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presentation at origins 2014
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Molecular evolution before the ancestors of the bacterial and archaeal domains and before the Last
Universal Common Ancestor
Funded through the NASA Exobiology and NSF Assembling the Tree of Life Programs Origins 2014, Nara, Japan, July 6-11, 2014
J. Peter Gogarten University of Connecticut
Dept. of Molecular and Cell Biol.
Collaborators: Dr. Greg Fournier (UConn/MIT) Dr. Cheryl Andam (UConn/Harvard)
Outline:
Mural at N
AS
A Am
es Research C
enter
• Gene duplica,ons and deep molecular phylogenies • Proper,es of the Last Universal Common Ancestor(s) • The history of the transla,on machinery during the expansion of the gene,c code
• The ribosomal tree of life and inferred op,mal growth temperature • Tree shape, the ar,fact of apparent “lonely ancestors” • Indica,ons for early ex,nc,on events due to increased environmental temperature
• Phylogene,c evidence for LUCA’s compatriots
Catalytic subunits Non catalytic subunits
speciation
gene duplication time
ATPase / ATPsynthase ATP binding Subunits
N C
V-proteolipid
N C N C
A-proteolipids
Halobacterium Methanococcus
β
α α β
c
A
B A
A B
B
c
N C
F-proteolipid
V-type ATPase A-type ATPase
F-type ATPase
α β
Methanopyrus
?
mesophilicthermophilic
Archaea Eukarya Bacteria
endosymbionts
1
2
3
4
5
A
B
C
D E
12 proteolipid Ds / 6 cataly,c SU = 2 H+(Na+) / ATP
12 proteolipid Ds / 3 cataly,c SU = 4H+(Na+) / ATP
6 proteolipid Ds / 3 cataly,c SU = 2H+(Na+) / ATP
12 proteolipid Ds / 3 cataly,c SU = 4H+(Na+) / ATP
12 proteolipid Ds / 3 cataly,c SU = 4H+(Na+) / ATP
Reversible Enzyme Reversible Enzyme Dedicated Ion Pump
Dedicated Ion Pump
Reversible Enzyme
C. R. Woese and G. E. Fox (1977) J. Mol. Evol. 10, 1-‐6: “Eucaryotes did arise from procaryotes, but only in the sense that the procaryo6c is an organiza6onal, not a phylogene6c dis6nc6on. In analogous fashion procaryotes arose from simpler en66es. The la<er are properly called progenotes, because they are s6ll in the process of evolving the rela6onship between genotype and phenotype.”
According to Woese and Fox According to V/F/A-‐ATPases
From: GOGARTEN J.P., OLENDZENSKI L., (1999) The Progenote, Encyclopedia of Molecular Biology, Thomas Creighton, ed., John Wiley and Sons, NY (submieed version at gogarten.uconn.edu)
In R.P. Mortlock: (ed), The Evolu,on of Metabolic Func,on , CRC Press,1992
Organisms represented by the root of the universal evolu,onary tree were most likely complex cells with a sophis,cated protein transla,on system and a DNA genome encoding hundreds of genes.
Outline:
Mural at N
AS
A Am
es Research C
enter
• Gene duplica,ons and deep molecular phylogenies • Proper,es of the Last Universal Common Ancestor(s) • The history of the transla:on machinery during the expansion of the gene:c code
• The ribosomal tree of life and inferred op,mal growth temperature • Tree shape, the ar,fact of apparent “lonely ancestors” • Indica,ons for early ex,nc,on events due to increased environmental temperature
• Phylogene,c evidence for LUCA’s compatriots
A Radical Proposal by Eugene Koonin : Anthropic Chemical Evolution (The Logic of Chance – FT Press 2012)
• Modern cosmologies postulate parallel worlds, for example assuming an eternal inflation period, resulting in an infinite number of universes (Villinkin, 2007).
• Given an infinite number of universes, even unlikely events are bound to happen in some universes (and because we are made from two biopolymers, we are in one of the universes where this rare event occurred).
• Koonin suggests that the assembly of the translation machinery is a candidate for such an unlikely event.
• Finding exceedingly rare events in evolution would argue for a Multi World Cosmology.
These hypotheses can be tested by examining the composi,on of reconstructed ancestor sequences
Do synthetase paralogs retain evidence of pre-‐LUCA evolu,onary events?
Hypothesis Testing
1-2: neofunctionalization 3: subfunctionalization 4: takeover (parafunctionalization)
Probability density graph of all positions with X+Y plurality consensus in ancestral reconstruction of cognate paralog ancestor.
Results
• Majority of high-probabilitiy positions are resolved for Ile or Val • Supports both amino acids are specifically encoded at the time of the paralog ancestor, Parafunctionalization • Large number of nondiscriminating positions between Ile and Val would support subfunctionalization • However, these positions are all low-probability, and match with the control simulation, so probably artifact of poorly conserved positions.
"RNA – world" (single biopolymer world) Replica,on Machinery
"RNA – world" (single biopolymer world) Replica,on Machinery
Rise of protein as second biopolymer tRNAs, "RNA" Ribosome, RNA based tRNA charging mechanisms
"RNA – world" (single biopolymer world) Replica,on Machinery
Rise of protein as second biopolymer tRNAs, "RNA" Ribosome, RNA based tRNA charging mechanisms
Expansion of the gene,c code to include Isoleucine and Valine
"RNA – world" (single biopolymer world) Replica,on Machinery
Rise of protein as second biopolymer tRNAs, "RNA" Ribosome, RNA based tRNA charging mechanisms
Expansion of the gene,c code to include Isoleucine and Valine
Takeover of charging mechanism by proteins (inven,on of aminoacyl tRNA synthetases)
1IVS.pdb valRS + tRNAval
"RNA – world" (single biopolymer world) Replica,on Machinery
Rise of protein as second biopolymer tRNAs, "RNA" Ribosome, RNA based tRNA charging mechanisms
Expansion of the gene,c code to include Isoleucine and Valine
Takeover of charging mechanism by proteins (inven,on of aminoacyl tRNA synthetases)
Expansion of the gene,c code to include Tryptophan
1IVS.pdb valRS + tRNAval
Conclusions 1st part
• Extrapolation of ATPsynthase structure suggests that LUCA was able to use transmembrane ion gradients to synthesize ATP.
• LUCA was not a progenote • The expansion of the genetic code did not parallel the
divergence of aaRSs; rather aaRS acquired specificity in cells that were already able to charge tRNAs with their cognate aa through other means (likely exception tryptophan).
Outline:
Mural at N
AS
A Am
es Research C
enter
• Gene duplica,ons and deep molecular phylogenies • Proper,es of the Last Universal Common Ancestor(s) • The history of the transla,on machinery during the expansion of the gene,c code
• The ribosomal tree of life and inferred op:mal growth temperature • Tree shape, the ar,fact of apparent “lonely ancestors” • Indica,ons for early ex,nc,on events due to increased environmental temperature
• Phylogene,c evidence for LUCA’s compatriots
Evolution of the Ribosome
• “Core” of ribosome consists of RNA + subset of ribosomal proteins universally conserved in all life (~29 proteins) (Harris et al., 2003)
• Likely coevolved with genetic code within an RNA world (Wolf & Koonin, 2007)
Compositional Stratigraphy
“We perform a compositional analysis of ribosomal proteins and ATPase subunits in bacterial and archaeal lineages, using conserved positions that came and remained under purifying selection before and up to the most recent common ancestor. An observable shift in amino acid usage at these conserved positions likely provides an untapped window into the history of protein sequence space, allowing events of genetic code expansion to be identified.”
Fournier GP, Gogarten JP. 2007. Signature of a primitive genetic code in ancient protein lineages. J Mol Evol. 65(4):425-436
Roo,ng the Ribosomal Tree of Life using an Echo from the Early Expansion of the Gene,c Code (Fournier and Gogarten, MBE 2010)
Fig. 3. The classical SSUrRNA distance tree, presented as rooted in the bacterial branch. Bold lines indicate extreme hyperthermophiles. From Steeer (1996).
LUCA (located on the “bacterial branch”) was less thermophilic than the ancestor of the bacterial and archaeal domains
• Boussau, B, Blanquart, S, Necsulea, A, Lartillot, N and Gouy, M (2008). Parallel adaptations to high temperatures in the Archaean eon. Nature 456(7224): 942-945���Reconstruction of ancestral protein and rRNA sequences ���Based on IVYWREL and rRNA stem G+C content LUCA was less thermophilic than the domain ancestors.
• Galtier, N, Tourasse, N and Gouy, M (1999). A nonhyperthermophilic common ancestor to extant life forms. Science 283(5399): 220-221.8
• rRNA 60°C!80°C ���IVYWREL (corrected for GC content) 20°C!70°C
Outline:
Mural at N
AS
A Am
es Research C
enter
• Gene duplica,ons and deep molecular phylogenies • Proper,es of the Last Universal Common Ancestor(s) • The history of the transla,on machinery during the expansion of the gene,c code
• The ribosomal tree of life and inferred op,mal growth temperature • Tree shape, the ar:fact of apparent “lonely ancestors” • Indica:ons for early ex:nc:on events due to increased environmental temperature
• Phylogene,c evidence for LUCA’s compatriots
Tree, Web, or Coral of Life?
Charles Darwin painted by George Richmond in the late 1830 Page B26 from Charles Darwin’s (1809-1882)
notebook (1837/38)
“The tree of life should perhaps be called the coral of life, base of branches dead”
The Coral of Life (Darwin) ZHA
XY
BAY
EVA and G
OG
AR
TEN
(2004): C
ladogenesis, Coalescence and the E
volution of the Three Dom
ains of Life. Trends in G
enetics 20 (4): 182- 187
The Coral of Life (Darwin) ZHA
XY
BAY
EVA and G
OG
AR
TEN
(2004): C
ladogenesis, Coalescence and the E
volution of the Three Dom
ains of Life. Trends in G
enetics 20 (4): 182- 187
Coalescence – the process of tracing lineages backwards in ,me to their common ancestors. Every two extant lineages coalesce to their most recent common ancestor. Eventually, all lineages coalesce to the cenancestor.
t/2
(Kingman, 1982)
Illustra,on is from J. Felsenstein, “Inferring Phylogenies”, Sinauer, 2003
EXTA
NT LINEA
GES FO
R TH
E SIMULATIONS OF 50 LINEA
GES
Bacterial 16SrRNA based phylogeny (from P. D. Schloss and J. Handelsman, Microbiology and Molecular Biology Reviews, December 2004.)
The devia,on from the “long branches at the base” paeern could be due to • under sampling • an actual radia,on
• due to an inven,on that was not transferred • following a mass ex,nc,on
Near frustra,on of early life
From: Gogarten-‐Boekels M, Hilario E, Gogarten JP. Orig Life Evol Biosph. 1995 Jun;25(1-‐3):251-‐64. The effects of heavy meteorite bombardment on the early evolu:on —the emergence of the three domains of life.
From: he
p://www.origin-‐life.gr.jp/3603/3603055/3603055.htm
l
Alterna,ve: tail of early heavy bombardment – Nicolle Zellner’s talk on Tuesday See Marchi et al. Nature 2014 for a recent update.
Outline:
Mural at N
AS
A Am
es Research C
enter
• Gene duplica,ons and deep molecular phylogenies • Proper,es of the Last Universal Common Ancestor(s) • The history of the transla,on machinery during the expansion of the gene,c code
• The ribosomal tree of life and inferred op,mal growth temperature • Tree shape, the ar,fact of apparent “lonely ancestors” • Indica,ons for early ex,nc,on events due to increased environmental temperature
• Phylogene:c evidence for LUCA’s compatriots
Molecular Phylogenies " Lonely Ancestors
From: hep://itol.embl.de/ iTol The interac,ve Tree of Life Ciccarelli et al, Science. 2006 311 :1283-‐7
• Tree topology averaged over many genes (mainly ribosomal proteins).
• No re,cula,ons. • Branches do not
reflect ,me. • Only extant organisms
and their lucky ancestors are includes
Noteworthy:
The Coral of Life (Darwin) ZHA
XY
BAY
EVA and G
OG
AR
TEN
(2004): C
ladogenesis, Coalescence and the E
volution of the Three Dom
ains of Life. Trends in G
enetics 20 (4): 182- 187
The Coral of Life (Darwin) ZHA
XY
BAY
EVA and G
OG
AR
TEN
(2004): C
ladogenesis, Coalescence and the E
volution of the Three Dom
ains of Life. Trends in G
enetics 20 (4): 182- 187
Molecular phylogenies of aaRSs reveal other lineages that coexisted with LUCA and/or the domain ancestors and transferred some of their genes into extant lineages.
Pyrrolysine (Pyl) # 22nd genetically encoded amino acid to be discovered
# Uses dedicated aminoacyl-tRNA synthetase (PylS) and a UAG-recognizing tRNA.
# Found only within Methanosarcinae, Desulfitobacterium hafniense and a single marine worm symbiont delta-proteobacteria.
# Used exclusively at the catalytic site of three enzymes responsible for the initial step of methylotrophic methanogenesis from methylamines.
MtmB structure with Pyl residue in catalytic core (Hao et al., 2002)
Synthesized from Pro and Lys Contains a peptide bond in the side chain
Class II aaRS Phylogeny
LUCA -nodes
Horizontal Gene Transfer ● Pyl evolved and had a pervasive biological role in an ancient sister group to the
MRCA.
● Transfer of cassette encoding methyltransferases and pyrrolysine system, selected for by the transfer of the methyltransferase genes.
● Subsequent extinction of the entire donor lineage
Genetic Life Raft
Ancient origin of the divergent form
s of leucyl-‐tRNA synthetases
in the Halobacteriales Cheryl P Andam
, Timothy J
Harlow, R Thane Papke and
J Peter Gogarten BM
C Evolu6onary Biology 12:85
leucyl-tRNA synthetase (class I) phylogeny
Homeoalleles
• Variants that have the same general function, but can have distinct characteristics.
• Gene pool contains different homeoalleles, but individual strains and species usually contain only one of the alleles.
• Can be brought together temporarily in a lineage through HGT
Andam, Williams, Gogarten 2010 PNAS
Andam and Gogarten 2011
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Phylogeny of selected class II amino acyl tRNA synthetases
Andam and Gogarten 2011
Distribu:on of rare SerRS in
Archaea
thrRS and serRS phylogeny Eukaryotes
Euryachaeota Crenarchaeota
Bacteria
Alignment with PRANK and SATé, tree with phyml (WAG, gamma +I)
Conclusion 2nd part
• Tree shape and amino acid composition of ancestral sequences suggest a bottleneck due to increased environmental temperature at the base of the bacterial and archaeal domains.
• Studies of horizontal gene transfers of aaRSs suggest that more than two lineages passed through this bottleneck.
References
• Andam CP, Gogarten JP. 2011. Biased gene transfer in microbial evolu,on. Nat. Rev. Microbiol. 9:543–555.
• Andam CP, Harlow TJ, Papke RT, Gogarten JP. 2012. Ancient origin of the divergent forms of leucyl-‐tRNA synthetases in the Halobacteriales. BMC Evol. Biol. 12:85.
• Andam CP, Williams D, Gogarten JP. 2010. Biased gene transfer mimics paeerns created through shared ancestry. Proc. Natl. Acad. Sci. U. S. A. 107:10679–10684.
• Boussau B, Blanquart S, Necsulea A, Lar,llot N, Gouy M. 2008. Parallel adapta,ons to high temperatures in the Archaean eon. Nature 456:942–945.
• Ciccarelli FD, Doerks T, von Mering C, Creevey CJ, Snel B, Bork P. 2006. Toward automa,c reconstruc,on of a highly resolved tree of life. Science 311:1283–1287.
• Delaye L, Becerra A, Lazcano A. 2005. The last common ancestor: what’s in a name? Orig Life Evol Biosph 35:537–554.
• Felsenstein J. 2003. Inferring Phylogenies. Sinauer, Sunderland, MA • Fournier GP, Andam CP, Alm EJ, Gogarten JP. 2011. Molecular evolu,on of aminoacyl tRNA
synthetase proteins in the early history of life. Orig. Life Evol. Biosph. 41:621–632. • Fournier GP, Gogarten JP. 2007. Signature of a primi,ve gene,c code in ancient protein
lineages. J. Mol. Evol. 65:425–436. • Fournier GP, Gogarten JP. 2010. Roo,ng the ribosomal tree of life. Mol. Biol. Evol.
27:1792–1801. • Fournier GP, Huang J, Gogarten JP. 2009. Horizontal gene transfer from ex,nct and extant
lineages: biological innova,on and the coral of life. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 364:2229–2239.
References (con,nued)
• Gal,er N, Tourasse N, Gouy M. 1999. A nonhyperthermophilic common ancestor to extant life forms. Science 283:220–221.
• Gogarten JP, Kibak H, Dierich P, et al. 1989. Evolu,on of the vacuolar H+-‐ATPase: implica,ons for the origin of eukaryotes. Proc Natl Acad Sci U S A 86:6661–6665.
• Gogarten JP, Taiz L. 1992. Evolu,on of proton pumping ATPases: Roo,ng the tree of life. Photosynth. Res. 33:137–146.
• Gogarten-‐Boekels M, Hilario E, Gogarten JP. 1995. The effects of heavy meteorite bombardment on the early evolu,on-‐-‐the emergence of the three domains of life. Orig Life Evol Biosph 25:251–264.
• Goldman AD, Bernhard TM, Dolzhenko E, Landweber LF. 2013. LUCApedia: a database for the study of ancient life. Nucleic Acids Res. 41:D1079–82.
• Hao B, Gong W, Ferguson TK, James CM, Krzycki JA, Chan MK. 2002. A new UAG-‐encoded residue in the structure of a methanogen methyltransferase. Science 296:1462–1466.
• Harris JK, Kelley ST, Spiegelman GB, Pace NR. 2003. The gene,c core of the universal ancestor. Genome Res 13:407–412.
• Kim KM, Caetano-‐Anollés G. 2011. The proteomic complexity and rise of the primordial ancestor of diversified life. BMC Evol. Biol. 11:140.
• Kingman JFC. 1982. The coalescent. Stoch. Process. Their Appl. 13:235–248. • Koeberl C. 2006. Impact Processes on the Early Earth. Elements 2:211–216. • Koonin E V. 2011. The Logic of Chance: The Nature and Origin of Biological Evolu,on. FT
Press; 1 edi,on
References (con,nued)
• Marchi S, Boeke WF, Elkins-‐Tanton LT, Bierhaus M, Wuennemann K, Morbidelli A, Kring DA. 2014. Widespread mixing and burial of Earth’s Hadean crust by asteroid impacts. Nature 511:578–582.
• Schloss PD, Handelsman J. 2004. Status of the microbial census. Microbiol Mol Biol Rev 68:686–691.
• Steeer K. 1996. Hyperthermophilic procaryotes. FEMS Microbiol. Rev. 18:149–158. • Vilenkin A. 2007. Many Worlds in One: The Search for Other Universes. Farrar, Straus
and Giroux A • Williams D, Fournier GP, Lapierre P, Swithers KS, Green AG, Andam CP, Gogarten JP.
2011. A rooted net of life. Biol. Direct 6:45. • Woese CR, Fox GE. 1977. The concept of cellular evolu,on. J Mol Evol 10:1–6. • Wolf YI, Koonin E V. 2007. On the origin of the transla,on system and the gene,c code
in the RNA world by means of natural selec,on, exapta,on, and subfunc,onaliza,on. Biol. Direct 2:14.
• Xu Y, Glansdorff N. 2002. Was our ancestor a hyperthermophilic procaryote? Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 133:677–688.
• Zhaxybayeva O, Gogarten JP. 2004. Cladogenesis, coalescence and the evolu,on of the three domains of life. Trends Genet. 20:182–187.
• Zhaxybayeva O, Lapierre P, Gogarten JP. 2005. Ancient gene duplica,ons and the root(s) of the tree of life. Protoplasma 227:53–64.