Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-23T13:22:30.521Z Has data issue: false hasContentIssue false
  • English
  • Français

A wide variety of putative extremophiles and large beta-diversity at the Mars Desert Research Station (Utah)

Published online by Cambridge University Press:  04 February 2011

Susana O.L. Direito ,
Pascale Ehrenfreund ,
Andries Marees ,
Martijn Staats ,
Bernard Foing  and
Wilfred F.M. Röling
Susana O.L. Direito
Affiliation:
Molecular Cell Physiology, Faculty of Earth and Life Sciences, VU University Amsterdam, De Boelelaan 1085, 1081 HV Amsterdam, The Netherlands
Pascale Ehrenfreund
Affiliation:
Leiden Institute of Chemistry, P O Box 9502, 2300 RA Leiden, The Netherlands Space Policy Institute, Elliott School of International Affairs, Washington, DC 20052, USA
Andries Marees
Affiliation:
Molecular Cell Physiology, Faculty of Earth and Life Sciences, VU University Amsterdam, De Boelelaan 1085, 1081 HV Amsterdam, The Netherlands
Martijn Staats
Affiliation:
Molecular Cell Physiology, Faculty of Earth and Life Sciences, VU University Amsterdam, De Boelelaan 1085, 1081 HV Amsterdam, The Netherlands
Bernard Foing
Affiliation:
European Space Agency, ESA ESTEC/SRE-S Postbus 299, 2200 AG Noordwijk, The Netherlands Petrology, Faculty of Earth and Life Sciences, VU University Amsterdam, De Boelelaan 1085, 1081 HV Amsterdam, The Netherlands
Wilfred F.M. Röling*
Affiliation:
Molecular Cell Physiology, Faculty of Earth and Life Sciences, VU University Amsterdam, De Boelelaan 1085, 1081 HV Amsterdam, The Netherlands
*
e-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Humankind's innate curiosity makes us wonder whether life is or was present on other planetary bodies such as Mars. The EuroGeoMars 2009 campaign was organized at the Mars Desert Research Station (MDRS) to perform multidisciplinary astrobiology research. MDRS in southeast Utah is situated in a cold arid desert with mineralogy and erosion processes comparable to those on Mars. Insight into the microbial community composition of this terrestrial Mars analogue provides essential information for the search for life on Mars: including sampling and life detection methodology optimization and what kind of organisms to expect. Soil samples were collected from different locations. Culture-independent molecular analyses directed at ribosomal RNA genes revealed the presence of all three domains of life (Archaea, Bacteria and Eukarya), but these were not detected in all samples. Spiking experiments revealed that this appears to relate to low DNA recovery, due to adsorption or degradation. Bacteria were most frequently detected and showed high alpha- and beta-diversity. Members of the Actinobacteria, Proteobacteria, Bacteroidetes and Gemmatimonadetes phyla were found in the majority of samples. Archaea alpha- and beta-diversity was very low. For Eukarya, a diverse range of organisms was identified, such as fungi, green algae and several phyla of Protozoa. Phylogenetic analysis revealed an extraordinary variety of putative extremophiles, mainly Bacteria but also Archaea and Eukarya. These comprised radioresistant, endolithic, chasmolithic, xerophilic, hypolithic, thermophilic, thermoacidophilic, psychrophilic, halophilic, haloalkaliphilic and alkaliphilic micro-organisms. Overall, our data revealed large difference in occurrence and diversity over short distances, indicating the need for high-sampling frequency at similar sites. DNA extraction methods need to be optimized to improve extraction efficiencies.

Keywords

Mars analogueextremophilesbeta-diversitydesertDNA recovery
Type
Research Article
Information
International Journal of Astrobiology , Volume 10 , Special Issue 3: Special issue: Astrobiology field research in Moon/Mars analogue environments , July 2011 , pp. 191 - 207
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aller, J.Y. & Kemp, P.F. (2008). Are Archaea inherently less diverse than Bacteria in the same environments? FEMS Microbiol. Ecol. 65(1), 74–87.Google Scholar
Altschul, S.F., Gish, W., Miller, W., Myers, E.W. & Lipman, D.J. (1990). Basic local alignment search tool. J. Mol. Biol. 215(3), 403–410.Google Scholar
Amaral Zettler, L.A., Gomez, F., Zettler, E., Keenan, B.G., Amils, R. & Sogin, M.L. (2002). Microbiology: eukaryotic diversity in Spain's river of fire. Nature 417(6885), 137–137.CrossRefGoogle ScholarPubMed
Bamforth, S.S. (2008). Protozoa of biological soil crusts of a cool desert in Utah. J. Arid Environ. 72(5), 722–729.Google Scholar
Barns, S.M., Fundyga, R.E., Jeffries, M.W. & Pace, N.R. (1994). Remarkable Archaeal diversity detected in a Yellowstone-National-Park hot-spring environment. Proc. Natl. Acad. Sci. USA 91(5), 1609–1613.Google Scholar
Borst, A., Peters, S., Foing, B.H., Stoker, C., Wendt, L., Gross, C., Zavaleta, J., Sarrazin, P., Blake, D., Ehrenfreund, P. et al. (2010). Geochemical results from EuroGeoMars MDRS Utah 2009 campaign. In 41th Annual Lunar and Planetary Science Conference, Abstract No. 2744.Google Scholar
Bottos, E.M., Vincent, W.F., Greer, C.W. & Whyte, L.G. (2008). Prokaryotic diversity of arctic ice shelf microbial mats. Environ. Microbiol. 10(4), 950–966.Google Scholar
Boyd, E.S., Cummings, D.E. & Geesey, G.G. (2007). Mineralogy influences structure and diversity of bacterial communities associated with geological substrata in a pristine aquifer. Microb. Ecol. 54(1), 170–182.Google Scholar
Brambilla, E., Hippe, H., Hagelstein, A., Tindall, B.J. & Stackebrandt, E. (2001). 16S rDNA diversity of cultured and uncultured prokaryotes of a mat sample from Lake Fryxell, McMurdo Dry Valleys, Antarctica. Extremophiles 5(1), 23–33.CrossRefGoogle ScholarPubMed
Büdel, B. (1999). Ecology and diversity of rock-inhabiting cyanobacteria in tropical regions. Eur. J. Phycol. 34(4), 361–370.Google Scholar
Büdel, B. & Veste, M. (2008). Biological crusts. In Arid Dune Ecosystems, the Nizzana Sands in the Negev Desert, ed. Breckle, S.-W., Yair, A. & Veste, M., volume 200, pp. 149–155, Springer, Berlin Heidelberg.Google Scholar
Büdel, B. & Wessels, D.C.J. (1991). Rock inhabiting blue-green-algae cyanobacteria from hot arid regions. Arch. Hydrobiol. 64, 385–398.Google Scholar
Carson, J.K., Campbell, L., Rooney, D., Clipson, N. & Gleeson, D.B. (2009). Minerals in soil select distinct bacterial communities in their microhabitats. FEMS Microbiol. Ecol. 67(3), 381–388.Google Scholar
Cary, S.C., McDonald, I.R., Barrett, J.E. & Cowan, D.A. (2010). On the rocks: the microbiology of Antarctic Dry Valley soils. Nat. Rev. Microbiol. 8(2), 129–138.Google Scholar
Catling, D.C. & Moore, J.M. (2003). The nature of coarse-grained crystalline hematite and its implications for the early environment of Mars. Icarus 165(2), 277–300.Google Scholar
Chan, M.A., Beitler, B., Parry, W.T., Ormö, J. & Komatsu, G. (2004). A possible terrestrial analogue for haematite concretions on Mars. Nature 429(6993), 731–734.Google Scholar
Chanal, A., Chapon, V., Benzerara, K., Barakat, M., Christen, R., Achouak, W., Barras, F. & Heulin, T. (2006). The desert of Tataouine: an extreme environment that hosts a wide diversity of microorganisms and radiotolerant bacteria. Environ. Microbiol. 8(3), 514–525.Google Scholar
Chevrier, V. & Mathé, P.E. (2007). Mineralogy and evolution of the surface of Mars: a review. Planet. Space Sci. 55(3), 289–314.Google Scholar
Chronic, H. (1990). In Roadside Geology of Utah. Mountain Press, Missoula, Montana, USA.Google Scholar
Cockell, C.S., Schuerger, A.C., Billi, D., Friedmann, E.I. & Panitz, C. (2005). Effects of a simulated martian UV flux on the cyanobacterium, Chroococcidiopsis sp. 029. Astrobiology, 5(2), 127–140.Google Scholar
Connon, S.A., Lester, E.D., Shafaat, H.S., Obenhuber, D.C. & Ponce, A. (2007). Bacterial diversity in hyperarid Atacama Desert soils. J. Geophys. Res.–Biogeosci. 112(G04S17), doi:10.1029/2006JG000311.Google Scholar
de la Vega, U.P., Rettberg, P. & Reitz, G. (2007). Simulation of the environmental climate conditions on Martian surface and its effect on Deinococcus radiodurans. Adv. Space Res. 40(11), 1672–1677.CrossRefGoogle Scholar
Díez, B., Pedrós-Alió, C., Marsh, T.L. & Massana, R. (2001). Application of denaturing gradient gel electrophoresis (DGGE) to study the diversity of marine picoeukaryotic assemblages and comparison of DGGE with other molecular techniques. Appl. Environ. Microbiol. 67(7), 2942–2951.Google Scholar
Drees, K.P., Neilson, J.W., Betancourt, J.L., Quade, J., Henderson, D.A., Pryor, B.M. & Maier, R.M. (2006). Bacterial community structure in the hyperarid core of the Atacama Desert, Chile. Appl. Environ. Microbiol. 72(12), 7902–7908.Google Scholar
Ehrenfreund, P., Röling, W.F.M., Thiel, C., Quinn, R., Septhon, M., Stoker, C., Kotler, M., Direito, S.O.L., Martins, Z., Orzechowska, G.E., Kidd, R. & Foing, B.H. (2011). Astrobiology and habitability studies in preparation for future Mars missions: trends from investigating minerals, organics and biota. Int. J. Astrobiol, in press.Google Scholar
Ehrenfreund, P., Foing, B.H., Stoker, C., Zavaleta, J., Quinn, R., Blake, D., Martins, Z., Sephton, M., Becker, L., Orzechowska, G. et al. (2010). EuroGeoMars field campaign: sample analysis of organic matter and minerals. In 41th Annual Lunar and Planetary Science Conference, Abstract No. 1723.Google Scholar
Felske, A., Rheims, H., Wolterink, A., Stackebrandt, E. & Akkermans, A.D.L. (1997). Ribosome analysis reveals prominent activity of an uncultured member of the class Actinobacteria in grassland soils. Microbiology 143, 2983–2989.CrossRefGoogle ScholarPubMed
Fierer, N. & Jackson, R.B. (2006). The diversity and biogeography of soil bacterial communities. Proc. Natl. Acad. Sci. USA 103(3), 626–631.Google Scholar
Foing, B.H., Batenburg, P., Drijkoningen, G., Slob, E., Poulakis, P., Visentin, G., Page, J., Noroozi, A., Gill, E., Guglielmi, M. et al. (2009). Exogeolab lander/rover instruments and EuroGeoMars MDRS campaign. In 40th Annual Lunar and Planetary Science Conference, Abstract No. 2567.Google Scholar
Friedmann, E.I. & Ocampo-Friedmann, R. (1985). Blue-green algae in arid cryptoendolithic habitats. Algol. Stud./Arch. Hydrobiol. Suppl. 38–39, 349–350.Google Scholar
Garcia-Pichel, F. & Belnap, J. (1996). Microenvironments and microscale productivity of cyanobacterial desert crusts. J. Phycol. 32(5), 774–782.Google Scholar
Godfrey, A.E. (1997). Wind erosion of Mancos Shale badland ridges by sudden drops in pressure. Earth Surf. Process. Landforms 22(4), 345–352.3.0.CO;2-3>CrossRefGoogle Scholar
Godfrey, A.E., Everitt, B.L. & Duque, J.F.M. (2008). Episodic sediment delivery and landscape connectivity in the Mancos Shale badlands and Fremont River system, Utah, USA. Geomorphology 102(2), 242–251.Google Scholar
Gómez-Silva, B., Rainey, F.A., Warren-Rhodes, K.A., McKay, C.P. & Navarro-González, R. (2008). Atacama Desert soil microbiology. In Microbiology of Extreme Soils, ed. Dion, P., Nautiyal, C.S. & Varma, A., volume 13, pp. 117–132. Springer, Berlin, Heidelberg.CrossRefGoogle Scholar
Gommeaux, M., Barakat, M., Montagnac, G., Christen, R., Guyot, F. & Heulin, T. (2010). Mineral and bacterial diversities of desert sand grains from south-east Morocco. Geomicrobiol. J. 27(1), 76–92.Google Scholar
Grady, M.M. (2007). Astrobiology of the terrestrial planets, with emphasis on Mars. In Complete Course in Astrobiology, ed. Horneck, G. & Rettberg, P., pp. 203–222. Wiley-VCH, Verlag GmbH & Co. KGaA, Weinheim.Google Scholar
Greeley, R., Thompson, S.D., Whelley, P.L., Squyres, S., Neukum, G., Arvidson, R., Malin, M., Kuzmin, R., Christensen, P., Rafkin, S. et al. (2004). Coordinated observations of aeolian features from the Mars Exploration Rovers (MER) and the Mars Express High Resolution Stereo Camera and other orbiters. In 35th Annual Lunar and Planetary Science Conference, Abstract No. 2162.Google Scholar
Hecht, M.H., Kounaves, S.P., Quinn, R.C., West, S.J., Young, S.M.M., Ming, D.W., Catling, D.C., Clark, B.C., Boynton, W.V., Hoffman, J. et al. (2009). Detection of perchlorate and the soluble chemistry of Martian soil at the Phoenix lander site. Science 325(5936), 64–67.Google Scholar
Hughes, J. & Smith, H.G. (1989). Temperature relations of Heteromita globosa Stein in Signy Island fellfields. In University Research in Antarctica, Proceedings of British Antarctic Survey Antarctic Special Topic Award Scheme Symposium, 9–10 November 1988, ed. Heywood, R.B., pp. 117–122. British Antarctic Survey, Natural Environment Research Council, Cambridge.Google Scholar
Itoh, T., Yamanoi, K., Kudo, T., Ohkuma, M. & Takashina, T. (2010). Aciditerrimonas ferrireducens gen. nov., sp. nov., a novel iron-reducing thermoacidophilic actinobacterium isolated from a solfataric field in Japan. Int. J. Syst. Evol. Microbiol., doi:10.1099/ijs.0.023044-0.Google Scholar
Jukes, T.H. & Cantor, C.R. (1969). Evolution of protein molecules. In Mammalian Protein Metabolism, ed. Munro, H.N., volume 3, pp. 21–132. Academic Press, New York, NY.Google Scholar
Keller, W.D. (1958). Clay minerals in the Morrison formation on the Colorado Plateau. Clays Clay Miner. 7, 293–294.Google Scholar
Kotler, M., Quinn, R., Martins, Z., Foing, B. & Ehrenfreund, P. (2011). Analysis of mineral matrices of planetary soils analogs from the Utah desert. Int. J. Astrobiol., in press.CrossRefGoogle Scholar
Lester, E.D., Satomi, M. & Ponce, A. (2007). Microflora of extreme arid Atacama Desert soils. Soil Biol. Biochem. 39, 704–708.Google Scholar
Lewis, L.A. & Lewis, P.O. (2005). Unearthing the molecular phylodiversity of desert soil green algae (Chlorophyta). Syst. Biol. 54(6), 936–947.Google Scholar
Malin, M.C. & Edgett, K.S. (2000). Evidence for recent groundwater seepage and surface runoff on Mars. Science 288(5475), 2330–2335.Google Scholar
Martins, Z., Sephton, M.A., Foing, B.H. & Ehrenfreund, P. (2011). Extraction of amino acids from soils close to the Mars Desert Research Station (MDRS), Utah. Int. J. Astrobiol., in press.Google Scholar
Muyzer, G., Dewaal, E.C. & Uitterlinden, A.G. (1993). Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 59(3), 695–700.Google Scholar
Nagy, M.L., Pérez, A. & Garcia-Pichel, F. (2005). The prokaryotic diversity of biological soil crusts in the Sonoran Desert (Organ Pipe Cactus National Monument, AZ). FEMS Microbiol. Ecol. 54(2), 233–245.CrossRefGoogle ScholarPubMed
Navarro-González, R., Vargas, E., de la Rosa, J., Raga, A.C. & McKay, C.P. (2010). Reanalysis of the Viking results suggests perchlorate and organics at mid-latitudes on Mars. J. Geophys. Res.–Planets 115(E12010), 11. doi:10.1029/2010JE003599.CrossRefGoogle Scholar
Ormö, J., Komatsu, G., Chan, M.A., Beitler, B. & Parry, W.T. (2004). Geological features indicative of processes related to the hematite formation in Meridiani Planum and Aram Chaos, Mars: a comparison with diagenetic hematite deposits in southern Utah, USA. Icarus 171(2), 295–316.Google Scholar
Orzechowska, G.E., Kidd, R.D., Foing, B.H., Kanik, I., Stoker, C. & Ehrenfreund, P. (2011). Analysis of mars analog soil samples using solid phase microextraction, organic solvent extraction and gas-chromatography/mass spectrometry. Int. J. Astrobiol., in press.Google Scholar
Øvreås, L., Forney, L., Daae, F.L. & Torsvik, V. (1997). Distribution of bacterioplankton in meromictic Lake Sælenvannet, as determined by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA. Appl. Environ. Microbiol. 63(9), 3367–3373.Google Scholar
Pointing, S.B., Chan, Y., Lacap, D.C., Lau, M.C.Y., Jurgens, J.A. & Farrell, R.L. (2009). Highly specialized microbial diversity in hyper-arid polar desert. Proc. Natl. Acad. Sci. USA 106(47), 19964–19969.Google Scholar
Postmus, J., Canelas, A.B., Bouwman, J., Bakker, B.M., van Gulik, W., de Mattos, M.J.T., Brul, S. & Smits, G.J. (2008). Quantitative analysis of the high temperature-induced glycolytic flux increase in Saccharomyces cerevisiae reveals dominant metabolic regulation. J. Biol. Chem. 283(35), 23524–23532.Google Scholar
Poulet, F., Bibring, J.P., Mustard, J.F., Gendrin, A., Mangold, N., Langevin, Y., Arvidson, R.E., Gondet, B. & Gomez, C. (2005). Phyllosilicates on Mars and implications for early Martian climate. Nature 438(7068), 623–627.CrossRefGoogle ScholarPubMed
Prestel, E., Salamitou, S. & Dubow, M.S. (2008). An examination of the bacteriophages and bacteria of the Namib Desert. J. Microbiol. 46(4), 364–372.Google Scholar
Saeki, K. & Sakai, M. (2009). The influence of soil organic matter on DNA adsorptions on andosols. Microbes Environ. 24(2), 175–179.CrossRefGoogle ScholarPubMed
Saitou, N. & Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4(4), 406–425.Google Scholar
Stan-Lotter, H. (2007). Extremophiles, the physicochemical limits of life (growth and survival). In Complete Course in Astrobiology, ed. Horneck, G. & Rettberg, P., pp. 121–150. Wiley VCH, Verlag GmbH & Co. KGaA, Weinheim.CrossRefGoogle Scholar
Tamura, K., Dudley, J., Nei, M. & Kumar, S. (2007). MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24(8), 1596–1599.Google Scholar
Thiel, C.S., Ehrenfreund, P., Foing, B., Pletser, V. & Ullrich, O. (2011). PCR-based analysis of microbial communities during the EuroGeoMars campaign at Mars Desert Research Station, Utah. Int. J. Astrobiol., in press.Google Scholar
Torsvik, V. & Øvreås, L. (2008). Microbial diversity, life strategies, and adaptation to life in extreme soils. In Microbiology of Extreme Soils, ed. Dion, P., Nautiyal, C.S. & Varma, A., volume 13, pp. 15–43. Springer, Berlin, Heidelberg.Google Scholar
Vetriani, C., Jannasch, H.W., MacGregor, B.J., Stahl, D.A. & Reysenbach, A.L. (1999). Population structure and phylogenetic characterization of marine benthic archaea in deep-sea sediments. Appl. Environ. Microbiol. 65(10), 4375–4384.Google Scholar
Vítek, P., Edwards, H.G.M., Jehlička, J., Ascaso, C., De Los Ríos, A., Valea, S., Jorge-Villar, S.E., Davila, A.F. & Wierzchos, J. (2010). Microbial colonization of halite from the hyper-arid Atacama Desert studied by Raman spectroscopy. Philos. Trans. R. Soc. A: Math. Phys. Eng. Sci. 368(1922), 3205–3221.Google Scholar
Wessels, D.C.J. & Büdel, B. (1995). Epilithic and cryptoendolithic cyanobacteria of Clarens sandstone cliffs in the Golden Gate Highland. Botan. Acta 108(3), 220–226.Google Scholar
Wood, S.A., Rueckert, A., Cowan, D.A. & Cary, S.C. (2008). Sources of edaphic cyanobacterial diversity in the Dry Valleys of Eastern Antarctica. ISME J. 2(3), 308–320.Google Scholar
Worms, J.C., Lammer, H., Barucci, A., Beebe, R., Bibring, J.P., Blamont, J., Blanc, M., Bonnet, R., Brucato, J.R., Chassefiere, E. et al. (2009). ESSC-ESF position paper science-driven scenario for space Exploration: report from the Europe Space Sciences Committee (ESSC). Astrobiology 9(1), 23–41.Google Scholar
Yergeau, E., Newsham, K.K., Pearce, D.A. & Kowalchuk, G.A. (2007). Patterns of bacterial diversity across a range of Antarctic terrestrial habitats. Environ. Microbiol. 9, 2670–2682.Google Scholar