Advances in the Microbiology of the Atacama Desert and its Connection with Astrobiology

Advances in the Microbiology of the Atacama Desert and its Connection with

Astrobiology

Benito Gómez SilvaUniversidad de Antofagasta

ASTROBIO 2010 - SANTIAGO, CHILE

THE ATACAMA DESERT

• 1,200 km from approximately 18oS to 28oS• located between the Pacific coast and the Andes Mountains • the oldest and driest desert on Earth• temperate hyperarid desert with mean annual temperature of 14–16 °C• long term mean annual rainfall as low as 2 millimeters at its driest core• increase in precipitation along the North-to-South latitude gradient• became arid nearly 150 million years • extreme aridity conditions for at least 10 – 15 million years ago• large natural ore-grade nitrate deposits from atmospheric deposition,

due to absence of soil leaching and biological cycling.

Astrobiology 3, 393 (2003), Int. J. Climatol. 23, 1453 (2003), Geomorphology 73, 101 (2006), Microbiology of Extreme Soils. Soil Biology 13. P Dion, CS Nautiyal, eds. Springer, 2008.


CONTRIBUTING FACTORS TO THE ATACAMA ARIDITY:

(a) a zonal effect due to the subtropical high pressure belt which generates conditions for a strong precipitation deficit,

(b) a continentality effect due to the distance of Atacama to the Amazonia-Atlantic moisture source,

(c) a rainshadow effect due to the proximity of the Andes Range which prevents moisture advection from the east by disrupting zonal circulation, (in addition; “fog shadow” effect of the high coastal crest-line)

(d) the oceanic effect carried out by the cold north-flowing Humboldt Current that upwells along the Atacama coast and generates a constant temperature inversion that traps moisture below 800 m altitude

Astrobiology 3, 393 (2003) , Int. J. Climatol. 23, 1453 (2003), Atmospheric Res. 71, 127 (2004)Microbiology of Extreme Soils. Soil Biology 13. P Dion, CS Nautiyal, eds. Springer, 2008.,


IS THERE MICROBIAL LIFE IN THE ATACAMA SOILS? If there is …

What kind of microorganisms are at the Atacama?

Abundance and diversity? Major environmental factor controlling life at the Atacama?


“MARS-LIKE” SOILS AT THE HYPERARID CORE OF ATACAMA

Very low levels of soil organic matter (0.02-0.04 mg of C/g soil; 100 x lower than Dry Valleys soils, Antarctica)

None or very low levels of detectable soil bacteria (by culture or DNA amplification)

Soils contain a nonchirally specific oxidizing agent that equally oxidizes amino acid and glucose enantiomers.

Science 302, 1018 (2003)


EVIDENCE OF MICROBIAL LIFE IN THE ATACAMA SOILS:

1. Macroscopic and microscopic evidence: presence of microorganisms in hospitable habitats such as halites, quarzt, gypsum.

2. Biomarkers: soil organic matter (biomolecules) and biological, chemical, and photochemical decomposition mechanisms.

3. Microorganisms: culture dependent and independent methods

Science 302, 1018 (2003), Microb. Ecol. 52, 389 (2006), Astrobiology 4, 415 (2006)J. Geophys. Res., 112, G04S15, doi:10.1029/2006JG000305 (2007), J. Geophys. Res. 112, G02030, doi: 10.1029/2006JG000385 (2007), Proc. IV Int. Conference on Fog, Fog Collection and Dew, Santiago (2007), J. Geophys. Res. 113 doi:10.1029/2007JG000561 (2008), J. Photochem. Photobiol.B: Biology 90, 79 (2008)


1. SUITABLE NICHES FOR MICROBIAL COLONIZATION MUST BE:

a. an intercepting obstacle for water droplets deposition from incoming fog events

b. a surface for dew formation

c. a temperature-controlling environment

d. a filter to harmful solar UV radiation

e. translucent to PAR (photosynthetic active radiation)

J. Arid Environ. 65, 572 (2006) Astrobiology: Emergence, Search and Detection of Life. V.A. Basiuk, ed., American Scientific Publishers,

2009. In press.


Microorganisms in hospitable habitats from Atacama: hypolithic growth in quartz.

Astrobiology: Emergence, Search and Detection of Life. V.A. Basiuk, ed., American Scientific Publishers, 2009. In press.


Microorganisms in hospitable habitats from Atacama: growth of epilithic (A) and endolithic (B) cyanobacterial biofilms in halites.



Microorganisms in hospitable habitats from Atacama: epi-endolithic growth of melanized meristematic fungus in halites.



Microorganisms in hospitable habitats from Atacama: gypsum


J. Geophys. Res. 112, G02030, doi: 10.1029/2006JG000385 (2007)


ATACAMA SITE ORGANICS DETECTED METHOD REFERENCE

24°S, 70°W

28°S, 70°W

Formic acid, benzene

Formic acid, propenenitrile, benzene, ethylbenzene, 1, 2-dimethylbenzene, methylbenzene, benzenenitrile,1,2-butadiene, 1,3-pentadiene, 2-methylfuran, styrene

pyr-GC-MS Science 302, 1018 (2003)

24°-28°S Amino acids (gly, glu, asp, ala, ser; 10 – 500 ppb along the precipitation gradient)*

HPLC(MOA)

Proc. Nat. Acad. Sci. 102, 1041 (2005)*

27°S Amino acids (gly, ala, val; 20-100 ng/g)

GC-MS Planet. Space Sci. 54, 1592 (2006)

2. SOIL ORGANIC MATTER (SOM) AND BIOMOLECULES

* From the authors: “Results advance the technology for laboratory and field analyses of samples from and in Mars-like sites. Detection limits: parts per trillion.”

3. MICROORGANISMS IN ATACAMA SOILS

Large numbers and diversity of bacterial life at sites where water is available but, are there any bacteria at the hyperarid soils of Atacama?

Where? How abundant?

How diverse?

Heterotrophic bacteria are present in the surface and subsurface soils of the hyperarid Atacama Desert in an ecological pattern

of non-uniform distribution or patchiness.

Science 302, 1018 (2003), Appl. Environ. Microbiol. 70, 5923 (2004), Appl. Environ. Microbiol. 72, 7902 (2006)Soil Biol. Biochem. 39, 704 (2007), J. Geophys. Res. 112, G04S17, doi:10.1029/2006JG000311 (2007)Int. J. Syst. Evol. Microbiol. 57, 1408 (2007), Microbiology of Extreme Soils. Soil Biology 13. P Dion, CS Nautiyal, eds. Springer, 2008., Astrobiology: Emergence, Search and Detection of Life. V.A. Basiuk, ed., American Scientific Publishers, 2009. In press.


Atacama Sites Detection CFU per gram of soil References

24° to 28°S, 70°W Viable counts

<1 x 103 to 105 Science 302, 1018 (2003)

100 miles south of Yungay

(24°04’S, 69°5’W)DAPIstain

0.7 x 106 (surface)

9.6 x 106 (subsurface)

Appl. Environ. Microbiol.

70, 5923 (2004)

23°S, 70°W to 24°S, 69°W400 to 4,500 masl

Viable counts <1 x 103 to 107

Appl. Environ. Microbiol.

72, 7902 (2006)

24°S, 69°52’WViable counts 103 CFU/g

Soil Biol. Biochem. 39, 704 (2007)


ABUNDANCE OF HETEROTROPHIC MICROORGANISMS FROM ATACAMA SOILS


Phylogenetic Lineages Reference

FirmicutesProteobacteriaActinobacteria GeodermatophilaceaeGenera: Sphingomonas, Bacillus, Arthrobacter, Brevibacillus, Kocuria, Cellulomonas, Hymenobacter

Science 302, 1018 (2003)

Gemmatimonadetes, Planctomycetes, Actinobacteria, Thermomicrobia, Proteobacteria, Acidithiobacillus

Appl. Environ. Microbiol. 72, 7902 (2006)

Gemmatimonadetes, Actinobacteria, Planctomycetes, Thermomicrobia, Proteobacteria

Soil Biol. Biochem. 39, 704 (2007)

Proteobacteria, Firmicutes, uncultured MT7 phylum, Actinobacteria: Frankia

J. Geophys. Res. 112, G04S17,

doi:10.1029/2006JG000311 (2007)

Deinococcus Int. J. Syst. Evol. Microbiol. 57, 1408 (2007)

DIVERSITY OF HETEROTROPHIC MICROORGANISMS FROM ATACAMA SOILS


LIFE IN ATACAMA: THE CYANOBACTERIAL FACTOR


CYANOBACTERIA

Unicellular or filamentous Gram-negative photosynthetic prokaryotes

Key primary producers in a variety of habitats, including hot and cold deserts; particularly, under water stress conditions too limiting for most eukaryotic or prokaryotic life forms

Free-living microorganisms forming biofilms in lithobiontic niches

Symbiotic association in lichens (phycobionts)

Endolithic, epilithic, hypolithic colonization


CYANOBACTERIA-DOMINATED MICROBIAL CONSORTIA IN ATACAMA

QUARTZ STUDY AREA AT AGUAS CALIENTES (25°18’S)


DIVERSITY OF PHOTOAUTOTROPHIC AND HETEROTROPHIC MICROORGANISMS FROM ATACAMA LITHOBIONTIC BIOFILMS

LITHIC SUBSTRATE PHYLOGENETIC LINEAGES REFERENCE

QuartzChroococcidiopsis, Nostoc, Phormidium

alpha-proteobacteria, gamma-proteobacteria

acidobacteriales

Microb. Ecol. 52, 389 (2006)

GypsumCyanobacteriae, alphaproteobacteria Verrucomicrobia, Firmicutes, Bacillus, Gemmatimonadetes,Planctomycetes

J. Geophys. Res. 112, G02030, doi:

10.1029/2006JG000385 (2007)

Halites

Chroococcidiopsis-likeHeterotrophic bacteria

ChroococcidiopsisNectria sp.

Astrobiology 4, 415 (2006)

Astrobiology: Emergence, Search

and Detection of Life. V.A. Basiuk, ed.,

Am Sci. Pub. In press.


FACTOR WITH MINOR OR NULL IMPACT ON PHOTOAUTOTROPHIC LIFE AT ATACAMA

HABITAT AVAILABILITY

TEMPERATURE

SOIL TOXICITY AND pH

CARBON INFLOW

MAJOR ABIOTIC FACTORS AFFECTING LITHOBIONTIC LIFE AT ATACAMA

SUNLIGHT

MOISTURE


HABITAT AVAILABILITY(North-to-South transect)

SITE YUNGAY 24°06’

AGUAS CALIENTES

25°18’

ALTAMIRA25°45’

COPIAPÓ27°01’

RELATIVEDISTANCE (Km) 0 162 250 460

MEAN ANNUAL RAINFALL (mm) 2.4 4.7 - 21

NUMBER OF STONES/m2 4 32 1.5 0.31

TOTAL STONES COUNTED 3723 6892 1466 1093

% COLONIZED STONES 0.08 0.33 7.37 27.63

Microb. Ecol. 52, 389 (2006)


COLONIZED NICHES TEMPERATURE (°C)

Maximum Minimum

QUARTZ (coastal desert, 23°48’ S)

AIR (17.2°C mean annual) 29.5 7.5

STONE SURFACE 40.7 11.6

BELOW THE STONE 38.8 14.9

SOIL SURFACE 47.3 11.9

SOIL (5 cm deep) 46.4 14.1

QUARTZ (Yungay, desert core; 24°04’ S)

AIR (16.5°C mean annual) 37.9 - 5.7

STONE SURFACE 57.4 - 4.9

QUARTZ (Aguas calientes, desert core; 25°18’ S)

AIR (17.9°C mean annual) 37.7 - 5.8

SOIL (2-5 cm deep) 42.5 - 5.8

HALITES (Yungay, desert core, 24°49’ S)

INSIDE THE CRUST 48.5 - 3.9

OUTSIDE THE CRUST 51.8 - 3.4


Location(70° W)

Mean annual rainfall

% of quartz stones with colonization

24° S 2 mm 0.1

25° S 4 mm 0.3

27° S 21 mm 28

LIQUID WATER AVAILABILITY FOR CYANOBACTERIAL QUARTZ COLONIZATION (NORTH-TO-SOUTH TRANSECT)

Microb. Ecol. 52, 389 (2006)J. Geophys. Res., 112, G04S15, doi:10.1029/2006JG000305 (2007)

SOURCE OF LIQUID WATERRAINFOGDEW


DESSICATION TOLERANCE:

biosynthesis of exopolysaccharides

(EPS)

EPS


SOLAR AND UV RADIATION

Annual average sunlight at the Atacama core: 335 Wm-2 Daily maximum over 1,000 Wm-2

Maximum values for PAR Yungay: 2.37 mmoles m-2 s-1

Salar Grande: 2.21 mmoles m-2 s-1

Quartz stones transmit from 0.08% to 1% of midday incident light (depending upon thickness and coloration).

The lowest end of this intensity range is closer to or below the light compensation for photosynthesis of primary producers.

ASTROBIO 2010 - SANTIAGO, CHILEJ. Photochem. Photobiol. B: Biology 90, 79 (2008)


MICROORGANISMS FROM ATACAMA

STRATEGIES TO COPE WITH HIGH SOLAR UV RADIATION(UV-A: 315-400 nm; UV-B: 280-315 nm)

PIGMENT ABSORBANCE MAXIMA

MAAs(mycosporine-like amino acids 309-362 nm

MELANIN in vivo: 335 nm in vitro: 280-310; 420-450 nm

SCYTONEMIN* in vivo: 370 nm in vitro: 384 nm

*only in cyanobacteria; aprox. 300 species.


ABSOPTION SPECTRUM OF CRUDE EXTRACT FROM CYANOBACTERIAL BIOFILMS

300 400 500 600 700 8000.0

0.1

0.2

0.3

0.4

0.5

Longitud de onda (nm)

Abs

orba

ncia


Minutes

0,0 0,5 1,0 1,5 2,0 2,5 3,0 3,5 4,0 4,5 5,0 5,5 6,0 6,5 7,0 7,5 8,0 8,5

mA

U

0,0

2,5

5,0

7,5

10,0

12,5

15,0

17,5

20,0

22,5

25,0

27,5

30,0

32,5

35,0

mA

U

0,0

2,5

5,0

7,5

10,0

12,5

15,0

17,5

20,0

22,5

25,0

27,5

30,0

32,5

35,0DAD-CH1 320 nmLL 1 neu

DAD-CH1 320 nm

HPLC CHROMATOGRAM OF SCYTONEMIN FROM TWO CYANOBACTERIAL BIOFILMS


nm

250 300 350 400 450 500 550 600 650 700 750 800

mA

U

0

20

40

60

80

mA

U

0

20

40

60

80

382

251

298

759

51

8

567

5,99 MinLL 1 neu

Lambda MaxLambda Min

ABSORPTION SPECTRUM OF SCYTONEMIN AFTER PURIFICATION BY HPLC


HALITE COLONIZATION PIGMENT CONTENT (mg g proteins-1)

Scytonemin Chlorophyll a Carotenoids

EPILITHIC 12.0 0.7 0.2

ENDOLITHIC 0.5 0.2 0.06

EPIILITHIC COLONIZATION ENDOLITHIC COLONIZATION


Héctor Olivares, Universidad de Antofagasta, ChileCatherine Lizama, Universidad de Antofagasta, ChileArmando Azua, PUC, ChileJacek Wierzchos, CCMA – CSIC, SpainCarlos González, UNAP, ChileE. Imre Friedmann, NASA, USAChris McKay, AMES – NASA, USAAlfonso F Dávila, NASA, USAFred A Rainey, Louisiana State University, USARafael Navarro-González, UNAM, MéxicoKlaus Dose, Johannes Gutemberg-Universität, Mainz, GermanySergio Risi, Johannes Gutemberg-Universität, Mainz, Germany


Dr. E. Imre Friedmann1921-2007

An ”extreme” microbiologist

Microbial ecology of absolute extreme environments, astrobiology, experimental and molecular taxonomy of cyanobacteria.

Documents

Advances in the Microbiology of the Atacama Desert and its Connection with Astrobiology