advances in the microbiology of the atacama desert and its connection with astrobiology
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Advances in the Microbiology of the Atacama Desert and its Connection with Astrobiology. Benito Gómez Silva Universidad de Antofagasta. THE ATACAMA DESERT 1,200 km from approximately 18 o S to 28 o S located between the Pacific coast and the Andes Mountains - PowerPoint PPT PresentationTRANSCRIPT
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.
ASTROBIO 2010 - SANTIAGO, CHILE
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.,
ASTROBIO 2010 - SANTIAGO, CHILE
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?
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“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)
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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)
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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.
ASTROBIO 2010 - SANTIAGO, CHILE
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.
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Microorganisms in hospitable habitats from Atacama: growth of epilithic (A) and endolithic (B) cyanobacterial biofilms in halites.
Astrobiology: Emergence, Search and Detection of Life. V.A. Basiuk, ed., American Scientific Publishers, 2009. In press.
ASTROBIO 2010 - SANTIAGO, CHILE
Microorganisms in hospitable habitats from Atacama: epi-endolithic growth of melanized meristematic fungus in halites.
Astrobiology: Emergence, Search and Detection of Life. V.A. Basiuk, ed., American Scientific Publishers, 2009. In press.
ASTROBIO 2010 - SANTIAGO, CHILE
Microorganisms in hospitable habitats from Atacama: gypsum
ASTROBIO 2010 - SANTIAGO, CHILE
J. Geophys. Res. 112, G02030, doi: 10.1029/2006JG000385 (2007)
ASTROBIO 2010 - SANTIAGO, CHILE
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.
ASTROBIO 2010 - SANTIAGO, CHILE
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)
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ABUNDANCE OF HETEROTROPHIC MICROORGANISMS FROM ATACAMA SOILS
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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
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LIFE IN ATACAMA: THE CYANOBACTERIAL FACTOR
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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
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CYANOBACTERIA-DOMINATED MICROBIAL CONSORTIA IN ATACAMA
QUARTZ STUDY AREA AT AGUAS CALIENTES (25°18’S)
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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.
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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
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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)
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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
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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
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DESSICATION TOLERANCE:
biosynthesis of exopolysaccharides
(EPS)
EPS
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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)
ASTROBIO 2010 - SANTIAGO, CHILE
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.
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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
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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
ASTROBIO 2010 - SANTIAGO, CHILE
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
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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
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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
ASTROBIO 2010 - SANTIAGO, CHILE
Dr. E. Imre Friedmann1921-2007
An ”extreme” microbiologist
Microbial ecology of absolute extreme environments, astrobiology, experimental and molecular taxonomy of cyanobacteria.