Transcript Advances in the Microbiology of the Atacama Desert and its

Advances in the Microbiology of the
Atacama Desert and its Connection
with Astrobiology
Benito Gómez Silva
Universidad 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?
ASTROBIO 2010 - SANTIAGO, CHILE
“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)
ASTROBIO 2010 - SANTIAGO, CHILE
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.
ASTROBIO 2010 - SANTIAGO, CHILE
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
J. Geophys. Res. 112, G02030, doi: 10.1029/2006JG000385 (2007)
ASTROBIO 2010 - SANTIAGO, CHILE
2. SOIL ORGANIC MATTER (SOM) AND BIOMOLECULES
ATACAMA SITE
ORGANICS DETECTED
METHOD
REFERENCE
pyr-GC-MS
Science
302, 1018 (2003)
Amino acids
(gly, glu, asp, ala, ser; 10 – 500 ppb
along the precipitation gradient)*
HPLC
(MOA)
Proc. Nat. Acad. Sci.
102, 1041 (2005)*
Amino acids
(gly, ala, val; 20-100 ng/g)
GC-MS
Planet. Space Sci.
54, 1592 (2006)
24°S, 70°W
Formic acid, benzene
28°S, 70°W
Formic acid, propenenitrile, benzene,
ethylbenzene, 1, 2-dimethylbenzene,
methylbenzene, benzenenitrile,
1,2-butadiene, 1,3-pentadiene, 2methylfuran, styrene
24°-28°S
27°S
* 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.”
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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
ABUNDANCE OF HETEROTROPHIC MICROORGANISMS FROM ATACAMA SOILS
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)
23°S, 70°W to 24°S, 69°W
400 to 4,500 masl
24°S, 69°52’W
0.7 x 106
(surface)
DAPI
stain
Viable
counts
Viable
counts
9.6 x 106
(subsurface)
<1 x 103 to 107
103
CFU/g
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Appl. Environ.
Microbiol.
70, 5923 (2004)
Appl. Environ.
Microbiol.
72, 7902 (2006)
Soil Biol. Biochem.
39, 704 (2007)
DIVERSITY OF HETEROTROPHIC MICROORGANISMS FROM ATACAMA SOILS
Phylogenetic Lineages
Reference
Firmicutes
Proteobacteria
Actinobacteria
Geodermatophilaceae
Genera: 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)
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LIFE IN ATACAMA:
THE CYANOBACTERIAL FACTOR
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CYANOBACTERIA
Unicellular or filamentous Gramnegative 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
Quartz
Gypsum
Halites
PHYLOGENETIC LINEAGES
REFERENCE
Chroococcidiopsis, Nostoc, Phormidium
alpha-proteobacteria,
gamma-proteobacteria
acidobacteriales
Microb. Ecol.
52, 389 (2006)
Cyanobacteriae, alphaproteobacteria
Verrucomicrobia, Firmicutes, Bacillus,
Gemmatimonadetes,Planctomycetes
J. Geophys. Res.
112, G02030, doi:
10.1029/2006JG000
385 (2007)
Chroococcidiopsis-like
Heterotrophic bacteria
Astrobiology
4, 415 (2006)
Chroococcidiopsis
Nectria sp.
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’
ALTAMIRA
25°45’
COPIAPÓ
27°01’
RELATIVE
DISTANCE (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)
ASTROBIO 2010 - SANTIAGO, CHILE
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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LIQUID WATER AVAILABILITY FOR CYANOBACTERIAL QUARTZ COLONIZATION
(NORTH-TO-SOUTH TRANSECT)
% of quartz stones
with colonization
Location
(70° W)
Mean annual
rainfall
24° S
2 mm
0.1
25° S
4 mm
0.3
27° S
21 mm
28
SOURCE OF LIQUID WATER
RAIN
FOG
DEW
Microb. Ecol. 52, 389 (2006)
J. Geophys. Res., 112, G04S15, doi:10.1029/2006JG000305 (2007)
ASTROBIO 2010 - SANTIAGO, CHILE
EPS
DESSICATION
TOLERANCE:
biosynthesis of
exopolysaccharides
(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:
Salar Grande:
2.37 mmoles m-2 s-1
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.
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J. 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
0.5
Absorbancia
0.4
0.3
0.2
0.1
0.0
300
400
500
600
Longitud de onda (nm)
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700
800
HPLC CHROMATOGRAM OF SCYTONEMIN FROM TWO CYANOBACTERIAL BIOFILMS
DAD-CH1 320 nm
LL 1 neu
35,0
DAD-CH1 320 nm
32,5
32,5
30,0
30,0
27,5
27,5
25,0
25,0
22,5
22,5
20,0
20,0
17,5
17,5
15,0
15,0
12,5
12,5
10,0
10,0
7,5
7,5
5,0
5,0
2,5
2,5
0,0
0,0
0,0
0,5
1,0
1,5
2,0
2,5
3,0
3,5
4,0
4,5
5,0
5,5
Minutes
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6,0
6,5
7,0
7,5
8,0
8,5
mAU
mAU
35,0
ABSORPTION SPECTRUM OF SCYTONEMIN AFTER PURIFICATION BY HPLC
5,99 Min
LL 1 neu
80
80
382
Lambda Max
Lambda Min
60
40
759
567
20
518
20
0
250
300
350
400
450
500
550
nm
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600
650
700
750
0
800
mAU
40
298
mAU
251
60
EPIILITHIC COLONIZATION
HALITE COLONIZATION
ENDOLITHIC 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
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Héctor Olivares, Universidad de Antofagasta, Chile
Catherine Lizama, Universidad de Antofagasta, Chile
Armando Azua, PUC, Chile
Jacek Wierzchos, CCMA – CSIC, Spain
Carlos González, UNAP, Chile
E. Imre Friedmann, NASA, USA
Chris McKay, AMES – NASA, USA
Alfonso F Dávila, NASA, USA
Fred A Rainey, Louisiana State University, USA
Rafael Navarro-González, UNAM, México
Klaus Dose, Johannes Gutemberg-Universität, Mainz, Germany
Sergio Risi, Johannes Gutemberg-Universität, Mainz, Germany
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Dr. E. Imre Friedmann
1921-2007
An ”extreme” microbiologist
Microbial ecology of absolute extreme
environments, astrobiology,
experimental and molecular taxonomy of
cyanobacteria.
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