The OMEGA/Mars Express hyperspectral imager identified gypsum at several sites on Mars in 2005. These minerals constitute a direct record of past aqueous activity and are important with regard to the search of extraterrestrial life. Gale Crater was chosen as Mars Science Laboratory Curiosity's landing site because it is rich in gypsum, as are some desert soils of the Cuatro Ciénegas Basin (CCB) (Chihuahuan Desert, Mexico). The gypsum of the CCB, which is overlain by minimal carbonate deposits, was the product of magmatic activity that occurred under the Tethys Sea. To examine this Mars analogue, we retrieved gypsum-rich soil samples from two contrasting sites with different humidity in the CCB. To characterize the site, we obtained nutrient data and analyzed the genes related to the N cycle (nifH, nirS, and nirK) and the bacterial community composition by using 16S rRNA clone libraries. As expected, the soil content for almost all measured forms of carbon, nitrogen, and phosphorus were higher at the more humid site than at the drier site. What was unexpected is the presence of a rich and divergent community at both sites, with higher taxonomic diversity at the humid site and almost no taxonomic overlap. Our results suggest that the gypsum-rich soils of the CCB host a unique microbial ecosystem that includes novel microbial assemblies. Key Words: Cuatro Ciénegas Basin—Gale Crater—Gypsum soil microbial diversity—Molecular ecology—Nitrogen cycle. Astrobiology 12, 699–709.
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References
1.
AguileraL.E., GutierrezJ.R., MeserveP.L.1999. Variation in soil micro-organisms and nutrients underneath and outside the canopy of Adesmia bedwellii (Papilionaceae) shrubs in arid coastal Chile following drought and above average rainfall. J Arid Environ, 42:61–70.
2.
BååthE., AndersonT.H.2003. Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLFA-based techniques. Soil Biol Biochem, 35:955–963.
3.
BanfieldJ.F., MoreauJ.W., ChanC.S., WelchS.A., LittleB.2001. Mineralogical biosignatures and the search for life on Mars. Astrobiology, 1:447–465.
4.
Bonilla-RossoG., PeimbertM., AlcarazL.D., HernándezI., EguiarteL.E., Olmedo-AlvarezG., SouzaV.2012. Comparative metagenomics of two microbial mats at Cuatro Ciénegas Basin II: community structure and composition in oligotrophic environments. Astrobiology, 12:659–673.
5.
BreitbartM., HoareA., NittiA., SiefertJ., HaynesM., DinsdaleE., EdwardsR., SouzaV., RohwerF., HollanderD.2009. Metagenomic and stable isotopic analyses of modern freshwater microbialites in Cuatro Ciénegas, Mexico. Environ Microbiol, 11:16–34.
6.
BremmerJ.M., MulvaneyC.S.1982. Nitrogen-total. Methods of Soil Analysis. Part 2. Chemical and Microbiological Properties. PageA., MillerR.H., KeeneyD.R.American Society of Agronomy: Madison, WI, 595–624.
7.
BrakerG., ZhouJ., WuL., DevolA.H., TiedjeJ.M.2000. Nitrite reductase genes (nirK and nirS) as functional markers to investigate diversity of denitrifying bacteria in Pacific Northwest marine sediment communities. Appl Environ Microbiol, 66:2096–2104.
8.
BrookesP., LandmanA., PrudenG., JenkinsonD.1985. Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem, 17:837–842.
9.
ButlerC., RichardsonD. 2005. The emerging molecular structure of the nitrogen cycle: an introduction to the proceedings of the 10th annual N-cycle meeting. Biochem Soc Trans, 33:113–118.
10.
CaryS.C., McDonaldI.R., BarrettJ.E., CowanD.A.2010. On the rocks: the microbiology of Antarctic Dry Valley soils. Nat Rev Microbiol, 8:129–138.
11.
CerritosR., EguiarteL.E., AvitiaM., SiefertJ., TravisanoM., Rodríguez-VerdugoA., SouzaV.2011. Diversity of culturable thermo-resistant aquatic bacteria along an environmental gradient in Cuatro Ciénegas, Coahuila, México. Antonie van Leeuwenhoek, 99:303–318.
12.
ChowdhuryS.P., SchmidM., HartmannA., TripathiA.K.2009. Diversity of 16S-rRNA and nifH genes derived from rhizosphere soil and roots of an endemic drought tolerant grass, Lasiurus sindicus. European Journal of Soil Biology, 45:114–122.
CooksonW.R., MüllerC., O'BrienP.A., MurphyD.V., GriersonP.F.2006. Nitrogen dynamics in an Australian semiarid grassland soil. Ecology, 87:2047–2057.
15.
DeSantisT.Z., HugenholtzP., LarsenN., RojasM., BrodieE.L., KellerK., HuberT., DaleviD., HuP., AndersenG.L.2006. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol, 72:5069–5072.
16.
DesnuesC., Rodriguez-BritoB., RayhawkS., KelleyS., TranT., HaynesM., LiuH., FurlanM., WegleyL., ChauB., RuanY., HallD., AnglyF.E., EdwardsR.A., LiL., ThurberR.V., ReidR.P., SiefertJ., SouzaV., ValentineD.L., SwanB.K., BreitbartM., RohwerF.2008. Biodiversity and biogeography of phages in modern stromatolites and thrombolites. Nature, 452:340–343.
17.
DevolA.H.1991. Direct measurement of nitrogen gas fluxes from continental shelf sediments. Nature, 349:319–321.
18.
DongH., RechJ.A., JiangH., SunH., BuckB.J.2007. Endolithic cyanobacteria in soil gypsum: occurrences in Atacama (Chile), Mojave (United States), and Al-Jafr Basin (Jordan) Deserts. J Geophys Res, 112:1–11.
19.
DreesK.P., NeilsonJ.W., BetancourtJ.L., QuadeJ., HendersonD.A., PryorB.M., MaierR.M.2006. Bacterial community structure in the hyperarid core of the Atacama Desert, Chile. Appl Environ Microbiol, 72:7902–7908.
20.
EdwardsH.G.M., Jorge-VillarS.E., ParnellJ., CockellC.S., LeeP.2005. Spectroscopic analysis of cyanobacterial gypsum halotrophs and relevance for sulfate deposits on Mars. Analyst, 130:917–923.
21.
ElserJ.J., SchampelJ.H., Garcia-PichelF., WadeB.D., SouzaV., EguiarteL., EscalanteA., FarmerJ.D.2005. Effects of phosphorus enrichment and grazing snails on modern stromatolitic microbial communities. Freshw Biol, 50:1808–1825.
22.
EscalanteA.E., EguiarteL.E., Espinosa-AsuarL., ForneyL.J., NoguezA.M., Souza-SaldivarV.2008. Diversity of aquatic prokaryotic communities in the Cuatro Cienegas Basin. FEMS Microbiol Ecol, 65:50–60.
23.
FiererN., BradfordM.A., JacksonR.B.2007. Toward an ecological classification of soil bacteria. Ecology, 88:1354–1364.
GundlapallyS.R., Garcia-PichelF.2006. The community and phylogenetic diversity of biological soil crusts in the Colorado Plateau studied by molecular fingerprinting and intensive cultivation. Microb Ecol, 52:345–357.
26.
HallT.A.1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser, 41:95–98.
27.
HallinS., LindgrenP.E.1999. PCR detection of genes encoding nitrite reductase in denitrifying bacteria. Appl Environ Microbiol, 65:1652–1657.
28.
HanadaS., PiersonB.2006. The family Chloroflexaceae. The Prokaryotes: An Evolving Electronic Resource for the Microbiological Community, 3rd. DworkinM., FalkowS., RosenbergE., SchleiferK.H.StackebrandtE.Springer: New York, 815–842.
29.
HeffernanJ.B., SponsellerR.A., FisherS.G.2008. Consequences of a biogeomorphic regime shift for the hyporheic zone of a Sonoran Desert stream. Freshw Biol, 53:1954–1968.
30.
HiraishiA.ImhoffJ.F.2005. Genus Porphyrobacter. Bergey's Manual of Systematic Bacteriology, the Alpha-, Beta-, Delta- and Epsilonproteobacteria. BrennerD.J., KriegN.R., StaleyJ.T.Springer Science and Business Media Inc.: New York, 275–279.
31.
HolbenW.E., JanssonJ.K., ChelmB.K., TiedjeJ.M.1988. DNA probe method for the detection of specific microorganisms in the soil bacterial community. Appl Environ Microbiol, 54:703–711.
32.
HuffmanE.W.D.1977. Performance of a new automatic carbon dioxide coulometer. Microchem J, 22:567–573.
33.
IzawaM.R.M., BanerjeeN.R., OsinskiG.R., FlemmingR.L., ParnellJ., CockellC.S.2011. Weathering of post-impact hydrothermal deposits from the Haughton impact structure: implications for microbial colonization and biosignature preservation. Astrobiology, 11:537–550.
34.
JanssenP.H.2006. Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol, 72:1719–1728.
35.
JoergensenR.G.1996. The fumigation-extraction method to estimate soil microbial biomass: calibration of the kEC value. Soil Biol Biochem, 28:25–31.
36.
JoergensenR.G., MuellerT.1996. The fumigation-extraction method to estimate soil microbial biomass: calibration of the kEN value. Soil Biol Biochem, 28:33–37.
37.
JonesC.M., HallinS.2010. Ecological and evolutionary factors underlying global and local assembly of denitrifier communities. ISME J, 4:633–641.
38.
KindtR., CoeR.2005. Tree Diversity Analysis. A Manual and Software for Some Common Statistical Methods for Ecological and Biodiversity Studies. World Agroforestry Centre (ICRAF): Nairobi.
39.
LarkinM.A., BlackshieldsG., BrownN.P., ChennaR., McGettiganP.A., McWilliamH., ValentinF., WallaceI.M., WilmA., LopezR., ThompsonJ.D., GibsonT.J., HigginsD.G.2007. Clustal W and CLustal X version 2.0. Bioinformatics, 23:2947–2948.
40.
LetunicI., BorkP.2007. Interactive Tree Of Life (iTOL): an on line tool for phylogenetic tree display and annotation. Bioinformatics, 23:127–128.
41.
MartiK., KerridgeJ.2010. Nitrogen in the Solar System. Science, 328:1112–1113.
42.
Moreno-LetelierA., OlmedoG., EguiarteL.E., SouzaV.2012. Divergence and phylogeny of Firmicutes from the Cuatro Ciénegas Basin, Mexico: a window to an ancient ocean. Astrobiology, 12. 10.1089/ast.2011.0685.
43.
MontañoN.M., García-OlivaF., JaramilloV.J.2007. Dissolved organic carbon affects soil microbial activity and nitrogen dynamics in a Mexican tropical deciduous forest. Plant Soil, 295:265–277.
44.
MurphyJ., RileyJ.P.1962. A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta, 27:31–36.
45.
NagyM.L., PérezA., Garcia-PichelF.2005. The prokaryotic diversity of biological soil crusts in the Sonoran Desert (Organ Pipe Cactus National Monument, AZ)FEMS Microbiol Ecol, 54:233–245.
46.
NewsomH.E., HagertyJ.J., ThorsosI.E.2001. Location and sampling of aqueous and hydrothermal deposits in martian impact craters. Astrobiology, 1:71–88.
47.
OksanenJ., BlanchetF.G., KindtR., LegendreP., O'HaraR.B., SimpsonG.L., SolymosP., StevensM.H.H., WagnerH.2010. Vegan—Community Ecology Package. R package version 1.17-0. http://CRAN.R-project.org/package=vegan.
48.
PeimbertM., AlcarazL.D., Bonilla-RossoG., Olmedo-AlvarezG., García-OlivaF., SegoviaL., EguiarteL.E., SouzaV.2012. Comparative metagenomics of two microbial mats at Cuatro Ciénegas Basin I: ancient lessons on how to cope with an environment under severe nutrient stress. Astrobiology, 12:648–658.
49.
PointingS.B., ChanY., LacapD.C., LauM.C., JurgensJ., FarrellR.L.2009. Highly specialized microbial diversity in hyper-arid polar desert. Proc Natl Acad Sci USA, 106:19964–19969.
50.
PosadaD., CrandallK.A.1998. MODELTEST: testing the model of DNA substitution. Bioinformatics, 14:817–818.
51.
R Development Core Team. 2011. R: a language and environment for statistical computing. R Foundation for Statistical Computing: Vienna, Austriahttp://www.R-project.org.
52.
RíosA., ValeaS., AscasoC., KastovskyJ., McKayC.P., WierzchosJ.2010. Comparative analysis of the microbial communities inhabiting halite evaporites of the Atacama Desert. Int Microbiol, 13:79–89.
53.
SchlesingerW.H., RaikesJ.A., HartleyA.E., CrossA.F.1996. On the spatial pattern of soil nutrients in desert ecosystems. Ecology, 77:364–374.
54.
SchlossP.D., HandelsmanJ.2005. Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol, 71:1501–1506.
55.
SchlossP.D., WestcottS.L., RyabinT., HallJ.R., HartmannM., HollisterE.B., LesniewskiR.A., OakleyB.B., ParksD.H., RobinsonC.J., SahlJ.W., StresB., ThallingerG.G., Van HornD.J., WeberC.F.2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol, 75:7537–7541.
56.
SingletonD.R., FurlongM.A., RathbunS.L., WhitmanW.B.2001. Quantitative comparisons of 16S rRNA gene sequence libraries from environmental samples. Appl Environ Microbiol, 67:4374–4376.
57.
SouzaV., Espinosa-AsuarL., EscalanteA.E., EguiarteL.E., FarmerJ., ForneyL., LloretL., Rodríguez-MartínezJ.M., SoberónX., DirzoR., ElserJ.J.2006. An endangered oasis of aquatic microbial biodiversity in the Chihuahuan Desert. Proc Natl Acad Sci USA, 103:6565–6570.
58.
SouzaV., SiefertJ., EscalanteA.E., ElserJ., EguiarteL.E.2012. The Cuatro Ciénegas Basin in Coahuila, Mexico: an astrobiological Precambrian Park. Astrobiology, 12:641–647.
59.
SponsellerR.A., FisherS.G.2008. The influence of drainage networks on patterns of soil respiration in a desert catchment. Ecology, 89:1089–1090.
60.
SwoffordD.L.2003. PAUP*Phylogenetic Analysis Using Parsimony (*and other methods) ver. 4. Sinauer Associates: Sunderland, MA.
61.
SzynkiewiczA., EwingR.C., MooreC.H., GlamoclijaM., BustosD., PrattL.M.2010. Origin of terrestrial gypsum dunes—implications for martian gypsum-rich dunes of Olympia Undae. Geomorphology, 121:69–83.
62.
ThrobäckI.N., EnwallK., JarvisA., HallinS.2004. Reassessing PCR primers targeting nirS, nirK and nosZ genes for community surveys of denitrifying bacteria with DGGE. FEMS Microbiol Ecol, 49:401–417.
63.
VanceE., BrookesP., JenkinsonD.1987. An extraction method for measuring soil microbial biomass C. Soil Biol Biochem, 19:703–707.
64.
VitousekP.M.2002. Nutrient Cycling and Limitation. Hawai'i as a Model System. Princeton University Press: Princeton, NJ.
65.
WalvoordM.A., PhillipsF.M., StonestromD.A., EvansR.D., HartsoughP.C, NewmanB.D., StrieglR.G.2003. A reservoir of nitrate beneath desert soils. Science, 302:1021–1024.
66.
WilmotteA., Van der AuweraG., De WachterR.1993. Structure of the 16 S ribosomal RNA of the thermophilic cyanobacterium chlorogloeopsis HTF (‘Mastigocladus laminosus HTF’) strain PCC7518, and phylogenetic analysis. FEBS Lett, 317:96–100.
67.
YeagerC.M., KornoskyJ.L., HousmanD.C., GroteE.E., BelnapJ., KuskeC.R.2004. Diazotrophic community structure and function in two successional stages of biological soil crusts from the Colorado Plateau and Chihuahuan Desert. Appl Environ Microbiol, 70:973–983.
68.
YoussefN.H., ElshahedM.S.2009. Diversity rankings among bacterial lineages in soil. ISME J, 3:305–313.
69.
ZaniS., MellonM.T., CollierJ.L., ZehrJ.P.2000. Expression of nifH genes in natural microbial assemblages in Lake George, New York, detected by reverse transcriptase PCR. Appl Environ Microbiol, 66:3119–3124.
70.
ZehrJ.P., KudelaR.M.2011. Nitrogen cycle of the open ocean: from genes to ecosystems. Ann Rev Mar Sci, 3:197–225.
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