME-2ab could possibly couple AOMto metal oxide reduction or any other suitable electronacceptor (discussed in Section 33) However it needs to beproven if in ANME-2SRB aggregates no pili are formed andif the mechanism of DIET is fundamentally different fromANME-1

As for the polysulfide shuttling theory [102] canonicalgenes for dissimilatory sulfate reduction such as adenylyl-transferase (Sat) APS reductase (Apr) and dissimilatorysulfite reductase (Dsr) which are all present in the sulfate-reducing archeon A fulgidus (Table S2) were not found in

Archaea 15

metagenomes of ANME-1 [41] and ANME-2a (Table S1)The enzymes Sat and Dsr were also not detected in ANMEcells using fluorescent immunolabelling [126] ANME-1 werepreviously found to encode most proteins for assimilatorysulfate reduction [41] ANME-2d only harbor gene domainsthat encode Sat and assimilatoryATP sulfurylase APS kinaseand sodiumsulfate symporters which were not present inANME-2a (Table S1) It is therefore clear that at least ANME-2a cannot donate electrons to sulfate but need to donateelectrons to a sulfate-reducing partner

32 Nitrate-Dependent AOM Unlike during S-AOMANME-2d that perform N-AOM do not need a bacterialpartner but transfer electrons directly to a membrane boundnitrate reductase (Nar) [28 43] (Figure 5) The ANME-2dgenomes contain most MHCs found so far in archaea[107 115] (Table 2) Of the 87 proteins that contained aCxxCH binding motif of which 43 seemed to be true c-typecytochromes [115] 23 CxxCH motif-encoding transcriptswere expressed during N-AOM [43] The function of mostof these MHCs is not known but they are likely involvedin nitrate reduction since c-type cytochromes are capableof operating in the wide range of redox potentials thatcouple nitrate reduction (11986401015840 (NO

3

minusNO2

minus) = +433mV) andmethane oxidation (11986401015840 (CoM-S-S-CoBCoM-SH+CoB-SH)= minus143mV) [43] Nitrate as terminal electron acceptor inanaerobic respiration has been found in halophilic andthermophilic archaea [127] The nar gene cluster of ldquoCaM nitroreducensrdquo comprises several genes including thecatalytic alpha (NarG molybdopterin) and beta (NarHiron sulfur cluster) subunit of nitrate reductase [28 43] The(halo)archaeal nitrate reductase complex was reported to belocated at the extracellular side of the cytoplasmic membrane[128] and in most archaea associated with the cytoplasmicmembrane via NarM [129] The ldquoCa M nitroreducensrdquogenome does not encode NarM but encodes a TAT signalpeptide at the N-terminus of NarG for translocation acrossthe cytoplasmic membrane [28 43] Interestingly theNarG and NarH seem to have been acquired from theProteobacteria via lateral gene transfer [28]

It is not yet clear at which point in themetabolism ldquoCaMnitroreducensrdquo conserves energy During reverse methano-genesis N5-methyl-H

4MPTCoM methyltransferase (Mtr)

dissipates the sodium ion potential across the cytoplasmicmembrane so subsequent steps inN-AOMhave to be coupledto the build-up of a proton or sodium motive force to makethe overall process energetically favourable The analysis ofan environmental genome [43] indicated presence of severalprotein complexes involved in electron transport and energyconservation Electrons that enter the respiratory chain couldbe transported by membrane-integral electron carriers (iemenaquinones) to a Rieske-cytochrome b complex that mayuse cytochrome c as electron acceptor This in turn maybe the electron donor for the unusual nitrate reductasecomplex Energy conservation is thermodynamically andmechanistically feasible at the F

420H2dehydrogenase and the

Rieske-cytochrome b complex (Figure 5) (Figure 2 in [43])Further investigations are needed to determine whether

nitrate reductase is also involved in energy conservationbut this working hypothesis is strengthened by the presenceof cupredoxin multicopper oxidase domains and coppercenters related to the periplasmic domain of cytochrome coxidase subunit II (HCO II) in ANME-2d (Table S1)

BothANME-2d genomes discussed here are derived frombioreactors where ldquoCaM nitroreducensrdquo formed syntrophiccultures with nitrite scavenging bacteria either with ldquoCaKuenenia stuttgartiensisrdquo (anammox bacteria) [28] or ldquoCaMethylomirabilis oxyferardquo (NC10 bacteria) [31 43]This indi-cated that ANME-2d could be dependent on those bacteriafor nitrite removal However in addition to nitrite ldquoCa Mnitroreducensrdquo may also produce ammonium during AOMby a pentaheme c-type nitrite reductase (NrfAH) encodedin the genome [43] (Figure 5) In fact both ANME-2dgenomes contain domains for NrfA (IPR003321) and NrfH(IPR017571) (Table S1) implying that both ANME-2d speciesare not necessarily dependent on a nitrite scavenger duringAOM

33 Metal-Dependent AOM Evidence for metal-dependentAOM was found in marine sediments [130ndash132] In non-marine environments AOM was also hypothesized to becoupled to iron andor manganese oxide reduction [26 133ndash136] or even coupled to the reduction of humic acids [136137] However organisms responsible for metal-dependentAOM were not identified in these studies It was speculatedthat JS1 bacteria methanogenic archaea and Methanohalo-biumANME-3 could be responsible for iron-dependentAOM [138] Other researchers speculated that either ANME-1 or MethanococcoidesANME-3 together with a bacterialpartner were responsible for manganese-dependent AOM[139] In another study where AOM was decoupled from SRANME were not detected which leaves open the possibilitythat other archaeal clades besides ANME could performmetal-dependent AOM [131]

It was recently observed that cultures containing ANME-2a and ANME-2c could decouple AOM from SR in thepresence of artificial electron acceptors humic acids andsoluble iron [125] which confirmed previous findings ofAOM not connected to SR in ANME dominated samples[140] This suggests that ANME-2 could also use insolublemetal oxide minerals as electron acceptor during AOM TheMHCs of ANME-2ab and ANME-2d are larger than thosein Shewanella and Geobacter species [107] which are knownto be capable of extracellular electron conduction It wasspeculated that both ANME-2d and Ferroglobus placidus ofwhich the latter can perform solid iron reduction can foldCxxCHmotifs into extracellular conductive structures or pili[115] Many of the MHCs of ANME-2d were not expressedwhen grown with nitrate (discussed in section 32) implyingthat these are not needed for nitrate reduction [43] Thisstrengthens the hypothesis that also ANME-2d could coupleAOM to reduction of other extracellular electron acceptorsthan nitrate and even to insoluble metal oxides Indeedrecent work showed that ANME-2d could be involved inAOM coupled to chromium(VI) reduction [141] (Table 1reaction (5)) and in AOM coupled to the reduction of soluble

16 Archaea

iron and insoluble ferrihydrite and birnessite minerals [142](Table 1 reactions (3) and (4)) ANME-2d could even possiblydonate electrons to a bacterial partner besides nitrate-richenvironments ANME-2d archaea have been found inwells ofan aquifer where sulfate and methane concentrations overlap[143] Moreover ANME-2d was the only clade detected insediments of a freshwater lake where S-AOM occurred [144]Sulfate concentrations in these studies were low but above1mM and thus higher than the lowest reported concen-trations for S-AOM to occur [145 146] Lastly sequencesof ANME-2d were relatively more abundant in freshwatersediments fed with methane and sulfate than in sedimentsfed with onlymethane or only sulfate and noN-AOMactivitywas detected when fed with nitrate and methane [27] Theseindications hold promise that direct experimental evidencefor sulfate-dependent AOM by ANME-2d could be found inthe future

TheANME-1 genome contains fewerMHCgene domainsas compared to ANME-2a and ANME-2d and some otherarchaea such as somemethylotrophicmethanogens (Table 2)and some members of the Archaeoglobales [115] The MHCsof ANME-1 also have a smaller heme count as compared toother ANME and some other archaea with the largest beingan octaheme cytochrome [107] Each hemewithin aMHChasits own redox potential and therefore structurally differentMHCs represent a large range of redox potentials that canbe used for bioenergetic electron transfer (reviewed in [147])For instance metal oxide reduction in Shewanella oneidensisMR-1 is catalyzed by a chain of a tetraheme (CymA) twodecaheme (MtrA and MtrB) and eventually extracellulardecaheme cytochromes OmcAMtrC that reduce the ironminerals [121 148 149] In Geobacter sulfurreducens ironmineral reduction seems to be catalyzed by the tetrahemecytochrome OmcE and hexaheme cytochrome OmcS trans-ferring electrons from the outer membrane to type IV pilithat transmit the electrons to iron minerals [121 150 151]Since ANME-1 lack MHCs of the correct size and lack genedomains for pili production [116] they seem unable to reduceminerals via both mechanisms present in Shewanella andGeobacter It can therefore be speculated that ANME-1 areless versatile in electron acceptor use and are not able toreduce solid metal oxides However DIET mechanisms arestill not well understood and the true differences betweenMHCs of different ANME types need to be investigated usingbiochemical methods This would allow uncovering the truecapabilities concerning DIET

34 Menaquinones and Methanophenazines ANME-2a en-coded a protein with a domain specific for PhzF which is anenzyme involved in phenazine biosynthesis in Pseudomonasfluorescens [152 153] The respective gene is not present in allmethanophenazine containing methanogens (in our genomecomparison only inM acetivorans andM formicica Table 2)so it is unclear whether this enzyme is really involved inmethanophenazine biosynthesis It is however likely thatANME-2a use methanophenazines in their respiratory chainsince gene domains for menaquinone biosynthesis wereabsent (Table 2) ldquoCa M nitroreducensrdquo probably uses

menaquinones as membrane-integral electron carrier sinceenvironmental genomes [28 43] encoded the futalosine(mqn) biosynthesis pathway as reported for Archaeoglobusfulgidus [154] (Table 2) Moreover ldquoCa M nitroreducensrdquoenrichment cultures showed absence of methanophenazines[43] ANME-1 also contained gene domains formenaquinonebiosynthesis via the futalosine (mqn) biosynthesis pathway(Table 2) Indications for a quinone biosynthesis pathwayin ANME-1 were previously found to be weak since onlysome of the Ubi homologues of the oxic ubiquinone biosyn-thesis pathway were detected [41] but the futalosine (mqn)biosynthesis pathway was overlooked in that particular anal-ysis Additionally ANME-1 have Fqo homologues similarto Archaeoglobus fulgidus [44] and expressed the catalyticsubunit FqoF [41] However since the phenazine biosynthesisdomain PhzF was also present in the ANME-1 genomes(Table 2) and Fpo and Fqo are homologues we cannotconclude on genomic information alone which redox shuttleis used by ANME-1 during AOM If ANME-1 would usemenaquinones this would have implications for subsequentelectron transfer to MHCs since methanophenazine (1198640 =minus165mV) [155] and menaquinone (1198640 = minus80mV) [156] havedifferent redox potentials

35 Cell Adhesion Some gene domains involved in cel-lular adhesion were more abundant in ANME than inmethanogens (Table 2) especially in ANME-2a and ANME-1that are known to form syntrophic interactions for electrontransfer during respiration These domains include HYR(IPR003410) and CARDB domains (IPR011635) that bothhave a direct role in cellular adhesion [157] (Table 2) Interest-ingly also domains related to the cellulosome of Clostridiumspecies termed dockerin and cohesin were highly abundantin both ANME-1 and ANME-2a as compared to ANME-2dand methanogens together with many carbohydrate bindingdomains (Table 2) In Clostridium species dockerin andcohesin form an anchor to the bacterial cell wall that containsa scaffold with cellulose-degrading enzymes and a carbohy-drate bindingmodule that binds cellulose altogether formingthe cellulosome [158] These domains have been found in alldomains of life irrespective of cellulose utilization but thefunction of such proteins outside of the cellulosome is notknown [159]Therefore dockerin cohesin and carbohydratebinding domains in ANME could hypothetically form aconstruct that binds to carbohydrates and could possibly havea function in cell-to-cell contact or MHC adhesion but thisneeds further investigation

4 Future Challenges

Advances in (meta)genomics transcriptomics and pro-teomics have produced the valuable metabolic blueprints ofdifferent ANMEwith hypotheses on how centralmetabolismelectron transport and energy conservation may functionFuture experiments are needed to biochemically demonstratethat these hypotheses are correct

The bottleneck for biochemical studies of ANME isthe lack of pure cultures due to the slow and syntrophic

Archaea 17

growth However the recent milestone discovery of directelectron transfer provides opportunities to grow ANMEas stated previously on electron accepting electrodes (ieanodes) [160] In this way pure or highly enriched culturesof different ANME without their respective syntrophic part-ner could be obtained and MHCs responsible for electricconduction could be biochemically characterized It seemsthat ANME-1 are limited by the size and abundance ofMHCs which could relate to differences in behavior onan anode The partner bacteria of ANME-1 and ANME-2could be investigated on an electron donating electrode (iecathode) with specific focus on the ability to produce pili (ienanowires) Also worth investigating is if besides ANME-2d ANME-2ab could also use insoluble electron acceptorsand if ANME-2d could donate electrons to a bacterialpartner

Another future challenge is to isolate and characterizeMcr from different ANME clades It needs to be investi-gated if Mcr abundance in ANME cells compensates forthe slow reverse activity or if modifications in the Mcrof ANME-1 also contribute to a better reverse activity ofMcr Moreover the effect of methane partial pressure onreaction rates and enzyme kinetics needs to be determined insitu

ANME-1 are potentially able to perform hydrogeno-trophic methanogenesis due to the presence of a hydrogenasein the genome Genetic indications of menaquinones aselectron carrier in ANME-1 and the various cellulosome andcell adhesion related gene domains in all ANME are alsotopics that could be explored further Methanogenic archaeaare likely not able to perform AOM but additional studieson TMO and more genetic modifications to stimulate AOMin methanogens could help in understanding the param-eters needed for AOM to occur Ultimately physiologicalunderstanding of ANME will help to explain the observedecological niche separation of different ANME clades and theoccurrence of ANMEwithout a bacterial partnerThis wouldgreatly enhance our knowledge of themethane cycle in anoxicenvironments

Competing Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors thank Stefanie Berger (RU Nijmegen) for criticalreading of the manuscript This research is supported bythe Soehngen Institute of Anaerobic Microbiology (SIAM)Gravitation grant (024002002) of the Netherlands Ministryof Education Culture and Science and the NetherlandsOrganisation for Scientific Research (NWO) Mike S MJetten was further supported by ERC AG 339880 Eco-MoMand Alfons J M Stams was supported by ERC AG 323009Novel Anaerobes

References

[1] A Boetius K Ravenschlag C J Schubert et al ldquoA marinemicrobial consortium apparently mediating anaerobic oxida-tion of methanerdquo Nature vol 407 no 6804 pp 623ndash626 2000

[2] K-U Hinrichs J M Hayes S P Sylva P G Brewert andE F DeLong ldquoMethane-consuming archaebacteria in marinesedimentsrdquo Nature vol 398 no 6730 pp 802ndash805 1999

[3] V J Orphan C H House K-U Hinrichs K D McKeeganand E F DeLong ldquoMethane-consuming archaea revealed bydirectly coupled isotopic and phylogenetic analysisrdquo Sciencevol 293 no 5529 pp 484ndash487 2001

[4] K-U Hinrichs and A Boetius ldquoThe anaerobic oxidation ofmethane new insights in microbial ecology and biogeochem-istryrdquo inOceanMargin Systems GWefer D Billett D HebbelnB B Joslashrgensen M Schluter and T VanWeering Eds pp 457ndash477 Springer Berlin Germany 2002

[5] K Knittel T Losekann A Boetius R Kort and R AmannldquoDiversity and distribution of methanotrophic archaea at coldseepsrdquo Applied and Environmental Microbiology vol 71 no 1pp 467ndash479 2005

[6] K Knittel and A Boetius ldquoAnaerobic oxidation of methaneprogress with an unknown processrdquo Annual Review of Micro-biology vol 63 pp 311ndash334 2009

[7] V J Orphan K-U Hinrichs W Ussler III et al ldquoComparativeanalysis of methane-oxidizing archaea and sulfate-reducingbacteria in anoxic marine sedimentsrdquoApplied and Environmen-tal Microbiology vol 67 no 4 pp 1922ndash1934 2001

[8] T Losekann K Knittel T Nadalig et al ldquoDiversity andabundance of aerobic and anaerobic methane oxidizers atthe Haakon Mosby Mud Volcano Barents Seardquo Applied andEnvironmentalMicrobiology vol 73 no 10 pp 3348ndash3362 2007

[9] H Niemann T Losekann D De Beer et al ldquoNovel microbialcommunities of the Haakon Mosby mud volcano and their roleas amethane sinkrdquoNature vol 443 no 7113 pp 854ndash858 2006

[10] TNunouraHOida T Toki J Ashi K Takai andKHorikoshildquoQuantification of mcrA by quantitative fluorescent PCR insediments from methane seep of the Nankai Troughrdquo FEMSMicrobiology Ecology vol 57 no 1 pp 149ndash157 2006

[11] B Orcutt A Boetius M Elvert V Samarkin and S B JoyeldquoMolecular biogeochemistry of sulfate reduction methanogen-esis and the anaerobic oxidation of methane at Gulf of Mexicocold seepsrdquoGeochimica et Cosmochimica Acta vol 69 no 17 pp4267ndash4281 2005

[12] V J Orphan W Ussler III T H Naehr C H House K-U Hinrichs and C K Paull ldquoGeological geochemical andmicrobiological heterogeneity of the seafloor around methanevents in the Eel River Basin offshore Californiardquo ChemicalGeology vol 205 no 3-4 pp 265ndash289 2004

[13] M G Pachiadaki A Kallionaki A Dahlmann G J De Langeand K A Kormas ldquoDiversity and spatial distribution ofprokaryotic communities along a sediment vertical profile ofa deep-sea mud volcanordquo Microbial Ecology vol 62 no 3 pp655ndash668 2011

[14] I Roalkvam H Dahle Y Chen S L Joslashrgensen H Haflidasonand I H Steen ldquoFine-scale community structure analysis ofANME in Nyegga sediments with high and low methane fluxrdquoFrontiers in Microbiology vol 3 p 216 2012

[15] K Yanagawa M Sunamura M A Lever et al ldquoNiche separa-tion of methanotrophic archaea (ANME-1 and -2) in methane-seep sediments of the Eastern Japan Sea offshore JoetsurdquoGeomicrobiology Journal vol 28 no 2 pp 118ndash129 2011

18 Archaea

[16] A Pernthaler A E Dekas C T Brown S K Goffredi TEmbaye and V J Orphan ldquoDiverse syntrophic partnershipsfromdeep-seamethane vents revealed by direct cell capture andmetagenomicsrdquo Proceedings of the National Academy of Sciencesof the United States of America vol 105 no 19 pp 7052ndash70572008

[17] R Hatzenpichler S A Connon D Goudeau R R Malm-strom T Woyke and V J Orphan ldquoVisualizing in situtranslational activity for identifying and sorting slow-growingarchaealminusbacterial consortiardquo Proceedings of the NationalAcademy of Sciences vol 113 no 28 pp E4069ndashE4078 2016

[18] L Maignien R J Parkes B Cragg et al ldquoAnaerobic oxidationof methane in hypersaline cold seep sedimentsrdquo FEMS Micro-biology Ecology vol 83 no 1 pp 214ndash231 2013

[19] V J Orphan C H House K-U Hinrichs K D McKeeganand E F DeLong ldquoMultiple archaeal groups mediate methaneoxidation in anoxic cold seep sedimentsrdquo Proceedings of theNational Academy of Sciences of the United States of Americavol 99 no 11 pp 7663ndash7668 2002

[20] T TreudeM Kruger A Boetius and B B Joslashrgensen ldquoEnviron-mental control on anaerobic oxidation of methane in the gassysediments of Eckernforde Bay (German Baltic)rdquo Limnology andOceanography vol 50 no 6 pp 1771ndash1786 2005

[21] G C Jagersma R J W Meulepas I Heikamp-De Jong etal ldquoMicrobial diversity and community structure of a highlyactive anaerobic methane-oxidizing sulfate-reducing enrich-mentrdquo Environmental Microbiology vol 11 no 12 pp 3223ndash3232 2009

[22] M Blumenberg R Seifert J Reitner T Pape andWMichaelisldquoMembrane lipid patterns typify distinct anaerobic methan-otrophic consortiardquo Proceedings of the National Academy ofSciences of the United States of America vol 101 no 30 pp 11111ndash11116 2004

[23] S Bertram M Blumenberg W Michaelis M Siegert MKruger and R Seifert ldquoMethanogenic capabilities of ANME-archaea deduced from 13C-labelling approachesrdquo Environmen-tal Microbiology vol 15 no 8 pp 2384ndash2393 2013

[24] K G Lloyd M J Alperin and A Teske ldquoEnvironmental evi-dence for net methane production and oxidation in putativeANaerobic MEthanotrophic (ANME) archaeardquo EnvironmentalMicrobiology vol 13 no 9 pp 2548ndash2564 2011

[25] M Takeuchi H Yoshioka Y Seo et al ldquoA distinct freshwater-adapted subgroup of ANME-1 dominates active archaeal com-munities in terrestrial subsurfaces in Japanrdquo EnvironmentalMicrobiology vol 13 no 12 pp 3206ndash3218 2011

[26] R T Amos B A Bekins I M Cozzarelli et al ldquoEvidence foriron-mediated anaerobic methane oxidation in a crude oil-contaminated aquiferrdquo Geobiology vol 10 no 6 pp 506ndash5172012

[27] P H Timmers D A Suarez-Zuluaga M van Rossem MDiender A J Stams and C M Plugge ldquoAnaerobic oxidationof methane associated with sulfate reduction in a naturalfreshwater gas sourcerdquo ISME Journal vol 10 pp 1400ndash14122015

[28] M F Haroon S Hu Y Shi et al ldquoAnaerobic oxidation ofmethane coupled to nitrate reduction in a novel archaeallineagerdquo Nature vol 500 no 7468 pp 567ndash570 2013

[29] H J Mills C Hodges K Wilson I R MacDonald and PA Sobecky ldquoMicrobial diversity in sediments associated withsurface-breaching gas hydrate mounds in the Gulf of MexicordquoFEMS Microbiology Ecology vol 46 no 1 pp 39ndash52 2003

[30] K G Lloyd L Lapham and A Teske ldquoAn anaerobic methane-oxidizing community of ANME-1b archaea in hypersaline gulfofMexico sedimentsrdquoApplied and EnvironmentalMicrobiologyvol 72 no 11 pp 7218ndash7230 2006

[31] A A Raghoebarsing A Pol K T Van De Pas-Schoonen et alldquoA microbial consortium couples anaerobic methane oxidationto denitrificationrdquoNature vol 440 no 7086 pp 918ndash921 2006

[32] S Hu R J Zeng L C Burow P Lant J Keller and Z YuanldquoEnrichment of denitrifying anaerobic methane oxidizingmicroorganismsrdquo Environmental Microbiology Reports vol 1no 5 pp 377ndash384 2009

[33] Z-W Ding J Ding L Fu F Zhang and R J Zeng ldquoSimultane-ous enrichment of denitrifying methanotrophs and anammoxbacteriardquo Applied Microbiology and Biotechnology vol 98 no24 pp 10211ndash10221 2014

[34] R Seifert K Nauhaus M Blumenberg M Kruger and WMichaelis ldquoMethane dynamics in a microbial community ofthe Black Sea traced by stable carbon isotopes in vitrordquoOrganicGeochemistry vol 37 no 10 pp 1411ndash1419 2006

[35] J Ding Z-W Ding L Fu Y-Z Lu S H Cheng and R JZeng ldquoNew primers for detecting and quantifying denitrifyinganaerobic methane oxidation archaea in different ecologicalnichesrdquo Applied Microbiology and Biotechnology vol 99 no 22pp 9805ndash9812 2015

[36] A Vaksmaa C Luke T van Alen et al ldquoDistribution and activ-ity of the anaerobic methanotrophic community in a nitrogen-fertilized Italian paddy soilrdquo FEMS Microbiology Ecology vol92 no 12 2016

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[40] R Stokke I Roalkvam A Lanzen H Haflidason and I HSteen ldquoIntegrated metagenomic and metaproteomic analysesof an ANME-1-dominated community in marine cold seepsedimentsrdquo Environmental Microbiology vol 14 no 5 pp 1333ndash1346 2012

[41] A Meyerdierks M Kube I Kostadinov et al ldquoMetagenomeand mRNA expression analyses of anaerobic methanotrophicarchaea of the ANME-1 grouprdquo Environmental Microbiologyvol 12 no 2 pp 422ndash439 2010

[42] F-P Wang Y Zhang Y Chen et al ldquoMethanotrophicarchaea possessing diverging methane-oxidizing and electron-transporting pathwaysrdquo ISME Journal vol 8 no 5 pp 1069ndash1078 2014

[43] A Arshad D R Speth R M de Graaf H J Op den Camp MS Jetten and C U Welte ldquoA metagenomics-based metabolicmodel of nitrate-dependent anaerobic oxidation of methane byMethanoperedens-like archaeardquo Frontiers inMicrobiology vol 6article1423 2015

[44] S J Hallam N Putnam CM Preston et al ldquoReversemethano-genesis testing the hypothesis with environmental genomicsrdquoScience vol 305 no 5689 pp 1457ndash1462 2004

Archaea 19

[45] R K Thauer ldquoAnaerobic oxidation of methane with sulfate onthe reversibility of the reactions that are catalyzed by enzymesalso involved inmethanogenesis fromCO

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energy conservation in methanogenic archaeardquo Archives ofMicrobiology vol 165 no 3 pp 149ndash163 1996

[47] A-K Kaster J Moll K Parey and R K Thauer ldquoCoupling offerredoxin and heterodisulfide reduction via electron bifurca-tion in hydrogenotrophic methanogenic archaeardquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 108 no 7 pp 2981ndash2986 2011

[48] R K Thauer A-K Kaster H Seedorf W Buckel and RHedderich ldquoMethanogenic archaea ecologically relevant dif-ferences in energy conservationrdquo Nature Reviews Microbiologyvol 6 no 8 pp 579ndash591 2008

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[52] P V Welander and W W Metcalf ldquoLoss of the mtr operon inMethanosarcina blocks growth on methanol but not methano-genesis and reveals an unknown methanogenic pathwayrdquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 102 no 30 pp 10664ndash10669 2005

[53] P V Welander and W W Metcalf ldquoMutagenesis of the C1oxidation pathway inmethanosarcina barkeri new insights intothe MtrMer bypass pathwayrdquo Journal of Bacteriology vol 190no 6 pp 1928ndash1936 2008

[54] M Goenrich R K Thauer H Yurimoto and N KatoldquoFormaldehyde activating enzyme (Fae) and hexulose-6-phosphate synthase (Hps) inMethanosarcina barkeri a possiblefunction in ribose-5-phosphate biosynthesisrdquoArchives ofMicro-biology vol 184 no 1 pp 41ndash48 2005

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2by methan-

otrophicmicrobial mats from gas seeps of the anoxic Black SeardquoApplied and EnvironmentalMicrobiology vol 73 no 7 pp 2271ndash2283 2007

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[66] T Holler G Wegener H Niemann et al ldquoCarbon and sulfurback flux during anaerobic microbial oxidation of methane andcoupled sulfate reductionrdquo Proceedings of the National Academyof Sciences of the United States of America vol 108 no 52 ppE1484ndashE1490 2011

[67] M Kruger AMeyerdierks F O Glockner et al ldquoA conspicuousnickel protein in microbial mats that oxidize methane anaero-bicallyrdquo Nature vol 426 no 6968 pp 878ndash881 2003

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variant from archaea associated with anaerobic oxidation ofmethanerdquo Journal of the American Chemical Society vol 130 no32 pp 10758ndash10767 2008

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[70] R K Thauer and S Shima ldquoMethane as fuel for anaerobicmicroorganismsrdquo Annals of the New York Academy of Sciencesvol 1125 pp 158ndash170 2008

[71] S Yamamoto J B Alcauskas and T E Crozier ldquoSolubility ofmethane in distilled water and seawaterrdquo Journal of Chemicaland Engineering Data vol 21 no 1 pp 78ndash80 1976

[72] P H A Timmers J Gieteling H C A Widjaja-Greefkeset al ldquoGrowth of anaerobic methane-oxidizing archaea andsulfate-reducing bacteria in a high-pressure membrane capsulebioreactorrdquoApplied and EnvironmentalMicrobiology vol 81 no4 pp 1286ndash1296 2015

[73] MKruger HWoltersMGehre S B Joye andH-H RichnowldquoTracing the slow growth of anaerobic methane-oxidizingcommunities by 15N-labelling techniquesrdquo FEMS MicrobiologyEcology vol 63 no 3 pp 401ndash411 2008

[74] R J W Meulepas C G Jagersma A F Khadem C J N Buis-man A J M Stams and P N L Lens ldquoEffect of environmentalconditions on sulfate reduction withmethane as electron donorby an Eckernforde Bay enrichmentrdquo Environmental Science andTechnology vol 43 no 17 pp 6553ndash6559 2009

20 Archaea

[75] M W Bowles V A Samarkin and S B Joye ldquoImprovedmeasurement of microbial activity in deep-sea sediments atin situ pressure and methane concentrationrdquo Limnology andOceanography Methods vol 9 pp 499ndash506 2011

[76] S Shima M Krueger T Weinert et al ldquoStructure of a methyl-coenzyme M reductase from Black Sea mats that oxidizemethane anaerobicallyrdquo Nature vol 481 no 7379 pp 98ndash1012012

[77] K D Allen G Wegener and R H White ldquoDiscovery of multi-ple modified F-430 coenzymes in methanogens and anaerobicmethanotrophic archaea suggests possible new roles for F-430in naturerdquoApplied and Environmental Microbiology vol 80 no20 pp 6403ndash6412 2014

[78] V W Soo M J McAnulty A Tripathi et al ldquoReversingmethanogenesis to capture methane for liquid biofuel precur-sorsrdquoMicrobial Cell Factories vol 15 article 11 2016

[79] D L Valentine and W S Reeburgh ldquoNew perspectives onanaerobicmethane oxidationrdquoEnvironmentalMicrobiology vol2 no 5 pp 477ndash484 2000

[80] D L Valentine ldquoBiogeochemistry and microbial ecology ofmethane oxidation in anoxic environments a reviewrdquo Antonievan Leeuwenhoek International Journal of General and Molecu-lar Microbiology vol 81 no 1-4 pp 271ndash282 2002

[81] A J B Zehnder and T D Brock ldquoMethane formation andmethane oxidation by methanogenic bacteriardquo Journal of Bac-teriology vol 137 no 1 pp 420ndash432 1979

[82] J Harder ldquoAnaerobic methane oxidation by bacteria employ-ing 14C-methane uncontaminated with 14C-carbon monoxiderdquoMarine Geology vol 137 no 1-2 pp 13ndash23 1997

[83] J J Moran C H House K H Freeman and J G FerryldquoTrace methane oxidation studied in several Euryarchaeotaunder diverse conditionsrdquo Archaea vol 1 no 5 pp 303ndash3092005

[84] J J Moran C H House B Thomas and K H FreemanldquoProducts of tracemethane oxidation during nonmethyltrophicgrowth by Methanosarcinardquo Journal of Geophysical ResearchBiogeosciences vol 112 no 2 2007

[85] R J W Meulepas C G Jagersma Y Zhang et al ldquoTracemethane oxidation and the methane dependency of sulfatereduction in anaerobic granular sludgerdquo FEMS MicrobiologyEcology vol 72 no 2 pp 261ndash271 2010

[86] A J B Zehnder andTD Brock ldquoAnaerobicmethane oxidationoccurrence and ecologyrdquoApplied and Environmental Microbiol-ogy vol 39 no 1 pp 194ndash204 1980

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[88] K A Smemo and J B Yavitt ldquoEvidence for anaerobic CH4

oxidation in freshwater peatlandsrdquo Geomicrobiology Journalvol 24 no 7-8 pp 583ndash597 2007

[89] M J Alperin and T M Hoehler ldquoAnaerobic methane oxidationby archaeasulfate-reducing bacteria aggregates 1 Thermody-namic and physical constraintsrdquo American Journal of Sciencevol 309 no 10 pp 869ndash957 2009

[90] S L Caldwell J R Laidler E A Brewer J O Eberly S CSandborgh and F S Colwell ldquoAnaerobic oxidation of methanemechanisms bioenergetics and the ecology of associatedmicroorganismsrdquo Environmental Science and Technology vol42 no 18 pp 6791ndash6799 2008

[91] GWang A J Spivack and S DrsquoHondt ldquoGibbs energies of reac-tion and microbial mutualism in anaerobic deep subseafloorsediments of ODP Site 1226rdquoGeochimica et Cosmochimica Actavol 74 no 14 pp 3938ndash3947 2010

[92] P R Girguis A E Cozen and E F DeLong ldquoGrowth andpopulation dynamics of anaerobic methane-oxidizing archaeaand sulfate-reducing bacteria in a continuous-flow bioreactorrdquoApplied and EnvironmentalMicrobiology vol 71 no 7 pp 3725ndash3733 2005

[93] K Nauhaus M Albrecht M Elvert A Boetius and F WiddelldquoIn vitro cell growth ofmarine archaeal-bacterial consortia dur-ing anaerobic oxidation ofmethanewith sulfaterdquoEnvironmentalMicrobiology vol 9 no 1 pp 187ndash196 2007

[94] B Orcutt V Samarkin A Boetius and S Joye ldquoOn the relation-ship between methane production and oxidation by anaerobicmethanotrophic communities from cold seeps of the Gulf ofMexicordquo Environmental Microbiology vol 10 no 5 pp 1108ndash1117 2008

[95] M Y Yoshinaga T Holler T Goldhammer et al ldquoCarbon iso-tope equilibration during sulphate-limited anaerobic oxidationof methanerdquo Nature Geoscience vol 7 no 3 pp 190ndash194 2014

[96] T Treude J Niggemann J Kallmeyer et al ldquoAnaerobic oxi-dation of methane and sulfate reduction along the Chileancontinental marginrdquo Geochimica et Cosmochimica Acta vol 69no 11 pp 2767ndash2779 2005

[97] R J Parkes B A Cragg N Banning et al ldquoBiogeochemistryand biodiversity of methane cycling in subsurface marinesediments (SkagerrakDenmark)rdquoEnvironmentalMicrobiologyvol 9 no 5 pp 1146ndash1161 2007

[98] N J Knab B A Cragg E R C Hornibrook et al ldquoRegulationof anaerobic methane oxidation in sediments of the Black SeardquoBiogeosciences vol 6 no 8 pp 1505ndash1518 2009

[99] H Yoshioka A Maruyama T Nakamura et al ldquoActivities anddistribution of methanogenic and methane-oxidizing microbesin marine sediments from the Cascadia Marginrdquo Geobiologyvol 8 no 3 pp 223ndash233 2010

[100] G Wegener V Krukenberg S E Ruff M Y Kellermann andK Knittel ldquoMetabolic capabilities of microorganisms involvedin and associated with the anaerobic oxidation of methanerdquoFrontiers in Microbiology vol 7 article 46 2016

[101] R J W Meulepas C G Jagersma A F Khadem A J MStams and P N L Lens ldquoEffect of methanogenic substrateson anaerobic oxidation of methane and sulfate reduction by ananaerobic methanotrophic enrichmentrdquo Applied Microbiologyand Biotechnology vol 87 no 4 pp 1499ndash1506 2010

[102] J Milucka T G Ferdelman L Polerecky et al ldquoZero-valentsulphur is a key intermediate in marine methane oxidationrdquoNature vol 491 no 7425 pp 541ndash546 2012

[103] W Michaelis R Seifert K Nauhaus et al ldquoMicrobial reefs inthe black sea fueled by anaerobic oxidation ofmethanerdquo Sciencevol 297 no 5583 pp 1013ndash1015 2002

[104] A Vigneron P Cruaud P Pignet et al ldquoArchaeal and anaerobicmethane oxidizer communities in the Sonora Margin coldseeps Guaymas Basin (Gulf of California)rdquo ISME Journal vol7 no 8 pp 1595ndash1608 2013

[105] M Alperin and T Hoehler ldquoThe ongoing mystery of sea-floormethanerdquo Science vol 329 no 5989 pp 288ndash289 2010

[106] B Orcutt and C Meile ldquoConstraints on mechanisms and ratesof anaerobic oxidation of methane by microbial consortiaprocess-basedmodeling of ANME-2 archaea and sulfate reduc-ing bacteria interactionsrdquo Biogeosciences vol 5 no 6 pp 1587ndash1599 2008

Archaea 21

[107] S E McGlynn G L Chadwick C P Kempes and V J OrphanldquoSingle cell activity reveals direct electron transfer in methan-otrophic consortiardquoNature vol 526 no 7574 pp 531ndash535 2015

[108] D R Lovley ldquoElectromicrobiologyrdquo Annual Review of Microbi-ology vol 66 pp 391ndash409 2012

[109] S M Strycharz-Glaven R M Snider A Guiseppi-Elie andL M Tender ldquoOn the electrical conductivity of microbialnanowires and biofilmsrdquoEnergy and Environmental Science vol4 no 11 pp 4366ndash4379 2011

[110] D J Richardson J N Butt J K Fredrickson et al ldquoThe lsquoporinndashcytochromersquo model for microbe-to-mineral electron transferrdquoMolecular Microbiology vol 85 no 2 pp 201ndash212 2012

[111] A Okamoto K Hashimoto and R Nakamura ldquoLong-rangeelectron conduction of Shewanella biofilms mediated by outermembrane C-type cytochromesrdquo Bioelectrochemistry vol 85pp 61ndash65 2012

[112] M Y El-Naggar G Wanger K M Leung et al ldquoElectricaltransport along bacterial nanowires from Shewanella oneidensisMR-1rdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 107 no 42 pp 18127ndash18131 2010

[113] G Reguera K D McCarthy T Mehta J S Nicoll M TTuominen and D R Lovley ldquoExtracellular electron transfer viamicrobial nanowiresrdquo Nature vol 435 no 7045 pp 1098ndash11012005

[114] Z M Summers H E Fogarty C Leang A E Franks N SMalvankar and D R Lovley ldquoDirect exchange of electronswithin aggregates of an evolved syntrophic coculture of anaer-obic bacteriardquo Science vol 330 no 6009 pp 1413ndash1415 2010

[115] A Kletzin T Heimerl J Flechsler L V Niftrik R Rachel andA Klingl ldquoCytochromes c in archaea distribution maturationcell architecture and the special case of Ignicoccus hospitalisrdquoFrontiers in Microbiology vol 6 article 439 2015

[116] GWegener V Krukenberg D Riedel H E Tegetmeyer and ABoetius ldquoIntercellular wiring enables electron transfer betweenmethanotrophic archaea and bacteriardquo Nature vol 526 no7574 pp 587ndash590 2015

[117] D HHaft S H Payne and J D Selengut ldquoArchaeosortases andexosortases are widely distributed systems linking membranetransit with posttranslational modificationrdquo Journal of Bacteri-ology vol 194 no 1 pp 36ndash48 2012

[118] A Marchler-Bauer M K Derbyshire N R Gonzales et alldquoCDD NCBIrsquos conserved domain databaserdquo Nucleic AcidsResearch vol 43 no 1 pp D222ndashD226 2015

[119] A Mitchell H-Y Chang L Daugherty et al ldquoThe InterProprotein families database the classification resource after 15yearsrdquo Nucleic Acids Research vol 43 no 1 pp D213ndashD2212015

[120] V Krukenberg K Harding M Richter et al ldquoCandidatusdesulfofervidus auxilii a hydrogenotrophic sulfate-reducingbacterium involved in the thermophilic anaerobic oxidation ofmethanerdquo Environmental Microbiology vol 18 pp 3073ndash30912016

[121] L Shi T C Squier J M Zachara and J K Fredrickson ldquoRes-piration of metal (hydr)oxides by Shewanella and Geobactera key role for multihaem c-type cytochromesrdquo MolecularMicrobiology vol 65 no 1 pp 12ndash20 2007

[122] N S Malvankar and D R Lovley ldquoMicrobial nanowires forbioenergy applicationsrdquo Current Opinion in Biotechnology vol27 pp 88ndash95 2014

[123] A-E Rotaru T LWoodard K PNevin andDR Lovley ldquoLinkbetween capacity for current production and syntrophic growth

in Geobacter speciesrdquo Frontiers in Microbiology vol 6 article744 2015

[124] A-E Rotaru P M Shrestha F Liu et al ldquoDirect interspecieselectron transfer between Geobacter metallireducens andMethanosarcina barkerirdquo Applied and Environmental Microbi-ology vol 80 no 15 pp 4599ndash4605 2014

[125] S Scheller H Yu G L Chadwick S E McGlynn and VJ Orphan ldquoArtificial electron acceptors decouple archaealmethane oxidation from sulfate reductionrdquo Science vol 351 no6274 pp 703ndash707 2016

[126] J Milucka F Widdel and S Shima ldquoImmunological detec-tion of enzymes for sulfate reduction in anaerobic methane-oxidizing consortiardquo Environmental Microbiology vol 15 no 5pp 1561ndash1571 2013

[127] P Cabello M D Roldan and C Moreno-Vivian ldquoNitratereduction and the nitrogen cycle in archaeardquoMicrobiology vol150 no 11 pp 3527ndash3546 2004

[128] R MMartinez-Espinosa E J Dridge M J Bonete et al ldquoLookon the positive sideThe orientation identification and bioener-getics of lsquoArchaealrsquomembrane-boundnitrate reductasesrdquoFEMSMicrobiology Letters vol 276 no 2 pp 129ndash139 2007

[129] S de VriesMMomcilovicM J F Strampraad J PWhiteleggeA Baghai and I Schroder ldquoAdaptation to a high-tungsten envi-ronment pyrobaculum aerophilum contains an active tungstennitrate reductaserdquo Biochemistry vol 49 no 45 pp 9911ndash99212010

[130] M Egger O Rasigraf C J Sapart et al ldquoIron-mediated anaer-obic oxidation of methane in brackish coastal sedimentsrdquoEnvironmental Science and Technology vol 49 no 1 pp 277ndash283 2015

[131] T Treude S Krause J Maltby A W Dale R Coffin and LJ Hamdan ldquoSulfate reduction and methane oxidation activitybelow the sulfate-methane transition zone in Alaskan BeaufortSea continental margin sediments implications for deep sulfurcyclingrdquo Geochimica et Cosmochimica Acta vol 144 pp 217ndash237 2014

[132] N Riedinger M J Formolo T W Lyons S Henkel A Beckand S Kasten ldquoAn inorganic geochemical argument for coupledanaerobic oxidation of methane and iron reduction in marinesedimentsrdquo Geobiology vol 12 no 2 pp 172ndash181 2014

[133] Y-H Chang T-W Cheng W-J Lai et al ldquoMicrobial methanecycling in a terrestrialmud volcano in eastern Taiwanrdquo Environ-mental Microbiology vol 14 no 4 pp 895ndash908 2012

[134] S A Crowe S Katsev K Leslie et al ldquoThe methane cycle inferruginous Lake Matanordquo Geobiology vol 9 no 1 pp 61ndash782011

[135] O Sivan M Adler A Pearson et al ldquoGeochemical evidence foriron-mediated anaerobic oxidation of methanerdquo Limnology andOceanography vol 56 no 4 pp 1536ndash1544 2011

[136] K E A Segarra C Comerford J Slaughter and S B JoyeldquoImpact of electron acceptor availability on the anaerobic oxi-dation of methane in coastal freshwater and brackish wetlandsedimentsrdquo Geochimica et Cosmochimica Acta vol 115 pp 15ndash30 2013

[137] V Gupta K A Smemo J B Yavitt D Fowle B Branfireunand N Basiliko ldquoStable isotopes reveal widespread anaerobicmethane oxidation across latitude and peatland typerdquo Environ-mental Science and Technology vol 47 no 15 pp 8273ndash82792013

[138] O Oni T Miyatake S Kasten et al ldquoDistinct microbialpopulations are tightly linked to the profile of dissolved iron in

22 Archaea

the methanic sediments of the Helgolandmud area North SeardquoFrontiers in Microbiology vol 6 2015

[139] E J Beal C H House and V J Orphan ldquoManganese- andiron-dependent marine methane oxidationrdquo Science vol 325no 5937 pp 184ndash187 2009

[140] M W Bowles V A Samarkin K M Bowles and S B JoyeldquoWeak coupling between sulfate reduction and the anaerobicoxidation of methane in methane-rich seafloor sedimentsduring ex situ incubationrdquo Geochimica et Cosmochimica Actavol 75 no 2 pp 500ndash519 2011

[141] Y Z Lu L Fu J Ding Z Ding N Li and R J Zeng ldquoCr(VI)reduction coupled with anaerobic oxidation of methane in alaboratory reactorrdquoWater Research vol 102 pp 445ndash452 2016

[142] K F Ettwig B Zhu D Speth J T Keltjens M S Jetten and BKartal ldquoArchaea catalyze iron-dependent anaerobic oxidationof methanerdquo Proceedings of the National Academy of Sciences ofthe United States of America vol 113 no 45 pp 12792ndash127962016

[143] T M Flynn R A Sanford H Ryu et al ldquoFunctional microbialdiversity explains groundwater chemistry in a pristine aquiferrdquoBMCMicrobiology vol 13 no 1 article no 146 2013

[144] C J Schubert F Vazquez T Losekann-Behrens K KnittelM Tonolla and A Boetius ldquoEvidence for anaerobic oxidationof methane in sediments of a freshwater system (Lago diCadagno)rdquo FEMS Microbiology Ecology vol 76 no 1 pp 26ndash38 2011

[145] K E A Segarra F Schubotz V Samarkin M Y Yoshinaga K-U Hinrichs and S B Joye ldquoHigh rates of anaerobic methaneoxidation in freshwater wetlands reduce potential atmosphericmethane emissionsrdquo Nature Communications vol 6 article7477 2015

[146] E J Beal M W Claire and C H House ldquoHigh rates ofanaerobic methanotrophy at low sulfate concentrations withimplications for past and present methane levelsrdquo Geobiologyvol 9 no 2 pp 131ndash139 2011

[147] F Kracke I Vassilev and J O Kromer ldquoMicrobial electrontransport and energy conservationmdashthe foundation for opti-mizing bioelectrochemical systemsrdquo Frontiers in Microbiologyvol 6 article 575 2015

[148] C L Reardon A C Dohnalkova P Nachimuthu et al ldquoRoleof outer-membrane cytochromes MtrC and OmcA in thebiomineralization of ferrihydrite by Shewanella oneidensisMR-1rdquo Geobiology vol 8 no 1 pp 56ndash68 2010

[149] L Shi B Chen Z Wang et al ldquoIsolation of a high-affinityfunctional protein complex between OmcA and MtrC twoouter membrane decaheme c-type cytochromes of Shewanellaoneidensis MR-1rdquo Journal of Bacteriology vol 188 no 13 pp4705ndash4714 2006

[150] X Qian T Mester L Morgado et al ldquoBiochemical charac-terization of purified OmcS a c-type cytochrome requiredfor insoluble Fe(III) reduction in Geobacter sulfurreducensrdquoBiochimica et BiophysicaActamdashBioenergetics vol 1807 no 4 pp404ndash412 2011

[151] T Mehta M V Coppi S E Childers and D R Lovley ldquoOutermembrane c-type cytochromes required for Fe(III) andMn(IV)oxide reduction in Geobacter sulfurreducensrdquo Applied andEnvironmentalMicrobiology vol 71 no 12 pp 8634ndash8641 2005

[152] W Blankenfeldt A P Kuzin T Skarina et al ldquoStructure andfunction of the phenazine biosynthetic protein PhzF fromPseudomonas fluorescensrdquoProceedings of theNational Academyof Sciences of the United States of America vol 101 no 47 pp16431ndash16436 2004

[153] J F Parsons F Song L Parsons K Calabrese E Eisensteinand J E Ladner ldquoStructure and function of the phenazinebiosynthesis protein PhzF fromPseudomonas fluorescens 2-79rdquoBiochemistry vol 43 no 39 pp 12427ndash12435 2004

[154] T Hiratsuka K Furihata J Ishikawa et al ldquoAn alternativemenaquinone biosynthetic pathway operating in microorgan-ismsrdquo Science vol 321 no 5896 pp 1670ndash1673 2008

[155] M Tietze A Beuchle I Lamla et al ldquoRedox potentials ofmethanophenazine and CoB-S-S-CoM factors involved inelectron transport in methanogenic archaeardquo ChemBioChemvol 4 no 4 pp 333ndash335 2003

[156] Q H Tran and G Unden ldquoChanges in the proton potentialand the cellular energetics of Escherichia coli during growth byaerobic and anaerobic respiration or by fermentationrdquoEuropeanJournal of Biochemistry vol 251 no 1-2 pp 538ndash543 1998

[157] I Callebaut D Gilges I Vigon and J-P Mornon ldquoHYR anextracellular module involved in cellular adhesion and relatedto the immunoglobulin-like foldrdquo Protein Science vol 9 no 7pp 1382ndash1390 2000

[158] H J Gilbert ldquoCellulosomes microbial nanomachines that dis-play plasticity in quaternary structurerdquoMolecular Microbiologyvol 63 no 6 pp 1568ndash1576 2007

[159] A Peer S P Smith E A Bayer R Lamed and I BorovokldquoNoncellulosomal cohesin- and dockerin-like modules in thethree domains of liferdquo FEMS Microbiology Letters vol 291 no1 pp 1ndash16 2009

[160] M Wagner ldquoMicrobiology conductive consortiardquo Nature vol526 no 7574 pp 513ndash514 2015

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

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BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

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Nucleic AcidsJournal of

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Archaea 15

metagenomes of ANME-1 [41] and ANME-2a (Table S1)The enzymes Sat and Dsr were also not detected in ANMEcells using fluorescent immunolabelling [126] ANME-1 werepreviously found to encode most proteins for assimilatorysulfate reduction [41] ANME-2d only harbor gene domainsthat encode Sat and assimilatoryATP sulfurylase APS kinaseand sodiumsulfate symporters which were not present inANME-2a (Table S1) It is therefore clear that at least ANME-2a cannot donate electrons to sulfate but need to donateelectrons to a sulfate-reducing partner

32 Nitrate-Dependent AOM Unlike during S-AOMANME-2d that perform N-AOM do not need a bacterialpartner but transfer electrons directly to a membrane boundnitrate reductase (Nar) [28 43] (Figure 5) The ANME-2dgenomes contain most MHCs found so far in archaea[107 115] (Table 2) Of the 87 proteins that contained aCxxCH binding motif of which 43 seemed to be true c-typecytochromes [115] 23 CxxCH motif-encoding transcriptswere expressed during N-AOM [43] The function of mostof these MHCs is not known but they are likely involvedin nitrate reduction since c-type cytochromes are capableof operating in the wide range of redox potentials thatcouple nitrate reduction (11986401015840 (NO

3

minusNO2

minus) = +433mV) andmethane oxidation (11986401015840 (CoM-S-S-CoBCoM-SH+CoB-SH)= minus143mV) [43] Nitrate as terminal electron acceptor inanaerobic respiration has been found in halophilic andthermophilic archaea [127] The nar gene cluster of ldquoCaM nitroreducensrdquo comprises several genes including thecatalytic alpha (NarG molybdopterin) and beta (NarHiron sulfur cluster) subunit of nitrate reductase [28 43] The(halo)archaeal nitrate reductase complex was reported to belocated at the extracellular side of the cytoplasmic membrane[128] and in most archaea associated with the cytoplasmicmembrane via NarM [129] The ldquoCa M nitroreducensrdquogenome does not encode NarM but encodes a TAT signalpeptide at the N-terminus of NarG for translocation acrossthe cytoplasmic membrane [28 43] Interestingly theNarG and NarH seem to have been acquired from theProteobacteria via lateral gene transfer [28]

It is not yet clear at which point in themetabolism ldquoCaMnitroreducensrdquo conserves energy During reverse methano-genesis N5-methyl-H

4MPTCoM methyltransferase (Mtr)

dissipates the sodium ion potential across the cytoplasmicmembrane so subsequent steps inN-AOMhave to be coupledto the build-up of a proton or sodium motive force to makethe overall process energetically favourable The analysis ofan environmental genome [43] indicated presence of severalprotein complexes involved in electron transport and energyconservation Electrons that enter the respiratory chain couldbe transported by membrane-integral electron carriers (iemenaquinones) to a Rieske-cytochrome b complex that mayuse cytochrome c as electron acceptor This in turn maybe the electron donor for the unusual nitrate reductasecomplex Energy conservation is thermodynamically andmechanistically feasible at the F

420H2dehydrogenase and the

Rieske-cytochrome b complex (Figure 5) (Figure 2 in [43])Further investigations are needed to determine whether

nitrate reductase is also involved in energy conservationbut this working hypothesis is strengthened by the presenceof cupredoxin multicopper oxidase domains and coppercenters related to the periplasmic domain of cytochrome coxidase subunit II (HCO II) in ANME-2d (Table S1)

BothANME-2d genomes discussed here are derived frombioreactors where ldquoCaM nitroreducensrdquo formed syntrophiccultures with nitrite scavenging bacteria either with ldquoCaKuenenia stuttgartiensisrdquo (anammox bacteria) [28] or ldquoCaMethylomirabilis oxyferardquo (NC10 bacteria) [31 43]This indi-cated that ANME-2d could be dependent on those bacteriafor nitrite removal However in addition to nitrite ldquoCa Mnitroreducensrdquo may also produce ammonium during AOMby a pentaheme c-type nitrite reductase (NrfAH) encodedin the genome [43] (Figure 5) In fact both ANME-2dgenomes contain domains for NrfA (IPR003321) and NrfH(IPR017571) (Table S1) implying that both ANME-2d speciesare not necessarily dependent on a nitrite scavenger duringAOM

33 Metal-Dependent AOM Evidence for metal-dependentAOM was found in marine sediments [130ndash132] In non-marine environments AOM was also hypothesized to becoupled to iron andor manganese oxide reduction [26 133ndash136] or even coupled to the reduction of humic acids [136137] However organisms responsible for metal-dependentAOM were not identified in these studies It was speculatedthat JS1 bacteria methanogenic archaea and Methanohalo-biumANME-3 could be responsible for iron-dependentAOM [138] Other researchers speculated that either ANME-1 or MethanococcoidesANME-3 together with a bacterialpartner were responsible for manganese-dependent AOM[139] In another study where AOM was decoupled from SRANME were not detected which leaves open the possibilitythat other archaeal clades besides ANME could performmetal-dependent AOM [131]

It was recently observed that cultures containing ANME-2a and ANME-2c could decouple AOM from SR in thepresence of artificial electron acceptors humic acids andsoluble iron [125] which confirmed previous findings ofAOM not connected to SR in ANME dominated samples[140] This suggests that ANME-2 could also use insolublemetal oxide minerals as electron acceptor during AOM TheMHCs of ANME-2ab and ANME-2d are larger than thosein Shewanella and Geobacter species [107] which are knownto be capable of extracellular electron conduction It wasspeculated that both ANME-2d and Ferroglobus placidus ofwhich the latter can perform solid iron reduction can foldCxxCHmotifs into extracellular conductive structures or pili[115] Many of the MHCs of ANME-2d were not expressedwhen grown with nitrate (discussed in section 32) implyingthat these are not needed for nitrate reduction [43] Thisstrengthens the hypothesis that also ANME-2d could coupleAOM to reduction of other extracellular electron acceptorsthan nitrate and even to insoluble metal oxides Indeedrecent work showed that ANME-2d could be involved inAOM coupled to chromium(VI) reduction [141] (Table 1reaction (5)) and in AOM coupled to the reduction of soluble

16 Archaea

iron and insoluble ferrihydrite and birnessite minerals [142](Table 1 reactions (3) and (4)) ANME-2d could even possiblydonate electrons to a bacterial partner besides nitrate-richenvironments ANME-2d archaea have been found inwells ofan aquifer where sulfate and methane concentrations overlap[143] Moreover ANME-2d was the only clade detected insediments of a freshwater lake where S-AOM occurred [144]Sulfate concentrations in these studies were low but above1mM and thus higher than the lowest reported concen-trations for S-AOM to occur [145 146] Lastly sequencesof ANME-2d were relatively more abundant in freshwatersediments fed with methane and sulfate than in sedimentsfed with onlymethane or only sulfate and noN-AOMactivitywas detected when fed with nitrate and methane [27] Theseindications hold promise that direct experimental evidencefor sulfate-dependent AOM by ANME-2d could be found inthe future

TheANME-1 genome contains fewerMHCgene domainsas compared to ANME-2a and ANME-2d and some otherarchaea such as somemethylotrophicmethanogens (Table 2)and some members of the Archaeoglobales [115] The MHCsof ANME-1 also have a smaller heme count as compared toother ANME and some other archaea with the largest beingan octaheme cytochrome [107] Each hemewithin aMHChasits own redox potential and therefore structurally differentMHCs represent a large range of redox potentials that canbe used for bioenergetic electron transfer (reviewed in [147])For instance metal oxide reduction in Shewanella oneidensisMR-1 is catalyzed by a chain of a tetraheme (CymA) twodecaheme (MtrA and MtrB) and eventually extracellulardecaheme cytochromes OmcAMtrC that reduce the ironminerals [121 148 149] In Geobacter sulfurreducens ironmineral reduction seems to be catalyzed by the tetrahemecytochrome OmcE and hexaheme cytochrome OmcS trans-ferring electrons from the outer membrane to type IV pilithat transmit the electrons to iron minerals [121 150 151]Since ANME-1 lack MHCs of the correct size and lack genedomains for pili production [116] they seem unable to reduceminerals via both mechanisms present in Shewanella andGeobacter It can therefore be speculated that ANME-1 areless versatile in electron acceptor use and are not able toreduce solid metal oxides However DIET mechanisms arestill not well understood and the true differences betweenMHCs of different ANME types need to be investigated usingbiochemical methods This would allow uncovering the truecapabilities concerning DIET

34 Menaquinones and Methanophenazines ANME-2a en-coded a protein with a domain specific for PhzF which is anenzyme involved in phenazine biosynthesis in Pseudomonasfluorescens [152 153] The respective gene is not present in allmethanophenazine containing methanogens (in our genomecomparison only inM acetivorans andM formicica Table 2)so it is unclear whether this enzyme is really involved inmethanophenazine biosynthesis It is however likely thatANME-2a use methanophenazines in their respiratory chainsince gene domains for menaquinone biosynthesis wereabsent (Table 2) ldquoCa M nitroreducensrdquo probably uses

menaquinones as membrane-integral electron carrier sinceenvironmental genomes [28 43] encoded the futalosine(mqn) biosynthesis pathway as reported for Archaeoglobusfulgidus [154] (Table 2) Moreover ldquoCa M nitroreducensrdquoenrichment cultures showed absence of methanophenazines[43] ANME-1 also contained gene domains formenaquinonebiosynthesis via the futalosine (mqn) biosynthesis pathway(Table 2) Indications for a quinone biosynthesis pathwayin ANME-1 were previously found to be weak since onlysome of the Ubi homologues of the oxic ubiquinone biosyn-thesis pathway were detected [41] but the futalosine (mqn)biosynthesis pathway was overlooked in that particular anal-ysis Additionally ANME-1 have Fqo homologues similarto Archaeoglobus fulgidus [44] and expressed the catalyticsubunit FqoF [41] However since the phenazine biosynthesisdomain PhzF was also present in the ANME-1 genomes(Table 2) and Fpo and Fqo are homologues we cannotconclude on genomic information alone which redox shuttleis used by ANME-1 during AOM If ANME-1 would usemenaquinones this would have implications for subsequentelectron transfer to MHCs since methanophenazine (1198640 =minus165mV) [155] and menaquinone (1198640 = minus80mV) [156] havedifferent redox potentials

35 Cell Adhesion Some gene domains involved in cel-lular adhesion were more abundant in ANME than inmethanogens (Table 2) especially in ANME-2a and ANME-1that are known to form syntrophic interactions for electrontransfer during respiration These domains include HYR(IPR003410) and CARDB domains (IPR011635) that bothhave a direct role in cellular adhesion [157] (Table 2) Interest-ingly also domains related to the cellulosome of Clostridiumspecies termed dockerin and cohesin were highly abundantin both ANME-1 and ANME-2a as compared to ANME-2dand methanogens together with many carbohydrate bindingdomains (Table 2) In Clostridium species dockerin andcohesin form an anchor to the bacterial cell wall that containsa scaffold with cellulose-degrading enzymes and a carbohy-drate bindingmodule that binds cellulose altogether formingthe cellulosome [158] These domains have been found in alldomains of life irrespective of cellulose utilization but thefunction of such proteins outside of the cellulosome is notknown [159]Therefore dockerin cohesin and carbohydratebinding domains in ANME could hypothetically form aconstruct that binds to carbohydrates and could possibly havea function in cell-to-cell contact or MHC adhesion but thisneeds further investigation

4 Future Challenges

Advances in (meta)genomics transcriptomics and pro-teomics have produced the valuable metabolic blueprints ofdifferent ANMEwith hypotheses on how centralmetabolismelectron transport and energy conservation may functionFuture experiments are needed to biochemically demonstratethat these hypotheses are correct

The bottleneck for biochemical studies of ANME isthe lack of pure cultures due to the slow and syntrophic

Archaea 17

growth However the recent milestone discovery of directelectron transfer provides opportunities to grow ANMEas stated previously on electron accepting electrodes (ieanodes) [160] In this way pure or highly enriched culturesof different ANME without their respective syntrophic part-ner could be obtained and MHCs responsible for electricconduction could be biochemically characterized It seemsthat ANME-1 are limited by the size and abundance ofMHCs which could relate to differences in behavior onan anode The partner bacteria of ANME-1 and ANME-2could be investigated on an electron donating electrode (iecathode) with specific focus on the ability to produce pili (ienanowires) Also worth investigating is if besides ANME-2d ANME-2ab could also use insoluble electron acceptorsand if ANME-2d could donate electrons to a bacterialpartner

Another future challenge is to isolate and characterizeMcr from different ANME clades It needs to be investi-gated if Mcr abundance in ANME cells compensates forthe slow reverse activity or if modifications in the Mcrof ANME-1 also contribute to a better reverse activity ofMcr Moreover the effect of methane partial pressure onreaction rates and enzyme kinetics needs to be determined insitu

ANME-1 are potentially able to perform hydrogeno-trophic methanogenesis due to the presence of a hydrogenasein the genome Genetic indications of menaquinones aselectron carrier in ANME-1 and the various cellulosome andcell adhesion related gene domains in all ANME are alsotopics that could be explored further Methanogenic archaeaare likely not able to perform AOM but additional studieson TMO and more genetic modifications to stimulate AOMin methanogens could help in understanding the param-eters needed for AOM to occur Ultimately physiologicalunderstanding of ANME will help to explain the observedecological niche separation of different ANME clades and theoccurrence of ANMEwithout a bacterial partnerThis wouldgreatly enhance our knowledge of themethane cycle in anoxicenvironments

Competing Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors thank Stefanie Berger (RU Nijmegen) for criticalreading of the manuscript This research is supported bythe Soehngen Institute of Anaerobic Microbiology (SIAM)Gravitation grant (024002002) of the Netherlands Ministryof Education Culture and Science and the NetherlandsOrganisation for Scientific Research (NWO) Mike S MJetten was further supported by ERC AG 339880 Eco-MoMand Alfons J M Stams was supported by ERC AG 323009Novel Anaerobes

References

[1] A Boetius K Ravenschlag C J Schubert et al ldquoA marinemicrobial consortium apparently mediating anaerobic oxida-tion of methanerdquo Nature vol 407 no 6804 pp 623ndash626 2000

[2] K-U Hinrichs J M Hayes S P Sylva P G Brewert andE F DeLong ldquoMethane-consuming archaebacteria in marinesedimentsrdquo Nature vol 398 no 6730 pp 802ndash805 1999

[3] V J Orphan C H House K-U Hinrichs K D McKeeganand E F DeLong ldquoMethane-consuming archaea revealed bydirectly coupled isotopic and phylogenetic analysisrdquo Sciencevol 293 no 5529 pp 484ndash487 2001

[4] K-U Hinrichs and A Boetius ldquoThe anaerobic oxidation ofmethane new insights in microbial ecology and biogeochem-istryrdquo inOceanMargin Systems GWefer D Billett D HebbelnB B Joslashrgensen M Schluter and T VanWeering Eds pp 457ndash477 Springer Berlin Germany 2002

[5] K Knittel T Losekann A Boetius R Kort and R AmannldquoDiversity and distribution of methanotrophic archaea at coldseepsrdquo Applied and Environmental Microbiology vol 71 no 1pp 467ndash479 2005

[6] K Knittel and A Boetius ldquoAnaerobic oxidation of methaneprogress with an unknown processrdquo Annual Review of Micro-biology vol 63 pp 311ndash334 2009

[7] V J Orphan K-U Hinrichs W Ussler III et al ldquoComparativeanalysis of methane-oxidizing archaea and sulfate-reducingbacteria in anoxic marine sedimentsrdquoApplied and Environmen-tal Microbiology vol 67 no 4 pp 1922ndash1934 2001

[8] T Losekann K Knittel T Nadalig et al ldquoDiversity andabundance of aerobic and anaerobic methane oxidizers atthe Haakon Mosby Mud Volcano Barents Seardquo Applied andEnvironmentalMicrobiology vol 73 no 10 pp 3348ndash3362 2007

[9] H Niemann T Losekann D De Beer et al ldquoNovel microbialcommunities of the Haakon Mosby mud volcano and their roleas amethane sinkrdquoNature vol 443 no 7113 pp 854ndash858 2006

[10] TNunouraHOida T Toki J Ashi K Takai andKHorikoshildquoQuantification of mcrA by quantitative fluorescent PCR insediments from methane seep of the Nankai Troughrdquo FEMSMicrobiology Ecology vol 57 no 1 pp 149ndash157 2006

[11] B Orcutt A Boetius M Elvert V Samarkin and S B JoyeldquoMolecular biogeochemistry of sulfate reduction methanogen-esis and the anaerobic oxidation of methane at Gulf of Mexicocold seepsrdquoGeochimica et Cosmochimica Acta vol 69 no 17 pp4267ndash4281 2005

[12] V J Orphan W Ussler III T H Naehr C H House K-U Hinrichs and C K Paull ldquoGeological geochemical andmicrobiological heterogeneity of the seafloor around methanevents in the Eel River Basin offshore Californiardquo ChemicalGeology vol 205 no 3-4 pp 265ndash289 2004

[13] M G Pachiadaki A Kallionaki A Dahlmann G J De Langeand K A Kormas ldquoDiversity and spatial distribution ofprokaryotic communities along a sediment vertical profile ofa deep-sea mud volcanordquo Microbial Ecology vol 62 no 3 pp655ndash668 2011

[14] I Roalkvam H Dahle Y Chen S L Joslashrgensen H Haflidasonand I H Steen ldquoFine-scale community structure analysis ofANME in Nyegga sediments with high and low methane fluxrdquoFrontiers in Microbiology vol 3 p 216 2012

[15] K Yanagawa M Sunamura M A Lever et al ldquoNiche separa-tion of methanotrophic archaea (ANME-1 and -2) in methane-seep sediments of the Eastern Japan Sea offshore JoetsurdquoGeomicrobiology Journal vol 28 no 2 pp 118ndash129 2011

18 Archaea

[16] A Pernthaler A E Dekas C T Brown S K Goffredi TEmbaye and V J Orphan ldquoDiverse syntrophic partnershipsfromdeep-seamethane vents revealed by direct cell capture andmetagenomicsrdquo Proceedings of the National Academy of Sciencesof the United States of America vol 105 no 19 pp 7052ndash70572008

[17] R Hatzenpichler S A Connon D Goudeau R R Malm-strom T Woyke and V J Orphan ldquoVisualizing in situtranslational activity for identifying and sorting slow-growingarchaealminusbacterial consortiardquo Proceedings of the NationalAcademy of Sciences vol 113 no 28 pp E4069ndashE4078 2016

[18] L Maignien R J Parkes B Cragg et al ldquoAnaerobic oxidationof methane in hypersaline cold seep sedimentsrdquo FEMS Micro-biology Ecology vol 83 no 1 pp 214ndash231 2013

[19] V J Orphan C H House K-U Hinrichs K D McKeeganand E F DeLong ldquoMultiple archaeal groups mediate methaneoxidation in anoxic cold seep sedimentsrdquo Proceedings of theNational Academy of Sciences of the United States of Americavol 99 no 11 pp 7663ndash7668 2002

[20] T TreudeM Kruger A Boetius and B B Joslashrgensen ldquoEnviron-mental control on anaerobic oxidation of methane in the gassysediments of Eckernforde Bay (German Baltic)rdquo Limnology andOceanography vol 50 no 6 pp 1771ndash1786 2005

[21] G C Jagersma R J W Meulepas I Heikamp-De Jong etal ldquoMicrobial diversity and community structure of a highlyactive anaerobic methane-oxidizing sulfate-reducing enrich-mentrdquo Environmental Microbiology vol 11 no 12 pp 3223ndash3232 2009

[22] M Blumenberg R Seifert J Reitner T Pape andWMichaelisldquoMembrane lipid patterns typify distinct anaerobic methan-otrophic consortiardquo Proceedings of the National Academy ofSciences of the United States of America vol 101 no 30 pp 11111ndash11116 2004

[23] S Bertram M Blumenberg W Michaelis M Siegert MKruger and R Seifert ldquoMethanogenic capabilities of ANME-archaea deduced from 13C-labelling approachesrdquo Environmen-tal Microbiology vol 15 no 8 pp 2384ndash2393 2013

[24] K G Lloyd M J Alperin and A Teske ldquoEnvironmental evi-dence for net methane production and oxidation in putativeANaerobic MEthanotrophic (ANME) archaeardquo EnvironmentalMicrobiology vol 13 no 9 pp 2548ndash2564 2011

[25] M Takeuchi H Yoshioka Y Seo et al ldquoA distinct freshwater-adapted subgroup of ANME-1 dominates active archaeal com-munities in terrestrial subsurfaces in Japanrdquo EnvironmentalMicrobiology vol 13 no 12 pp 3206ndash3218 2011

[26] R T Amos B A Bekins I M Cozzarelli et al ldquoEvidence foriron-mediated anaerobic methane oxidation in a crude oil-contaminated aquiferrdquo Geobiology vol 10 no 6 pp 506ndash5172012

[27] P H Timmers D A Suarez-Zuluaga M van Rossem MDiender A J Stams and C M Plugge ldquoAnaerobic oxidationof methane associated with sulfate reduction in a naturalfreshwater gas sourcerdquo ISME Journal vol 10 pp 1400ndash14122015

[28] M F Haroon S Hu Y Shi et al ldquoAnaerobic oxidation ofmethane coupled to nitrate reduction in a novel archaeallineagerdquo Nature vol 500 no 7468 pp 567ndash570 2013

[29] H J Mills C Hodges K Wilson I R MacDonald and PA Sobecky ldquoMicrobial diversity in sediments associated withsurface-breaching gas hydrate mounds in the Gulf of MexicordquoFEMS Microbiology Ecology vol 46 no 1 pp 39ndash52 2003

[30] K G Lloyd L Lapham and A Teske ldquoAn anaerobic methane-oxidizing community of ANME-1b archaea in hypersaline gulfofMexico sedimentsrdquoApplied and EnvironmentalMicrobiologyvol 72 no 11 pp 7218ndash7230 2006

[31] A A Raghoebarsing A Pol K T Van De Pas-Schoonen et alldquoA microbial consortium couples anaerobic methane oxidationto denitrificationrdquoNature vol 440 no 7086 pp 918ndash921 2006

[32] S Hu R J Zeng L C Burow P Lant J Keller and Z YuanldquoEnrichment of denitrifying anaerobic methane oxidizingmicroorganismsrdquo Environmental Microbiology Reports vol 1no 5 pp 377ndash384 2009

[33] Z-W Ding J Ding L Fu F Zhang and R J Zeng ldquoSimultane-ous enrichment of denitrifying methanotrophs and anammoxbacteriardquo Applied Microbiology and Biotechnology vol 98 no24 pp 10211ndash10221 2014

[34] R Seifert K Nauhaus M Blumenberg M Kruger and WMichaelis ldquoMethane dynamics in a microbial community ofthe Black Sea traced by stable carbon isotopes in vitrordquoOrganicGeochemistry vol 37 no 10 pp 1411ndash1419 2006

[35] J Ding Z-W Ding L Fu Y-Z Lu S H Cheng and R JZeng ldquoNew primers for detecting and quantifying denitrifyinganaerobic methane oxidation archaea in different ecologicalnichesrdquo Applied Microbiology and Biotechnology vol 99 no 22pp 9805ndash9812 2015

[36] A Vaksmaa C Luke T van Alen et al ldquoDistribution and activ-ity of the anaerobic methanotrophic community in a nitrogen-fertilized Italian paddy soilrdquo FEMS Microbiology Ecology vol92 no 12 2016

[37] P N Evans D H Parks G L Chadwick et al ldquoMethanemetabolism in the archaeal phylum Bathyarchaeota revealed bygenome-centric metagenomicsrdquo Science vol 350 no 6259 pp434ndash438 2015

[38] I Vanwonterghem P N Evans D H Parks et al ldquoMethy-lotrophic methanogenesis discovered in the archaeal phylumVerstraetearchaeotardquo Nature Microbiology vol 1 Article ID16170 2016

[39] P Worm J J Koehorst M Visser et al ldquoA genomic view onsyntrophic versus non-syntrophic lifestyle in anaerobic fattyacid degrading communitiesrdquo Biochimica et Biophysica ActamdashBioenergetics vol 1837 no 12 pp 2004ndash2016 2014

[40] R Stokke I Roalkvam A Lanzen H Haflidason and I HSteen ldquoIntegrated metagenomic and metaproteomic analysesof an ANME-1-dominated community in marine cold seepsedimentsrdquo Environmental Microbiology vol 14 no 5 pp 1333ndash1346 2012

[41] A Meyerdierks M Kube I Kostadinov et al ldquoMetagenomeand mRNA expression analyses of anaerobic methanotrophicarchaea of the ANME-1 grouprdquo Environmental Microbiologyvol 12 no 2 pp 422ndash439 2010

[42] F-P Wang Y Zhang Y Chen et al ldquoMethanotrophicarchaea possessing diverging methane-oxidizing and electron-transporting pathwaysrdquo ISME Journal vol 8 no 5 pp 1069ndash1078 2014

[43] A Arshad D R Speth R M de Graaf H J Op den Camp MS Jetten and C U Welte ldquoA metagenomics-based metabolicmodel of nitrate-dependent anaerobic oxidation of methane byMethanoperedens-like archaeardquo Frontiers inMicrobiology vol 6article1423 2015

[44] S J Hallam N Putnam CM Preston et al ldquoReversemethano-genesis testing the hypothesis with environmental genomicsrdquoScience vol 305 no 5689 pp 1457ndash1462 2004

Archaea 19

[45] R K Thauer ldquoAnaerobic oxidation of methane with sulfate onthe reversibility of the reactions that are catalyzed by enzymesalso involved inmethanogenesis fromCO

2rdquoCurrent Opinion in

Microbiology vol 14 no 3 pp 292ndash299 2011[46] U Deppenmeier V Muller and G Gottschalk ldquoPathways of

energy conservation in methanogenic archaeardquo Archives ofMicrobiology vol 165 no 3 pp 149ndash163 1996

[47] A-K Kaster J Moll K Parey and R K Thauer ldquoCoupling offerredoxin and heterodisulfide reduction via electron bifurca-tion in hydrogenotrophic methanogenic archaeardquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 108 no 7 pp 2981ndash2986 2011

[48] R K Thauer A-K Kaster H Seedorf W Buckel and RHedderich ldquoMethanogenic archaea ecologically relevant dif-ferences in energy conservationrdquo Nature Reviews Microbiologyvol 6 no 8 pp 579ndash591 2008

[49] W Ludwig O Strunk R Westram et al ldquoARB a softwareenvironment for sequence datardquoNucleic Acids Research vol 32no 4 pp 1363ndash1371 2004

[50] E Pruesse C Quast K Knittel et al ldquoSILVA a comprehensiveonline resource for quality checked and aligned ribosomal RNAsequence data compatible with ARBrdquo Nucleic Acids Researchvol 35 no 21 pp 7188ndash7196 2007

[51] J J Marlow C T Skennerton Z Li et al ldquoProteomic stableisotope probing reveals biosynthesis dynamics of slow growingmethane based microbial communitiesrdquo Frontiers in Microbiol-ogy vol 7 article 386 2016

[52] P V Welander and W W Metcalf ldquoLoss of the mtr operon inMethanosarcina blocks growth on methanol but not methano-genesis and reveals an unknown methanogenic pathwayrdquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 102 no 30 pp 10664ndash10669 2005

[53] P V Welander and W W Metcalf ldquoMutagenesis of the C1oxidation pathway inmethanosarcina barkeri new insights intothe MtrMer bypass pathwayrdquo Journal of Bacteriology vol 190no 6 pp 1928ndash1936 2008

[54] M Goenrich R K Thauer H Yurimoto and N KatoldquoFormaldehyde activating enzyme (Fae) and hexulose-6-phosphate synthase (Hps) inMethanosarcina barkeri a possiblefunction in ribose-5-phosphate biosynthesisrdquoArchives ofMicro-biology vol 184 no 1 pp 41ndash48 2005

[55] M Goenrich FMahlert E C Duin C Bauer B Jaun and R KThauer ldquoProbing the reactivity of Ni in the active site of methyl-coenzyme M reductase with substrate analoguesrdquo Journal ofBiological Inorganic Chemistry vol 9 no 6 pp 691ndash705 2004

[56] S Scheller M Goenrich R Boecher R K Thauer and BJaun ldquoThe key nickel enzyme of methanogenesis catalyses theanaerobic oxidation of methanerdquo Nature vol 465 no 7298 pp606ndash608 2010

[57] K Nauhaus A Boetius M Kruger and F Widdel ldquoIn vitrodemonstration of anaerobic oxidation of methane coupled tosulphate reduction in sediment from amarine gas hydrate areardquoEnvironmental Microbiology vol 4 no 5 pp 296ndash305 2002

[58] Y Zhang J-P Henriet J Bursens and N Boon ldquoStimulationof in vitro anaerobic oxidation of methane rate in a continuoushigh-pressure bioreactorrdquo Bioresource Technology vol 101 no9 pp 3132ndash3138 2010

[59] M Kruger T Treude H Wolters K Nauhaus and A BoetiusldquoMicrobial methane turnover in different marine habitatsrdquoPalaeogeography Palaeoclimatology Palaeoecology vol 227 no1ndash3 pp 6ndash17 2005

[60] C Deusner V Meyer and T G Ferdelman ldquoHigh-pressuresystems for gas-phase free continuous incubation of enrichedmarinemicrobial communities performing anaerobic oxidationof methanerdquo Biotechnology and Bioengineering vol 105 no 3pp 524ndash533 2010

[61] K Nauhaus T Treude A Boetius and M Kruger ldquoEnviron-mental regulation of the anaerobic oxidation of methane acomparison of ANME-I and ANME-II communitiesrdquo Environ-mental Microbiology vol 7 no 1 pp 98ndash106 2005

[62] T Treude V Orphan K Knittel A Gieseke C H House andA Boetius ldquoConsumption of methane and CO

2by methan-

otrophicmicrobial mats from gas seeps of the anoxic Black SeardquoApplied and EnvironmentalMicrobiology vol 73 no 7 pp 2271ndash2283 2007

[63] T Holler F Widdel K Knittel et al ldquoThermophilic anaerobicoxidation of methane by marine microbial consortiardquo ISMEJournal vol 5 no 12 pp 1946ndash1956 2011

[64] M Kruger M Blumenberg S Kasten et al ldquoA novel multi-layered methanotrophic microbial mat system growing on thesediment of the Black Seardquo Environmental Microbiology vol 10no 8 pp 1934ndash1947 2008

[65] R J WMeulepas C G Jagersma J Gieteling C J N BuismanA J M Stams and P N L Lens ldquoEnrichment of anaerobicmethanotrophs in sulfate-reducing membrane bioreactorsrdquoBiotechnology and Bioengineering vol 104 no 3 pp 458ndash4702009

[66] T Holler G Wegener H Niemann et al ldquoCarbon and sulfurback flux during anaerobic microbial oxidation of methane andcoupled sulfate reductionrdquo Proceedings of the National Academyof Sciences of the United States of America vol 108 no 52 ppE1484ndashE1490 2011

[67] M Kruger AMeyerdierks F O Glockner et al ldquoA conspicuousnickel protein in microbial mats that oxidize methane anaero-bicallyrdquo Nature vol 426 no 6968 pp 878ndash881 2003

[68] S Mayr C Latkoczy M Kruger et al ldquoStructure of an F430

variant from archaea associated with anaerobic oxidation ofmethanerdquo Journal of the American Chemical Society vol 130 no32 pp 10758ndash10767 2008

[69] S Shima and R K Thauer ldquoMethyl-coenzyme M reductaseand the anaerobic oxidation of methane in methanotrophicArchaeardquo Current Opinion in Microbiology vol 8 no 6 pp643ndash648 2005

[70] R K Thauer and S Shima ldquoMethane as fuel for anaerobicmicroorganismsrdquo Annals of the New York Academy of Sciencesvol 1125 pp 158ndash170 2008

[71] S Yamamoto J B Alcauskas and T E Crozier ldquoSolubility ofmethane in distilled water and seawaterrdquo Journal of Chemicaland Engineering Data vol 21 no 1 pp 78ndash80 1976

[72] P H A Timmers J Gieteling H C A Widjaja-Greefkeset al ldquoGrowth of anaerobic methane-oxidizing archaea andsulfate-reducing bacteria in a high-pressure membrane capsulebioreactorrdquoApplied and EnvironmentalMicrobiology vol 81 no4 pp 1286ndash1296 2015

[73] MKruger HWoltersMGehre S B Joye andH-H RichnowldquoTracing the slow growth of anaerobic methane-oxidizingcommunities by 15N-labelling techniquesrdquo FEMS MicrobiologyEcology vol 63 no 3 pp 401ndash411 2008

[74] R J W Meulepas C G Jagersma A F Khadem C J N Buis-man A J M Stams and P N L Lens ldquoEffect of environmentalconditions on sulfate reduction withmethane as electron donorby an Eckernforde Bay enrichmentrdquo Environmental Science andTechnology vol 43 no 17 pp 6553ndash6559 2009

20 Archaea

[75] M W Bowles V A Samarkin and S B Joye ldquoImprovedmeasurement of microbial activity in deep-sea sediments atin situ pressure and methane concentrationrdquo Limnology andOceanography Methods vol 9 pp 499ndash506 2011

[76] S Shima M Krueger T Weinert et al ldquoStructure of a methyl-coenzyme M reductase from Black Sea mats that oxidizemethane anaerobicallyrdquo Nature vol 481 no 7379 pp 98ndash1012012

[77] K D Allen G Wegener and R H White ldquoDiscovery of multi-ple modified F-430 coenzymes in methanogens and anaerobicmethanotrophic archaea suggests possible new roles for F-430in naturerdquoApplied and Environmental Microbiology vol 80 no20 pp 6403ndash6412 2014

[78] V W Soo M J McAnulty A Tripathi et al ldquoReversingmethanogenesis to capture methane for liquid biofuel precur-sorsrdquoMicrobial Cell Factories vol 15 article 11 2016

[79] D L Valentine and W S Reeburgh ldquoNew perspectives onanaerobicmethane oxidationrdquoEnvironmentalMicrobiology vol2 no 5 pp 477ndash484 2000

[80] D L Valentine ldquoBiogeochemistry and microbial ecology ofmethane oxidation in anoxic environments a reviewrdquo Antonievan Leeuwenhoek International Journal of General and Molecu-lar Microbiology vol 81 no 1-4 pp 271ndash282 2002

[81] A J B Zehnder and T D Brock ldquoMethane formation andmethane oxidation by methanogenic bacteriardquo Journal of Bac-teriology vol 137 no 1 pp 420ndash432 1979

[82] J Harder ldquoAnaerobic methane oxidation by bacteria employ-ing 14C-methane uncontaminated with 14C-carbon monoxiderdquoMarine Geology vol 137 no 1-2 pp 13ndash23 1997

[83] J J Moran C H House K H Freeman and J G FerryldquoTrace methane oxidation studied in several Euryarchaeotaunder diverse conditionsrdquo Archaea vol 1 no 5 pp 303ndash3092005

[84] J J Moran C H House B Thomas and K H FreemanldquoProducts of tracemethane oxidation during nonmethyltrophicgrowth by Methanosarcinardquo Journal of Geophysical ResearchBiogeosciences vol 112 no 2 2007

[85] R J W Meulepas C G Jagersma Y Zhang et al ldquoTracemethane oxidation and the methane dependency of sulfatereduction in anaerobic granular sludgerdquo FEMS MicrobiologyEcology vol 72 no 2 pp 261ndash271 2010

[86] A J B Zehnder andTD Brock ldquoAnaerobicmethane oxidationoccurrence and ecologyrdquoApplied and Environmental Microbiol-ogy vol 39 no 1 pp 194ndash204 1980

[87] S J Blazewicz D G Petersen M P Waldrop and M K Fire-stone ldquoAnaerobic oxidation of methane in tropical and borealsoils ecological significance in terrestrial methane cyclingrdquoJournal of Geophysical Research Biogeosciences vol 117 no 2Article ID G02033 2012

[88] K A Smemo and J B Yavitt ldquoEvidence for anaerobic CH4

oxidation in freshwater peatlandsrdquo Geomicrobiology Journalvol 24 no 7-8 pp 583ndash597 2007

[89] M J Alperin and T M Hoehler ldquoAnaerobic methane oxidationby archaeasulfate-reducing bacteria aggregates 1 Thermody-namic and physical constraintsrdquo American Journal of Sciencevol 309 no 10 pp 869ndash957 2009

[90] S L Caldwell J R Laidler E A Brewer J O Eberly S CSandborgh and F S Colwell ldquoAnaerobic oxidation of methanemechanisms bioenergetics and the ecology of associatedmicroorganismsrdquo Environmental Science and Technology vol42 no 18 pp 6791ndash6799 2008

[91] GWang A J Spivack and S DrsquoHondt ldquoGibbs energies of reac-tion and microbial mutualism in anaerobic deep subseafloorsediments of ODP Site 1226rdquoGeochimica et Cosmochimica Actavol 74 no 14 pp 3938ndash3947 2010

[92] P R Girguis A E Cozen and E F DeLong ldquoGrowth andpopulation dynamics of anaerobic methane-oxidizing archaeaand sulfate-reducing bacteria in a continuous-flow bioreactorrdquoApplied and EnvironmentalMicrobiology vol 71 no 7 pp 3725ndash3733 2005

[93] K Nauhaus M Albrecht M Elvert A Boetius and F WiddelldquoIn vitro cell growth ofmarine archaeal-bacterial consortia dur-ing anaerobic oxidation ofmethanewith sulfaterdquoEnvironmentalMicrobiology vol 9 no 1 pp 187ndash196 2007

[94] B Orcutt V Samarkin A Boetius and S Joye ldquoOn the relation-ship between methane production and oxidation by anaerobicmethanotrophic communities from cold seeps of the Gulf ofMexicordquo Environmental Microbiology vol 10 no 5 pp 1108ndash1117 2008

[95] M Y Yoshinaga T Holler T Goldhammer et al ldquoCarbon iso-tope equilibration during sulphate-limited anaerobic oxidationof methanerdquo Nature Geoscience vol 7 no 3 pp 190ndash194 2014

[96] T Treude J Niggemann J Kallmeyer et al ldquoAnaerobic oxi-dation of methane and sulfate reduction along the Chileancontinental marginrdquo Geochimica et Cosmochimica Acta vol 69no 11 pp 2767ndash2779 2005

[97] R J Parkes B A Cragg N Banning et al ldquoBiogeochemistryand biodiversity of methane cycling in subsurface marinesediments (SkagerrakDenmark)rdquoEnvironmentalMicrobiologyvol 9 no 5 pp 1146ndash1161 2007

[98] N J Knab B A Cragg E R C Hornibrook et al ldquoRegulationof anaerobic methane oxidation in sediments of the Black SeardquoBiogeosciences vol 6 no 8 pp 1505ndash1518 2009

[99] H Yoshioka A Maruyama T Nakamura et al ldquoActivities anddistribution of methanogenic and methane-oxidizing microbesin marine sediments from the Cascadia Marginrdquo Geobiologyvol 8 no 3 pp 223ndash233 2010

[100] G Wegener V Krukenberg S E Ruff M Y Kellermann andK Knittel ldquoMetabolic capabilities of microorganisms involvedin and associated with the anaerobic oxidation of methanerdquoFrontiers in Microbiology vol 7 article 46 2016

[101] R J W Meulepas C G Jagersma A F Khadem A J MStams and P N L Lens ldquoEffect of methanogenic substrateson anaerobic oxidation of methane and sulfate reduction by ananaerobic methanotrophic enrichmentrdquo Applied Microbiologyand Biotechnology vol 87 no 4 pp 1499ndash1506 2010

[102] J Milucka T G Ferdelman L Polerecky et al ldquoZero-valentsulphur is a key intermediate in marine methane oxidationrdquoNature vol 491 no 7425 pp 541ndash546 2012

[103] W Michaelis R Seifert K Nauhaus et al ldquoMicrobial reefs inthe black sea fueled by anaerobic oxidation ofmethanerdquo Sciencevol 297 no 5583 pp 1013ndash1015 2002

[104] A Vigneron P Cruaud P Pignet et al ldquoArchaeal and anaerobicmethane oxidizer communities in the Sonora Margin coldseeps Guaymas Basin (Gulf of California)rdquo ISME Journal vol7 no 8 pp 1595ndash1608 2013

[105] M Alperin and T Hoehler ldquoThe ongoing mystery of sea-floormethanerdquo Science vol 329 no 5989 pp 288ndash289 2010

[106] B Orcutt and C Meile ldquoConstraints on mechanisms and ratesof anaerobic oxidation of methane by microbial consortiaprocess-basedmodeling of ANME-2 archaea and sulfate reduc-ing bacteria interactionsrdquo Biogeosciences vol 5 no 6 pp 1587ndash1599 2008

Archaea 21

[107] S E McGlynn G L Chadwick C P Kempes and V J OrphanldquoSingle cell activity reveals direct electron transfer in methan-otrophic consortiardquoNature vol 526 no 7574 pp 531ndash535 2015

[108] D R Lovley ldquoElectromicrobiologyrdquo Annual Review of Microbi-ology vol 66 pp 391ndash409 2012

[109] S M Strycharz-Glaven R M Snider A Guiseppi-Elie andL M Tender ldquoOn the electrical conductivity of microbialnanowires and biofilmsrdquoEnergy and Environmental Science vol4 no 11 pp 4366ndash4379 2011

[110] D J Richardson J N Butt J K Fredrickson et al ldquoThe lsquoporinndashcytochromersquo model for microbe-to-mineral electron transferrdquoMolecular Microbiology vol 85 no 2 pp 201ndash212 2012

[111] A Okamoto K Hashimoto and R Nakamura ldquoLong-rangeelectron conduction of Shewanella biofilms mediated by outermembrane C-type cytochromesrdquo Bioelectrochemistry vol 85pp 61ndash65 2012

[112] M Y El-Naggar G Wanger K M Leung et al ldquoElectricaltransport along bacterial nanowires from Shewanella oneidensisMR-1rdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 107 no 42 pp 18127ndash18131 2010

[113] G Reguera K D McCarthy T Mehta J S Nicoll M TTuominen and D R Lovley ldquoExtracellular electron transfer viamicrobial nanowiresrdquo Nature vol 435 no 7045 pp 1098ndash11012005

[114] Z M Summers H E Fogarty C Leang A E Franks N SMalvankar and D R Lovley ldquoDirect exchange of electronswithin aggregates of an evolved syntrophic coculture of anaer-obic bacteriardquo Science vol 330 no 6009 pp 1413ndash1415 2010

[115] A Kletzin T Heimerl J Flechsler L V Niftrik R Rachel andA Klingl ldquoCytochromes c in archaea distribution maturationcell architecture and the special case of Ignicoccus hospitalisrdquoFrontiers in Microbiology vol 6 article 439 2015

[116] GWegener V Krukenberg D Riedel H E Tegetmeyer and ABoetius ldquoIntercellular wiring enables electron transfer betweenmethanotrophic archaea and bacteriardquo Nature vol 526 no7574 pp 587ndash590 2015

[117] D HHaft S H Payne and J D Selengut ldquoArchaeosortases andexosortases are widely distributed systems linking membranetransit with posttranslational modificationrdquo Journal of Bacteri-ology vol 194 no 1 pp 36ndash48 2012

[118] A Marchler-Bauer M K Derbyshire N R Gonzales et alldquoCDD NCBIrsquos conserved domain databaserdquo Nucleic AcidsResearch vol 43 no 1 pp D222ndashD226 2015

[119] A Mitchell H-Y Chang L Daugherty et al ldquoThe InterProprotein families database the classification resource after 15yearsrdquo Nucleic Acids Research vol 43 no 1 pp D213ndashD2212015

[120] V Krukenberg K Harding M Richter et al ldquoCandidatusdesulfofervidus auxilii a hydrogenotrophic sulfate-reducingbacterium involved in the thermophilic anaerobic oxidation ofmethanerdquo Environmental Microbiology vol 18 pp 3073ndash30912016

[121] L Shi T C Squier J M Zachara and J K Fredrickson ldquoRes-piration of metal (hydr)oxides by Shewanella and Geobactera key role for multihaem c-type cytochromesrdquo MolecularMicrobiology vol 65 no 1 pp 12ndash20 2007

[122] N S Malvankar and D R Lovley ldquoMicrobial nanowires forbioenergy applicationsrdquo Current Opinion in Biotechnology vol27 pp 88ndash95 2014

[123] A-E Rotaru T LWoodard K PNevin andDR Lovley ldquoLinkbetween capacity for current production and syntrophic growth

in Geobacter speciesrdquo Frontiers in Microbiology vol 6 article744 2015

[124] A-E Rotaru P M Shrestha F Liu et al ldquoDirect interspecieselectron transfer between Geobacter metallireducens andMethanosarcina barkerirdquo Applied and Environmental Microbi-ology vol 80 no 15 pp 4599ndash4605 2014

[125] S Scheller H Yu G L Chadwick S E McGlynn and VJ Orphan ldquoArtificial electron acceptors decouple archaealmethane oxidation from sulfate reductionrdquo Science vol 351 no6274 pp 703ndash707 2016

[126] J Milucka F Widdel and S Shima ldquoImmunological detec-tion of enzymes for sulfate reduction in anaerobic methane-oxidizing consortiardquo Environmental Microbiology vol 15 no 5pp 1561ndash1571 2013

[127] P Cabello M D Roldan and C Moreno-Vivian ldquoNitratereduction and the nitrogen cycle in archaeardquoMicrobiology vol150 no 11 pp 3527ndash3546 2004

[128] R MMartinez-Espinosa E J Dridge M J Bonete et al ldquoLookon the positive sideThe orientation identification and bioener-getics of lsquoArchaealrsquomembrane-boundnitrate reductasesrdquoFEMSMicrobiology Letters vol 276 no 2 pp 129ndash139 2007

[129] S de VriesMMomcilovicM J F Strampraad J PWhiteleggeA Baghai and I Schroder ldquoAdaptation to a high-tungsten envi-ronment pyrobaculum aerophilum contains an active tungstennitrate reductaserdquo Biochemistry vol 49 no 45 pp 9911ndash99212010

[130] M Egger O Rasigraf C J Sapart et al ldquoIron-mediated anaer-obic oxidation of methane in brackish coastal sedimentsrdquoEnvironmental Science and Technology vol 49 no 1 pp 277ndash283 2015

[131] T Treude S Krause J Maltby A W Dale R Coffin and LJ Hamdan ldquoSulfate reduction and methane oxidation activitybelow the sulfate-methane transition zone in Alaskan BeaufortSea continental margin sediments implications for deep sulfurcyclingrdquo Geochimica et Cosmochimica Acta vol 144 pp 217ndash237 2014

[132] N Riedinger M J Formolo T W Lyons S Henkel A Beckand S Kasten ldquoAn inorganic geochemical argument for coupledanaerobic oxidation of methane and iron reduction in marinesedimentsrdquo Geobiology vol 12 no 2 pp 172ndash181 2014

[133] Y-H Chang T-W Cheng W-J Lai et al ldquoMicrobial methanecycling in a terrestrialmud volcano in eastern Taiwanrdquo Environ-mental Microbiology vol 14 no 4 pp 895ndash908 2012

[134] S A Crowe S Katsev K Leslie et al ldquoThe methane cycle inferruginous Lake Matanordquo Geobiology vol 9 no 1 pp 61ndash782011

[135] O Sivan M Adler A Pearson et al ldquoGeochemical evidence foriron-mediated anaerobic oxidation of methanerdquo Limnology andOceanography vol 56 no 4 pp 1536ndash1544 2011

[136] K E A Segarra C Comerford J Slaughter and S B JoyeldquoImpact of electron acceptor availability on the anaerobic oxi-dation of methane in coastal freshwater and brackish wetlandsedimentsrdquo Geochimica et Cosmochimica Acta vol 115 pp 15ndash30 2013

[137] V Gupta K A Smemo J B Yavitt D Fowle B Branfireunand N Basiliko ldquoStable isotopes reveal widespread anaerobicmethane oxidation across latitude and peatland typerdquo Environ-mental Science and Technology vol 47 no 15 pp 8273ndash82792013

[138] O Oni T Miyatake S Kasten et al ldquoDistinct microbialpopulations are tightly linked to the profile of dissolved iron in

22 Archaea

the methanic sediments of the Helgolandmud area North SeardquoFrontiers in Microbiology vol 6 2015

[139] E J Beal C H House and V J Orphan ldquoManganese- andiron-dependent marine methane oxidationrdquo Science vol 325no 5937 pp 184ndash187 2009

[140] M W Bowles V A Samarkin K M Bowles and S B JoyeldquoWeak coupling between sulfate reduction and the anaerobicoxidation of methane in methane-rich seafloor sedimentsduring ex situ incubationrdquo Geochimica et Cosmochimica Actavol 75 no 2 pp 500ndash519 2011

[141] Y Z Lu L Fu J Ding Z Ding N Li and R J Zeng ldquoCr(VI)reduction coupled with anaerobic oxidation of methane in alaboratory reactorrdquoWater Research vol 102 pp 445ndash452 2016

[142] K F Ettwig B Zhu D Speth J T Keltjens M S Jetten and BKartal ldquoArchaea catalyze iron-dependent anaerobic oxidationof methanerdquo Proceedings of the National Academy of Sciences ofthe United States of America vol 113 no 45 pp 12792ndash127962016

[143] T M Flynn R A Sanford H Ryu et al ldquoFunctional microbialdiversity explains groundwater chemistry in a pristine aquiferrdquoBMCMicrobiology vol 13 no 1 article no 146 2013

[144] C J Schubert F Vazquez T Losekann-Behrens K KnittelM Tonolla and A Boetius ldquoEvidence for anaerobic oxidationof methane in sediments of a freshwater system (Lago diCadagno)rdquo FEMS Microbiology Ecology vol 76 no 1 pp 26ndash38 2011

[145] K E A Segarra F Schubotz V Samarkin M Y Yoshinaga K-U Hinrichs and S B Joye ldquoHigh rates of anaerobic methaneoxidation in freshwater wetlands reduce potential atmosphericmethane emissionsrdquo Nature Communications vol 6 article7477 2015

[146] E J Beal M W Claire and C H House ldquoHigh rates ofanaerobic methanotrophy at low sulfate concentrations withimplications for past and present methane levelsrdquo Geobiologyvol 9 no 2 pp 131ndash139 2011

[147] F Kracke I Vassilev and J O Kromer ldquoMicrobial electrontransport and energy conservationmdashthe foundation for opti-mizing bioelectrochemical systemsrdquo Frontiers in Microbiologyvol 6 article 575 2015

[148] C L Reardon A C Dohnalkova P Nachimuthu et al ldquoRoleof outer-membrane cytochromes MtrC and OmcA in thebiomineralization of ferrihydrite by Shewanella oneidensisMR-1rdquo Geobiology vol 8 no 1 pp 56ndash68 2010

[149] L Shi B Chen Z Wang et al ldquoIsolation of a high-affinityfunctional protein complex between OmcA and MtrC twoouter membrane decaheme c-type cytochromes of Shewanellaoneidensis MR-1rdquo Journal of Bacteriology vol 188 no 13 pp4705ndash4714 2006

[150] X Qian T Mester L Morgado et al ldquoBiochemical charac-terization of purified OmcS a c-type cytochrome requiredfor insoluble Fe(III) reduction in Geobacter sulfurreducensrdquoBiochimica et BiophysicaActamdashBioenergetics vol 1807 no 4 pp404ndash412 2011

[151] T Mehta M V Coppi S E Childers and D R Lovley ldquoOutermembrane c-type cytochromes required for Fe(III) andMn(IV)oxide reduction in Geobacter sulfurreducensrdquo Applied andEnvironmentalMicrobiology vol 71 no 12 pp 8634ndash8641 2005

[152] W Blankenfeldt A P Kuzin T Skarina et al ldquoStructure andfunction of the phenazine biosynthetic protein PhzF fromPseudomonas fluorescensrdquoProceedings of theNational Academyof Sciences of the United States of America vol 101 no 47 pp16431ndash16436 2004

[153] J F Parsons F Song L Parsons K Calabrese E Eisensteinand J E Ladner ldquoStructure and function of the phenazinebiosynthesis protein PhzF fromPseudomonas fluorescens 2-79rdquoBiochemistry vol 43 no 39 pp 12427ndash12435 2004

[154] T Hiratsuka K Furihata J Ishikawa et al ldquoAn alternativemenaquinone biosynthetic pathway operating in microorgan-ismsrdquo Science vol 321 no 5896 pp 1670ndash1673 2008

[155] M Tietze A Beuchle I Lamla et al ldquoRedox potentials ofmethanophenazine and CoB-S-S-CoM factors involved inelectron transport in methanogenic archaeardquo ChemBioChemvol 4 no 4 pp 333ndash335 2003

[156] Q H Tran and G Unden ldquoChanges in the proton potentialand the cellular energetics of Escherichia coli during growth byaerobic and anaerobic respiration or by fermentationrdquoEuropeanJournal of Biochemistry vol 251 no 1-2 pp 538ndash543 1998

[157] I Callebaut D Gilges I Vigon and J-P Mornon ldquoHYR anextracellular module involved in cellular adhesion and relatedto the immunoglobulin-like foldrdquo Protein Science vol 9 no 7pp 1382ndash1390 2000

[158] H J Gilbert ldquoCellulosomes microbial nanomachines that dis-play plasticity in quaternary structurerdquoMolecular Microbiologyvol 63 no 6 pp 1568ndash1576 2007

[159] A Peer S P Smith E A Bayer R Lamed and I BorovokldquoNoncellulosomal cohesin- and dockerin-like modules in thethree domains of liferdquo FEMS Microbiology Letters vol 291 no1 pp 1ndash16 2009

[160] M Wagner ldquoMicrobiology conductive consortiardquo Nature vol526 no 7574 pp 513ndash514 2015

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

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The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

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Signal TransductionJournal of

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BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

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Advances in

Virolog y

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Nucleic AcidsJournal of

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Stem CellsInternational

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Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

16 Archaea

iron and insoluble ferrihydrite and birnessite minerals [142](Table 1 reactions (3) and (4)) ANME-2d could even possiblydonate electrons to a bacterial partner besides nitrate-richenvironments ANME-2d archaea have been found inwells ofan aquifer where sulfate and methane concentrations overlap[143] Moreover ANME-2d was the only clade detected insediments of a freshwater lake where S-AOM occurred [144]Sulfate concentrations in these studies were low but above1mM and thus higher than the lowest reported concen-trations for S-AOM to occur [145 146] Lastly sequencesof ANME-2d were relatively more abundant in freshwatersediments fed with methane and sulfate than in sedimentsfed with onlymethane or only sulfate and noN-AOMactivitywas detected when fed with nitrate and methane [27] Theseindications hold promise that direct experimental evidencefor sulfate-dependent AOM by ANME-2d could be found inthe future

TheANME-1 genome contains fewerMHCgene domainsas compared to ANME-2a and ANME-2d and some otherarchaea such as somemethylotrophicmethanogens (Table 2)and some members of the Archaeoglobales [115] The MHCsof ANME-1 also have a smaller heme count as compared toother ANME and some other archaea with the largest beingan octaheme cytochrome [107] Each hemewithin aMHChasits own redox potential and therefore structurally differentMHCs represent a large range of redox potentials that canbe used for bioenergetic electron transfer (reviewed in [147])For instance metal oxide reduction in Shewanella oneidensisMR-1 is catalyzed by a chain of a tetraheme (CymA) twodecaheme (MtrA and MtrB) and eventually extracellulardecaheme cytochromes OmcAMtrC that reduce the ironminerals [121 148 149] In Geobacter sulfurreducens ironmineral reduction seems to be catalyzed by the tetrahemecytochrome OmcE and hexaheme cytochrome OmcS trans-ferring electrons from the outer membrane to type IV pilithat transmit the electrons to iron minerals [121 150 151]Since ANME-1 lack MHCs of the correct size and lack genedomains for pili production [116] they seem unable to reduceminerals via both mechanisms present in Shewanella andGeobacter It can therefore be speculated that ANME-1 areless versatile in electron acceptor use and are not able toreduce solid metal oxides However DIET mechanisms arestill not well understood and the true differences betweenMHCs of different ANME types need to be investigated usingbiochemical methods This would allow uncovering the truecapabilities concerning DIET

34 Menaquinones and Methanophenazines ANME-2a en-coded a protein with a domain specific for PhzF which is anenzyme involved in phenazine biosynthesis in Pseudomonasfluorescens [152 153] The respective gene is not present in allmethanophenazine containing methanogens (in our genomecomparison only inM acetivorans andM formicica Table 2)so it is unclear whether this enzyme is really involved inmethanophenazine biosynthesis It is however likely thatANME-2a use methanophenazines in their respiratory chainsince gene domains for menaquinone biosynthesis wereabsent (Table 2) ldquoCa M nitroreducensrdquo probably uses

menaquinones as membrane-integral electron carrier sinceenvironmental genomes [28 43] encoded the futalosine(mqn) biosynthesis pathway as reported for Archaeoglobusfulgidus [154] (Table 2) Moreover ldquoCa M nitroreducensrdquoenrichment cultures showed absence of methanophenazines[43] ANME-1 also contained gene domains formenaquinonebiosynthesis via the futalosine (mqn) biosynthesis pathway(Table 2) Indications for a quinone biosynthesis pathwayin ANME-1 were previously found to be weak since onlysome of the Ubi homologues of the oxic ubiquinone biosyn-thesis pathway were detected [41] but the futalosine (mqn)biosynthesis pathway was overlooked in that particular anal-ysis Additionally ANME-1 have Fqo homologues similarto Archaeoglobus fulgidus [44] and expressed the catalyticsubunit FqoF [41] However since the phenazine biosynthesisdomain PhzF was also present in the ANME-1 genomes(Table 2) and Fpo and Fqo are homologues we cannotconclude on genomic information alone which redox shuttleis used by ANME-1 during AOM If ANME-1 would usemenaquinones this would have implications for subsequentelectron transfer to MHCs since methanophenazine (1198640 =minus165mV) [155] and menaquinone (1198640 = minus80mV) [156] havedifferent redox potentials

35 Cell Adhesion Some gene domains involved in cel-lular adhesion were more abundant in ANME than inmethanogens (Table 2) especially in ANME-2a and ANME-1that are known to form syntrophic interactions for electrontransfer during respiration These domains include HYR(IPR003410) and CARDB domains (IPR011635) that bothhave a direct role in cellular adhesion [157] (Table 2) Interest-ingly also domains related to the cellulosome of Clostridiumspecies termed dockerin and cohesin were highly abundantin both ANME-1 and ANME-2a as compared to ANME-2dand methanogens together with many carbohydrate bindingdomains (Table 2) In Clostridium species dockerin andcohesin form an anchor to the bacterial cell wall that containsa scaffold with cellulose-degrading enzymes and a carbohy-drate bindingmodule that binds cellulose altogether formingthe cellulosome [158] These domains have been found in alldomains of life irrespective of cellulose utilization but thefunction of such proteins outside of the cellulosome is notknown [159]Therefore dockerin cohesin and carbohydratebinding domains in ANME could hypothetically form aconstruct that binds to carbohydrates and could possibly havea function in cell-to-cell contact or MHC adhesion but thisneeds further investigation

4 Future Challenges

Advances in (meta)genomics transcriptomics and pro-teomics have produced the valuable metabolic blueprints ofdifferent ANMEwith hypotheses on how centralmetabolismelectron transport and energy conservation may functionFuture experiments are needed to biochemically demonstratethat these hypotheses are correct

The bottleneck for biochemical studies of ANME isthe lack of pure cultures due to the slow and syntrophic

Archaea 17

growth However the recent milestone discovery of directelectron transfer provides opportunities to grow ANMEas stated previously on electron accepting electrodes (ieanodes) [160] In this way pure or highly enriched culturesof different ANME without their respective syntrophic part-ner could be obtained and MHCs responsible for electricconduction could be biochemically characterized It seemsthat ANME-1 are limited by the size and abundance ofMHCs which could relate to differences in behavior onan anode The partner bacteria of ANME-1 and ANME-2could be investigated on an electron donating electrode (iecathode) with specific focus on the ability to produce pili (ienanowires) Also worth investigating is if besides ANME-2d ANME-2ab could also use insoluble electron acceptorsand if ANME-2d could donate electrons to a bacterialpartner

Another future challenge is to isolate and characterizeMcr from different ANME clades It needs to be investi-gated if Mcr abundance in ANME cells compensates forthe slow reverse activity or if modifications in the Mcrof ANME-1 also contribute to a better reverse activity ofMcr Moreover the effect of methane partial pressure onreaction rates and enzyme kinetics needs to be determined insitu

ANME-1 are potentially able to perform hydrogeno-trophic methanogenesis due to the presence of a hydrogenasein the genome Genetic indications of menaquinones aselectron carrier in ANME-1 and the various cellulosome andcell adhesion related gene domains in all ANME are alsotopics that could be explored further Methanogenic archaeaare likely not able to perform AOM but additional studieson TMO and more genetic modifications to stimulate AOMin methanogens could help in understanding the param-eters needed for AOM to occur Ultimately physiologicalunderstanding of ANME will help to explain the observedecological niche separation of different ANME clades and theoccurrence of ANMEwithout a bacterial partnerThis wouldgreatly enhance our knowledge of themethane cycle in anoxicenvironments

Competing Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors thank Stefanie Berger (RU Nijmegen) for criticalreading of the manuscript This research is supported bythe Soehngen Institute of Anaerobic Microbiology (SIAM)Gravitation grant (024002002) of the Netherlands Ministryof Education Culture and Science and the NetherlandsOrganisation for Scientific Research (NWO) Mike S MJetten was further supported by ERC AG 339880 Eco-MoMand Alfons J M Stams was supported by ERC AG 323009Novel Anaerobes

References

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[2] K-U Hinrichs J M Hayes S P Sylva P G Brewert andE F DeLong ldquoMethane-consuming archaebacteria in marinesedimentsrdquo Nature vol 398 no 6730 pp 802ndash805 1999

[3] V J Orphan C H House K-U Hinrichs K D McKeeganand E F DeLong ldquoMethane-consuming archaea revealed bydirectly coupled isotopic and phylogenetic analysisrdquo Sciencevol 293 no 5529 pp 484ndash487 2001

[4] K-U Hinrichs and A Boetius ldquoThe anaerobic oxidation ofmethane new insights in microbial ecology and biogeochem-istryrdquo inOceanMargin Systems GWefer D Billett D HebbelnB B Joslashrgensen M Schluter and T VanWeering Eds pp 457ndash477 Springer Berlin Germany 2002

[5] K Knittel T Losekann A Boetius R Kort and R AmannldquoDiversity and distribution of methanotrophic archaea at coldseepsrdquo Applied and Environmental Microbiology vol 71 no 1pp 467ndash479 2005

[6] K Knittel and A Boetius ldquoAnaerobic oxidation of methaneprogress with an unknown processrdquo Annual Review of Micro-biology vol 63 pp 311ndash334 2009

[7] V J Orphan K-U Hinrichs W Ussler III et al ldquoComparativeanalysis of methane-oxidizing archaea and sulfate-reducingbacteria in anoxic marine sedimentsrdquoApplied and Environmen-tal Microbiology vol 67 no 4 pp 1922ndash1934 2001

[8] T Losekann K Knittel T Nadalig et al ldquoDiversity andabundance of aerobic and anaerobic methane oxidizers atthe Haakon Mosby Mud Volcano Barents Seardquo Applied andEnvironmentalMicrobiology vol 73 no 10 pp 3348ndash3362 2007

[9] H Niemann T Losekann D De Beer et al ldquoNovel microbialcommunities of the Haakon Mosby mud volcano and their roleas amethane sinkrdquoNature vol 443 no 7113 pp 854ndash858 2006

[10] TNunouraHOida T Toki J Ashi K Takai andKHorikoshildquoQuantification of mcrA by quantitative fluorescent PCR insediments from methane seep of the Nankai Troughrdquo FEMSMicrobiology Ecology vol 57 no 1 pp 149ndash157 2006

[11] B Orcutt A Boetius M Elvert V Samarkin and S B JoyeldquoMolecular biogeochemistry of sulfate reduction methanogen-esis and the anaerobic oxidation of methane at Gulf of Mexicocold seepsrdquoGeochimica et Cosmochimica Acta vol 69 no 17 pp4267ndash4281 2005

[12] V J Orphan W Ussler III T H Naehr C H House K-U Hinrichs and C K Paull ldquoGeological geochemical andmicrobiological heterogeneity of the seafloor around methanevents in the Eel River Basin offshore Californiardquo ChemicalGeology vol 205 no 3-4 pp 265ndash289 2004

[13] M G Pachiadaki A Kallionaki A Dahlmann G J De Langeand K A Kormas ldquoDiversity and spatial distribution ofprokaryotic communities along a sediment vertical profile ofa deep-sea mud volcanordquo Microbial Ecology vol 62 no 3 pp655ndash668 2011

[14] I Roalkvam H Dahle Y Chen S L Joslashrgensen H Haflidasonand I H Steen ldquoFine-scale community structure analysis ofANME in Nyegga sediments with high and low methane fluxrdquoFrontiers in Microbiology vol 3 p 216 2012

[15] K Yanagawa M Sunamura M A Lever et al ldquoNiche separa-tion of methanotrophic archaea (ANME-1 and -2) in methane-seep sediments of the Eastern Japan Sea offshore JoetsurdquoGeomicrobiology Journal vol 28 no 2 pp 118ndash129 2011

18 Archaea

[16] A Pernthaler A E Dekas C T Brown S K Goffredi TEmbaye and V J Orphan ldquoDiverse syntrophic partnershipsfromdeep-seamethane vents revealed by direct cell capture andmetagenomicsrdquo Proceedings of the National Academy of Sciencesof the United States of America vol 105 no 19 pp 7052ndash70572008

[17] R Hatzenpichler S A Connon D Goudeau R R Malm-strom T Woyke and V J Orphan ldquoVisualizing in situtranslational activity for identifying and sorting slow-growingarchaealminusbacterial consortiardquo Proceedings of the NationalAcademy of Sciences vol 113 no 28 pp E4069ndashE4078 2016

[18] L Maignien R J Parkes B Cragg et al ldquoAnaerobic oxidationof methane in hypersaline cold seep sedimentsrdquo FEMS Micro-biology Ecology vol 83 no 1 pp 214ndash231 2013

[19] V J Orphan C H House K-U Hinrichs K D McKeeganand E F DeLong ldquoMultiple archaeal groups mediate methaneoxidation in anoxic cold seep sedimentsrdquo Proceedings of theNational Academy of Sciences of the United States of Americavol 99 no 11 pp 7663ndash7668 2002

[20] T TreudeM Kruger A Boetius and B B Joslashrgensen ldquoEnviron-mental control on anaerobic oxidation of methane in the gassysediments of Eckernforde Bay (German Baltic)rdquo Limnology andOceanography vol 50 no 6 pp 1771ndash1786 2005

[21] G C Jagersma R J W Meulepas I Heikamp-De Jong etal ldquoMicrobial diversity and community structure of a highlyactive anaerobic methane-oxidizing sulfate-reducing enrich-mentrdquo Environmental Microbiology vol 11 no 12 pp 3223ndash3232 2009

[22] M Blumenberg R Seifert J Reitner T Pape andWMichaelisldquoMembrane lipid patterns typify distinct anaerobic methan-otrophic consortiardquo Proceedings of the National Academy ofSciences of the United States of America vol 101 no 30 pp 11111ndash11116 2004

[23] S Bertram M Blumenberg W Michaelis M Siegert MKruger and R Seifert ldquoMethanogenic capabilities of ANME-archaea deduced from 13C-labelling approachesrdquo Environmen-tal Microbiology vol 15 no 8 pp 2384ndash2393 2013

[24] K G Lloyd M J Alperin and A Teske ldquoEnvironmental evi-dence for net methane production and oxidation in putativeANaerobic MEthanotrophic (ANME) archaeardquo EnvironmentalMicrobiology vol 13 no 9 pp 2548ndash2564 2011

[25] M Takeuchi H Yoshioka Y Seo et al ldquoA distinct freshwater-adapted subgroup of ANME-1 dominates active archaeal com-munities in terrestrial subsurfaces in Japanrdquo EnvironmentalMicrobiology vol 13 no 12 pp 3206ndash3218 2011

[26] R T Amos B A Bekins I M Cozzarelli et al ldquoEvidence foriron-mediated anaerobic methane oxidation in a crude oil-contaminated aquiferrdquo Geobiology vol 10 no 6 pp 506ndash5172012

[27] P H Timmers D A Suarez-Zuluaga M van Rossem MDiender A J Stams and C M Plugge ldquoAnaerobic oxidationof methane associated with sulfate reduction in a naturalfreshwater gas sourcerdquo ISME Journal vol 10 pp 1400ndash14122015

[28] M F Haroon S Hu Y Shi et al ldquoAnaerobic oxidation ofmethane coupled to nitrate reduction in a novel archaeallineagerdquo Nature vol 500 no 7468 pp 567ndash570 2013

[29] H J Mills C Hodges K Wilson I R MacDonald and PA Sobecky ldquoMicrobial diversity in sediments associated withsurface-breaching gas hydrate mounds in the Gulf of MexicordquoFEMS Microbiology Ecology vol 46 no 1 pp 39ndash52 2003

[30] K G Lloyd L Lapham and A Teske ldquoAn anaerobic methane-oxidizing community of ANME-1b archaea in hypersaline gulfofMexico sedimentsrdquoApplied and EnvironmentalMicrobiologyvol 72 no 11 pp 7218ndash7230 2006

[31] A A Raghoebarsing A Pol K T Van De Pas-Schoonen et alldquoA microbial consortium couples anaerobic methane oxidationto denitrificationrdquoNature vol 440 no 7086 pp 918ndash921 2006

[32] S Hu R J Zeng L C Burow P Lant J Keller and Z YuanldquoEnrichment of denitrifying anaerobic methane oxidizingmicroorganismsrdquo Environmental Microbiology Reports vol 1no 5 pp 377ndash384 2009

[33] Z-W Ding J Ding L Fu F Zhang and R J Zeng ldquoSimultane-ous enrichment of denitrifying methanotrophs and anammoxbacteriardquo Applied Microbiology and Biotechnology vol 98 no24 pp 10211ndash10221 2014

[34] R Seifert K Nauhaus M Blumenberg M Kruger and WMichaelis ldquoMethane dynamics in a microbial community ofthe Black Sea traced by stable carbon isotopes in vitrordquoOrganicGeochemistry vol 37 no 10 pp 1411ndash1419 2006

[35] J Ding Z-W Ding L Fu Y-Z Lu S H Cheng and R JZeng ldquoNew primers for detecting and quantifying denitrifyinganaerobic methane oxidation archaea in different ecologicalnichesrdquo Applied Microbiology and Biotechnology vol 99 no 22pp 9805ndash9812 2015

[36] A Vaksmaa C Luke T van Alen et al ldquoDistribution and activ-ity of the anaerobic methanotrophic community in a nitrogen-fertilized Italian paddy soilrdquo FEMS Microbiology Ecology vol92 no 12 2016

[37] P N Evans D H Parks G L Chadwick et al ldquoMethanemetabolism in the archaeal phylum Bathyarchaeota revealed bygenome-centric metagenomicsrdquo Science vol 350 no 6259 pp434ndash438 2015

[38] I Vanwonterghem P N Evans D H Parks et al ldquoMethy-lotrophic methanogenesis discovered in the archaeal phylumVerstraetearchaeotardquo Nature Microbiology vol 1 Article ID16170 2016

[39] P Worm J J Koehorst M Visser et al ldquoA genomic view onsyntrophic versus non-syntrophic lifestyle in anaerobic fattyacid degrading communitiesrdquo Biochimica et Biophysica ActamdashBioenergetics vol 1837 no 12 pp 2004ndash2016 2014

[40] R Stokke I Roalkvam A Lanzen H Haflidason and I HSteen ldquoIntegrated metagenomic and metaproteomic analysesof an ANME-1-dominated community in marine cold seepsedimentsrdquo Environmental Microbiology vol 14 no 5 pp 1333ndash1346 2012

[41] A Meyerdierks M Kube I Kostadinov et al ldquoMetagenomeand mRNA expression analyses of anaerobic methanotrophicarchaea of the ANME-1 grouprdquo Environmental Microbiologyvol 12 no 2 pp 422ndash439 2010

[42] F-P Wang Y Zhang Y Chen et al ldquoMethanotrophicarchaea possessing diverging methane-oxidizing and electron-transporting pathwaysrdquo ISME Journal vol 8 no 5 pp 1069ndash1078 2014

[43] A Arshad D R Speth R M de Graaf H J Op den Camp MS Jetten and C U Welte ldquoA metagenomics-based metabolicmodel of nitrate-dependent anaerobic oxidation of methane byMethanoperedens-like archaeardquo Frontiers inMicrobiology vol 6article1423 2015

[44] S J Hallam N Putnam CM Preston et al ldquoReversemethano-genesis testing the hypothesis with environmental genomicsrdquoScience vol 305 no 5689 pp 1457ndash1462 2004

Archaea 19

[45] R K Thauer ldquoAnaerobic oxidation of methane with sulfate onthe reversibility of the reactions that are catalyzed by enzymesalso involved inmethanogenesis fromCO

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Microbiology vol 14 no 3 pp 292ndash299 2011[46] U Deppenmeier V Muller and G Gottschalk ldquoPathways of

energy conservation in methanogenic archaeardquo Archives ofMicrobiology vol 165 no 3 pp 149ndash163 1996

[47] A-K Kaster J Moll K Parey and R K Thauer ldquoCoupling offerredoxin and heterodisulfide reduction via electron bifurca-tion in hydrogenotrophic methanogenic archaeardquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 108 no 7 pp 2981ndash2986 2011

[48] R K Thauer A-K Kaster H Seedorf W Buckel and RHedderich ldquoMethanogenic archaea ecologically relevant dif-ferences in energy conservationrdquo Nature Reviews Microbiologyvol 6 no 8 pp 579ndash591 2008

[49] W Ludwig O Strunk R Westram et al ldquoARB a softwareenvironment for sequence datardquoNucleic Acids Research vol 32no 4 pp 1363ndash1371 2004

[50] E Pruesse C Quast K Knittel et al ldquoSILVA a comprehensiveonline resource for quality checked and aligned ribosomal RNAsequence data compatible with ARBrdquo Nucleic Acids Researchvol 35 no 21 pp 7188ndash7196 2007

[51] J J Marlow C T Skennerton Z Li et al ldquoProteomic stableisotope probing reveals biosynthesis dynamics of slow growingmethane based microbial communitiesrdquo Frontiers in Microbiol-ogy vol 7 article 386 2016

[52] P V Welander and W W Metcalf ldquoLoss of the mtr operon inMethanosarcina blocks growth on methanol but not methano-genesis and reveals an unknown methanogenic pathwayrdquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 102 no 30 pp 10664ndash10669 2005

[53] P V Welander and W W Metcalf ldquoMutagenesis of the C1oxidation pathway inmethanosarcina barkeri new insights intothe MtrMer bypass pathwayrdquo Journal of Bacteriology vol 190no 6 pp 1928ndash1936 2008

[54] M Goenrich R K Thauer H Yurimoto and N KatoldquoFormaldehyde activating enzyme (Fae) and hexulose-6-phosphate synthase (Hps) inMethanosarcina barkeri a possiblefunction in ribose-5-phosphate biosynthesisrdquoArchives ofMicro-biology vol 184 no 1 pp 41ndash48 2005

[55] M Goenrich FMahlert E C Duin C Bauer B Jaun and R KThauer ldquoProbing the reactivity of Ni in the active site of methyl-coenzyme M reductase with substrate analoguesrdquo Journal ofBiological Inorganic Chemistry vol 9 no 6 pp 691ndash705 2004

[56] S Scheller M Goenrich R Boecher R K Thauer and BJaun ldquoThe key nickel enzyme of methanogenesis catalyses theanaerobic oxidation of methanerdquo Nature vol 465 no 7298 pp606ndash608 2010

[57] K Nauhaus A Boetius M Kruger and F Widdel ldquoIn vitrodemonstration of anaerobic oxidation of methane coupled tosulphate reduction in sediment from amarine gas hydrate areardquoEnvironmental Microbiology vol 4 no 5 pp 296ndash305 2002

[58] Y Zhang J-P Henriet J Bursens and N Boon ldquoStimulationof in vitro anaerobic oxidation of methane rate in a continuoushigh-pressure bioreactorrdquo Bioresource Technology vol 101 no9 pp 3132ndash3138 2010

[59] M Kruger T Treude H Wolters K Nauhaus and A BoetiusldquoMicrobial methane turnover in different marine habitatsrdquoPalaeogeography Palaeoclimatology Palaeoecology vol 227 no1ndash3 pp 6ndash17 2005

[60] C Deusner V Meyer and T G Ferdelman ldquoHigh-pressuresystems for gas-phase free continuous incubation of enrichedmarinemicrobial communities performing anaerobic oxidationof methanerdquo Biotechnology and Bioengineering vol 105 no 3pp 524ndash533 2010

[61] K Nauhaus T Treude A Boetius and M Kruger ldquoEnviron-mental regulation of the anaerobic oxidation of methane acomparison of ANME-I and ANME-II communitiesrdquo Environ-mental Microbiology vol 7 no 1 pp 98ndash106 2005

[62] T Treude V Orphan K Knittel A Gieseke C H House andA Boetius ldquoConsumption of methane and CO

2by methan-

otrophicmicrobial mats from gas seeps of the anoxic Black SeardquoApplied and EnvironmentalMicrobiology vol 73 no 7 pp 2271ndash2283 2007

[63] T Holler F Widdel K Knittel et al ldquoThermophilic anaerobicoxidation of methane by marine microbial consortiardquo ISMEJournal vol 5 no 12 pp 1946ndash1956 2011

[64] M Kruger M Blumenberg S Kasten et al ldquoA novel multi-layered methanotrophic microbial mat system growing on thesediment of the Black Seardquo Environmental Microbiology vol 10no 8 pp 1934ndash1947 2008

[65] R J WMeulepas C G Jagersma J Gieteling C J N BuismanA J M Stams and P N L Lens ldquoEnrichment of anaerobicmethanotrophs in sulfate-reducing membrane bioreactorsrdquoBiotechnology and Bioengineering vol 104 no 3 pp 458ndash4702009

[66] T Holler G Wegener H Niemann et al ldquoCarbon and sulfurback flux during anaerobic microbial oxidation of methane andcoupled sulfate reductionrdquo Proceedings of the National Academyof Sciences of the United States of America vol 108 no 52 ppE1484ndashE1490 2011

[67] M Kruger AMeyerdierks F O Glockner et al ldquoA conspicuousnickel protein in microbial mats that oxidize methane anaero-bicallyrdquo Nature vol 426 no 6968 pp 878ndash881 2003

[68] S Mayr C Latkoczy M Kruger et al ldquoStructure of an F430

variant from archaea associated with anaerobic oxidation ofmethanerdquo Journal of the American Chemical Society vol 130 no32 pp 10758ndash10767 2008

[69] S Shima and R K Thauer ldquoMethyl-coenzyme M reductaseand the anaerobic oxidation of methane in methanotrophicArchaeardquo Current Opinion in Microbiology vol 8 no 6 pp643ndash648 2005

[70] R K Thauer and S Shima ldquoMethane as fuel for anaerobicmicroorganismsrdquo Annals of the New York Academy of Sciencesvol 1125 pp 158ndash170 2008

[71] S Yamamoto J B Alcauskas and T E Crozier ldquoSolubility ofmethane in distilled water and seawaterrdquo Journal of Chemicaland Engineering Data vol 21 no 1 pp 78ndash80 1976

[72] P H A Timmers J Gieteling H C A Widjaja-Greefkeset al ldquoGrowth of anaerobic methane-oxidizing archaea andsulfate-reducing bacteria in a high-pressure membrane capsulebioreactorrdquoApplied and EnvironmentalMicrobiology vol 81 no4 pp 1286ndash1296 2015

[73] MKruger HWoltersMGehre S B Joye andH-H RichnowldquoTracing the slow growth of anaerobic methane-oxidizingcommunities by 15N-labelling techniquesrdquo FEMS MicrobiologyEcology vol 63 no 3 pp 401ndash411 2008

[74] R J W Meulepas C G Jagersma A F Khadem C J N Buis-man A J M Stams and P N L Lens ldquoEffect of environmentalconditions on sulfate reduction withmethane as electron donorby an Eckernforde Bay enrichmentrdquo Environmental Science andTechnology vol 43 no 17 pp 6553ndash6559 2009

20 Archaea

[75] M W Bowles V A Samarkin and S B Joye ldquoImprovedmeasurement of microbial activity in deep-sea sediments atin situ pressure and methane concentrationrdquo Limnology andOceanography Methods vol 9 pp 499ndash506 2011

[76] S Shima M Krueger T Weinert et al ldquoStructure of a methyl-coenzyme M reductase from Black Sea mats that oxidizemethane anaerobicallyrdquo Nature vol 481 no 7379 pp 98ndash1012012

[77] K D Allen G Wegener and R H White ldquoDiscovery of multi-ple modified F-430 coenzymes in methanogens and anaerobicmethanotrophic archaea suggests possible new roles for F-430in naturerdquoApplied and Environmental Microbiology vol 80 no20 pp 6403ndash6412 2014

[78] V W Soo M J McAnulty A Tripathi et al ldquoReversingmethanogenesis to capture methane for liquid biofuel precur-sorsrdquoMicrobial Cell Factories vol 15 article 11 2016

[79] D L Valentine and W S Reeburgh ldquoNew perspectives onanaerobicmethane oxidationrdquoEnvironmentalMicrobiology vol2 no 5 pp 477ndash484 2000

[80] D L Valentine ldquoBiogeochemistry and microbial ecology ofmethane oxidation in anoxic environments a reviewrdquo Antonievan Leeuwenhoek International Journal of General and Molecu-lar Microbiology vol 81 no 1-4 pp 271ndash282 2002

[81] A J B Zehnder and T D Brock ldquoMethane formation andmethane oxidation by methanogenic bacteriardquo Journal of Bac-teriology vol 137 no 1 pp 420ndash432 1979

[82] J Harder ldquoAnaerobic methane oxidation by bacteria employ-ing 14C-methane uncontaminated with 14C-carbon monoxiderdquoMarine Geology vol 137 no 1-2 pp 13ndash23 1997

[83] J J Moran C H House K H Freeman and J G FerryldquoTrace methane oxidation studied in several Euryarchaeotaunder diverse conditionsrdquo Archaea vol 1 no 5 pp 303ndash3092005

[84] J J Moran C H House B Thomas and K H FreemanldquoProducts of tracemethane oxidation during nonmethyltrophicgrowth by Methanosarcinardquo Journal of Geophysical ResearchBiogeosciences vol 112 no 2 2007

[85] R J W Meulepas C G Jagersma Y Zhang et al ldquoTracemethane oxidation and the methane dependency of sulfatereduction in anaerobic granular sludgerdquo FEMS MicrobiologyEcology vol 72 no 2 pp 261ndash271 2010

[86] A J B Zehnder andTD Brock ldquoAnaerobicmethane oxidationoccurrence and ecologyrdquoApplied and Environmental Microbiol-ogy vol 39 no 1 pp 194ndash204 1980

[87] S J Blazewicz D G Petersen M P Waldrop and M K Fire-stone ldquoAnaerobic oxidation of methane in tropical and borealsoils ecological significance in terrestrial methane cyclingrdquoJournal of Geophysical Research Biogeosciences vol 117 no 2Article ID G02033 2012

[88] K A Smemo and J B Yavitt ldquoEvidence for anaerobic CH4

oxidation in freshwater peatlandsrdquo Geomicrobiology Journalvol 24 no 7-8 pp 583ndash597 2007

[89] M J Alperin and T M Hoehler ldquoAnaerobic methane oxidationby archaeasulfate-reducing bacteria aggregates 1 Thermody-namic and physical constraintsrdquo American Journal of Sciencevol 309 no 10 pp 869ndash957 2009

[90] S L Caldwell J R Laidler E A Brewer J O Eberly S CSandborgh and F S Colwell ldquoAnaerobic oxidation of methanemechanisms bioenergetics and the ecology of associatedmicroorganismsrdquo Environmental Science and Technology vol42 no 18 pp 6791ndash6799 2008

[91] GWang A J Spivack and S DrsquoHondt ldquoGibbs energies of reac-tion and microbial mutualism in anaerobic deep subseafloorsediments of ODP Site 1226rdquoGeochimica et Cosmochimica Actavol 74 no 14 pp 3938ndash3947 2010

[92] P R Girguis A E Cozen and E F DeLong ldquoGrowth andpopulation dynamics of anaerobic methane-oxidizing archaeaand sulfate-reducing bacteria in a continuous-flow bioreactorrdquoApplied and EnvironmentalMicrobiology vol 71 no 7 pp 3725ndash3733 2005

[93] K Nauhaus M Albrecht M Elvert A Boetius and F WiddelldquoIn vitro cell growth ofmarine archaeal-bacterial consortia dur-ing anaerobic oxidation ofmethanewith sulfaterdquoEnvironmentalMicrobiology vol 9 no 1 pp 187ndash196 2007

[94] B Orcutt V Samarkin A Boetius and S Joye ldquoOn the relation-ship between methane production and oxidation by anaerobicmethanotrophic communities from cold seeps of the Gulf ofMexicordquo Environmental Microbiology vol 10 no 5 pp 1108ndash1117 2008

[95] M Y Yoshinaga T Holler T Goldhammer et al ldquoCarbon iso-tope equilibration during sulphate-limited anaerobic oxidationof methanerdquo Nature Geoscience vol 7 no 3 pp 190ndash194 2014

[96] T Treude J Niggemann J Kallmeyer et al ldquoAnaerobic oxi-dation of methane and sulfate reduction along the Chileancontinental marginrdquo Geochimica et Cosmochimica Acta vol 69no 11 pp 2767ndash2779 2005

[97] R J Parkes B A Cragg N Banning et al ldquoBiogeochemistryand biodiversity of methane cycling in subsurface marinesediments (SkagerrakDenmark)rdquoEnvironmentalMicrobiologyvol 9 no 5 pp 1146ndash1161 2007

[98] N J Knab B A Cragg E R C Hornibrook et al ldquoRegulationof anaerobic methane oxidation in sediments of the Black SeardquoBiogeosciences vol 6 no 8 pp 1505ndash1518 2009

[99] H Yoshioka A Maruyama T Nakamura et al ldquoActivities anddistribution of methanogenic and methane-oxidizing microbesin marine sediments from the Cascadia Marginrdquo Geobiologyvol 8 no 3 pp 223ndash233 2010

[100] G Wegener V Krukenberg S E Ruff M Y Kellermann andK Knittel ldquoMetabolic capabilities of microorganisms involvedin and associated with the anaerobic oxidation of methanerdquoFrontiers in Microbiology vol 7 article 46 2016

[101] R J W Meulepas C G Jagersma A F Khadem A J MStams and P N L Lens ldquoEffect of methanogenic substrateson anaerobic oxidation of methane and sulfate reduction by ananaerobic methanotrophic enrichmentrdquo Applied Microbiologyand Biotechnology vol 87 no 4 pp 1499ndash1506 2010

[102] J Milucka T G Ferdelman L Polerecky et al ldquoZero-valentsulphur is a key intermediate in marine methane oxidationrdquoNature vol 491 no 7425 pp 541ndash546 2012

[103] W Michaelis R Seifert K Nauhaus et al ldquoMicrobial reefs inthe black sea fueled by anaerobic oxidation ofmethanerdquo Sciencevol 297 no 5583 pp 1013ndash1015 2002

[104] A Vigneron P Cruaud P Pignet et al ldquoArchaeal and anaerobicmethane oxidizer communities in the Sonora Margin coldseeps Guaymas Basin (Gulf of California)rdquo ISME Journal vol7 no 8 pp 1595ndash1608 2013

[105] M Alperin and T Hoehler ldquoThe ongoing mystery of sea-floormethanerdquo Science vol 329 no 5989 pp 288ndash289 2010

[106] B Orcutt and C Meile ldquoConstraints on mechanisms and ratesof anaerobic oxidation of methane by microbial consortiaprocess-basedmodeling of ANME-2 archaea and sulfate reduc-ing bacteria interactionsrdquo Biogeosciences vol 5 no 6 pp 1587ndash1599 2008

Archaea 21

[107] S E McGlynn G L Chadwick C P Kempes and V J OrphanldquoSingle cell activity reveals direct electron transfer in methan-otrophic consortiardquoNature vol 526 no 7574 pp 531ndash535 2015

[108] D R Lovley ldquoElectromicrobiologyrdquo Annual Review of Microbi-ology vol 66 pp 391ndash409 2012

[109] S M Strycharz-Glaven R M Snider A Guiseppi-Elie andL M Tender ldquoOn the electrical conductivity of microbialnanowires and biofilmsrdquoEnergy and Environmental Science vol4 no 11 pp 4366ndash4379 2011

[110] D J Richardson J N Butt J K Fredrickson et al ldquoThe lsquoporinndashcytochromersquo model for microbe-to-mineral electron transferrdquoMolecular Microbiology vol 85 no 2 pp 201ndash212 2012

[111] A Okamoto K Hashimoto and R Nakamura ldquoLong-rangeelectron conduction of Shewanella biofilms mediated by outermembrane C-type cytochromesrdquo Bioelectrochemistry vol 85pp 61ndash65 2012

[112] M Y El-Naggar G Wanger K M Leung et al ldquoElectricaltransport along bacterial nanowires from Shewanella oneidensisMR-1rdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 107 no 42 pp 18127ndash18131 2010

[113] G Reguera K D McCarthy T Mehta J S Nicoll M TTuominen and D R Lovley ldquoExtracellular electron transfer viamicrobial nanowiresrdquo Nature vol 435 no 7045 pp 1098ndash11012005

[114] Z M Summers H E Fogarty C Leang A E Franks N SMalvankar and D R Lovley ldquoDirect exchange of electronswithin aggregates of an evolved syntrophic coculture of anaer-obic bacteriardquo Science vol 330 no 6009 pp 1413ndash1415 2010

[115] A Kletzin T Heimerl J Flechsler L V Niftrik R Rachel andA Klingl ldquoCytochromes c in archaea distribution maturationcell architecture and the special case of Ignicoccus hospitalisrdquoFrontiers in Microbiology vol 6 article 439 2015

[116] GWegener V Krukenberg D Riedel H E Tegetmeyer and ABoetius ldquoIntercellular wiring enables electron transfer betweenmethanotrophic archaea and bacteriardquo Nature vol 526 no7574 pp 587ndash590 2015

[117] D HHaft S H Payne and J D Selengut ldquoArchaeosortases andexosortases are widely distributed systems linking membranetransit with posttranslational modificationrdquo Journal of Bacteri-ology vol 194 no 1 pp 36ndash48 2012

[118] A Marchler-Bauer M K Derbyshire N R Gonzales et alldquoCDD NCBIrsquos conserved domain databaserdquo Nucleic AcidsResearch vol 43 no 1 pp D222ndashD226 2015

[119] A Mitchell H-Y Chang L Daugherty et al ldquoThe InterProprotein families database the classification resource after 15yearsrdquo Nucleic Acids Research vol 43 no 1 pp D213ndashD2212015

[120] V Krukenberg K Harding M Richter et al ldquoCandidatusdesulfofervidus auxilii a hydrogenotrophic sulfate-reducingbacterium involved in the thermophilic anaerobic oxidation ofmethanerdquo Environmental Microbiology vol 18 pp 3073ndash30912016

[121] L Shi T C Squier J M Zachara and J K Fredrickson ldquoRes-piration of metal (hydr)oxides by Shewanella and Geobactera key role for multihaem c-type cytochromesrdquo MolecularMicrobiology vol 65 no 1 pp 12ndash20 2007

[122] N S Malvankar and D R Lovley ldquoMicrobial nanowires forbioenergy applicationsrdquo Current Opinion in Biotechnology vol27 pp 88ndash95 2014

[123] A-E Rotaru T LWoodard K PNevin andDR Lovley ldquoLinkbetween capacity for current production and syntrophic growth

in Geobacter speciesrdquo Frontiers in Microbiology vol 6 article744 2015

[124] A-E Rotaru P M Shrestha F Liu et al ldquoDirect interspecieselectron transfer between Geobacter metallireducens andMethanosarcina barkerirdquo Applied and Environmental Microbi-ology vol 80 no 15 pp 4599ndash4605 2014

[125] S Scheller H Yu G L Chadwick S E McGlynn and VJ Orphan ldquoArtificial electron acceptors decouple archaealmethane oxidation from sulfate reductionrdquo Science vol 351 no6274 pp 703ndash707 2016

[126] J Milucka F Widdel and S Shima ldquoImmunological detec-tion of enzymes for sulfate reduction in anaerobic methane-oxidizing consortiardquo Environmental Microbiology vol 15 no 5pp 1561ndash1571 2013

[127] P Cabello M D Roldan and C Moreno-Vivian ldquoNitratereduction and the nitrogen cycle in archaeardquoMicrobiology vol150 no 11 pp 3527ndash3546 2004

[128] R MMartinez-Espinosa E J Dridge M J Bonete et al ldquoLookon the positive sideThe orientation identification and bioener-getics of lsquoArchaealrsquomembrane-boundnitrate reductasesrdquoFEMSMicrobiology Letters vol 276 no 2 pp 129ndash139 2007

[129] S de VriesMMomcilovicM J F Strampraad J PWhiteleggeA Baghai and I Schroder ldquoAdaptation to a high-tungsten envi-ronment pyrobaculum aerophilum contains an active tungstennitrate reductaserdquo Biochemistry vol 49 no 45 pp 9911ndash99212010

[130] M Egger O Rasigraf C J Sapart et al ldquoIron-mediated anaer-obic oxidation of methane in brackish coastal sedimentsrdquoEnvironmental Science and Technology vol 49 no 1 pp 277ndash283 2015

[131] T Treude S Krause J Maltby A W Dale R Coffin and LJ Hamdan ldquoSulfate reduction and methane oxidation activitybelow the sulfate-methane transition zone in Alaskan BeaufortSea continental margin sediments implications for deep sulfurcyclingrdquo Geochimica et Cosmochimica Acta vol 144 pp 217ndash237 2014

[132] N Riedinger M J Formolo T W Lyons S Henkel A Beckand S Kasten ldquoAn inorganic geochemical argument for coupledanaerobic oxidation of methane and iron reduction in marinesedimentsrdquo Geobiology vol 12 no 2 pp 172ndash181 2014

[133] Y-H Chang T-W Cheng W-J Lai et al ldquoMicrobial methanecycling in a terrestrialmud volcano in eastern Taiwanrdquo Environ-mental Microbiology vol 14 no 4 pp 895ndash908 2012

[134] S A Crowe S Katsev K Leslie et al ldquoThe methane cycle inferruginous Lake Matanordquo Geobiology vol 9 no 1 pp 61ndash782011

[135] O Sivan M Adler A Pearson et al ldquoGeochemical evidence foriron-mediated anaerobic oxidation of methanerdquo Limnology andOceanography vol 56 no 4 pp 1536ndash1544 2011

[136] K E A Segarra C Comerford J Slaughter and S B JoyeldquoImpact of electron acceptor availability on the anaerobic oxi-dation of methane in coastal freshwater and brackish wetlandsedimentsrdquo Geochimica et Cosmochimica Acta vol 115 pp 15ndash30 2013

[137] V Gupta K A Smemo J B Yavitt D Fowle B Branfireunand N Basiliko ldquoStable isotopes reveal widespread anaerobicmethane oxidation across latitude and peatland typerdquo Environ-mental Science and Technology vol 47 no 15 pp 8273ndash82792013

[138] O Oni T Miyatake S Kasten et al ldquoDistinct microbialpopulations are tightly linked to the profile of dissolved iron in

22 Archaea

the methanic sediments of the Helgolandmud area North SeardquoFrontiers in Microbiology vol 6 2015

[139] E J Beal C H House and V J Orphan ldquoManganese- andiron-dependent marine methane oxidationrdquo Science vol 325no 5937 pp 184ndash187 2009

[140] M W Bowles V A Samarkin K M Bowles and S B JoyeldquoWeak coupling between sulfate reduction and the anaerobicoxidation of methane in methane-rich seafloor sedimentsduring ex situ incubationrdquo Geochimica et Cosmochimica Actavol 75 no 2 pp 500ndash519 2011

[141] Y Z Lu L Fu J Ding Z Ding N Li and R J Zeng ldquoCr(VI)reduction coupled with anaerobic oxidation of methane in alaboratory reactorrdquoWater Research vol 102 pp 445ndash452 2016

[142] K F Ettwig B Zhu D Speth J T Keltjens M S Jetten and BKartal ldquoArchaea catalyze iron-dependent anaerobic oxidationof methanerdquo Proceedings of the National Academy of Sciences ofthe United States of America vol 113 no 45 pp 12792ndash127962016

[143] T M Flynn R A Sanford H Ryu et al ldquoFunctional microbialdiversity explains groundwater chemistry in a pristine aquiferrdquoBMCMicrobiology vol 13 no 1 article no 146 2013

[144] C J Schubert F Vazquez T Losekann-Behrens K KnittelM Tonolla and A Boetius ldquoEvidence for anaerobic oxidationof methane in sediments of a freshwater system (Lago diCadagno)rdquo FEMS Microbiology Ecology vol 76 no 1 pp 26ndash38 2011

[145] K E A Segarra F Schubotz V Samarkin M Y Yoshinaga K-U Hinrichs and S B Joye ldquoHigh rates of anaerobic methaneoxidation in freshwater wetlands reduce potential atmosphericmethane emissionsrdquo Nature Communications vol 6 article7477 2015

[146] E J Beal M W Claire and C H House ldquoHigh rates ofanaerobic methanotrophy at low sulfate concentrations withimplications for past and present methane levelsrdquo Geobiologyvol 9 no 2 pp 131ndash139 2011

[147] F Kracke I Vassilev and J O Kromer ldquoMicrobial electrontransport and energy conservationmdashthe foundation for opti-mizing bioelectrochemical systemsrdquo Frontiers in Microbiologyvol 6 article 575 2015

[148] C L Reardon A C Dohnalkova P Nachimuthu et al ldquoRoleof outer-membrane cytochromes MtrC and OmcA in thebiomineralization of ferrihydrite by Shewanella oneidensisMR-1rdquo Geobiology vol 8 no 1 pp 56ndash68 2010

[149] L Shi B Chen Z Wang et al ldquoIsolation of a high-affinityfunctional protein complex between OmcA and MtrC twoouter membrane decaheme c-type cytochromes of Shewanellaoneidensis MR-1rdquo Journal of Bacteriology vol 188 no 13 pp4705ndash4714 2006

[150] X Qian T Mester L Morgado et al ldquoBiochemical charac-terization of purified OmcS a c-type cytochrome requiredfor insoluble Fe(III) reduction in Geobacter sulfurreducensrdquoBiochimica et BiophysicaActamdashBioenergetics vol 1807 no 4 pp404ndash412 2011

[151] T Mehta M V Coppi S E Childers and D R Lovley ldquoOutermembrane c-type cytochromes required for Fe(III) andMn(IV)oxide reduction in Geobacter sulfurreducensrdquo Applied andEnvironmentalMicrobiology vol 71 no 12 pp 8634ndash8641 2005

[152] W Blankenfeldt A P Kuzin T Skarina et al ldquoStructure andfunction of the phenazine biosynthetic protein PhzF fromPseudomonas fluorescensrdquoProceedings of theNational Academyof Sciences of the United States of America vol 101 no 47 pp16431ndash16436 2004

[153] J F Parsons F Song L Parsons K Calabrese E Eisensteinand J E Ladner ldquoStructure and function of the phenazinebiosynthesis protein PhzF fromPseudomonas fluorescens 2-79rdquoBiochemistry vol 43 no 39 pp 12427ndash12435 2004

[154] T Hiratsuka K Furihata J Ishikawa et al ldquoAn alternativemenaquinone biosynthetic pathway operating in microorgan-ismsrdquo Science vol 321 no 5896 pp 1670ndash1673 2008

[155] M Tietze A Beuchle I Lamla et al ldquoRedox potentials ofmethanophenazine and CoB-S-S-CoM factors involved inelectron transport in methanogenic archaeardquo ChemBioChemvol 4 no 4 pp 333ndash335 2003

[156] Q H Tran and G Unden ldquoChanges in the proton potentialand the cellular energetics of Escherichia coli during growth byaerobic and anaerobic respiration or by fermentationrdquoEuropeanJournal of Biochemistry vol 251 no 1-2 pp 538ndash543 1998

[157] I Callebaut D Gilges I Vigon and J-P Mornon ldquoHYR anextracellular module involved in cellular adhesion and relatedto the immunoglobulin-like foldrdquo Protein Science vol 9 no 7pp 1382ndash1390 2000

[158] H J Gilbert ldquoCellulosomes microbial nanomachines that dis-play plasticity in quaternary structurerdquoMolecular Microbiologyvol 63 no 6 pp 1568ndash1576 2007

[159] A Peer S P Smith E A Bayer R Lamed and I BorovokldquoNoncellulosomal cohesin- and dockerin-like modules in thethree domains of liferdquo FEMS Microbiology Letters vol 291 no1 pp 1ndash16 2009

[160] M Wagner ldquoMicrobiology conductive consortiardquo Nature vol526 no 7574 pp 513ndash514 2015

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

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Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Archaea 17

growth However the recent milestone discovery of directelectron transfer provides opportunities to grow ANMEas stated previously on electron accepting electrodes (ieanodes) [160] In this way pure or highly enriched culturesof different ANME without their respective syntrophic part-ner could be obtained and MHCs responsible for electricconduction could be biochemically characterized It seemsthat ANME-1 are limited by the size and abundance ofMHCs which could relate to differences in behavior onan anode The partner bacteria of ANME-1 and ANME-2could be investigated on an electron donating electrode (iecathode) with specific focus on the ability to produce pili (ienanowires) Also worth investigating is if besides ANME-2d ANME-2ab could also use insoluble electron acceptorsand if ANME-2d could donate electrons to a bacterialpartner

Another future challenge is to isolate and characterizeMcr from different ANME clades It needs to be investi-gated if Mcr abundance in ANME cells compensates forthe slow reverse activity or if modifications in the Mcrof ANME-1 also contribute to a better reverse activity ofMcr Moreover the effect of methane partial pressure onreaction rates and enzyme kinetics needs to be determined insitu

ANME-1 are potentially able to perform hydrogeno-trophic methanogenesis due to the presence of a hydrogenasein the genome Genetic indications of menaquinones aselectron carrier in ANME-1 and the various cellulosome andcell adhesion related gene domains in all ANME are alsotopics that could be explored further Methanogenic archaeaare likely not able to perform AOM but additional studieson TMO and more genetic modifications to stimulate AOMin methanogens could help in understanding the param-eters needed for AOM to occur Ultimately physiologicalunderstanding of ANME will help to explain the observedecological niche separation of different ANME clades and theoccurrence of ANMEwithout a bacterial partnerThis wouldgreatly enhance our knowledge of themethane cycle in anoxicenvironments

Competing Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors thank Stefanie Berger (RU Nijmegen) for criticalreading of the manuscript This research is supported bythe Soehngen Institute of Anaerobic Microbiology (SIAM)Gravitation grant (024002002) of the Netherlands Ministryof Education Culture and Science and the NetherlandsOrganisation for Scientific Research (NWO) Mike S MJetten was further supported by ERC AG 339880 Eco-MoMand Alfons J M Stams was supported by ERC AG 323009Novel Anaerobes

References

[1] A Boetius K Ravenschlag C J Schubert et al ldquoA marinemicrobial consortium apparently mediating anaerobic oxida-tion of methanerdquo Nature vol 407 no 6804 pp 623ndash626 2000

[2] K-U Hinrichs J M Hayes S P Sylva P G Brewert andE F DeLong ldquoMethane-consuming archaebacteria in marinesedimentsrdquo Nature vol 398 no 6730 pp 802ndash805 1999

[3] V J Orphan C H House K-U Hinrichs K D McKeeganand E F DeLong ldquoMethane-consuming archaea revealed bydirectly coupled isotopic and phylogenetic analysisrdquo Sciencevol 293 no 5529 pp 484ndash487 2001

[4] K-U Hinrichs and A Boetius ldquoThe anaerobic oxidation ofmethane new insights in microbial ecology and biogeochem-istryrdquo inOceanMargin Systems GWefer D Billett D HebbelnB B Joslashrgensen M Schluter and T VanWeering Eds pp 457ndash477 Springer Berlin Germany 2002

[5] K Knittel T Losekann A Boetius R Kort and R AmannldquoDiversity and distribution of methanotrophic archaea at coldseepsrdquo Applied and Environmental Microbiology vol 71 no 1pp 467ndash479 2005

[6] K Knittel and A Boetius ldquoAnaerobic oxidation of methaneprogress with an unknown processrdquo Annual Review of Micro-biology vol 63 pp 311ndash334 2009

[7] V J Orphan K-U Hinrichs W Ussler III et al ldquoComparativeanalysis of methane-oxidizing archaea and sulfate-reducingbacteria in anoxic marine sedimentsrdquoApplied and Environmen-tal Microbiology vol 67 no 4 pp 1922ndash1934 2001

[8] T Losekann K Knittel T Nadalig et al ldquoDiversity andabundance of aerobic and anaerobic methane oxidizers atthe Haakon Mosby Mud Volcano Barents Seardquo Applied andEnvironmentalMicrobiology vol 73 no 10 pp 3348ndash3362 2007

[9] H Niemann T Losekann D De Beer et al ldquoNovel microbialcommunities of the Haakon Mosby mud volcano and their roleas amethane sinkrdquoNature vol 443 no 7113 pp 854ndash858 2006

[10] TNunouraHOida T Toki J Ashi K Takai andKHorikoshildquoQuantification of mcrA by quantitative fluorescent PCR insediments from methane seep of the Nankai Troughrdquo FEMSMicrobiology Ecology vol 57 no 1 pp 149ndash157 2006

[11] B Orcutt A Boetius M Elvert V Samarkin and S B JoyeldquoMolecular biogeochemistry of sulfate reduction methanogen-esis and the anaerobic oxidation of methane at Gulf of Mexicocold seepsrdquoGeochimica et Cosmochimica Acta vol 69 no 17 pp4267ndash4281 2005

[12] V J Orphan W Ussler III T H Naehr C H House K-U Hinrichs and C K Paull ldquoGeological geochemical andmicrobiological heterogeneity of the seafloor around methanevents in the Eel River Basin offshore Californiardquo ChemicalGeology vol 205 no 3-4 pp 265ndash289 2004

[13] M G Pachiadaki A Kallionaki A Dahlmann G J De Langeand K A Kormas ldquoDiversity and spatial distribution ofprokaryotic communities along a sediment vertical profile ofa deep-sea mud volcanordquo Microbial Ecology vol 62 no 3 pp655ndash668 2011

[14] I Roalkvam H Dahle Y Chen S L Joslashrgensen H Haflidasonand I H Steen ldquoFine-scale community structure analysis ofANME in Nyegga sediments with high and low methane fluxrdquoFrontiers in Microbiology vol 3 p 216 2012

[15] K Yanagawa M Sunamura M A Lever et al ldquoNiche separa-tion of methanotrophic archaea (ANME-1 and -2) in methane-seep sediments of the Eastern Japan Sea offshore JoetsurdquoGeomicrobiology Journal vol 28 no 2 pp 118ndash129 2011

18 Archaea

[16] A Pernthaler A E Dekas C T Brown S K Goffredi TEmbaye and V J Orphan ldquoDiverse syntrophic partnershipsfromdeep-seamethane vents revealed by direct cell capture andmetagenomicsrdquo Proceedings of the National Academy of Sciencesof the United States of America vol 105 no 19 pp 7052ndash70572008

[17] R Hatzenpichler S A Connon D Goudeau R R Malm-strom T Woyke and V J Orphan ldquoVisualizing in situtranslational activity for identifying and sorting slow-growingarchaealminusbacterial consortiardquo Proceedings of the NationalAcademy of Sciences vol 113 no 28 pp E4069ndashE4078 2016

[18] L Maignien R J Parkes B Cragg et al ldquoAnaerobic oxidationof methane in hypersaline cold seep sedimentsrdquo FEMS Micro-biology Ecology vol 83 no 1 pp 214ndash231 2013

[19] V J Orphan C H House K-U Hinrichs K D McKeeganand E F DeLong ldquoMultiple archaeal groups mediate methaneoxidation in anoxic cold seep sedimentsrdquo Proceedings of theNational Academy of Sciences of the United States of Americavol 99 no 11 pp 7663ndash7668 2002

[20] T TreudeM Kruger A Boetius and B B Joslashrgensen ldquoEnviron-mental control on anaerobic oxidation of methane in the gassysediments of Eckernforde Bay (German Baltic)rdquo Limnology andOceanography vol 50 no 6 pp 1771ndash1786 2005

[21] G C Jagersma R J W Meulepas I Heikamp-De Jong etal ldquoMicrobial diversity and community structure of a highlyactive anaerobic methane-oxidizing sulfate-reducing enrich-mentrdquo Environmental Microbiology vol 11 no 12 pp 3223ndash3232 2009

[22] M Blumenberg R Seifert J Reitner T Pape andWMichaelisldquoMembrane lipid patterns typify distinct anaerobic methan-otrophic consortiardquo Proceedings of the National Academy ofSciences of the United States of America vol 101 no 30 pp 11111ndash11116 2004

[23] S Bertram M Blumenberg W Michaelis M Siegert MKruger and R Seifert ldquoMethanogenic capabilities of ANME-archaea deduced from 13C-labelling approachesrdquo Environmen-tal Microbiology vol 15 no 8 pp 2384ndash2393 2013

[24] K G Lloyd M J Alperin and A Teske ldquoEnvironmental evi-dence for net methane production and oxidation in putativeANaerobic MEthanotrophic (ANME) archaeardquo EnvironmentalMicrobiology vol 13 no 9 pp 2548ndash2564 2011

[25] M Takeuchi H Yoshioka Y Seo et al ldquoA distinct freshwater-adapted subgroup of ANME-1 dominates active archaeal com-munities in terrestrial subsurfaces in Japanrdquo EnvironmentalMicrobiology vol 13 no 12 pp 3206ndash3218 2011

[26] R T Amos B A Bekins I M Cozzarelli et al ldquoEvidence foriron-mediated anaerobic methane oxidation in a crude oil-contaminated aquiferrdquo Geobiology vol 10 no 6 pp 506ndash5172012

[27] P H Timmers D A Suarez-Zuluaga M van Rossem MDiender A J Stams and C M Plugge ldquoAnaerobic oxidationof methane associated with sulfate reduction in a naturalfreshwater gas sourcerdquo ISME Journal vol 10 pp 1400ndash14122015

[28] M F Haroon S Hu Y Shi et al ldquoAnaerobic oxidation ofmethane coupled to nitrate reduction in a novel archaeallineagerdquo Nature vol 500 no 7468 pp 567ndash570 2013

[29] H J Mills C Hodges K Wilson I R MacDonald and PA Sobecky ldquoMicrobial diversity in sediments associated withsurface-breaching gas hydrate mounds in the Gulf of MexicordquoFEMS Microbiology Ecology vol 46 no 1 pp 39ndash52 2003

[30] K G Lloyd L Lapham and A Teske ldquoAn anaerobic methane-oxidizing community of ANME-1b archaea in hypersaline gulfofMexico sedimentsrdquoApplied and EnvironmentalMicrobiologyvol 72 no 11 pp 7218ndash7230 2006

[31] A A Raghoebarsing A Pol K T Van De Pas-Schoonen et alldquoA microbial consortium couples anaerobic methane oxidationto denitrificationrdquoNature vol 440 no 7086 pp 918ndash921 2006

[32] S Hu R J Zeng L C Burow P Lant J Keller and Z YuanldquoEnrichment of denitrifying anaerobic methane oxidizingmicroorganismsrdquo Environmental Microbiology Reports vol 1no 5 pp 377ndash384 2009

[33] Z-W Ding J Ding L Fu F Zhang and R J Zeng ldquoSimultane-ous enrichment of denitrifying methanotrophs and anammoxbacteriardquo Applied Microbiology and Biotechnology vol 98 no24 pp 10211ndash10221 2014

[34] R Seifert K Nauhaus M Blumenberg M Kruger and WMichaelis ldquoMethane dynamics in a microbial community ofthe Black Sea traced by stable carbon isotopes in vitrordquoOrganicGeochemistry vol 37 no 10 pp 1411ndash1419 2006

[35] J Ding Z-W Ding L Fu Y-Z Lu S H Cheng and R JZeng ldquoNew primers for detecting and quantifying denitrifyinganaerobic methane oxidation archaea in different ecologicalnichesrdquo Applied Microbiology and Biotechnology vol 99 no 22pp 9805ndash9812 2015

[36] A Vaksmaa C Luke T van Alen et al ldquoDistribution and activ-ity of the anaerobic methanotrophic community in a nitrogen-fertilized Italian paddy soilrdquo FEMS Microbiology Ecology vol92 no 12 2016

[37] P N Evans D H Parks G L Chadwick et al ldquoMethanemetabolism in the archaeal phylum Bathyarchaeota revealed bygenome-centric metagenomicsrdquo Science vol 350 no 6259 pp434ndash438 2015

[38] I Vanwonterghem P N Evans D H Parks et al ldquoMethy-lotrophic methanogenesis discovered in the archaeal phylumVerstraetearchaeotardquo Nature Microbiology vol 1 Article ID16170 2016

[39] P Worm J J Koehorst M Visser et al ldquoA genomic view onsyntrophic versus non-syntrophic lifestyle in anaerobic fattyacid degrading communitiesrdquo Biochimica et Biophysica ActamdashBioenergetics vol 1837 no 12 pp 2004ndash2016 2014

[40] R Stokke I Roalkvam A Lanzen H Haflidason and I HSteen ldquoIntegrated metagenomic and metaproteomic analysesof an ANME-1-dominated community in marine cold seepsedimentsrdquo Environmental Microbiology vol 14 no 5 pp 1333ndash1346 2012

[41] A Meyerdierks M Kube I Kostadinov et al ldquoMetagenomeand mRNA expression analyses of anaerobic methanotrophicarchaea of the ANME-1 grouprdquo Environmental Microbiologyvol 12 no 2 pp 422ndash439 2010

[42] F-P Wang Y Zhang Y Chen et al ldquoMethanotrophicarchaea possessing diverging methane-oxidizing and electron-transporting pathwaysrdquo ISME Journal vol 8 no 5 pp 1069ndash1078 2014

[43] A Arshad D R Speth R M de Graaf H J Op den Camp MS Jetten and C U Welte ldquoA metagenomics-based metabolicmodel of nitrate-dependent anaerobic oxidation of methane byMethanoperedens-like archaeardquo Frontiers inMicrobiology vol 6article1423 2015

[44] S J Hallam N Putnam CM Preston et al ldquoReversemethano-genesis testing the hypothesis with environmental genomicsrdquoScience vol 305 no 5689 pp 1457ndash1462 2004

Archaea 19

[45] R K Thauer ldquoAnaerobic oxidation of methane with sulfate onthe reversibility of the reactions that are catalyzed by enzymesalso involved inmethanogenesis fromCO

2rdquoCurrent Opinion in

Microbiology vol 14 no 3 pp 292ndash299 2011[46] U Deppenmeier V Muller and G Gottschalk ldquoPathways of

energy conservation in methanogenic archaeardquo Archives ofMicrobiology vol 165 no 3 pp 149ndash163 1996

[47] A-K Kaster J Moll K Parey and R K Thauer ldquoCoupling offerredoxin and heterodisulfide reduction via electron bifurca-tion in hydrogenotrophic methanogenic archaeardquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 108 no 7 pp 2981ndash2986 2011

[48] R K Thauer A-K Kaster H Seedorf W Buckel and RHedderich ldquoMethanogenic archaea ecologically relevant dif-ferences in energy conservationrdquo Nature Reviews Microbiologyvol 6 no 8 pp 579ndash591 2008

[49] W Ludwig O Strunk R Westram et al ldquoARB a softwareenvironment for sequence datardquoNucleic Acids Research vol 32no 4 pp 1363ndash1371 2004

[50] E Pruesse C Quast K Knittel et al ldquoSILVA a comprehensiveonline resource for quality checked and aligned ribosomal RNAsequence data compatible with ARBrdquo Nucleic Acids Researchvol 35 no 21 pp 7188ndash7196 2007

[51] J J Marlow C T Skennerton Z Li et al ldquoProteomic stableisotope probing reveals biosynthesis dynamics of slow growingmethane based microbial communitiesrdquo Frontiers in Microbiol-ogy vol 7 article 386 2016

[52] P V Welander and W W Metcalf ldquoLoss of the mtr operon inMethanosarcina blocks growth on methanol but not methano-genesis and reveals an unknown methanogenic pathwayrdquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 102 no 30 pp 10664ndash10669 2005

[53] P V Welander and W W Metcalf ldquoMutagenesis of the C1oxidation pathway inmethanosarcina barkeri new insights intothe MtrMer bypass pathwayrdquo Journal of Bacteriology vol 190no 6 pp 1928ndash1936 2008

[54] M Goenrich R K Thauer H Yurimoto and N KatoldquoFormaldehyde activating enzyme (Fae) and hexulose-6-phosphate synthase (Hps) inMethanosarcina barkeri a possiblefunction in ribose-5-phosphate biosynthesisrdquoArchives ofMicro-biology vol 184 no 1 pp 41ndash48 2005

[55] M Goenrich FMahlert E C Duin C Bauer B Jaun and R KThauer ldquoProbing the reactivity of Ni in the active site of methyl-coenzyme M reductase with substrate analoguesrdquo Journal ofBiological Inorganic Chemistry vol 9 no 6 pp 691ndash705 2004

[56] S Scheller M Goenrich R Boecher R K Thauer and BJaun ldquoThe key nickel enzyme of methanogenesis catalyses theanaerobic oxidation of methanerdquo Nature vol 465 no 7298 pp606ndash608 2010

[57] K Nauhaus A Boetius M Kruger and F Widdel ldquoIn vitrodemonstration of anaerobic oxidation of methane coupled tosulphate reduction in sediment from amarine gas hydrate areardquoEnvironmental Microbiology vol 4 no 5 pp 296ndash305 2002

[58] Y Zhang J-P Henriet J Bursens and N Boon ldquoStimulationof in vitro anaerobic oxidation of methane rate in a continuoushigh-pressure bioreactorrdquo Bioresource Technology vol 101 no9 pp 3132ndash3138 2010

[59] M Kruger T Treude H Wolters K Nauhaus and A BoetiusldquoMicrobial methane turnover in different marine habitatsrdquoPalaeogeography Palaeoclimatology Palaeoecology vol 227 no1ndash3 pp 6ndash17 2005

[60] C Deusner V Meyer and T G Ferdelman ldquoHigh-pressuresystems for gas-phase free continuous incubation of enrichedmarinemicrobial communities performing anaerobic oxidationof methanerdquo Biotechnology and Bioengineering vol 105 no 3pp 524ndash533 2010

[61] K Nauhaus T Treude A Boetius and M Kruger ldquoEnviron-mental regulation of the anaerobic oxidation of methane acomparison of ANME-I and ANME-II communitiesrdquo Environ-mental Microbiology vol 7 no 1 pp 98ndash106 2005

[62] T Treude V Orphan K Knittel A Gieseke C H House andA Boetius ldquoConsumption of methane and CO

2by methan-

otrophicmicrobial mats from gas seeps of the anoxic Black SeardquoApplied and EnvironmentalMicrobiology vol 73 no 7 pp 2271ndash2283 2007

[63] T Holler F Widdel K Knittel et al ldquoThermophilic anaerobicoxidation of methane by marine microbial consortiardquo ISMEJournal vol 5 no 12 pp 1946ndash1956 2011

[64] M Kruger M Blumenberg S Kasten et al ldquoA novel multi-layered methanotrophic microbial mat system growing on thesediment of the Black Seardquo Environmental Microbiology vol 10no 8 pp 1934ndash1947 2008

[65] R J WMeulepas C G Jagersma J Gieteling C J N BuismanA J M Stams and P N L Lens ldquoEnrichment of anaerobicmethanotrophs in sulfate-reducing membrane bioreactorsrdquoBiotechnology and Bioengineering vol 104 no 3 pp 458ndash4702009

[66] T Holler G Wegener H Niemann et al ldquoCarbon and sulfurback flux during anaerobic microbial oxidation of methane andcoupled sulfate reductionrdquo Proceedings of the National Academyof Sciences of the United States of America vol 108 no 52 ppE1484ndashE1490 2011

[67] M Kruger AMeyerdierks F O Glockner et al ldquoA conspicuousnickel protein in microbial mats that oxidize methane anaero-bicallyrdquo Nature vol 426 no 6968 pp 878ndash881 2003

[68] S Mayr C Latkoczy M Kruger et al ldquoStructure of an F430

variant from archaea associated with anaerobic oxidation ofmethanerdquo Journal of the American Chemical Society vol 130 no32 pp 10758ndash10767 2008

[69] S Shima and R K Thauer ldquoMethyl-coenzyme M reductaseand the anaerobic oxidation of methane in methanotrophicArchaeardquo Current Opinion in Microbiology vol 8 no 6 pp643ndash648 2005

[70] R K Thauer and S Shima ldquoMethane as fuel for anaerobicmicroorganismsrdquo Annals of the New York Academy of Sciencesvol 1125 pp 158ndash170 2008

[71] S Yamamoto J B Alcauskas and T E Crozier ldquoSolubility ofmethane in distilled water and seawaterrdquo Journal of Chemicaland Engineering Data vol 21 no 1 pp 78ndash80 1976

[72] P H A Timmers J Gieteling H C A Widjaja-Greefkeset al ldquoGrowth of anaerobic methane-oxidizing archaea andsulfate-reducing bacteria in a high-pressure membrane capsulebioreactorrdquoApplied and EnvironmentalMicrobiology vol 81 no4 pp 1286ndash1296 2015

[73] MKruger HWoltersMGehre S B Joye andH-H RichnowldquoTracing the slow growth of anaerobic methane-oxidizingcommunities by 15N-labelling techniquesrdquo FEMS MicrobiologyEcology vol 63 no 3 pp 401ndash411 2008

[74] R J W Meulepas C G Jagersma A F Khadem C J N Buis-man A J M Stams and P N L Lens ldquoEffect of environmentalconditions on sulfate reduction withmethane as electron donorby an Eckernforde Bay enrichmentrdquo Environmental Science andTechnology vol 43 no 17 pp 6553ndash6559 2009

20 Archaea

[75] M W Bowles V A Samarkin and S B Joye ldquoImprovedmeasurement of microbial activity in deep-sea sediments atin situ pressure and methane concentrationrdquo Limnology andOceanography Methods vol 9 pp 499ndash506 2011

[76] S Shima M Krueger T Weinert et al ldquoStructure of a methyl-coenzyme M reductase from Black Sea mats that oxidizemethane anaerobicallyrdquo Nature vol 481 no 7379 pp 98ndash1012012

[77] K D Allen G Wegener and R H White ldquoDiscovery of multi-ple modified F-430 coenzymes in methanogens and anaerobicmethanotrophic archaea suggests possible new roles for F-430in naturerdquoApplied and Environmental Microbiology vol 80 no20 pp 6403ndash6412 2014

[78] V W Soo M J McAnulty A Tripathi et al ldquoReversingmethanogenesis to capture methane for liquid biofuel precur-sorsrdquoMicrobial Cell Factories vol 15 article 11 2016

[79] D L Valentine and W S Reeburgh ldquoNew perspectives onanaerobicmethane oxidationrdquoEnvironmentalMicrobiology vol2 no 5 pp 477ndash484 2000

[80] D L Valentine ldquoBiogeochemistry and microbial ecology ofmethane oxidation in anoxic environments a reviewrdquo Antonievan Leeuwenhoek International Journal of General and Molecu-lar Microbiology vol 81 no 1-4 pp 271ndash282 2002

[81] A J B Zehnder and T D Brock ldquoMethane formation andmethane oxidation by methanogenic bacteriardquo Journal of Bac-teriology vol 137 no 1 pp 420ndash432 1979

[82] J Harder ldquoAnaerobic methane oxidation by bacteria employ-ing 14C-methane uncontaminated with 14C-carbon monoxiderdquoMarine Geology vol 137 no 1-2 pp 13ndash23 1997

[83] J J Moran C H House K H Freeman and J G FerryldquoTrace methane oxidation studied in several Euryarchaeotaunder diverse conditionsrdquo Archaea vol 1 no 5 pp 303ndash3092005

[84] J J Moran C H House B Thomas and K H FreemanldquoProducts of tracemethane oxidation during nonmethyltrophicgrowth by Methanosarcinardquo Journal of Geophysical ResearchBiogeosciences vol 112 no 2 2007

[85] R J W Meulepas C G Jagersma Y Zhang et al ldquoTracemethane oxidation and the methane dependency of sulfatereduction in anaerobic granular sludgerdquo FEMS MicrobiologyEcology vol 72 no 2 pp 261ndash271 2010

[86] A J B Zehnder andTD Brock ldquoAnaerobicmethane oxidationoccurrence and ecologyrdquoApplied and Environmental Microbiol-ogy vol 39 no 1 pp 194ndash204 1980

[87] S J Blazewicz D G Petersen M P Waldrop and M K Fire-stone ldquoAnaerobic oxidation of methane in tropical and borealsoils ecological significance in terrestrial methane cyclingrdquoJournal of Geophysical Research Biogeosciences vol 117 no 2Article ID G02033 2012

[88] K A Smemo and J B Yavitt ldquoEvidence for anaerobic CH4

oxidation in freshwater peatlandsrdquo Geomicrobiology Journalvol 24 no 7-8 pp 583ndash597 2007

[89] M J Alperin and T M Hoehler ldquoAnaerobic methane oxidationby archaeasulfate-reducing bacteria aggregates 1 Thermody-namic and physical constraintsrdquo American Journal of Sciencevol 309 no 10 pp 869ndash957 2009

[90] S L Caldwell J R Laidler E A Brewer J O Eberly S CSandborgh and F S Colwell ldquoAnaerobic oxidation of methanemechanisms bioenergetics and the ecology of associatedmicroorganismsrdquo Environmental Science and Technology vol42 no 18 pp 6791ndash6799 2008

[91] GWang A J Spivack and S DrsquoHondt ldquoGibbs energies of reac-tion and microbial mutualism in anaerobic deep subseafloorsediments of ODP Site 1226rdquoGeochimica et Cosmochimica Actavol 74 no 14 pp 3938ndash3947 2010

[92] P R Girguis A E Cozen and E F DeLong ldquoGrowth andpopulation dynamics of anaerobic methane-oxidizing archaeaand sulfate-reducing bacteria in a continuous-flow bioreactorrdquoApplied and EnvironmentalMicrobiology vol 71 no 7 pp 3725ndash3733 2005

[93] K Nauhaus M Albrecht M Elvert A Boetius and F WiddelldquoIn vitro cell growth ofmarine archaeal-bacterial consortia dur-ing anaerobic oxidation ofmethanewith sulfaterdquoEnvironmentalMicrobiology vol 9 no 1 pp 187ndash196 2007

[94] B Orcutt V Samarkin A Boetius and S Joye ldquoOn the relation-ship between methane production and oxidation by anaerobicmethanotrophic communities from cold seeps of the Gulf ofMexicordquo Environmental Microbiology vol 10 no 5 pp 1108ndash1117 2008

[95] M Y Yoshinaga T Holler T Goldhammer et al ldquoCarbon iso-tope equilibration during sulphate-limited anaerobic oxidationof methanerdquo Nature Geoscience vol 7 no 3 pp 190ndash194 2014

[96] T Treude J Niggemann J Kallmeyer et al ldquoAnaerobic oxi-dation of methane and sulfate reduction along the Chileancontinental marginrdquo Geochimica et Cosmochimica Acta vol 69no 11 pp 2767ndash2779 2005

[97] R J Parkes B A Cragg N Banning et al ldquoBiogeochemistryand biodiversity of methane cycling in subsurface marinesediments (SkagerrakDenmark)rdquoEnvironmentalMicrobiologyvol 9 no 5 pp 1146ndash1161 2007

[98] N J Knab B A Cragg E R C Hornibrook et al ldquoRegulationof anaerobic methane oxidation in sediments of the Black SeardquoBiogeosciences vol 6 no 8 pp 1505ndash1518 2009

[99] H Yoshioka A Maruyama T Nakamura et al ldquoActivities anddistribution of methanogenic and methane-oxidizing microbesin marine sediments from the Cascadia Marginrdquo Geobiologyvol 8 no 3 pp 223ndash233 2010

[100] G Wegener V Krukenberg S E Ruff M Y Kellermann andK Knittel ldquoMetabolic capabilities of microorganisms involvedin and associated with the anaerobic oxidation of methanerdquoFrontiers in Microbiology vol 7 article 46 2016

[101] R J W Meulepas C G Jagersma A F Khadem A J MStams and P N L Lens ldquoEffect of methanogenic substrateson anaerobic oxidation of methane and sulfate reduction by ananaerobic methanotrophic enrichmentrdquo Applied Microbiologyand Biotechnology vol 87 no 4 pp 1499ndash1506 2010

[102] J Milucka T G Ferdelman L Polerecky et al ldquoZero-valentsulphur is a key intermediate in marine methane oxidationrdquoNature vol 491 no 7425 pp 541ndash546 2012

[103] W Michaelis R Seifert K Nauhaus et al ldquoMicrobial reefs inthe black sea fueled by anaerobic oxidation ofmethanerdquo Sciencevol 297 no 5583 pp 1013ndash1015 2002

[104] A Vigneron P Cruaud P Pignet et al ldquoArchaeal and anaerobicmethane oxidizer communities in the Sonora Margin coldseeps Guaymas Basin (Gulf of California)rdquo ISME Journal vol7 no 8 pp 1595ndash1608 2013

[105] M Alperin and T Hoehler ldquoThe ongoing mystery of sea-floormethanerdquo Science vol 329 no 5989 pp 288ndash289 2010

[106] B Orcutt and C Meile ldquoConstraints on mechanisms and ratesof anaerobic oxidation of methane by microbial consortiaprocess-basedmodeling of ANME-2 archaea and sulfate reduc-ing bacteria interactionsrdquo Biogeosciences vol 5 no 6 pp 1587ndash1599 2008

Archaea 21

[107] S E McGlynn G L Chadwick C P Kempes and V J OrphanldquoSingle cell activity reveals direct electron transfer in methan-otrophic consortiardquoNature vol 526 no 7574 pp 531ndash535 2015

[108] D R Lovley ldquoElectromicrobiologyrdquo Annual Review of Microbi-ology vol 66 pp 391ndash409 2012

[109] S M Strycharz-Glaven R M Snider A Guiseppi-Elie andL M Tender ldquoOn the electrical conductivity of microbialnanowires and biofilmsrdquoEnergy and Environmental Science vol4 no 11 pp 4366ndash4379 2011

[110] D J Richardson J N Butt J K Fredrickson et al ldquoThe lsquoporinndashcytochromersquo model for microbe-to-mineral electron transferrdquoMolecular Microbiology vol 85 no 2 pp 201ndash212 2012

[111] A Okamoto K Hashimoto and R Nakamura ldquoLong-rangeelectron conduction of Shewanella biofilms mediated by outermembrane C-type cytochromesrdquo Bioelectrochemistry vol 85pp 61ndash65 2012

[112] M Y El-Naggar G Wanger K M Leung et al ldquoElectricaltransport along bacterial nanowires from Shewanella oneidensisMR-1rdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 107 no 42 pp 18127ndash18131 2010

[113] G Reguera K D McCarthy T Mehta J S Nicoll M TTuominen and D R Lovley ldquoExtracellular electron transfer viamicrobial nanowiresrdquo Nature vol 435 no 7045 pp 1098ndash11012005

[114] Z M Summers H E Fogarty C Leang A E Franks N SMalvankar and D R Lovley ldquoDirect exchange of electronswithin aggregates of an evolved syntrophic coculture of anaer-obic bacteriardquo Science vol 330 no 6009 pp 1413ndash1415 2010

[115] A Kletzin T Heimerl J Flechsler L V Niftrik R Rachel andA Klingl ldquoCytochromes c in archaea distribution maturationcell architecture and the special case of Ignicoccus hospitalisrdquoFrontiers in Microbiology vol 6 article 439 2015

[116] GWegener V Krukenberg D Riedel H E Tegetmeyer and ABoetius ldquoIntercellular wiring enables electron transfer betweenmethanotrophic archaea and bacteriardquo Nature vol 526 no7574 pp 587ndash590 2015

[117] D HHaft S H Payne and J D Selengut ldquoArchaeosortases andexosortases are widely distributed systems linking membranetransit with posttranslational modificationrdquo Journal of Bacteri-ology vol 194 no 1 pp 36ndash48 2012

[118] A Marchler-Bauer M K Derbyshire N R Gonzales et alldquoCDD NCBIrsquos conserved domain databaserdquo Nucleic AcidsResearch vol 43 no 1 pp D222ndashD226 2015

[119] A Mitchell H-Y Chang L Daugherty et al ldquoThe InterProprotein families database the classification resource after 15yearsrdquo Nucleic Acids Research vol 43 no 1 pp D213ndashD2212015

[120] V Krukenberg K Harding M Richter et al ldquoCandidatusdesulfofervidus auxilii a hydrogenotrophic sulfate-reducingbacterium involved in the thermophilic anaerobic oxidation ofmethanerdquo Environmental Microbiology vol 18 pp 3073ndash30912016

[121] L Shi T C Squier J M Zachara and J K Fredrickson ldquoRes-piration of metal (hydr)oxides by Shewanella and Geobactera key role for multihaem c-type cytochromesrdquo MolecularMicrobiology vol 65 no 1 pp 12ndash20 2007

[122] N S Malvankar and D R Lovley ldquoMicrobial nanowires forbioenergy applicationsrdquo Current Opinion in Biotechnology vol27 pp 88ndash95 2014

[123] A-E Rotaru T LWoodard K PNevin andDR Lovley ldquoLinkbetween capacity for current production and syntrophic growth

in Geobacter speciesrdquo Frontiers in Microbiology vol 6 article744 2015

[124] A-E Rotaru P M Shrestha F Liu et al ldquoDirect interspecieselectron transfer between Geobacter metallireducens andMethanosarcina barkerirdquo Applied and Environmental Microbi-ology vol 80 no 15 pp 4599ndash4605 2014

[125] S Scheller H Yu G L Chadwick S E McGlynn and VJ Orphan ldquoArtificial electron acceptors decouple archaealmethane oxidation from sulfate reductionrdquo Science vol 351 no6274 pp 703ndash707 2016

[126] J Milucka F Widdel and S Shima ldquoImmunological detec-tion of enzymes for sulfate reduction in anaerobic methane-oxidizing consortiardquo Environmental Microbiology vol 15 no 5pp 1561ndash1571 2013

[127] P Cabello M D Roldan and C Moreno-Vivian ldquoNitratereduction and the nitrogen cycle in archaeardquoMicrobiology vol150 no 11 pp 3527ndash3546 2004

[128] R MMartinez-Espinosa E J Dridge M J Bonete et al ldquoLookon the positive sideThe orientation identification and bioener-getics of lsquoArchaealrsquomembrane-boundnitrate reductasesrdquoFEMSMicrobiology Letters vol 276 no 2 pp 129ndash139 2007

[129] S de VriesMMomcilovicM J F Strampraad J PWhiteleggeA Baghai and I Schroder ldquoAdaptation to a high-tungsten envi-ronment pyrobaculum aerophilum contains an active tungstennitrate reductaserdquo Biochemistry vol 49 no 45 pp 9911ndash99212010

[130] M Egger O Rasigraf C J Sapart et al ldquoIron-mediated anaer-obic oxidation of methane in brackish coastal sedimentsrdquoEnvironmental Science and Technology vol 49 no 1 pp 277ndash283 2015

[131] T Treude S Krause J Maltby A W Dale R Coffin and LJ Hamdan ldquoSulfate reduction and methane oxidation activitybelow the sulfate-methane transition zone in Alaskan BeaufortSea continental margin sediments implications for deep sulfurcyclingrdquo Geochimica et Cosmochimica Acta vol 144 pp 217ndash237 2014

[132] N Riedinger M J Formolo T W Lyons S Henkel A Beckand S Kasten ldquoAn inorganic geochemical argument for coupledanaerobic oxidation of methane and iron reduction in marinesedimentsrdquo Geobiology vol 12 no 2 pp 172ndash181 2014

[133] Y-H Chang T-W Cheng W-J Lai et al ldquoMicrobial methanecycling in a terrestrialmud volcano in eastern Taiwanrdquo Environ-mental Microbiology vol 14 no 4 pp 895ndash908 2012

[134] S A Crowe S Katsev K Leslie et al ldquoThe methane cycle inferruginous Lake Matanordquo Geobiology vol 9 no 1 pp 61ndash782011

[135] O Sivan M Adler A Pearson et al ldquoGeochemical evidence foriron-mediated anaerobic oxidation of methanerdquo Limnology andOceanography vol 56 no 4 pp 1536ndash1544 2011

[136] K E A Segarra C Comerford J Slaughter and S B JoyeldquoImpact of electron acceptor availability on the anaerobic oxi-dation of methane in coastal freshwater and brackish wetlandsedimentsrdquo Geochimica et Cosmochimica Acta vol 115 pp 15ndash30 2013

[137] V Gupta K A Smemo J B Yavitt D Fowle B Branfireunand N Basiliko ldquoStable isotopes reveal widespread anaerobicmethane oxidation across latitude and peatland typerdquo Environ-mental Science and Technology vol 47 no 15 pp 8273ndash82792013

[138] O Oni T Miyatake S Kasten et al ldquoDistinct microbialpopulations are tightly linked to the profile of dissolved iron in

22 Archaea

the methanic sediments of the Helgolandmud area North SeardquoFrontiers in Microbiology vol 6 2015

[139] E J Beal C H House and V J Orphan ldquoManganese- andiron-dependent marine methane oxidationrdquo Science vol 325no 5937 pp 184ndash187 2009

[140] M W Bowles V A Samarkin K M Bowles and S B JoyeldquoWeak coupling between sulfate reduction and the anaerobicoxidation of methane in methane-rich seafloor sedimentsduring ex situ incubationrdquo Geochimica et Cosmochimica Actavol 75 no 2 pp 500ndash519 2011

[141] Y Z Lu L Fu J Ding Z Ding N Li and R J Zeng ldquoCr(VI)reduction coupled with anaerobic oxidation of methane in alaboratory reactorrdquoWater Research vol 102 pp 445ndash452 2016

[142] K F Ettwig B Zhu D Speth J T Keltjens M S Jetten and BKartal ldquoArchaea catalyze iron-dependent anaerobic oxidationof methanerdquo Proceedings of the National Academy of Sciences ofthe United States of America vol 113 no 45 pp 12792ndash127962016

[143] T M Flynn R A Sanford H Ryu et al ldquoFunctional microbialdiversity explains groundwater chemistry in a pristine aquiferrdquoBMCMicrobiology vol 13 no 1 article no 146 2013

[144] C J Schubert F Vazquez T Losekann-Behrens K KnittelM Tonolla and A Boetius ldquoEvidence for anaerobic oxidationof methane in sediments of a freshwater system (Lago diCadagno)rdquo FEMS Microbiology Ecology vol 76 no 1 pp 26ndash38 2011

[145] K E A Segarra F Schubotz V Samarkin M Y Yoshinaga K-U Hinrichs and S B Joye ldquoHigh rates of anaerobic methaneoxidation in freshwater wetlands reduce potential atmosphericmethane emissionsrdquo Nature Communications vol 6 article7477 2015

[146] E J Beal M W Claire and C H House ldquoHigh rates ofanaerobic methanotrophy at low sulfate concentrations withimplications for past and present methane levelsrdquo Geobiologyvol 9 no 2 pp 131ndash139 2011

[147] F Kracke I Vassilev and J O Kromer ldquoMicrobial electrontransport and energy conservationmdashthe foundation for opti-mizing bioelectrochemical systemsrdquo Frontiers in Microbiologyvol 6 article 575 2015

[148] C L Reardon A C Dohnalkova P Nachimuthu et al ldquoRoleof outer-membrane cytochromes MtrC and OmcA in thebiomineralization of ferrihydrite by Shewanella oneidensisMR-1rdquo Geobiology vol 8 no 1 pp 56ndash68 2010

[149] L Shi B Chen Z Wang et al ldquoIsolation of a high-affinityfunctional protein complex between OmcA and MtrC twoouter membrane decaheme c-type cytochromes of Shewanellaoneidensis MR-1rdquo Journal of Bacteriology vol 188 no 13 pp4705ndash4714 2006

[150] X Qian T Mester L Morgado et al ldquoBiochemical charac-terization of purified OmcS a c-type cytochrome requiredfor insoluble Fe(III) reduction in Geobacter sulfurreducensrdquoBiochimica et BiophysicaActamdashBioenergetics vol 1807 no 4 pp404ndash412 2011

[151] T Mehta M V Coppi S E Childers and D R Lovley ldquoOutermembrane c-type cytochromes required for Fe(III) andMn(IV)oxide reduction in Geobacter sulfurreducensrdquo Applied andEnvironmentalMicrobiology vol 71 no 12 pp 8634ndash8641 2005

[152] W Blankenfeldt A P Kuzin T Skarina et al ldquoStructure andfunction of the phenazine biosynthetic protein PhzF fromPseudomonas fluorescensrdquoProceedings of theNational Academyof Sciences of the United States of America vol 101 no 47 pp16431ndash16436 2004

[153] J F Parsons F Song L Parsons K Calabrese E Eisensteinand J E Ladner ldquoStructure and function of the phenazinebiosynthesis protein PhzF fromPseudomonas fluorescens 2-79rdquoBiochemistry vol 43 no 39 pp 12427ndash12435 2004

[154] T Hiratsuka K Furihata J Ishikawa et al ldquoAn alternativemenaquinone biosynthetic pathway operating in microorgan-ismsrdquo Science vol 321 no 5896 pp 1670ndash1673 2008

[155] M Tietze A Beuchle I Lamla et al ldquoRedox potentials ofmethanophenazine and CoB-S-S-CoM factors involved inelectron transport in methanogenic archaeardquo ChemBioChemvol 4 no 4 pp 333ndash335 2003

[156] Q H Tran and G Unden ldquoChanges in the proton potentialand the cellular energetics of Escherichia coli during growth byaerobic and anaerobic respiration or by fermentationrdquoEuropeanJournal of Biochemistry vol 251 no 1-2 pp 538ndash543 1998

[157] I Callebaut D Gilges I Vigon and J-P Mornon ldquoHYR anextracellular module involved in cellular adhesion and relatedto the immunoglobulin-like foldrdquo Protein Science vol 9 no 7pp 1382ndash1390 2000

[158] H J Gilbert ldquoCellulosomes microbial nanomachines that dis-play plasticity in quaternary structurerdquoMolecular Microbiologyvol 63 no 6 pp 1568ndash1576 2007

[159] A Peer S P Smith E A Bayer R Lamed and I BorovokldquoNoncellulosomal cohesin- and dockerin-like modules in thethree domains of liferdquo FEMS Microbiology Letters vol 291 no1 pp 1ndash16 2009

[160] M Wagner ldquoMicrobiology conductive consortiardquo Nature vol526 no 7574 pp 513ndash514 2015

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

18 Archaea

[16] A Pernthaler A E Dekas C T Brown S K Goffredi TEmbaye and V J Orphan ldquoDiverse syntrophic partnershipsfromdeep-seamethane vents revealed by direct cell capture andmetagenomicsrdquo Proceedings of the National Academy of Sciencesof the United States of America vol 105 no 19 pp 7052ndash70572008

[17] R Hatzenpichler S A Connon D Goudeau R R Malm-strom T Woyke and V J Orphan ldquoVisualizing in situtranslational activity for identifying and sorting slow-growingarchaealminusbacterial consortiardquo Proceedings of the NationalAcademy of Sciences vol 113 no 28 pp E4069ndashE4078 2016

[18] L Maignien R J Parkes B Cragg et al ldquoAnaerobic oxidationof methane in hypersaline cold seep sedimentsrdquo FEMS Micro-biology Ecology vol 83 no 1 pp 214ndash231 2013

[19] V J Orphan C H House K-U Hinrichs K D McKeeganand E F DeLong ldquoMultiple archaeal groups mediate methaneoxidation in anoxic cold seep sedimentsrdquo Proceedings of theNational Academy of Sciences of the United States of Americavol 99 no 11 pp 7663ndash7668 2002

[20] T TreudeM Kruger A Boetius and B B Joslashrgensen ldquoEnviron-mental control on anaerobic oxidation of methane in the gassysediments of Eckernforde Bay (German Baltic)rdquo Limnology andOceanography vol 50 no 6 pp 1771ndash1786 2005

[21] G C Jagersma R J W Meulepas I Heikamp-De Jong etal ldquoMicrobial diversity and community structure of a highlyactive anaerobic methane-oxidizing sulfate-reducing enrich-mentrdquo Environmental Microbiology vol 11 no 12 pp 3223ndash3232 2009

[22] M Blumenberg R Seifert J Reitner T Pape andWMichaelisldquoMembrane lipid patterns typify distinct anaerobic methan-otrophic consortiardquo Proceedings of the National Academy ofSciences of the United States of America vol 101 no 30 pp 11111ndash11116 2004

[23] S Bertram M Blumenberg W Michaelis M Siegert MKruger and R Seifert ldquoMethanogenic capabilities of ANME-archaea deduced from 13C-labelling approachesrdquo Environmen-tal Microbiology vol 15 no 8 pp 2384ndash2393 2013

[24] K G Lloyd M J Alperin and A Teske ldquoEnvironmental evi-dence for net methane production and oxidation in putativeANaerobic MEthanotrophic (ANME) archaeardquo EnvironmentalMicrobiology vol 13 no 9 pp 2548ndash2564 2011

[25] M Takeuchi H Yoshioka Y Seo et al ldquoA distinct freshwater-adapted subgroup of ANME-1 dominates active archaeal com-munities in terrestrial subsurfaces in Japanrdquo EnvironmentalMicrobiology vol 13 no 12 pp 3206ndash3218 2011

[26] R T Amos B A Bekins I M Cozzarelli et al ldquoEvidence foriron-mediated anaerobic methane oxidation in a crude oil-contaminated aquiferrdquo Geobiology vol 10 no 6 pp 506ndash5172012

[27] P H Timmers D A Suarez-Zuluaga M van Rossem MDiender A J Stams and C M Plugge ldquoAnaerobic oxidationof methane associated with sulfate reduction in a naturalfreshwater gas sourcerdquo ISME Journal vol 10 pp 1400ndash14122015

[28] M F Haroon S Hu Y Shi et al ldquoAnaerobic oxidation ofmethane coupled to nitrate reduction in a novel archaeallineagerdquo Nature vol 500 no 7468 pp 567ndash570 2013

[29] H J Mills C Hodges K Wilson I R MacDonald and PA Sobecky ldquoMicrobial diversity in sediments associated withsurface-breaching gas hydrate mounds in the Gulf of MexicordquoFEMS Microbiology Ecology vol 46 no 1 pp 39ndash52 2003

[30] K G Lloyd L Lapham and A Teske ldquoAn anaerobic methane-oxidizing community of ANME-1b archaea in hypersaline gulfofMexico sedimentsrdquoApplied and EnvironmentalMicrobiologyvol 72 no 11 pp 7218ndash7230 2006

[31] A A Raghoebarsing A Pol K T Van De Pas-Schoonen et alldquoA microbial consortium couples anaerobic methane oxidationto denitrificationrdquoNature vol 440 no 7086 pp 918ndash921 2006

[32] S Hu R J Zeng L C Burow P Lant J Keller and Z YuanldquoEnrichment of denitrifying anaerobic methane oxidizingmicroorganismsrdquo Environmental Microbiology Reports vol 1no 5 pp 377ndash384 2009

[33] Z-W Ding J Ding L Fu F Zhang and R J Zeng ldquoSimultane-ous enrichment of denitrifying methanotrophs and anammoxbacteriardquo Applied Microbiology and Biotechnology vol 98 no24 pp 10211ndash10221 2014

[34] R Seifert K Nauhaus M Blumenberg M Kruger and WMichaelis ldquoMethane dynamics in a microbial community ofthe Black Sea traced by stable carbon isotopes in vitrordquoOrganicGeochemistry vol 37 no 10 pp 1411ndash1419 2006

[35] J Ding Z-W Ding L Fu Y-Z Lu S H Cheng and R JZeng ldquoNew primers for detecting and quantifying denitrifyinganaerobic methane oxidation archaea in different ecologicalnichesrdquo Applied Microbiology and Biotechnology vol 99 no 22pp 9805ndash9812 2015

[36] A Vaksmaa C Luke T van Alen et al ldquoDistribution and activ-ity of the anaerobic methanotrophic community in a nitrogen-fertilized Italian paddy soilrdquo FEMS Microbiology Ecology vol92 no 12 2016

[37] P N Evans D H Parks G L Chadwick et al ldquoMethanemetabolism in the archaeal phylum Bathyarchaeota revealed bygenome-centric metagenomicsrdquo Science vol 350 no 6259 pp434ndash438 2015

[38] I Vanwonterghem P N Evans D H Parks et al ldquoMethy-lotrophic methanogenesis discovered in the archaeal phylumVerstraetearchaeotardquo Nature Microbiology vol 1 Article ID16170 2016

[39] P Worm J J Koehorst M Visser et al ldquoA genomic view onsyntrophic versus non-syntrophic lifestyle in anaerobic fattyacid degrading communitiesrdquo Biochimica et Biophysica ActamdashBioenergetics vol 1837 no 12 pp 2004ndash2016 2014

[40] R Stokke I Roalkvam A Lanzen H Haflidason and I HSteen ldquoIntegrated metagenomic and metaproteomic analysesof an ANME-1-dominated community in marine cold seepsedimentsrdquo Environmental Microbiology vol 14 no 5 pp 1333ndash1346 2012

[41] A Meyerdierks M Kube I Kostadinov et al ldquoMetagenomeand mRNA expression analyses of anaerobic methanotrophicarchaea of the ANME-1 grouprdquo Environmental Microbiologyvol 12 no 2 pp 422ndash439 2010

[42] F-P Wang Y Zhang Y Chen et al ldquoMethanotrophicarchaea possessing diverging methane-oxidizing and electron-transporting pathwaysrdquo ISME Journal vol 8 no 5 pp 1069ndash1078 2014

[43] A Arshad D R Speth R M de Graaf H J Op den Camp MS Jetten and C U Welte ldquoA metagenomics-based metabolicmodel of nitrate-dependent anaerobic oxidation of methane byMethanoperedens-like archaeardquo Frontiers inMicrobiology vol 6article1423 2015

[44] S J Hallam N Putnam CM Preston et al ldquoReversemethano-genesis testing the hypothesis with environmental genomicsrdquoScience vol 305 no 5689 pp 1457ndash1462 2004

Archaea 19

[45] R K Thauer ldquoAnaerobic oxidation of methane with sulfate onthe reversibility of the reactions that are catalyzed by enzymesalso involved inmethanogenesis fromCO

2rdquoCurrent Opinion in

Microbiology vol 14 no 3 pp 292ndash299 2011[46] U Deppenmeier V Muller and G Gottschalk ldquoPathways of

energy conservation in methanogenic archaeardquo Archives ofMicrobiology vol 165 no 3 pp 149ndash163 1996

[47] A-K Kaster J Moll K Parey and R K Thauer ldquoCoupling offerredoxin and heterodisulfide reduction via electron bifurca-tion in hydrogenotrophic methanogenic archaeardquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 108 no 7 pp 2981ndash2986 2011

[48] R K Thauer A-K Kaster H Seedorf W Buckel and RHedderich ldquoMethanogenic archaea ecologically relevant dif-ferences in energy conservationrdquo Nature Reviews Microbiologyvol 6 no 8 pp 579ndash591 2008

[49] W Ludwig O Strunk R Westram et al ldquoARB a softwareenvironment for sequence datardquoNucleic Acids Research vol 32no 4 pp 1363ndash1371 2004

[50] E Pruesse C Quast K Knittel et al ldquoSILVA a comprehensiveonline resource for quality checked and aligned ribosomal RNAsequence data compatible with ARBrdquo Nucleic Acids Researchvol 35 no 21 pp 7188ndash7196 2007

[51] J J Marlow C T Skennerton Z Li et al ldquoProteomic stableisotope probing reveals biosynthesis dynamics of slow growingmethane based microbial communitiesrdquo Frontiers in Microbiol-ogy vol 7 article 386 2016

[52] P V Welander and W W Metcalf ldquoLoss of the mtr operon inMethanosarcina blocks growth on methanol but not methano-genesis and reveals an unknown methanogenic pathwayrdquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 102 no 30 pp 10664ndash10669 2005

[53] P V Welander and W W Metcalf ldquoMutagenesis of the C1oxidation pathway inmethanosarcina barkeri new insights intothe MtrMer bypass pathwayrdquo Journal of Bacteriology vol 190no 6 pp 1928ndash1936 2008

[54] M Goenrich R K Thauer H Yurimoto and N KatoldquoFormaldehyde activating enzyme (Fae) and hexulose-6-phosphate synthase (Hps) inMethanosarcina barkeri a possiblefunction in ribose-5-phosphate biosynthesisrdquoArchives ofMicro-biology vol 184 no 1 pp 41ndash48 2005

[55] M Goenrich FMahlert E C Duin C Bauer B Jaun and R KThauer ldquoProbing the reactivity of Ni in the active site of methyl-coenzyme M reductase with substrate analoguesrdquo Journal ofBiological Inorganic Chemistry vol 9 no 6 pp 691ndash705 2004

[56] S Scheller M Goenrich R Boecher R K Thauer and BJaun ldquoThe key nickel enzyme of methanogenesis catalyses theanaerobic oxidation of methanerdquo Nature vol 465 no 7298 pp606ndash608 2010

[57] K Nauhaus A Boetius M Kruger and F Widdel ldquoIn vitrodemonstration of anaerobic oxidation of methane coupled tosulphate reduction in sediment from amarine gas hydrate areardquoEnvironmental Microbiology vol 4 no 5 pp 296ndash305 2002

[58] Y Zhang J-P Henriet J Bursens and N Boon ldquoStimulationof in vitro anaerobic oxidation of methane rate in a continuoushigh-pressure bioreactorrdquo Bioresource Technology vol 101 no9 pp 3132ndash3138 2010

[59] M Kruger T Treude H Wolters K Nauhaus and A BoetiusldquoMicrobial methane turnover in different marine habitatsrdquoPalaeogeography Palaeoclimatology Palaeoecology vol 227 no1ndash3 pp 6ndash17 2005

[60] C Deusner V Meyer and T G Ferdelman ldquoHigh-pressuresystems for gas-phase free continuous incubation of enrichedmarinemicrobial communities performing anaerobic oxidationof methanerdquo Biotechnology and Bioengineering vol 105 no 3pp 524ndash533 2010

[61] K Nauhaus T Treude A Boetius and M Kruger ldquoEnviron-mental regulation of the anaerobic oxidation of methane acomparison of ANME-I and ANME-II communitiesrdquo Environ-mental Microbiology vol 7 no 1 pp 98ndash106 2005

[62] T Treude V Orphan K Knittel A Gieseke C H House andA Boetius ldquoConsumption of methane and CO

2by methan-

otrophicmicrobial mats from gas seeps of the anoxic Black SeardquoApplied and EnvironmentalMicrobiology vol 73 no 7 pp 2271ndash2283 2007

[63] T Holler F Widdel K Knittel et al ldquoThermophilic anaerobicoxidation of methane by marine microbial consortiardquo ISMEJournal vol 5 no 12 pp 1946ndash1956 2011

[64] M Kruger M Blumenberg S Kasten et al ldquoA novel multi-layered methanotrophic microbial mat system growing on thesediment of the Black Seardquo Environmental Microbiology vol 10no 8 pp 1934ndash1947 2008

[65] R J WMeulepas C G Jagersma J Gieteling C J N BuismanA J M Stams and P N L Lens ldquoEnrichment of anaerobicmethanotrophs in sulfate-reducing membrane bioreactorsrdquoBiotechnology and Bioengineering vol 104 no 3 pp 458ndash4702009

[66] T Holler G Wegener H Niemann et al ldquoCarbon and sulfurback flux during anaerobic microbial oxidation of methane andcoupled sulfate reductionrdquo Proceedings of the National Academyof Sciences of the United States of America vol 108 no 52 ppE1484ndashE1490 2011

[67] M Kruger AMeyerdierks F O Glockner et al ldquoA conspicuousnickel protein in microbial mats that oxidize methane anaero-bicallyrdquo Nature vol 426 no 6968 pp 878ndash881 2003

[68] S Mayr C Latkoczy M Kruger et al ldquoStructure of an F430

variant from archaea associated with anaerobic oxidation ofmethanerdquo Journal of the American Chemical Society vol 130 no32 pp 10758ndash10767 2008

[69] S Shima and R K Thauer ldquoMethyl-coenzyme M reductaseand the anaerobic oxidation of methane in methanotrophicArchaeardquo Current Opinion in Microbiology vol 8 no 6 pp643ndash648 2005

[70] R K Thauer and S Shima ldquoMethane as fuel for anaerobicmicroorganismsrdquo Annals of the New York Academy of Sciencesvol 1125 pp 158ndash170 2008

[71] S Yamamoto J B Alcauskas and T E Crozier ldquoSolubility ofmethane in distilled water and seawaterrdquo Journal of Chemicaland Engineering Data vol 21 no 1 pp 78ndash80 1976

[72] P H A Timmers J Gieteling H C A Widjaja-Greefkeset al ldquoGrowth of anaerobic methane-oxidizing archaea andsulfate-reducing bacteria in a high-pressure membrane capsulebioreactorrdquoApplied and EnvironmentalMicrobiology vol 81 no4 pp 1286ndash1296 2015

[73] MKruger HWoltersMGehre S B Joye andH-H RichnowldquoTracing the slow growth of anaerobic methane-oxidizingcommunities by 15N-labelling techniquesrdquo FEMS MicrobiologyEcology vol 63 no 3 pp 401ndash411 2008

[74] R J W Meulepas C G Jagersma A F Khadem C J N Buis-man A J M Stams and P N L Lens ldquoEffect of environmentalconditions on sulfate reduction withmethane as electron donorby an Eckernforde Bay enrichmentrdquo Environmental Science andTechnology vol 43 no 17 pp 6553ndash6559 2009

20 Archaea

[75] M W Bowles V A Samarkin and S B Joye ldquoImprovedmeasurement of microbial activity in deep-sea sediments atin situ pressure and methane concentrationrdquo Limnology andOceanography Methods vol 9 pp 499ndash506 2011

[76] S Shima M Krueger T Weinert et al ldquoStructure of a methyl-coenzyme M reductase from Black Sea mats that oxidizemethane anaerobicallyrdquo Nature vol 481 no 7379 pp 98ndash1012012

[77] K D Allen G Wegener and R H White ldquoDiscovery of multi-ple modified F-430 coenzymes in methanogens and anaerobicmethanotrophic archaea suggests possible new roles for F-430in naturerdquoApplied and Environmental Microbiology vol 80 no20 pp 6403ndash6412 2014

[78] V W Soo M J McAnulty A Tripathi et al ldquoReversingmethanogenesis to capture methane for liquid biofuel precur-sorsrdquoMicrobial Cell Factories vol 15 article 11 2016

[79] D L Valentine and W S Reeburgh ldquoNew perspectives onanaerobicmethane oxidationrdquoEnvironmentalMicrobiology vol2 no 5 pp 477ndash484 2000

[80] D L Valentine ldquoBiogeochemistry and microbial ecology ofmethane oxidation in anoxic environments a reviewrdquo Antonievan Leeuwenhoek International Journal of General and Molecu-lar Microbiology vol 81 no 1-4 pp 271ndash282 2002

[81] A J B Zehnder and T D Brock ldquoMethane formation andmethane oxidation by methanogenic bacteriardquo Journal of Bac-teriology vol 137 no 1 pp 420ndash432 1979

[82] J Harder ldquoAnaerobic methane oxidation by bacteria employ-ing 14C-methane uncontaminated with 14C-carbon monoxiderdquoMarine Geology vol 137 no 1-2 pp 13ndash23 1997

[83] J J Moran C H House K H Freeman and J G FerryldquoTrace methane oxidation studied in several Euryarchaeotaunder diverse conditionsrdquo Archaea vol 1 no 5 pp 303ndash3092005

[84] J J Moran C H House B Thomas and K H FreemanldquoProducts of tracemethane oxidation during nonmethyltrophicgrowth by Methanosarcinardquo Journal of Geophysical ResearchBiogeosciences vol 112 no 2 2007

[85] R J W Meulepas C G Jagersma Y Zhang et al ldquoTracemethane oxidation and the methane dependency of sulfatereduction in anaerobic granular sludgerdquo FEMS MicrobiologyEcology vol 72 no 2 pp 261ndash271 2010

[86] A J B Zehnder andTD Brock ldquoAnaerobicmethane oxidationoccurrence and ecologyrdquoApplied and Environmental Microbiol-ogy vol 39 no 1 pp 194ndash204 1980

[87] S J Blazewicz D G Petersen M P Waldrop and M K Fire-stone ldquoAnaerobic oxidation of methane in tropical and borealsoils ecological significance in terrestrial methane cyclingrdquoJournal of Geophysical Research Biogeosciences vol 117 no 2Article ID G02033 2012

[88] K A Smemo and J B Yavitt ldquoEvidence for anaerobic CH4

oxidation in freshwater peatlandsrdquo Geomicrobiology Journalvol 24 no 7-8 pp 583ndash597 2007

[89] M J Alperin and T M Hoehler ldquoAnaerobic methane oxidationby archaeasulfate-reducing bacteria aggregates 1 Thermody-namic and physical constraintsrdquo American Journal of Sciencevol 309 no 10 pp 869ndash957 2009

[90] S L Caldwell J R Laidler E A Brewer J O Eberly S CSandborgh and F S Colwell ldquoAnaerobic oxidation of methanemechanisms bioenergetics and the ecology of associatedmicroorganismsrdquo Environmental Science and Technology vol42 no 18 pp 6791ndash6799 2008

[91] GWang A J Spivack and S DrsquoHondt ldquoGibbs energies of reac-tion and microbial mutualism in anaerobic deep subseafloorsediments of ODP Site 1226rdquoGeochimica et Cosmochimica Actavol 74 no 14 pp 3938ndash3947 2010

[92] P R Girguis A E Cozen and E F DeLong ldquoGrowth andpopulation dynamics of anaerobic methane-oxidizing archaeaand sulfate-reducing bacteria in a continuous-flow bioreactorrdquoApplied and EnvironmentalMicrobiology vol 71 no 7 pp 3725ndash3733 2005

[93] K Nauhaus M Albrecht M Elvert A Boetius and F WiddelldquoIn vitro cell growth ofmarine archaeal-bacterial consortia dur-ing anaerobic oxidation ofmethanewith sulfaterdquoEnvironmentalMicrobiology vol 9 no 1 pp 187ndash196 2007

[94] B Orcutt V Samarkin A Boetius and S Joye ldquoOn the relation-ship between methane production and oxidation by anaerobicmethanotrophic communities from cold seeps of the Gulf ofMexicordquo Environmental Microbiology vol 10 no 5 pp 1108ndash1117 2008

[95] M Y Yoshinaga T Holler T Goldhammer et al ldquoCarbon iso-tope equilibration during sulphate-limited anaerobic oxidationof methanerdquo Nature Geoscience vol 7 no 3 pp 190ndash194 2014

[96] T Treude J Niggemann J Kallmeyer et al ldquoAnaerobic oxi-dation of methane and sulfate reduction along the Chileancontinental marginrdquo Geochimica et Cosmochimica Acta vol 69no 11 pp 2767ndash2779 2005

[97] R J Parkes B A Cragg N Banning et al ldquoBiogeochemistryand biodiversity of methane cycling in subsurface marinesediments (SkagerrakDenmark)rdquoEnvironmentalMicrobiologyvol 9 no 5 pp 1146ndash1161 2007

[98] N J Knab B A Cragg E R C Hornibrook et al ldquoRegulationof anaerobic methane oxidation in sediments of the Black SeardquoBiogeosciences vol 6 no 8 pp 1505ndash1518 2009

[99] H Yoshioka A Maruyama T Nakamura et al ldquoActivities anddistribution of methanogenic and methane-oxidizing microbesin marine sediments from the Cascadia Marginrdquo Geobiologyvol 8 no 3 pp 223ndash233 2010

[100] G Wegener V Krukenberg S E Ruff M Y Kellermann andK Knittel ldquoMetabolic capabilities of microorganisms involvedin and associated with the anaerobic oxidation of methanerdquoFrontiers in Microbiology vol 7 article 46 2016

[101] R J W Meulepas C G Jagersma A F Khadem A J MStams and P N L Lens ldquoEffect of methanogenic substrateson anaerobic oxidation of methane and sulfate reduction by ananaerobic methanotrophic enrichmentrdquo Applied Microbiologyand Biotechnology vol 87 no 4 pp 1499ndash1506 2010

[102] J Milucka T G Ferdelman L Polerecky et al ldquoZero-valentsulphur is a key intermediate in marine methane oxidationrdquoNature vol 491 no 7425 pp 541ndash546 2012

[103] W Michaelis R Seifert K Nauhaus et al ldquoMicrobial reefs inthe black sea fueled by anaerobic oxidation ofmethanerdquo Sciencevol 297 no 5583 pp 1013ndash1015 2002

[104] A Vigneron P Cruaud P Pignet et al ldquoArchaeal and anaerobicmethane oxidizer communities in the Sonora Margin coldseeps Guaymas Basin (Gulf of California)rdquo ISME Journal vol7 no 8 pp 1595ndash1608 2013

[105] M Alperin and T Hoehler ldquoThe ongoing mystery of sea-floormethanerdquo Science vol 329 no 5989 pp 288ndash289 2010

[106] B Orcutt and C Meile ldquoConstraints on mechanisms and ratesof anaerobic oxidation of methane by microbial consortiaprocess-basedmodeling of ANME-2 archaea and sulfate reduc-ing bacteria interactionsrdquo Biogeosciences vol 5 no 6 pp 1587ndash1599 2008

Archaea 21

[107] S E McGlynn G L Chadwick C P Kempes and V J OrphanldquoSingle cell activity reveals direct electron transfer in methan-otrophic consortiardquoNature vol 526 no 7574 pp 531ndash535 2015

[108] D R Lovley ldquoElectromicrobiologyrdquo Annual Review of Microbi-ology vol 66 pp 391ndash409 2012

[109] S M Strycharz-Glaven R M Snider A Guiseppi-Elie andL M Tender ldquoOn the electrical conductivity of microbialnanowires and biofilmsrdquoEnergy and Environmental Science vol4 no 11 pp 4366ndash4379 2011

[110] D J Richardson J N Butt J K Fredrickson et al ldquoThe lsquoporinndashcytochromersquo model for microbe-to-mineral electron transferrdquoMolecular Microbiology vol 85 no 2 pp 201ndash212 2012

[111] A Okamoto K Hashimoto and R Nakamura ldquoLong-rangeelectron conduction of Shewanella biofilms mediated by outermembrane C-type cytochromesrdquo Bioelectrochemistry vol 85pp 61ndash65 2012

[112] M Y El-Naggar G Wanger K M Leung et al ldquoElectricaltransport along bacterial nanowires from Shewanella oneidensisMR-1rdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 107 no 42 pp 18127ndash18131 2010

[113] G Reguera K D McCarthy T Mehta J S Nicoll M TTuominen and D R Lovley ldquoExtracellular electron transfer viamicrobial nanowiresrdquo Nature vol 435 no 7045 pp 1098ndash11012005

[114] Z M Summers H E Fogarty C Leang A E Franks N SMalvankar and D R Lovley ldquoDirect exchange of electronswithin aggregates of an evolved syntrophic coculture of anaer-obic bacteriardquo Science vol 330 no 6009 pp 1413ndash1415 2010

[115] A Kletzin T Heimerl J Flechsler L V Niftrik R Rachel andA Klingl ldquoCytochromes c in archaea distribution maturationcell architecture and the special case of Ignicoccus hospitalisrdquoFrontiers in Microbiology vol 6 article 439 2015

[116] GWegener V Krukenberg D Riedel H E Tegetmeyer and ABoetius ldquoIntercellular wiring enables electron transfer betweenmethanotrophic archaea and bacteriardquo Nature vol 526 no7574 pp 587ndash590 2015

[117] D HHaft S H Payne and J D Selengut ldquoArchaeosortases andexosortases are widely distributed systems linking membranetransit with posttranslational modificationrdquo Journal of Bacteri-ology vol 194 no 1 pp 36ndash48 2012

[118] A Marchler-Bauer M K Derbyshire N R Gonzales et alldquoCDD NCBIrsquos conserved domain databaserdquo Nucleic AcidsResearch vol 43 no 1 pp D222ndashD226 2015

[119] A Mitchell H-Y Chang L Daugherty et al ldquoThe InterProprotein families database the classification resource after 15yearsrdquo Nucleic Acids Research vol 43 no 1 pp D213ndashD2212015

[120] V Krukenberg K Harding M Richter et al ldquoCandidatusdesulfofervidus auxilii a hydrogenotrophic sulfate-reducingbacterium involved in the thermophilic anaerobic oxidation ofmethanerdquo Environmental Microbiology vol 18 pp 3073ndash30912016

[121] L Shi T C Squier J M Zachara and J K Fredrickson ldquoRes-piration of metal (hydr)oxides by Shewanella and Geobactera key role for multihaem c-type cytochromesrdquo MolecularMicrobiology vol 65 no 1 pp 12ndash20 2007

[122] N S Malvankar and D R Lovley ldquoMicrobial nanowires forbioenergy applicationsrdquo Current Opinion in Biotechnology vol27 pp 88ndash95 2014

[123] A-E Rotaru T LWoodard K PNevin andDR Lovley ldquoLinkbetween capacity for current production and syntrophic growth

in Geobacter speciesrdquo Frontiers in Microbiology vol 6 article744 2015

[124] A-E Rotaru P M Shrestha F Liu et al ldquoDirect interspecieselectron transfer between Geobacter metallireducens andMethanosarcina barkerirdquo Applied and Environmental Microbi-ology vol 80 no 15 pp 4599ndash4605 2014

[125] S Scheller H Yu G L Chadwick S E McGlynn and VJ Orphan ldquoArtificial electron acceptors decouple archaealmethane oxidation from sulfate reductionrdquo Science vol 351 no6274 pp 703ndash707 2016

[126] J Milucka F Widdel and S Shima ldquoImmunological detec-tion of enzymes for sulfate reduction in anaerobic methane-oxidizing consortiardquo Environmental Microbiology vol 15 no 5pp 1561ndash1571 2013

[127] P Cabello M D Roldan and C Moreno-Vivian ldquoNitratereduction and the nitrogen cycle in archaeardquoMicrobiology vol150 no 11 pp 3527ndash3546 2004

[128] R MMartinez-Espinosa E J Dridge M J Bonete et al ldquoLookon the positive sideThe orientation identification and bioener-getics of lsquoArchaealrsquomembrane-boundnitrate reductasesrdquoFEMSMicrobiology Letters vol 276 no 2 pp 129ndash139 2007

[129] S de VriesMMomcilovicM J F Strampraad J PWhiteleggeA Baghai and I Schroder ldquoAdaptation to a high-tungsten envi-ronment pyrobaculum aerophilum contains an active tungstennitrate reductaserdquo Biochemistry vol 49 no 45 pp 9911ndash99212010

[130] M Egger O Rasigraf C J Sapart et al ldquoIron-mediated anaer-obic oxidation of methane in brackish coastal sedimentsrdquoEnvironmental Science and Technology vol 49 no 1 pp 277ndash283 2015

[131] T Treude S Krause J Maltby A W Dale R Coffin and LJ Hamdan ldquoSulfate reduction and methane oxidation activitybelow the sulfate-methane transition zone in Alaskan BeaufortSea continental margin sediments implications for deep sulfurcyclingrdquo Geochimica et Cosmochimica Acta vol 144 pp 217ndash237 2014

[132] N Riedinger M J Formolo T W Lyons S Henkel A Beckand S Kasten ldquoAn inorganic geochemical argument for coupledanaerobic oxidation of methane and iron reduction in marinesedimentsrdquo Geobiology vol 12 no 2 pp 172ndash181 2014

[133] Y-H Chang T-W Cheng W-J Lai et al ldquoMicrobial methanecycling in a terrestrialmud volcano in eastern Taiwanrdquo Environ-mental Microbiology vol 14 no 4 pp 895ndash908 2012

[134] S A Crowe S Katsev K Leslie et al ldquoThe methane cycle inferruginous Lake Matanordquo Geobiology vol 9 no 1 pp 61ndash782011

[135] O Sivan M Adler A Pearson et al ldquoGeochemical evidence foriron-mediated anaerobic oxidation of methanerdquo Limnology andOceanography vol 56 no 4 pp 1536ndash1544 2011

[136] K E A Segarra C Comerford J Slaughter and S B JoyeldquoImpact of electron acceptor availability on the anaerobic oxi-dation of methane in coastal freshwater and brackish wetlandsedimentsrdquo Geochimica et Cosmochimica Acta vol 115 pp 15ndash30 2013

[137] V Gupta K A Smemo J B Yavitt D Fowle B Branfireunand N Basiliko ldquoStable isotopes reveal widespread anaerobicmethane oxidation across latitude and peatland typerdquo Environ-mental Science and Technology vol 47 no 15 pp 8273ndash82792013

[138] O Oni T Miyatake S Kasten et al ldquoDistinct microbialpopulations are tightly linked to the profile of dissolved iron in

22 Archaea

the methanic sediments of the Helgolandmud area North SeardquoFrontiers in Microbiology vol 6 2015

[139] E J Beal C H House and V J Orphan ldquoManganese- andiron-dependent marine methane oxidationrdquo Science vol 325no 5937 pp 184ndash187 2009

[140] M W Bowles V A Samarkin K M Bowles and S B JoyeldquoWeak coupling between sulfate reduction and the anaerobicoxidation of methane in methane-rich seafloor sedimentsduring ex situ incubationrdquo Geochimica et Cosmochimica Actavol 75 no 2 pp 500ndash519 2011

[141] Y Z Lu L Fu J Ding Z Ding N Li and R J Zeng ldquoCr(VI)reduction coupled with anaerobic oxidation of methane in alaboratory reactorrdquoWater Research vol 102 pp 445ndash452 2016

[142] K F Ettwig B Zhu D Speth J T Keltjens M S Jetten and BKartal ldquoArchaea catalyze iron-dependent anaerobic oxidationof methanerdquo Proceedings of the National Academy of Sciences ofthe United States of America vol 113 no 45 pp 12792ndash127962016

[143] T M Flynn R A Sanford H Ryu et al ldquoFunctional microbialdiversity explains groundwater chemistry in a pristine aquiferrdquoBMCMicrobiology vol 13 no 1 article no 146 2013

[144] C J Schubert F Vazquez T Losekann-Behrens K KnittelM Tonolla and A Boetius ldquoEvidence for anaerobic oxidationof methane in sediments of a freshwater system (Lago diCadagno)rdquo FEMS Microbiology Ecology vol 76 no 1 pp 26ndash38 2011

[145] K E A Segarra F Schubotz V Samarkin M Y Yoshinaga K-U Hinrichs and S B Joye ldquoHigh rates of anaerobic methaneoxidation in freshwater wetlands reduce potential atmosphericmethane emissionsrdquo Nature Communications vol 6 article7477 2015

[146] E J Beal M W Claire and C H House ldquoHigh rates ofanaerobic methanotrophy at low sulfate concentrations withimplications for past and present methane levelsrdquo Geobiologyvol 9 no 2 pp 131ndash139 2011

[147] F Kracke I Vassilev and J O Kromer ldquoMicrobial electrontransport and energy conservationmdashthe foundation for opti-mizing bioelectrochemical systemsrdquo Frontiers in Microbiologyvol 6 article 575 2015

[148] C L Reardon A C Dohnalkova P Nachimuthu et al ldquoRoleof outer-membrane cytochromes MtrC and OmcA in thebiomineralization of ferrihydrite by Shewanella oneidensisMR-1rdquo Geobiology vol 8 no 1 pp 56ndash68 2010

[149] L Shi B Chen Z Wang et al ldquoIsolation of a high-affinityfunctional protein complex between OmcA and MtrC twoouter membrane decaheme c-type cytochromes of Shewanellaoneidensis MR-1rdquo Journal of Bacteriology vol 188 no 13 pp4705ndash4714 2006

[150] X Qian T Mester L Morgado et al ldquoBiochemical charac-terization of purified OmcS a c-type cytochrome requiredfor insoluble Fe(III) reduction in Geobacter sulfurreducensrdquoBiochimica et BiophysicaActamdashBioenergetics vol 1807 no 4 pp404ndash412 2011

[151] T Mehta M V Coppi S E Childers and D R Lovley ldquoOutermembrane c-type cytochromes required for Fe(III) andMn(IV)oxide reduction in Geobacter sulfurreducensrdquo Applied andEnvironmentalMicrobiology vol 71 no 12 pp 8634ndash8641 2005

[152] W Blankenfeldt A P Kuzin T Skarina et al ldquoStructure andfunction of the phenazine biosynthetic protein PhzF fromPseudomonas fluorescensrdquoProceedings of theNational Academyof Sciences of the United States of America vol 101 no 47 pp16431ndash16436 2004

[153] J F Parsons F Song L Parsons K Calabrese E Eisensteinand J E Ladner ldquoStructure and function of the phenazinebiosynthesis protein PhzF fromPseudomonas fluorescens 2-79rdquoBiochemistry vol 43 no 39 pp 12427ndash12435 2004

[154] T Hiratsuka K Furihata J Ishikawa et al ldquoAn alternativemenaquinone biosynthetic pathway operating in microorgan-ismsrdquo Science vol 321 no 5896 pp 1670ndash1673 2008

[155] M Tietze A Beuchle I Lamla et al ldquoRedox potentials ofmethanophenazine and CoB-S-S-CoM factors involved inelectron transport in methanogenic archaeardquo ChemBioChemvol 4 no 4 pp 333ndash335 2003

[156] Q H Tran and G Unden ldquoChanges in the proton potentialand the cellular energetics of Escherichia coli during growth byaerobic and anaerobic respiration or by fermentationrdquoEuropeanJournal of Biochemistry vol 251 no 1-2 pp 538ndash543 1998

[157] I Callebaut D Gilges I Vigon and J-P Mornon ldquoHYR anextracellular module involved in cellular adhesion and relatedto the immunoglobulin-like foldrdquo Protein Science vol 9 no 7pp 1382ndash1390 2000

[158] H J Gilbert ldquoCellulosomes microbial nanomachines that dis-play plasticity in quaternary structurerdquoMolecular Microbiologyvol 63 no 6 pp 1568ndash1576 2007

[159] A Peer S P Smith E A Bayer R Lamed and I BorovokldquoNoncellulosomal cohesin- and dockerin-like modules in thethree domains of liferdquo FEMS Microbiology Letters vol 291 no1 pp 1ndash16 2009

[160] M Wagner ldquoMicrobiology conductive consortiardquo Nature vol526 no 7574 pp 513ndash514 2015

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Archaea 19

[45] R K Thauer ldquoAnaerobic oxidation of methane with sulfate onthe reversibility of the reactions that are catalyzed by enzymesalso involved inmethanogenesis fromCO

2rdquoCurrent Opinion in

Microbiology vol 14 no 3 pp 292ndash299 2011[46] U Deppenmeier V Muller and G Gottschalk ldquoPathways of

energy conservation in methanogenic archaeardquo Archives ofMicrobiology vol 165 no 3 pp 149ndash163 1996

[47] A-K Kaster J Moll K Parey and R K Thauer ldquoCoupling offerredoxin and heterodisulfide reduction via electron bifurca-tion in hydrogenotrophic methanogenic archaeardquo Proceedingsof the National Academy of Sciences of the United States ofAmerica vol 108 no 7 pp 2981ndash2986 2011

[48] R K Thauer A-K Kaster H Seedorf W Buckel and RHedderich ldquoMethanogenic archaea ecologically relevant dif-ferences in energy conservationrdquo Nature Reviews Microbiologyvol 6 no 8 pp 579ndash591 2008

[49] W Ludwig O Strunk R Westram et al ldquoARB a softwareenvironment for sequence datardquoNucleic Acids Research vol 32no 4 pp 1363ndash1371 2004

[50] E Pruesse C Quast K Knittel et al ldquoSILVA a comprehensiveonline resource for quality checked and aligned ribosomal RNAsequence data compatible with ARBrdquo Nucleic Acids Researchvol 35 no 21 pp 7188ndash7196 2007

[51] J J Marlow C T Skennerton Z Li et al ldquoProteomic stableisotope probing reveals biosynthesis dynamics of slow growingmethane based microbial communitiesrdquo Frontiers in Microbiol-ogy vol 7 article 386 2016

[52] P V Welander and W W Metcalf ldquoLoss of the mtr operon inMethanosarcina blocks growth on methanol but not methano-genesis and reveals an unknown methanogenic pathwayrdquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 102 no 30 pp 10664ndash10669 2005

[53] P V Welander and W W Metcalf ldquoMutagenesis of the C1oxidation pathway inmethanosarcina barkeri new insights intothe MtrMer bypass pathwayrdquo Journal of Bacteriology vol 190no 6 pp 1928ndash1936 2008

[54] M Goenrich R K Thauer H Yurimoto and N KatoldquoFormaldehyde activating enzyme (Fae) and hexulose-6-phosphate synthase (Hps) inMethanosarcina barkeri a possiblefunction in ribose-5-phosphate biosynthesisrdquoArchives ofMicro-biology vol 184 no 1 pp 41ndash48 2005

[55] M Goenrich FMahlert E C Duin C Bauer B Jaun and R KThauer ldquoProbing the reactivity of Ni in the active site of methyl-coenzyme M reductase with substrate analoguesrdquo Journal ofBiological Inorganic Chemistry vol 9 no 6 pp 691ndash705 2004

[56] S Scheller M Goenrich R Boecher R K Thauer and BJaun ldquoThe key nickel enzyme of methanogenesis catalyses theanaerobic oxidation of methanerdquo Nature vol 465 no 7298 pp606ndash608 2010

[57] K Nauhaus A Boetius M Kruger and F Widdel ldquoIn vitrodemonstration of anaerobic oxidation of methane coupled tosulphate reduction in sediment from amarine gas hydrate areardquoEnvironmental Microbiology vol 4 no 5 pp 296ndash305 2002

[58] Y Zhang J-P Henriet J Bursens and N Boon ldquoStimulationof in vitro anaerobic oxidation of methane rate in a continuoushigh-pressure bioreactorrdquo Bioresource Technology vol 101 no9 pp 3132ndash3138 2010

[59] M Kruger T Treude H Wolters K Nauhaus and A BoetiusldquoMicrobial methane turnover in different marine habitatsrdquoPalaeogeography Palaeoclimatology Palaeoecology vol 227 no1ndash3 pp 6ndash17 2005

[60] C Deusner V Meyer and T G Ferdelman ldquoHigh-pressuresystems for gas-phase free continuous incubation of enrichedmarinemicrobial communities performing anaerobic oxidationof methanerdquo Biotechnology and Bioengineering vol 105 no 3pp 524ndash533 2010

[61] K Nauhaus T Treude A Boetius and M Kruger ldquoEnviron-mental regulation of the anaerobic oxidation of methane acomparison of ANME-I and ANME-II communitiesrdquo Environ-mental Microbiology vol 7 no 1 pp 98ndash106 2005

[62] T Treude V Orphan K Knittel A Gieseke C H House andA Boetius ldquoConsumption of methane and CO

2by methan-

otrophicmicrobial mats from gas seeps of the anoxic Black SeardquoApplied and EnvironmentalMicrobiology vol 73 no 7 pp 2271ndash2283 2007

[63] T Holler F Widdel K Knittel et al ldquoThermophilic anaerobicoxidation of methane by marine microbial consortiardquo ISMEJournal vol 5 no 12 pp 1946ndash1956 2011

[64] M Kruger M Blumenberg S Kasten et al ldquoA novel multi-layered methanotrophic microbial mat system growing on thesediment of the Black Seardquo Environmental Microbiology vol 10no 8 pp 1934ndash1947 2008

[65] R J WMeulepas C G Jagersma J Gieteling C J N BuismanA J M Stams and P N L Lens ldquoEnrichment of anaerobicmethanotrophs in sulfate-reducing membrane bioreactorsrdquoBiotechnology and Bioengineering vol 104 no 3 pp 458ndash4702009

[66] T Holler G Wegener H Niemann et al ldquoCarbon and sulfurback flux during anaerobic microbial oxidation of methane andcoupled sulfate reductionrdquo Proceedings of the National Academyof Sciences of the United States of America vol 108 no 52 ppE1484ndashE1490 2011

[67] M Kruger AMeyerdierks F O Glockner et al ldquoA conspicuousnickel protein in microbial mats that oxidize methane anaero-bicallyrdquo Nature vol 426 no 6968 pp 878ndash881 2003

[68] S Mayr C Latkoczy M Kruger et al ldquoStructure of an F430

variant from archaea associated with anaerobic oxidation ofmethanerdquo Journal of the American Chemical Society vol 130 no32 pp 10758ndash10767 2008

[69] S Shima and R K Thauer ldquoMethyl-coenzyme M reductaseand the anaerobic oxidation of methane in methanotrophicArchaeardquo Current Opinion in Microbiology vol 8 no 6 pp643ndash648 2005

[70] R K Thauer and S Shima ldquoMethane as fuel for anaerobicmicroorganismsrdquo Annals of the New York Academy of Sciencesvol 1125 pp 158ndash170 2008

[71] S Yamamoto J B Alcauskas and T E Crozier ldquoSolubility ofmethane in distilled water and seawaterrdquo Journal of Chemicaland Engineering Data vol 21 no 1 pp 78ndash80 1976

[72] P H A Timmers J Gieteling H C A Widjaja-Greefkeset al ldquoGrowth of anaerobic methane-oxidizing archaea andsulfate-reducing bacteria in a high-pressure membrane capsulebioreactorrdquoApplied and EnvironmentalMicrobiology vol 81 no4 pp 1286ndash1296 2015

[73] MKruger HWoltersMGehre S B Joye andH-H RichnowldquoTracing the slow growth of anaerobic methane-oxidizingcommunities by 15N-labelling techniquesrdquo FEMS MicrobiologyEcology vol 63 no 3 pp 401ndash411 2008

[74] R J W Meulepas C G Jagersma A F Khadem C J N Buis-man A J M Stams and P N L Lens ldquoEffect of environmentalconditions on sulfate reduction withmethane as electron donorby an Eckernforde Bay enrichmentrdquo Environmental Science andTechnology vol 43 no 17 pp 6553ndash6559 2009

20 Archaea

[75] M W Bowles V A Samarkin and S B Joye ldquoImprovedmeasurement of microbial activity in deep-sea sediments atin situ pressure and methane concentrationrdquo Limnology andOceanography Methods vol 9 pp 499ndash506 2011

[76] S Shima M Krueger T Weinert et al ldquoStructure of a methyl-coenzyme M reductase from Black Sea mats that oxidizemethane anaerobicallyrdquo Nature vol 481 no 7379 pp 98ndash1012012

[77] K D Allen G Wegener and R H White ldquoDiscovery of multi-ple modified F-430 coenzymes in methanogens and anaerobicmethanotrophic archaea suggests possible new roles for F-430in naturerdquoApplied and Environmental Microbiology vol 80 no20 pp 6403ndash6412 2014

[78] V W Soo M J McAnulty A Tripathi et al ldquoReversingmethanogenesis to capture methane for liquid biofuel precur-sorsrdquoMicrobial Cell Factories vol 15 article 11 2016

[79] D L Valentine and W S Reeburgh ldquoNew perspectives onanaerobicmethane oxidationrdquoEnvironmentalMicrobiology vol2 no 5 pp 477ndash484 2000

[80] D L Valentine ldquoBiogeochemistry and microbial ecology ofmethane oxidation in anoxic environments a reviewrdquo Antonievan Leeuwenhoek International Journal of General and Molecu-lar Microbiology vol 81 no 1-4 pp 271ndash282 2002

[81] A J B Zehnder and T D Brock ldquoMethane formation andmethane oxidation by methanogenic bacteriardquo Journal of Bac-teriology vol 137 no 1 pp 420ndash432 1979

[82] J Harder ldquoAnaerobic methane oxidation by bacteria employ-ing 14C-methane uncontaminated with 14C-carbon monoxiderdquoMarine Geology vol 137 no 1-2 pp 13ndash23 1997

[83] J J Moran C H House K H Freeman and J G FerryldquoTrace methane oxidation studied in several Euryarchaeotaunder diverse conditionsrdquo Archaea vol 1 no 5 pp 303ndash3092005

[84] J J Moran C H House B Thomas and K H FreemanldquoProducts of tracemethane oxidation during nonmethyltrophicgrowth by Methanosarcinardquo Journal of Geophysical ResearchBiogeosciences vol 112 no 2 2007

[85] R J W Meulepas C G Jagersma Y Zhang et al ldquoTracemethane oxidation and the methane dependency of sulfatereduction in anaerobic granular sludgerdquo FEMS MicrobiologyEcology vol 72 no 2 pp 261ndash271 2010

[86] A J B Zehnder andTD Brock ldquoAnaerobicmethane oxidationoccurrence and ecologyrdquoApplied and Environmental Microbiol-ogy vol 39 no 1 pp 194ndash204 1980

[87] S J Blazewicz D G Petersen M P Waldrop and M K Fire-stone ldquoAnaerobic oxidation of methane in tropical and borealsoils ecological significance in terrestrial methane cyclingrdquoJournal of Geophysical Research Biogeosciences vol 117 no 2Article ID G02033 2012

[88] K A Smemo and J B Yavitt ldquoEvidence for anaerobic CH4

oxidation in freshwater peatlandsrdquo Geomicrobiology Journalvol 24 no 7-8 pp 583ndash597 2007

[89] M J Alperin and T M Hoehler ldquoAnaerobic methane oxidationby archaeasulfate-reducing bacteria aggregates 1 Thermody-namic and physical constraintsrdquo American Journal of Sciencevol 309 no 10 pp 869ndash957 2009

[90] S L Caldwell J R Laidler E A Brewer J O Eberly S CSandborgh and F S Colwell ldquoAnaerobic oxidation of methanemechanisms bioenergetics and the ecology of associatedmicroorganismsrdquo Environmental Science and Technology vol42 no 18 pp 6791ndash6799 2008

[91] GWang A J Spivack and S DrsquoHondt ldquoGibbs energies of reac-tion and microbial mutualism in anaerobic deep subseafloorsediments of ODP Site 1226rdquoGeochimica et Cosmochimica Actavol 74 no 14 pp 3938ndash3947 2010

[92] P R Girguis A E Cozen and E F DeLong ldquoGrowth andpopulation dynamics of anaerobic methane-oxidizing archaeaand sulfate-reducing bacteria in a continuous-flow bioreactorrdquoApplied and EnvironmentalMicrobiology vol 71 no 7 pp 3725ndash3733 2005

[93] K Nauhaus M Albrecht M Elvert A Boetius and F WiddelldquoIn vitro cell growth ofmarine archaeal-bacterial consortia dur-ing anaerobic oxidation ofmethanewith sulfaterdquoEnvironmentalMicrobiology vol 9 no 1 pp 187ndash196 2007

[94] B Orcutt V Samarkin A Boetius and S Joye ldquoOn the relation-ship between methane production and oxidation by anaerobicmethanotrophic communities from cold seeps of the Gulf ofMexicordquo Environmental Microbiology vol 10 no 5 pp 1108ndash1117 2008

[95] M Y Yoshinaga T Holler T Goldhammer et al ldquoCarbon iso-tope equilibration during sulphate-limited anaerobic oxidationof methanerdquo Nature Geoscience vol 7 no 3 pp 190ndash194 2014

[96] T Treude J Niggemann J Kallmeyer et al ldquoAnaerobic oxi-dation of methane and sulfate reduction along the Chileancontinental marginrdquo Geochimica et Cosmochimica Acta vol 69no 11 pp 2767ndash2779 2005

[97] R J Parkes B A Cragg N Banning et al ldquoBiogeochemistryand biodiversity of methane cycling in subsurface marinesediments (SkagerrakDenmark)rdquoEnvironmentalMicrobiologyvol 9 no 5 pp 1146ndash1161 2007

[98] N J Knab B A Cragg E R C Hornibrook et al ldquoRegulationof anaerobic methane oxidation in sediments of the Black SeardquoBiogeosciences vol 6 no 8 pp 1505ndash1518 2009

[99] H Yoshioka A Maruyama T Nakamura et al ldquoActivities anddistribution of methanogenic and methane-oxidizing microbesin marine sediments from the Cascadia Marginrdquo Geobiologyvol 8 no 3 pp 223ndash233 2010

[100] G Wegener V Krukenberg S E Ruff M Y Kellermann andK Knittel ldquoMetabolic capabilities of microorganisms involvedin and associated with the anaerobic oxidation of methanerdquoFrontiers in Microbiology vol 7 article 46 2016

[101] R J W Meulepas C G Jagersma A F Khadem A J MStams and P N L Lens ldquoEffect of methanogenic substrateson anaerobic oxidation of methane and sulfate reduction by ananaerobic methanotrophic enrichmentrdquo Applied Microbiologyand Biotechnology vol 87 no 4 pp 1499ndash1506 2010

[102] J Milucka T G Ferdelman L Polerecky et al ldquoZero-valentsulphur is a key intermediate in marine methane oxidationrdquoNature vol 491 no 7425 pp 541ndash546 2012

[103] W Michaelis R Seifert K Nauhaus et al ldquoMicrobial reefs inthe black sea fueled by anaerobic oxidation ofmethanerdquo Sciencevol 297 no 5583 pp 1013ndash1015 2002

[104] A Vigneron P Cruaud P Pignet et al ldquoArchaeal and anaerobicmethane oxidizer communities in the Sonora Margin coldseeps Guaymas Basin (Gulf of California)rdquo ISME Journal vol7 no 8 pp 1595ndash1608 2013

[105] M Alperin and T Hoehler ldquoThe ongoing mystery of sea-floormethanerdquo Science vol 329 no 5989 pp 288ndash289 2010

[106] B Orcutt and C Meile ldquoConstraints on mechanisms and ratesof anaerobic oxidation of methane by microbial consortiaprocess-basedmodeling of ANME-2 archaea and sulfate reduc-ing bacteria interactionsrdquo Biogeosciences vol 5 no 6 pp 1587ndash1599 2008

Archaea 21

[107] S E McGlynn G L Chadwick C P Kempes and V J OrphanldquoSingle cell activity reveals direct electron transfer in methan-otrophic consortiardquoNature vol 526 no 7574 pp 531ndash535 2015

[108] D R Lovley ldquoElectromicrobiologyrdquo Annual Review of Microbi-ology vol 66 pp 391ndash409 2012

[109] S M Strycharz-Glaven R M Snider A Guiseppi-Elie andL M Tender ldquoOn the electrical conductivity of microbialnanowires and biofilmsrdquoEnergy and Environmental Science vol4 no 11 pp 4366ndash4379 2011

[110] D J Richardson J N Butt J K Fredrickson et al ldquoThe lsquoporinndashcytochromersquo model for microbe-to-mineral electron transferrdquoMolecular Microbiology vol 85 no 2 pp 201ndash212 2012

[111] A Okamoto K Hashimoto and R Nakamura ldquoLong-rangeelectron conduction of Shewanella biofilms mediated by outermembrane C-type cytochromesrdquo Bioelectrochemistry vol 85pp 61ndash65 2012

[112] M Y El-Naggar G Wanger K M Leung et al ldquoElectricaltransport along bacterial nanowires from Shewanella oneidensisMR-1rdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 107 no 42 pp 18127ndash18131 2010

[113] G Reguera K D McCarthy T Mehta J S Nicoll M TTuominen and D R Lovley ldquoExtracellular electron transfer viamicrobial nanowiresrdquo Nature vol 435 no 7045 pp 1098ndash11012005

[114] Z M Summers H E Fogarty C Leang A E Franks N SMalvankar and D R Lovley ldquoDirect exchange of electronswithin aggregates of an evolved syntrophic coculture of anaer-obic bacteriardquo Science vol 330 no 6009 pp 1413ndash1415 2010

[115] A Kletzin T Heimerl J Flechsler L V Niftrik R Rachel andA Klingl ldquoCytochromes c in archaea distribution maturationcell architecture and the special case of Ignicoccus hospitalisrdquoFrontiers in Microbiology vol 6 article 439 2015

[116] GWegener V Krukenberg D Riedel H E Tegetmeyer and ABoetius ldquoIntercellular wiring enables electron transfer betweenmethanotrophic archaea and bacteriardquo Nature vol 526 no7574 pp 587ndash590 2015

[117] D HHaft S H Payne and J D Selengut ldquoArchaeosortases andexosortases are widely distributed systems linking membranetransit with posttranslational modificationrdquo Journal of Bacteri-ology vol 194 no 1 pp 36ndash48 2012

[118] A Marchler-Bauer M K Derbyshire N R Gonzales et alldquoCDD NCBIrsquos conserved domain databaserdquo Nucleic AcidsResearch vol 43 no 1 pp D222ndashD226 2015

[119] A Mitchell H-Y Chang L Daugherty et al ldquoThe InterProprotein families database the classification resource after 15yearsrdquo Nucleic Acids Research vol 43 no 1 pp D213ndashD2212015

[120] V Krukenberg K Harding M Richter et al ldquoCandidatusdesulfofervidus auxilii a hydrogenotrophic sulfate-reducingbacterium involved in the thermophilic anaerobic oxidation ofmethanerdquo Environmental Microbiology vol 18 pp 3073ndash30912016

[121] L Shi T C Squier J M Zachara and J K Fredrickson ldquoRes-piration of metal (hydr)oxides by Shewanella and Geobactera key role for multihaem c-type cytochromesrdquo MolecularMicrobiology vol 65 no 1 pp 12ndash20 2007

[122] N S Malvankar and D R Lovley ldquoMicrobial nanowires forbioenergy applicationsrdquo Current Opinion in Biotechnology vol27 pp 88ndash95 2014

[123] A-E Rotaru T LWoodard K PNevin andDR Lovley ldquoLinkbetween capacity for current production and syntrophic growth

in Geobacter speciesrdquo Frontiers in Microbiology vol 6 article744 2015

[124] A-E Rotaru P M Shrestha F Liu et al ldquoDirect interspecieselectron transfer between Geobacter metallireducens andMethanosarcina barkerirdquo Applied and Environmental Microbi-ology vol 80 no 15 pp 4599ndash4605 2014

[125] S Scheller H Yu G L Chadwick S E McGlynn and VJ Orphan ldquoArtificial electron acceptors decouple archaealmethane oxidation from sulfate reductionrdquo Science vol 351 no6274 pp 703ndash707 2016

[126] J Milucka F Widdel and S Shima ldquoImmunological detec-tion of enzymes for sulfate reduction in anaerobic methane-oxidizing consortiardquo Environmental Microbiology vol 15 no 5pp 1561ndash1571 2013

[127] P Cabello M D Roldan and C Moreno-Vivian ldquoNitratereduction and the nitrogen cycle in archaeardquoMicrobiology vol150 no 11 pp 3527ndash3546 2004

[128] R MMartinez-Espinosa E J Dridge M J Bonete et al ldquoLookon the positive sideThe orientation identification and bioener-getics of lsquoArchaealrsquomembrane-boundnitrate reductasesrdquoFEMSMicrobiology Letters vol 276 no 2 pp 129ndash139 2007

[129] S de VriesMMomcilovicM J F Strampraad J PWhiteleggeA Baghai and I Schroder ldquoAdaptation to a high-tungsten envi-ronment pyrobaculum aerophilum contains an active tungstennitrate reductaserdquo Biochemistry vol 49 no 45 pp 9911ndash99212010

[130] M Egger O Rasigraf C J Sapart et al ldquoIron-mediated anaer-obic oxidation of methane in brackish coastal sedimentsrdquoEnvironmental Science and Technology vol 49 no 1 pp 277ndash283 2015

[131] T Treude S Krause J Maltby A W Dale R Coffin and LJ Hamdan ldquoSulfate reduction and methane oxidation activitybelow the sulfate-methane transition zone in Alaskan BeaufortSea continental margin sediments implications for deep sulfurcyclingrdquo Geochimica et Cosmochimica Acta vol 144 pp 217ndash237 2014

[132] N Riedinger M J Formolo T W Lyons S Henkel A Beckand S Kasten ldquoAn inorganic geochemical argument for coupledanaerobic oxidation of methane and iron reduction in marinesedimentsrdquo Geobiology vol 12 no 2 pp 172ndash181 2014

[133] Y-H Chang T-W Cheng W-J Lai et al ldquoMicrobial methanecycling in a terrestrialmud volcano in eastern Taiwanrdquo Environ-mental Microbiology vol 14 no 4 pp 895ndash908 2012

[134] S A Crowe S Katsev K Leslie et al ldquoThe methane cycle inferruginous Lake Matanordquo Geobiology vol 9 no 1 pp 61ndash782011

[135] O Sivan M Adler A Pearson et al ldquoGeochemical evidence foriron-mediated anaerobic oxidation of methanerdquo Limnology andOceanography vol 56 no 4 pp 1536ndash1544 2011

[136] K E A Segarra C Comerford J Slaughter and S B JoyeldquoImpact of electron acceptor availability on the anaerobic oxi-dation of methane in coastal freshwater and brackish wetlandsedimentsrdquo Geochimica et Cosmochimica Acta vol 115 pp 15ndash30 2013

[137] V Gupta K A Smemo J B Yavitt D Fowle B Branfireunand N Basiliko ldquoStable isotopes reveal widespread anaerobicmethane oxidation across latitude and peatland typerdquo Environ-mental Science and Technology vol 47 no 15 pp 8273ndash82792013

[138] O Oni T Miyatake S Kasten et al ldquoDistinct microbialpopulations are tightly linked to the profile of dissolved iron in

22 Archaea

the methanic sediments of the Helgolandmud area North SeardquoFrontiers in Microbiology vol 6 2015

[139] E J Beal C H House and V J Orphan ldquoManganese- andiron-dependent marine methane oxidationrdquo Science vol 325no 5937 pp 184ndash187 2009

[140] M W Bowles V A Samarkin K M Bowles and S B JoyeldquoWeak coupling between sulfate reduction and the anaerobicoxidation of methane in methane-rich seafloor sedimentsduring ex situ incubationrdquo Geochimica et Cosmochimica Actavol 75 no 2 pp 500ndash519 2011

[141] Y Z Lu L Fu J Ding Z Ding N Li and R J Zeng ldquoCr(VI)reduction coupled with anaerobic oxidation of methane in alaboratory reactorrdquoWater Research vol 102 pp 445ndash452 2016

[142] K F Ettwig B Zhu D Speth J T Keltjens M S Jetten and BKartal ldquoArchaea catalyze iron-dependent anaerobic oxidationof methanerdquo Proceedings of the National Academy of Sciences ofthe United States of America vol 113 no 45 pp 12792ndash127962016

[143] T M Flynn R A Sanford H Ryu et al ldquoFunctional microbialdiversity explains groundwater chemistry in a pristine aquiferrdquoBMCMicrobiology vol 13 no 1 article no 146 2013

[144] C J Schubert F Vazquez T Losekann-Behrens K KnittelM Tonolla and A Boetius ldquoEvidence for anaerobic oxidationof methane in sediments of a freshwater system (Lago diCadagno)rdquo FEMS Microbiology Ecology vol 76 no 1 pp 26ndash38 2011

[145] K E A Segarra F Schubotz V Samarkin M Y Yoshinaga K-U Hinrichs and S B Joye ldquoHigh rates of anaerobic methaneoxidation in freshwater wetlands reduce potential atmosphericmethane emissionsrdquo Nature Communications vol 6 article7477 2015

[146] E J Beal M W Claire and C H House ldquoHigh rates ofanaerobic methanotrophy at low sulfate concentrations withimplications for past and present methane levelsrdquo Geobiologyvol 9 no 2 pp 131ndash139 2011

[147] F Kracke I Vassilev and J O Kromer ldquoMicrobial electrontransport and energy conservationmdashthe foundation for opti-mizing bioelectrochemical systemsrdquo Frontiers in Microbiologyvol 6 article 575 2015

[148] C L Reardon A C Dohnalkova P Nachimuthu et al ldquoRoleof outer-membrane cytochromes MtrC and OmcA in thebiomineralization of ferrihydrite by Shewanella oneidensisMR-1rdquo Geobiology vol 8 no 1 pp 56ndash68 2010

[149] L Shi B Chen Z Wang et al ldquoIsolation of a high-affinityfunctional protein complex between OmcA and MtrC twoouter membrane decaheme c-type cytochromes of Shewanellaoneidensis MR-1rdquo Journal of Bacteriology vol 188 no 13 pp4705ndash4714 2006

[150] X Qian T Mester L Morgado et al ldquoBiochemical charac-terization of purified OmcS a c-type cytochrome requiredfor insoluble Fe(III) reduction in Geobacter sulfurreducensrdquoBiochimica et BiophysicaActamdashBioenergetics vol 1807 no 4 pp404ndash412 2011

[151] T Mehta M V Coppi S E Childers and D R Lovley ldquoOutermembrane c-type cytochromes required for Fe(III) andMn(IV)oxide reduction in Geobacter sulfurreducensrdquo Applied andEnvironmentalMicrobiology vol 71 no 12 pp 8634ndash8641 2005

[152] W Blankenfeldt A P Kuzin T Skarina et al ldquoStructure andfunction of the phenazine biosynthetic protein PhzF fromPseudomonas fluorescensrdquoProceedings of theNational Academyof Sciences of the United States of America vol 101 no 47 pp16431ndash16436 2004

[153] J F Parsons F Song L Parsons K Calabrese E Eisensteinand J E Ladner ldquoStructure and function of the phenazinebiosynthesis protein PhzF fromPseudomonas fluorescens 2-79rdquoBiochemistry vol 43 no 39 pp 12427ndash12435 2004

[154] T Hiratsuka K Furihata J Ishikawa et al ldquoAn alternativemenaquinone biosynthetic pathway operating in microorgan-ismsrdquo Science vol 321 no 5896 pp 1670ndash1673 2008

[155] M Tietze A Beuchle I Lamla et al ldquoRedox potentials ofmethanophenazine and CoB-S-S-CoM factors involved inelectron transport in methanogenic archaeardquo ChemBioChemvol 4 no 4 pp 333ndash335 2003

[156] Q H Tran and G Unden ldquoChanges in the proton potentialand the cellular energetics of Escherichia coli during growth byaerobic and anaerobic respiration or by fermentationrdquoEuropeanJournal of Biochemistry vol 251 no 1-2 pp 538ndash543 1998

[157] I Callebaut D Gilges I Vigon and J-P Mornon ldquoHYR anextracellular module involved in cellular adhesion and relatedto the immunoglobulin-like foldrdquo Protein Science vol 9 no 7pp 1382ndash1390 2000

[158] H J Gilbert ldquoCellulosomes microbial nanomachines that dis-play plasticity in quaternary structurerdquoMolecular Microbiologyvol 63 no 6 pp 1568ndash1576 2007

[159] A Peer S P Smith E A Bayer R Lamed and I BorovokldquoNoncellulosomal cohesin- and dockerin-like modules in thethree domains of liferdquo FEMS Microbiology Letters vol 291 no1 pp 1ndash16 2009

[160] M Wagner ldquoMicrobiology conductive consortiardquo Nature vol526 no 7574 pp 513ndash514 2015

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

20 Archaea

[75] M W Bowles V A Samarkin and S B Joye ldquoImprovedmeasurement of microbial activity in deep-sea sediments atin situ pressure and methane concentrationrdquo Limnology andOceanography Methods vol 9 pp 499ndash506 2011

[76] S Shima M Krueger T Weinert et al ldquoStructure of a methyl-coenzyme M reductase from Black Sea mats that oxidizemethane anaerobicallyrdquo Nature vol 481 no 7379 pp 98ndash1012012

[77] K D Allen G Wegener and R H White ldquoDiscovery of multi-ple modified F-430 coenzymes in methanogens and anaerobicmethanotrophic archaea suggests possible new roles for F-430in naturerdquoApplied and Environmental Microbiology vol 80 no20 pp 6403ndash6412 2014

[78] V W Soo M J McAnulty A Tripathi et al ldquoReversingmethanogenesis to capture methane for liquid biofuel precur-sorsrdquoMicrobial Cell Factories vol 15 article 11 2016

[79] D L Valentine and W S Reeburgh ldquoNew perspectives onanaerobicmethane oxidationrdquoEnvironmentalMicrobiology vol2 no 5 pp 477ndash484 2000

[80] D L Valentine ldquoBiogeochemistry and microbial ecology ofmethane oxidation in anoxic environments a reviewrdquo Antonievan Leeuwenhoek International Journal of General and Molecu-lar Microbiology vol 81 no 1-4 pp 271ndash282 2002

[81] A J B Zehnder and T D Brock ldquoMethane formation andmethane oxidation by methanogenic bacteriardquo Journal of Bac-teriology vol 137 no 1 pp 420ndash432 1979

[82] J Harder ldquoAnaerobic methane oxidation by bacteria employ-ing 14C-methane uncontaminated with 14C-carbon monoxiderdquoMarine Geology vol 137 no 1-2 pp 13ndash23 1997

[83] J J Moran C H House K H Freeman and J G FerryldquoTrace methane oxidation studied in several Euryarchaeotaunder diverse conditionsrdquo Archaea vol 1 no 5 pp 303ndash3092005

[84] J J Moran C H House B Thomas and K H FreemanldquoProducts of tracemethane oxidation during nonmethyltrophicgrowth by Methanosarcinardquo Journal of Geophysical ResearchBiogeosciences vol 112 no 2 2007

[85] R J W Meulepas C G Jagersma Y Zhang et al ldquoTracemethane oxidation and the methane dependency of sulfatereduction in anaerobic granular sludgerdquo FEMS MicrobiologyEcology vol 72 no 2 pp 261ndash271 2010

[86] A J B Zehnder andTD Brock ldquoAnaerobicmethane oxidationoccurrence and ecologyrdquoApplied and Environmental Microbiol-ogy vol 39 no 1 pp 194ndash204 1980

[87] S J Blazewicz D G Petersen M P Waldrop and M K Fire-stone ldquoAnaerobic oxidation of methane in tropical and borealsoils ecological significance in terrestrial methane cyclingrdquoJournal of Geophysical Research Biogeosciences vol 117 no 2Article ID G02033 2012

[88] K A Smemo and J B Yavitt ldquoEvidence for anaerobic CH4

oxidation in freshwater peatlandsrdquo Geomicrobiology Journalvol 24 no 7-8 pp 583ndash597 2007

[89] M J Alperin and T M Hoehler ldquoAnaerobic methane oxidationby archaeasulfate-reducing bacteria aggregates 1 Thermody-namic and physical constraintsrdquo American Journal of Sciencevol 309 no 10 pp 869ndash957 2009

[90] S L Caldwell J R Laidler E A Brewer J O Eberly S CSandborgh and F S Colwell ldquoAnaerobic oxidation of methanemechanisms bioenergetics and the ecology of associatedmicroorganismsrdquo Environmental Science and Technology vol42 no 18 pp 6791ndash6799 2008

[91] GWang A J Spivack and S DrsquoHondt ldquoGibbs energies of reac-tion and microbial mutualism in anaerobic deep subseafloorsediments of ODP Site 1226rdquoGeochimica et Cosmochimica Actavol 74 no 14 pp 3938ndash3947 2010

[92] P R Girguis A E Cozen and E F DeLong ldquoGrowth andpopulation dynamics of anaerobic methane-oxidizing archaeaand sulfate-reducing bacteria in a continuous-flow bioreactorrdquoApplied and EnvironmentalMicrobiology vol 71 no 7 pp 3725ndash3733 2005

[93] K Nauhaus M Albrecht M Elvert A Boetius and F WiddelldquoIn vitro cell growth ofmarine archaeal-bacterial consortia dur-ing anaerobic oxidation ofmethanewith sulfaterdquoEnvironmentalMicrobiology vol 9 no 1 pp 187ndash196 2007

[94] B Orcutt V Samarkin A Boetius and S Joye ldquoOn the relation-ship between methane production and oxidation by anaerobicmethanotrophic communities from cold seeps of the Gulf ofMexicordquo Environmental Microbiology vol 10 no 5 pp 1108ndash1117 2008

[95] M Y Yoshinaga T Holler T Goldhammer et al ldquoCarbon iso-tope equilibration during sulphate-limited anaerobic oxidationof methanerdquo Nature Geoscience vol 7 no 3 pp 190ndash194 2014

[96] T Treude J Niggemann J Kallmeyer et al ldquoAnaerobic oxi-dation of methane and sulfate reduction along the Chileancontinental marginrdquo Geochimica et Cosmochimica Acta vol 69no 11 pp 2767ndash2779 2005

[97] R J Parkes B A Cragg N Banning et al ldquoBiogeochemistryand biodiversity of methane cycling in subsurface marinesediments (SkagerrakDenmark)rdquoEnvironmentalMicrobiologyvol 9 no 5 pp 1146ndash1161 2007

[98] N J Knab B A Cragg E R C Hornibrook et al ldquoRegulationof anaerobic methane oxidation in sediments of the Black SeardquoBiogeosciences vol 6 no 8 pp 1505ndash1518 2009

[99] H Yoshioka A Maruyama T Nakamura et al ldquoActivities anddistribution of methanogenic and methane-oxidizing microbesin marine sediments from the Cascadia Marginrdquo Geobiologyvol 8 no 3 pp 223ndash233 2010

[100] G Wegener V Krukenberg S E Ruff M Y Kellermann andK Knittel ldquoMetabolic capabilities of microorganisms involvedin and associated with the anaerobic oxidation of methanerdquoFrontiers in Microbiology vol 7 article 46 2016

[101] R J W Meulepas C G Jagersma A F Khadem A J MStams and P N L Lens ldquoEffect of methanogenic substrateson anaerobic oxidation of methane and sulfate reduction by ananaerobic methanotrophic enrichmentrdquo Applied Microbiologyand Biotechnology vol 87 no 4 pp 1499ndash1506 2010

[102] J Milucka T G Ferdelman L Polerecky et al ldquoZero-valentsulphur is a key intermediate in marine methane oxidationrdquoNature vol 491 no 7425 pp 541ndash546 2012

[103] W Michaelis R Seifert K Nauhaus et al ldquoMicrobial reefs inthe black sea fueled by anaerobic oxidation ofmethanerdquo Sciencevol 297 no 5583 pp 1013ndash1015 2002

[104] A Vigneron P Cruaud P Pignet et al ldquoArchaeal and anaerobicmethane oxidizer communities in the Sonora Margin coldseeps Guaymas Basin (Gulf of California)rdquo ISME Journal vol7 no 8 pp 1595ndash1608 2013

[105] M Alperin and T Hoehler ldquoThe ongoing mystery of sea-floormethanerdquo Science vol 329 no 5989 pp 288ndash289 2010

[106] B Orcutt and C Meile ldquoConstraints on mechanisms and ratesof anaerobic oxidation of methane by microbial consortiaprocess-basedmodeling of ANME-2 archaea and sulfate reduc-ing bacteria interactionsrdquo Biogeosciences vol 5 no 6 pp 1587ndash1599 2008

Archaea 21

[107] S E McGlynn G L Chadwick C P Kempes and V J OrphanldquoSingle cell activity reveals direct electron transfer in methan-otrophic consortiardquoNature vol 526 no 7574 pp 531ndash535 2015

[108] D R Lovley ldquoElectromicrobiologyrdquo Annual Review of Microbi-ology vol 66 pp 391ndash409 2012

[109] S M Strycharz-Glaven R M Snider A Guiseppi-Elie andL M Tender ldquoOn the electrical conductivity of microbialnanowires and biofilmsrdquoEnergy and Environmental Science vol4 no 11 pp 4366ndash4379 2011

[110] D J Richardson J N Butt J K Fredrickson et al ldquoThe lsquoporinndashcytochromersquo model for microbe-to-mineral electron transferrdquoMolecular Microbiology vol 85 no 2 pp 201ndash212 2012

[111] A Okamoto K Hashimoto and R Nakamura ldquoLong-rangeelectron conduction of Shewanella biofilms mediated by outermembrane C-type cytochromesrdquo Bioelectrochemistry vol 85pp 61ndash65 2012

[112] M Y El-Naggar G Wanger K M Leung et al ldquoElectricaltransport along bacterial nanowires from Shewanella oneidensisMR-1rdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 107 no 42 pp 18127ndash18131 2010

[113] G Reguera K D McCarthy T Mehta J S Nicoll M TTuominen and D R Lovley ldquoExtracellular electron transfer viamicrobial nanowiresrdquo Nature vol 435 no 7045 pp 1098ndash11012005

[114] Z M Summers H E Fogarty C Leang A E Franks N SMalvankar and D R Lovley ldquoDirect exchange of electronswithin aggregates of an evolved syntrophic coculture of anaer-obic bacteriardquo Science vol 330 no 6009 pp 1413ndash1415 2010

[115] A Kletzin T Heimerl J Flechsler L V Niftrik R Rachel andA Klingl ldquoCytochromes c in archaea distribution maturationcell architecture and the special case of Ignicoccus hospitalisrdquoFrontiers in Microbiology vol 6 article 439 2015

[116] GWegener V Krukenberg D Riedel H E Tegetmeyer and ABoetius ldquoIntercellular wiring enables electron transfer betweenmethanotrophic archaea and bacteriardquo Nature vol 526 no7574 pp 587ndash590 2015

[117] D HHaft S H Payne and J D Selengut ldquoArchaeosortases andexosortases are widely distributed systems linking membranetransit with posttranslational modificationrdquo Journal of Bacteri-ology vol 194 no 1 pp 36ndash48 2012

[118] A Marchler-Bauer M K Derbyshire N R Gonzales et alldquoCDD NCBIrsquos conserved domain databaserdquo Nucleic AcidsResearch vol 43 no 1 pp D222ndashD226 2015

[119] A Mitchell H-Y Chang L Daugherty et al ldquoThe InterProprotein families database the classification resource after 15yearsrdquo Nucleic Acids Research vol 43 no 1 pp D213ndashD2212015

[120] V Krukenberg K Harding M Richter et al ldquoCandidatusdesulfofervidus auxilii a hydrogenotrophic sulfate-reducingbacterium involved in the thermophilic anaerobic oxidation ofmethanerdquo Environmental Microbiology vol 18 pp 3073ndash30912016

[121] L Shi T C Squier J M Zachara and J K Fredrickson ldquoRes-piration of metal (hydr)oxides by Shewanella and Geobactera key role for multihaem c-type cytochromesrdquo MolecularMicrobiology vol 65 no 1 pp 12ndash20 2007

[122] N S Malvankar and D R Lovley ldquoMicrobial nanowires forbioenergy applicationsrdquo Current Opinion in Biotechnology vol27 pp 88ndash95 2014

[123] A-E Rotaru T LWoodard K PNevin andDR Lovley ldquoLinkbetween capacity for current production and syntrophic growth

in Geobacter speciesrdquo Frontiers in Microbiology vol 6 article744 2015

[124] A-E Rotaru P M Shrestha F Liu et al ldquoDirect interspecieselectron transfer between Geobacter metallireducens andMethanosarcina barkerirdquo Applied and Environmental Microbi-ology vol 80 no 15 pp 4599ndash4605 2014

[125] S Scheller H Yu G L Chadwick S E McGlynn and VJ Orphan ldquoArtificial electron acceptors decouple archaealmethane oxidation from sulfate reductionrdquo Science vol 351 no6274 pp 703ndash707 2016

[126] J Milucka F Widdel and S Shima ldquoImmunological detec-tion of enzymes for sulfate reduction in anaerobic methane-oxidizing consortiardquo Environmental Microbiology vol 15 no 5pp 1561ndash1571 2013

[127] P Cabello M D Roldan and C Moreno-Vivian ldquoNitratereduction and the nitrogen cycle in archaeardquoMicrobiology vol150 no 11 pp 3527ndash3546 2004

[128] R MMartinez-Espinosa E J Dridge M J Bonete et al ldquoLookon the positive sideThe orientation identification and bioener-getics of lsquoArchaealrsquomembrane-boundnitrate reductasesrdquoFEMSMicrobiology Letters vol 276 no 2 pp 129ndash139 2007

[129] S de VriesMMomcilovicM J F Strampraad J PWhiteleggeA Baghai and I Schroder ldquoAdaptation to a high-tungsten envi-ronment pyrobaculum aerophilum contains an active tungstennitrate reductaserdquo Biochemistry vol 49 no 45 pp 9911ndash99212010

[130] M Egger O Rasigraf C J Sapart et al ldquoIron-mediated anaer-obic oxidation of methane in brackish coastal sedimentsrdquoEnvironmental Science and Technology vol 49 no 1 pp 277ndash283 2015

[131] T Treude S Krause J Maltby A W Dale R Coffin and LJ Hamdan ldquoSulfate reduction and methane oxidation activitybelow the sulfate-methane transition zone in Alaskan BeaufortSea continental margin sediments implications for deep sulfurcyclingrdquo Geochimica et Cosmochimica Acta vol 144 pp 217ndash237 2014

[132] N Riedinger M J Formolo T W Lyons S Henkel A Beckand S Kasten ldquoAn inorganic geochemical argument for coupledanaerobic oxidation of methane and iron reduction in marinesedimentsrdquo Geobiology vol 12 no 2 pp 172ndash181 2014

[133] Y-H Chang T-W Cheng W-J Lai et al ldquoMicrobial methanecycling in a terrestrialmud volcano in eastern Taiwanrdquo Environ-mental Microbiology vol 14 no 4 pp 895ndash908 2012

[134] S A Crowe S Katsev K Leslie et al ldquoThe methane cycle inferruginous Lake Matanordquo Geobiology vol 9 no 1 pp 61ndash782011

[135] O Sivan M Adler A Pearson et al ldquoGeochemical evidence foriron-mediated anaerobic oxidation of methanerdquo Limnology andOceanography vol 56 no 4 pp 1536ndash1544 2011

[136] K E A Segarra C Comerford J Slaughter and S B JoyeldquoImpact of electron acceptor availability on the anaerobic oxi-dation of methane in coastal freshwater and brackish wetlandsedimentsrdquo Geochimica et Cosmochimica Acta vol 115 pp 15ndash30 2013

[137] V Gupta K A Smemo J B Yavitt D Fowle B Branfireunand N Basiliko ldquoStable isotopes reveal widespread anaerobicmethane oxidation across latitude and peatland typerdquo Environ-mental Science and Technology vol 47 no 15 pp 8273ndash82792013

[138] O Oni T Miyatake S Kasten et al ldquoDistinct microbialpopulations are tightly linked to the profile of dissolved iron in

22 Archaea

the methanic sediments of the Helgolandmud area North SeardquoFrontiers in Microbiology vol 6 2015

[139] E J Beal C H House and V J Orphan ldquoManganese- andiron-dependent marine methane oxidationrdquo Science vol 325no 5937 pp 184ndash187 2009

[140] M W Bowles V A Samarkin K M Bowles and S B JoyeldquoWeak coupling between sulfate reduction and the anaerobicoxidation of methane in methane-rich seafloor sedimentsduring ex situ incubationrdquo Geochimica et Cosmochimica Actavol 75 no 2 pp 500ndash519 2011

[141] Y Z Lu L Fu J Ding Z Ding N Li and R J Zeng ldquoCr(VI)reduction coupled with anaerobic oxidation of methane in alaboratory reactorrdquoWater Research vol 102 pp 445ndash452 2016

[142] K F Ettwig B Zhu D Speth J T Keltjens M S Jetten and BKartal ldquoArchaea catalyze iron-dependent anaerobic oxidationof methanerdquo Proceedings of the National Academy of Sciences ofthe United States of America vol 113 no 45 pp 12792ndash127962016

[143] T M Flynn R A Sanford H Ryu et al ldquoFunctional microbialdiversity explains groundwater chemistry in a pristine aquiferrdquoBMCMicrobiology vol 13 no 1 article no 146 2013

[144] C J Schubert F Vazquez T Losekann-Behrens K KnittelM Tonolla and A Boetius ldquoEvidence for anaerobic oxidationof methane in sediments of a freshwater system (Lago diCadagno)rdquo FEMS Microbiology Ecology vol 76 no 1 pp 26ndash38 2011

[145] K E A Segarra F Schubotz V Samarkin M Y Yoshinaga K-U Hinrichs and S B Joye ldquoHigh rates of anaerobic methaneoxidation in freshwater wetlands reduce potential atmosphericmethane emissionsrdquo Nature Communications vol 6 article7477 2015

[146] E J Beal M W Claire and C H House ldquoHigh rates ofanaerobic methanotrophy at low sulfate concentrations withimplications for past and present methane levelsrdquo Geobiologyvol 9 no 2 pp 131ndash139 2011

[147] F Kracke I Vassilev and J O Kromer ldquoMicrobial electrontransport and energy conservationmdashthe foundation for opti-mizing bioelectrochemical systemsrdquo Frontiers in Microbiologyvol 6 article 575 2015

[148] C L Reardon A C Dohnalkova P Nachimuthu et al ldquoRoleof outer-membrane cytochromes MtrC and OmcA in thebiomineralization of ferrihydrite by Shewanella oneidensisMR-1rdquo Geobiology vol 8 no 1 pp 56ndash68 2010

[149] L Shi B Chen Z Wang et al ldquoIsolation of a high-affinityfunctional protein complex between OmcA and MtrC twoouter membrane decaheme c-type cytochromes of Shewanellaoneidensis MR-1rdquo Journal of Bacteriology vol 188 no 13 pp4705ndash4714 2006

[150] X Qian T Mester L Morgado et al ldquoBiochemical charac-terization of purified OmcS a c-type cytochrome requiredfor insoluble Fe(III) reduction in Geobacter sulfurreducensrdquoBiochimica et BiophysicaActamdashBioenergetics vol 1807 no 4 pp404ndash412 2011

[151] T Mehta M V Coppi S E Childers and D R Lovley ldquoOutermembrane c-type cytochromes required for Fe(III) andMn(IV)oxide reduction in Geobacter sulfurreducensrdquo Applied andEnvironmentalMicrobiology vol 71 no 12 pp 8634ndash8641 2005

[152] W Blankenfeldt A P Kuzin T Skarina et al ldquoStructure andfunction of the phenazine biosynthetic protein PhzF fromPseudomonas fluorescensrdquoProceedings of theNational Academyof Sciences of the United States of America vol 101 no 47 pp16431ndash16436 2004

[153] J F Parsons F Song L Parsons K Calabrese E Eisensteinand J E Ladner ldquoStructure and function of the phenazinebiosynthesis protein PhzF fromPseudomonas fluorescens 2-79rdquoBiochemistry vol 43 no 39 pp 12427ndash12435 2004

[154] T Hiratsuka K Furihata J Ishikawa et al ldquoAn alternativemenaquinone biosynthetic pathway operating in microorgan-ismsrdquo Science vol 321 no 5896 pp 1670ndash1673 2008

[155] M Tietze A Beuchle I Lamla et al ldquoRedox potentials ofmethanophenazine and CoB-S-S-CoM factors involved inelectron transport in methanogenic archaeardquo ChemBioChemvol 4 no 4 pp 333ndash335 2003

[156] Q H Tran and G Unden ldquoChanges in the proton potentialand the cellular energetics of Escherichia coli during growth byaerobic and anaerobic respiration or by fermentationrdquoEuropeanJournal of Biochemistry vol 251 no 1-2 pp 538ndash543 1998

[157] I Callebaut D Gilges I Vigon and J-P Mornon ldquoHYR anextracellular module involved in cellular adhesion and relatedto the immunoglobulin-like foldrdquo Protein Science vol 9 no 7pp 1382ndash1390 2000

[158] H J Gilbert ldquoCellulosomes microbial nanomachines that dis-play plasticity in quaternary structurerdquoMolecular Microbiologyvol 63 no 6 pp 1568ndash1576 2007

[159] A Peer S P Smith E A Bayer R Lamed and I BorovokldquoNoncellulosomal cohesin- and dockerin-like modules in thethree domains of liferdquo FEMS Microbiology Letters vol 291 no1 pp 1ndash16 2009

[160] M Wagner ldquoMicrobiology conductive consortiardquo Nature vol526 no 7574 pp 513ndash514 2015

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Archaea 21

[107] S E McGlynn G L Chadwick C P Kempes and V J OrphanldquoSingle cell activity reveals direct electron transfer in methan-otrophic consortiardquoNature vol 526 no 7574 pp 531ndash535 2015

[108] D R Lovley ldquoElectromicrobiologyrdquo Annual Review of Microbi-ology vol 66 pp 391ndash409 2012

[109] S M Strycharz-Glaven R M Snider A Guiseppi-Elie andL M Tender ldquoOn the electrical conductivity of microbialnanowires and biofilmsrdquoEnergy and Environmental Science vol4 no 11 pp 4366ndash4379 2011

[110] D J Richardson J N Butt J K Fredrickson et al ldquoThe lsquoporinndashcytochromersquo model for microbe-to-mineral electron transferrdquoMolecular Microbiology vol 85 no 2 pp 201ndash212 2012

[111] A Okamoto K Hashimoto and R Nakamura ldquoLong-rangeelectron conduction of Shewanella biofilms mediated by outermembrane C-type cytochromesrdquo Bioelectrochemistry vol 85pp 61ndash65 2012

[112] M Y El-Naggar G Wanger K M Leung et al ldquoElectricaltransport along bacterial nanowires from Shewanella oneidensisMR-1rdquo Proceedings of the National Academy of Sciences of theUnited States of America vol 107 no 42 pp 18127ndash18131 2010

[113] G Reguera K D McCarthy T Mehta J S Nicoll M TTuominen and D R Lovley ldquoExtracellular electron transfer viamicrobial nanowiresrdquo Nature vol 435 no 7045 pp 1098ndash11012005

[114] Z M Summers H E Fogarty C Leang A E Franks N SMalvankar and D R Lovley ldquoDirect exchange of electronswithin aggregates of an evolved syntrophic coculture of anaer-obic bacteriardquo Science vol 330 no 6009 pp 1413ndash1415 2010

[115] A Kletzin T Heimerl J Flechsler L V Niftrik R Rachel andA Klingl ldquoCytochromes c in archaea distribution maturationcell architecture and the special case of Ignicoccus hospitalisrdquoFrontiers in Microbiology vol 6 article 439 2015

[116] GWegener V Krukenberg D Riedel H E Tegetmeyer and ABoetius ldquoIntercellular wiring enables electron transfer betweenmethanotrophic archaea and bacteriardquo Nature vol 526 no7574 pp 587ndash590 2015

[117] D HHaft S H Payne and J D Selengut ldquoArchaeosortases andexosortases are widely distributed systems linking membranetransit with posttranslational modificationrdquo Journal of Bacteri-ology vol 194 no 1 pp 36ndash48 2012

[118] A Marchler-Bauer M K Derbyshire N R Gonzales et alldquoCDD NCBIrsquos conserved domain databaserdquo Nucleic AcidsResearch vol 43 no 1 pp D222ndashD226 2015

[119] A Mitchell H-Y Chang L Daugherty et al ldquoThe InterProprotein families database the classification resource after 15yearsrdquo Nucleic Acids Research vol 43 no 1 pp D213ndashD2212015

[120] V Krukenberg K Harding M Richter et al ldquoCandidatusdesulfofervidus auxilii a hydrogenotrophic sulfate-reducingbacterium involved in the thermophilic anaerobic oxidation ofmethanerdquo Environmental Microbiology vol 18 pp 3073ndash30912016

[121] L Shi T C Squier J M Zachara and J K Fredrickson ldquoRes-piration of metal (hydr)oxides by Shewanella and Geobactera key role for multihaem c-type cytochromesrdquo MolecularMicrobiology vol 65 no 1 pp 12ndash20 2007

[122] N S Malvankar and D R Lovley ldquoMicrobial nanowires forbioenergy applicationsrdquo Current Opinion in Biotechnology vol27 pp 88ndash95 2014

[123] A-E Rotaru T LWoodard K PNevin andDR Lovley ldquoLinkbetween capacity for current production and syntrophic growth

in Geobacter speciesrdquo Frontiers in Microbiology vol 6 article744 2015

[124] A-E Rotaru P M Shrestha F Liu et al ldquoDirect interspecieselectron transfer between Geobacter metallireducens andMethanosarcina barkerirdquo Applied and Environmental Microbi-ology vol 80 no 15 pp 4599ndash4605 2014

[125] S Scheller H Yu G L Chadwick S E McGlynn and VJ Orphan ldquoArtificial electron acceptors decouple archaealmethane oxidation from sulfate reductionrdquo Science vol 351 no6274 pp 703ndash707 2016

[126] J Milucka F Widdel and S Shima ldquoImmunological detec-tion of enzymes for sulfate reduction in anaerobic methane-oxidizing consortiardquo Environmental Microbiology vol 15 no 5pp 1561ndash1571 2013

[127] P Cabello M D Roldan and C Moreno-Vivian ldquoNitratereduction and the nitrogen cycle in archaeardquoMicrobiology vol150 no 11 pp 3527ndash3546 2004

[128] R MMartinez-Espinosa E J Dridge M J Bonete et al ldquoLookon the positive sideThe orientation identification and bioener-getics of lsquoArchaealrsquomembrane-boundnitrate reductasesrdquoFEMSMicrobiology Letters vol 276 no 2 pp 129ndash139 2007

[129] S de VriesMMomcilovicM J F Strampraad J PWhiteleggeA Baghai and I Schroder ldquoAdaptation to a high-tungsten envi-ronment pyrobaculum aerophilum contains an active tungstennitrate reductaserdquo Biochemistry vol 49 no 45 pp 9911ndash99212010

[130] M Egger O Rasigraf C J Sapart et al ldquoIron-mediated anaer-obic oxidation of methane in brackish coastal sedimentsrdquoEnvironmental Science and Technology vol 49 no 1 pp 277ndash283 2015

[131] T Treude S Krause J Maltby A W Dale R Coffin and LJ Hamdan ldquoSulfate reduction and methane oxidation activitybelow the sulfate-methane transition zone in Alaskan BeaufortSea continental margin sediments implications for deep sulfurcyclingrdquo Geochimica et Cosmochimica Acta vol 144 pp 217ndash237 2014

[132] N Riedinger M J Formolo T W Lyons S Henkel A Beckand S Kasten ldquoAn inorganic geochemical argument for coupledanaerobic oxidation of methane and iron reduction in marinesedimentsrdquo Geobiology vol 12 no 2 pp 172ndash181 2014

[133] Y-H Chang T-W Cheng W-J Lai et al ldquoMicrobial methanecycling in a terrestrialmud volcano in eastern Taiwanrdquo Environ-mental Microbiology vol 14 no 4 pp 895ndash908 2012

[134] S A Crowe S Katsev K Leslie et al ldquoThe methane cycle inferruginous Lake Matanordquo Geobiology vol 9 no 1 pp 61ndash782011

[135] O Sivan M Adler A Pearson et al ldquoGeochemical evidence foriron-mediated anaerobic oxidation of methanerdquo Limnology andOceanography vol 56 no 4 pp 1536ndash1544 2011

[136] K E A Segarra C Comerford J Slaughter and S B JoyeldquoImpact of electron acceptor availability on the anaerobic oxi-dation of methane in coastal freshwater and brackish wetlandsedimentsrdquo Geochimica et Cosmochimica Acta vol 115 pp 15ndash30 2013

[137] V Gupta K A Smemo J B Yavitt D Fowle B Branfireunand N Basiliko ldquoStable isotopes reveal widespread anaerobicmethane oxidation across latitude and peatland typerdquo Environ-mental Science and Technology vol 47 no 15 pp 8273ndash82792013

[138] O Oni T Miyatake S Kasten et al ldquoDistinct microbialpopulations are tightly linked to the profile of dissolved iron in

22 Archaea

the methanic sediments of the Helgolandmud area North SeardquoFrontiers in Microbiology vol 6 2015

[139] E J Beal C H House and V J Orphan ldquoManganese- andiron-dependent marine methane oxidationrdquo Science vol 325no 5937 pp 184ndash187 2009

[140] M W Bowles V A Samarkin K M Bowles and S B JoyeldquoWeak coupling between sulfate reduction and the anaerobicoxidation of methane in methane-rich seafloor sedimentsduring ex situ incubationrdquo Geochimica et Cosmochimica Actavol 75 no 2 pp 500ndash519 2011

[141] Y Z Lu L Fu J Ding Z Ding N Li and R J Zeng ldquoCr(VI)reduction coupled with anaerobic oxidation of methane in alaboratory reactorrdquoWater Research vol 102 pp 445ndash452 2016

[142] K F Ettwig B Zhu D Speth J T Keltjens M S Jetten and BKartal ldquoArchaea catalyze iron-dependent anaerobic oxidationof methanerdquo Proceedings of the National Academy of Sciences ofthe United States of America vol 113 no 45 pp 12792ndash127962016

[143] T M Flynn R A Sanford H Ryu et al ldquoFunctional microbialdiversity explains groundwater chemistry in a pristine aquiferrdquoBMCMicrobiology vol 13 no 1 article no 146 2013

[144] C J Schubert F Vazquez T Losekann-Behrens K KnittelM Tonolla and A Boetius ldquoEvidence for anaerobic oxidationof methane in sediments of a freshwater system (Lago diCadagno)rdquo FEMS Microbiology Ecology vol 76 no 1 pp 26ndash38 2011

[145] K E A Segarra F Schubotz V Samarkin M Y Yoshinaga K-U Hinrichs and S B Joye ldquoHigh rates of anaerobic methaneoxidation in freshwater wetlands reduce potential atmosphericmethane emissionsrdquo Nature Communications vol 6 article7477 2015

[146] E J Beal M W Claire and C H House ldquoHigh rates ofanaerobic methanotrophy at low sulfate concentrations withimplications for past and present methane levelsrdquo Geobiologyvol 9 no 2 pp 131ndash139 2011

[147] F Kracke I Vassilev and J O Kromer ldquoMicrobial electrontransport and energy conservationmdashthe foundation for opti-mizing bioelectrochemical systemsrdquo Frontiers in Microbiologyvol 6 article 575 2015

[148] C L Reardon A C Dohnalkova P Nachimuthu et al ldquoRoleof outer-membrane cytochromes MtrC and OmcA in thebiomineralization of ferrihydrite by Shewanella oneidensisMR-1rdquo Geobiology vol 8 no 1 pp 56ndash68 2010

[149] L Shi B Chen Z Wang et al ldquoIsolation of a high-affinityfunctional protein complex between OmcA and MtrC twoouter membrane decaheme c-type cytochromes of Shewanellaoneidensis MR-1rdquo Journal of Bacteriology vol 188 no 13 pp4705ndash4714 2006

[150] X Qian T Mester L Morgado et al ldquoBiochemical charac-terization of purified OmcS a c-type cytochrome requiredfor insoluble Fe(III) reduction in Geobacter sulfurreducensrdquoBiochimica et BiophysicaActamdashBioenergetics vol 1807 no 4 pp404ndash412 2011

[151] T Mehta M V Coppi S E Childers and D R Lovley ldquoOutermembrane c-type cytochromes required for Fe(III) andMn(IV)oxide reduction in Geobacter sulfurreducensrdquo Applied andEnvironmentalMicrobiology vol 71 no 12 pp 8634ndash8641 2005

[152] W Blankenfeldt A P Kuzin T Skarina et al ldquoStructure andfunction of the phenazine biosynthetic protein PhzF fromPseudomonas fluorescensrdquoProceedings of theNational Academyof Sciences of the United States of America vol 101 no 47 pp16431ndash16436 2004

[153] J F Parsons F Song L Parsons K Calabrese E Eisensteinand J E Ladner ldquoStructure and function of the phenazinebiosynthesis protein PhzF fromPseudomonas fluorescens 2-79rdquoBiochemistry vol 43 no 39 pp 12427ndash12435 2004

[154] T Hiratsuka K Furihata J Ishikawa et al ldquoAn alternativemenaquinone biosynthetic pathway operating in microorgan-ismsrdquo Science vol 321 no 5896 pp 1670ndash1673 2008

[155] M Tietze A Beuchle I Lamla et al ldquoRedox potentials ofmethanophenazine and CoB-S-S-CoM factors involved inelectron transport in methanogenic archaeardquo ChemBioChemvol 4 no 4 pp 333ndash335 2003

[156] Q H Tran and G Unden ldquoChanges in the proton potentialand the cellular energetics of Escherichia coli during growth byaerobic and anaerobic respiration or by fermentationrdquoEuropeanJournal of Biochemistry vol 251 no 1-2 pp 538ndash543 1998

[157] I Callebaut D Gilges I Vigon and J-P Mornon ldquoHYR anextracellular module involved in cellular adhesion and relatedto the immunoglobulin-like foldrdquo Protein Science vol 9 no 7pp 1382ndash1390 2000

[158] H J Gilbert ldquoCellulosomes microbial nanomachines that dis-play plasticity in quaternary structurerdquoMolecular Microbiologyvol 63 no 6 pp 1568ndash1576 2007

[159] A Peer S P Smith E A Bayer R Lamed and I BorovokldquoNoncellulosomal cohesin- and dockerin-like modules in thethree domains of liferdquo FEMS Microbiology Letters vol 291 no1 pp 1ndash16 2009

[160] M Wagner ldquoMicrobiology conductive consortiardquo Nature vol526 no 7574 pp 513ndash514 2015

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

22 Archaea

the methanic sediments of the Helgolandmud area North SeardquoFrontiers in Microbiology vol 6 2015

[139] E J Beal C H House and V J Orphan ldquoManganese- andiron-dependent marine methane oxidationrdquo Science vol 325no 5937 pp 184ndash187 2009

[140] M W Bowles V A Samarkin K M Bowles and S B JoyeldquoWeak coupling between sulfate reduction and the anaerobicoxidation of methane in methane-rich seafloor sedimentsduring ex situ incubationrdquo Geochimica et Cosmochimica Actavol 75 no 2 pp 500ndash519 2011

[141] Y Z Lu L Fu J Ding Z Ding N Li and R J Zeng ldquoCr(VI)reduction coupled with anaerobic oxidation of methane in alaboratory reactorrdquoWater Research vol 102 pp 445ndash452 2016

[142] K F Ettwig B Zhu D Speth J T Keltjens M S Jetten and BKartal ldquoArchaea catalyze iron-dependent anaerobic oxidationof methanerdquo Proceedings of the National Academy of Sciences ofthe United States of America vol 113 no 45 pp 12792ndash127962016

[143] T M Flynn R A Sanford H Ryu et al ldquoFunctional microbialdiversity explains groundwater chemistry in a pristine aquiferrdquoBMCMicrobiology vol 13 no 1 article no 146 2013

[144] C J Schubert F Vazquez T Losekann-Behrens K KnittelM Tonolla and A Boetius ldquoEvidence for anaerobic oxidationof methane in sediments of a freshwater system (Lago diCadagno)rdquo FEMS Microbiology Ecology vol 76 no 1 pp 26ndash38 2011

[145] K E A Segarra F Schubotz V Samarkin M Y Yoshinaga K-U Hinrichs and S B Joye ldquoHigh rates of anaerobic methaneoxidation in freshwater wetlands reduce potential atmosphericmethane emissionsrdquo Nature Communications vol 6 article7477 2015

[146] E J Beal M W Claire and C H House ldquoHigh rates ofanaerobic methanotrophy at low sulfate concentrations withimplications for past and present methane levelsrdquo Geobiologyvol 9 no 2 pp 131ndash139 2011

[147] F Kracke I Vassilev and J O Kromer ldquoMicrobial electrontransport and energy conservationmdashthe foundation for opti-mizing bioelectrochemical systemsrdquo Frontiers in Microbiologyvol 6 article 575 2015

[148] C L Reardon A C Dohnalkova P Nachimuthu et al ldquoRoleof outer-membrane cytochromes MtrC and OmcA in thebiomineralization of ferrihydrite by Shewanella oneidensisMR-1rdquo Geobiology vol 8 no 1 pp 56ndash68 2010

[149] L Shi B Chen Z Wang et al ldquoIsolation of a high-affinityfunctional protein complex between OmcA and MtrC twoouter membrane decaheme c-type cytochromes of Shewanellaoneidensis MR-1rdquo Journal of Bacteriology vol 188 no 13 pp4705ndash4714 2006

[150] X Qian T Mester L Morgado et al ldquoBiochemical charac-terization of purified OmcS a c-type cytochrome requiredfor insoluble Fe(III) reduction in Geobacter sulfurreducensrdquoBiochimica et BiophysicaActamdashBioenergetics vol 1807 no 4 pp404ndash412 2011

[151] T Mehta M V Coppi S E Childers and D R Lovley ldquoOutermembrane c-type cytochromes required for Fe(III) andMn(IV)oxide reduction in Geobacter sulfurreducensrdquo Applied andEnvironmentalMicrobiology vol 71 no 12 pp 8634ndash8641 2005

[152] W Blankenfeldt A P Kuzin T Skarina et al ldquoStructure andfunction of the phenazine biosynthetic protein PhzF fromPseudomonas fluorescensrdquoProceedings of theNational Academyof Sciences of the United States of America vol 101 no 47 pp16431ndash16436 2004

[153] J F Parsons F Song L Parsons K Calabrese E Eisensteinand J E Ladner ldquoStructure and function of the phenazinebiosynthesis protein PhzF fromPseudomonas fluorescens 2-79rdquoBiochemistry vol 43 no 39 pp 12427ndash12435 2004

[154] T Hiratsuka K Furihata J Ishikawa et al ldquoAn alternativemenaquinone biosynthetic pathway operating in microorgan-ismsrdquo Science vol 321 no 5896 pp 1670ndash1673 2008

[155] M Tietze A Beuchle I Lamla et al ldquoRedox potentials ofmethanophenazine and CoB-S-S-CoM factors involved inelectron transport in methanogenic archaeardquo ChemBioChemvol 4 no 4 pp 333ndash335 2003

[156] Q H Tran and G Unden ldquoChanges in the proton potentialand the cellular energetics of Escherichia coli during growth byaerobic and anaerobic respiration or by fermentationrdquoEuropeanJournal of Biochemistry vol 251 no 1-2 pp 538ndash543 1998

[157] I Callebaut D Gilges I Vigon and J-P Mornon ldquoHYR anextracellular module involved in cellular adhesion and relatedto the immunoglobulin-like foldrdquo Protein Science vol 9 no 7pp 1382ndash1390 2000

[158] H J Gilbert ldquoCellulosomes microbial nanomachines that dis-play plasticity in quaternary structurerdquoMolecular Microbiologyvol 63 no 6 pp 1568ndash1576 2007

[159] A Peer S P Smith E A Bayer R Lamed and I BorovokldquoNoncellulosomal cohesin- and dockerin-like modules in thethree domains of liferdquo FEMS Microbiology Letters vol 291 no1 pp 1ndash16 2009

[160] M Wagner ldquoMicrobiology conductive consortiardquo Nature vol526 no 7574 pp 513ndash514 2015

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology