3
Advances in Microbial Ecology

Studies that can further reduce uncertainties in estimates of the potential for living entities to be included in martian samples also encompass those that seek to understand the ecological diversity and environmental extremes of terrestrial life. Understanding the range of environmental conditions to which terrestrial life has adapted has directly shaped current views of martian habitability and of the potential for samples returned from Mars to contain evidence of life. A substantial and growing body of evidence shows that life not only is present, but also frequently thrives under extreme environmental conditions.1 The known limits of life now extend from superheated deep ocean hydrothermal vents, to ice-brine environments of polar regions, from highly acidic waters of mine drainage systems, to ephemeral, hypersaline alkaline and acidic lakes, from sunlit surface environments, to perpetually dark subsurface aquifers located thousands of meters underground. Even more remarkably, biologists continue to discover new biological entities, such as the giant Acanthamoeba polyphaga mimivirus;2 virophages that prey on other viruses;3 and novel single-species ecosystems, such as the deep subsurface bedrock fractures inhabited solely by the chemoautotrophic Candidatus Desulforudis audaxviator.4

EXAMPLES OF LIFE IN EXTREME ENVIRONMENTS ON EARTH

The broad range of environmental extremes capable of sustaining terrestrial life is surpassed only by the physiological, metabolic, and phylogenetic diversity of their extremophile inhabitants (Table 3.1). These unique life forms include not only eukaryotes, bacteria, and archaea, but also viruses.5,6,7 Moreover, the discovery of independent viral growth outside a host cell, under acidic hyperthermophilic conditions, indicates that viruses are more complex biologically than the scientific community has previously assumed.8 Although geological extremophiles have not yet been shown to pose significant biological risks to humans given their inability to cause disease or environmental contamination, discoveries of new organisms and ecological interactions, such as those discussed above, do influence perceptions of the potential for martian life.

In many extreme ecosystems, chemoautotrophs are the sole primary producers of organic matter;9 this is especially so in perpetually dark environments of the deep seafloor or subsurface crust, where life fundamentally depends on inorganic forms of energy and carbon sources (e.g., hydrogen and carbon dioxide).10 By some estimates the subsurface biosphere accounts for as much as 85 percent of the microbial biomass, and up to 30 percent of the total living biomass, on Earth.11 These observations suggest that, given the hostile conditions at the martian surface, the potential for martian life is likely to be much greater in subsurface environments than at the surface of the planet.



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3 Advances in Microbial Ecology Studies that can further reduce uncertainties in estimates of the potential for living entities to be included in martian samples also encompass those that seek to understand the ecological diversity and environmental extremes of terrestrial life. Understanding the range of environmental conditions to which terrestrial life has adapted has directly shaped current views of martian habitability and of the potential for samples returned from Mars to contain evidence of life. A substantial and growing body of evidence shows that life not only is present, but also frequently thrives under extreme environmental conditions.1 The known limits of life now extend from superheated deep ocean hydrothermal vents, to ice-brine environments of polar regions, from highly acidic waters of mine drainage systems, to ephemeral, hypersaline alkaline and acidic lakes, from sunlit surface environments, to perpetually dark subsurface aquifers located thousands of meters underground. Even more remarkably, biologists continue to discover new biological entities, such as the giant Acanthamoeba polyphaga mimivirus;2 virophages that prey on other viruses;3 and novel single-species ecosystems, such as the deep subsurface bedrock fractures inhabited solely by the chemoautotrophic Candidatus Desulforudis audaxviator.4 EXAMPLES OF LIFE IN EXTREME ENVIRONMENTS ON EARTH The broad range of environmental extremes capable of sustaining terrestrial life is surpassed only by the physiological, metabolic, and phylogenetic diversity of their extremophile inhabitants (Table 3.1). These unique life forms include not only eukaryotes, bacteria, and archaea, but also viruses. 5,6,7 Moreover, the discovery of inde- pendent viral growth outside a host cell, under acidic hyperthermophilic conditions, indicates that viruses are more complex biologically than the scientific community has previously assumed. 8 Although geological extremophiles have not yet been shown to pose significant biological risks to humans given their inability to cause disease or environmental contamination, discoveries of new organisms and ecological interactions, such as those discussed above, do influence perceptions of the potential for martian life. In many extreme ecosystems, chemoautotrophs are the sole primary producers of organic matter; 9 this is especially so in perpetually dark environments of the deep seafloor or subsurface crust, where life fundamentally depends on inorganic forms of energy and carbon sources (e.g., hydrogen and carbon dioxide).10 By some estimates the subsurface biosphere accounts for as much as 85 percent of the microbial biomass, and up to 30 percent of the total living biomass, on Earth.11 These observations suggest that, given the hostile conditions at the martian surface, the potential for martian life is likely to be much greater in subsurface environments than at the surface of the planet. 

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 ADVANCES IN MICROBIAL ECOLOGY TABLE 3.1 Environmental Limits for the Growth of Extremophilic Organisms Parameter Classification Definition Example Archaeal strain 121;a 121ºC Temperature Hyperthermophile Growth >80ºC Methanopyrus kandlerib Thermophile Growth 60º to 80ºC Pyrolobus fumarii; ~116ºC Psychrophile Growth <15ºC Synechococcus lividis; ~73ºC Active at −18ºC Psychrobacter Himalayan midgec Ferroplasma acidarmanus;d pH 0 pH Acidophile Low pH (<5) Alkaliphilus transvaalensis,e pH 12.5 Alkaliphile High pH (>9) Natronobacterium; pH 10.5 Salinity Halophile 2 to 5 molar NaCl Halobacteriaceae Oxygen tension Aerobe Requires O2 Bacteria, archaea Neutral pH Fe2+-oxidizing bacteria Microaerophile Tolerates some O2 Methanogens, SO42− reducers Anaerobe Not tolerant of O2 Dessication Xerophile Anhydrobiotic Lichens, cyanobacteria; arid deserts Deinococcus radioduransf Radiation Radiophile Ionizing radiation to 15 kGy Piezophileg Obligate strain MT41;h 100 MPa Pressure Pressure-loving Chemical extremes Gases Cyanidium caldarium; pure CO2 Metals Metalotolerant Ferroplasma acidarmanus aK. Kashefi and D.R. Lovley, “Extending the Upper Temperature Limit for Life,” Science 301:934-934, 2003. bMethanopyrus kandleri, Growth at 122ºC at 20 MPa; survival for 3 hours at 130º C. S. Burggraf, K.O. Stetter, P. Rouviere, and C.R. Woese, “Methanopyrus kandleri—An Archaeal Methanogen Unrelated to All Other Known Methanogens,” Systematic and Applied Microbiol- ogy 14:346-351, 1991; K. Takai et al., “Cell Proliferation at 122 degrees C and Isotopically Heavy CH4 Production by a Hyperthermophilic Methanogen Under High-pressure Cultivation,” Proceedings of the National Academy of Sciences of the United States of America 105:10949- 10954, 2008. cS. Kohshima, “A Novel Cold-Tolerant Insect Found In A Himalayan Glacier,” Nature 310:225-227, 1984. dK.J. Edwards, P.L. Bond, T.M. Gihring, and J.F. Banfield, “An Archaeal Iron-oxidizing Extreme Acidophile Important in Acid Mine Drainage,” Science 287:1796-1799, 2000. eK. Takai et al., “Alkaliphilus transvaalensis Gen. Nov., Sp Nov., An Extremely Alkaliphilic Bacterium Isolated from a Deep South Afri- can Gold Mine,” International Journal of Systematic and Evolutionary Microbiology 51:1245-1256, 2001. fK.W. Minton, “Repair of Ionizing-radiation Damage in the Radiation Resistant Bacterium Deinococcus radiodurans,” Mutation Re- search-DNA Repair 363(1):1-7, 1996. gAlso designated “barophile.” hA.A. Yayanos, “Evolutional And Ecological Implications of the Properties of Deep-Sea Barophilic Bacteria,” Proceedings of the National Academy of Sciences of the United States of America 83(24):9542-9546, 1986. SOURCE: Adapted, by permission from Macmillan Publishers Ltd., from L.J. Rothschild and R.L. Mancinelli, “Life in Extreme Environ- ments,” Nature 409:1092-1101, 2001, Copyright 2001. Survival of Organisms in Geological Deposits Studies of the biology of extreme terrestrial environments have also revealed the potential for long-term sur- vival of viable organisms in ancient geological deposits. At high temperatures, the survival of biological materials is comparatively short, owing to the low thermostability of biomolecules (e.g., ribose and other sugars).12 Conversely, viable organisms have been retrieved from ancient salt crystals dated at 250 million years old,13,14 as well as from antarctic and siberian permafrost believed to be millions of years old.15,16,17 The combined effect of salts and ice is a dramatic reduction of water activity (aw), which is now considered to permit the maintenance of metabolism at aw = 0.3.18 This level is considerably lower than previous estimates of aw ~ 0.61 for the water activity limit of biological activity.19 Regardless, the precise impact of extreme low temperature and water activity stress (or other physicochemical environmental parameters for that matter) on the long-term survivability of viable organisms has still not been established with any degree of certainty.

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 ASSESSMENT OF PLANETARY PROTECTION REQUIREMENTS FOR MARS SAMPLE RETURN MISSIONS Resistance to Radiation Although ionizing radiation is detrimental to the survival of living organisms and is employed as a common method of sterilization, some microorganisms have evolved adaptations to survive under high radiation. Perhaps the most widely known adaptation to radiation is that exhibited by Deinococcus radiodurans, which achieves a high degree of resistance by combining multiple copies of its genome with highly efficient DNA repair mechanisms. 20 Less well appreciated is the fact that microorganisms living in a variety of mineralizing environments protect themselves against high doses of ultraviolet radiation with biomediated mineral coatings (e.g., silica, iron oxides, and so on; Figure 3.1).21 Similarly, endolithic microorganisms—i.e., those residing within the interior spaces of porous rocks and sediments—are afforded protection from radiation, desiccation, and extreme fluctuations of temperature by enclosing mineral matrices.22 FIGURE 3.1 Transmission electron micrographs of3.1_from word.epscoatings that can form around microorganisms the biomediated mineral in mineralizing environments. A—A microbial virus (bacteriophage) from the acidic (pH 2.3) Rio Tinto, Spain. Scale bar = bitmap image 0.10 μm. For related information, see J.E. Kyle, K. Pedersen, and F.G. Ferris, “Virus Mineralization at Low pH in the Rio Tinto, Spain,” Geomicrobiology Journal 25:338-345, 2008. B—Jarosite (ferric hydroxy-sulfate) mineral precipitates (arrow) on the surface of a bacterial cell from the Rio Tinto, Spain. Scale bar = 1.0 μm. For related information, see F.G. Ferris, L. Hallbeck, C.B. Kennedy, and K. Pedersen, “Geochemistry of Acidic Rio Tinto Headwaters and Role of Bacteria in Solid Phase Metal Partitioning,” Chemical Geology 212:291-300, 2004. C—Silica mineral precipitates (arrows) on the sheath of a cyanobacterial cell from a hot spring in the Atacama Desert, Chile. Scale bar = 5.0 μm. For related information, see V.R. Phoenix, P.C. Bennett, A. Summers Engel, S.W. Tyler, and F.G. Ferris, “Chilean High-altitude Hot Spring Sinters: A Model System for UV Screening Mechanisms by Early Precambrian Cyanobacteria,” Geobiology 4:15-28, 2006. SOURCE: Images courtesy of F. Grant Ferris, University of Toronto.

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 ADVANCES IN MICROBIAL ECOLOGY CONCLuSIONS Consideration of advances in microbial ecology over the past decade led the committee to reach the follow- ing conclusions: • Biological studies have continued to expand the known environmental limits for life and have led to the discovery of novel organisms and ecosystems. • Some living species on Earth have been shown to survive under conditions of extreme radiation, subfreezing temperatures, high salinity, extremely high and low pH, and cycles of hydration to dehydration present on Mars today. • The discovery in deep subsurface environments on Earth of microbial ecosystems that are able to survive on inorganic sources of energy has greatly enhanced the prospect of chemoautotrophic life in subsurface environ- ments on Mars. • Studies have confirmed the potential for the long-term viability of terrestrial microorganisms captured in deposits of some extreme terrestrial environments (e.g., ices and evaporates) that have high relevance for Mars exploration. • Uncertainties in the current assessment of martian habitability and the potential for the inclusion of living entities in samples returned from Mars may be reduced by continued studies of the metabolic diversity and envi- ronmental limits of microbial life. NOTES 1 . L.J. Rothschild and R.L. Mancinelli, “Life in Extreme Environments,” Nature 409:1092-1101, 2001. 2 . J.M. Claverie, H. Ogata, S. Audic, C. Abergel, K. Suhre, and P.E. Fournie, “Mimivirus and the Emerging Concept of “Giant” Virus,” Virus Research 117:133-144, 2006. 3 . B. La Scola, C. Desnues, I. Pagnier, C. Robert, L. Barrassi1, G. Fournous, M. Merchat, M. Suzan-Monti1, P. Forterre, E. Koonin, and D. Raoult, “The Virophage as a Unique Parasite of the Giant Mimivirus,” Nature 455:100-104, 2008. 4 . D. Chivian, E.L. Brodie, E.J. Alm, D.E. Culley, P.S. Dehal, T.Z. DeSantis, T.M. Gihring, A. Lapidus, L.-H. Lin, S.R. Lowry, D.P. Moser, P.M. Richardson, G. Southam, G. Wanger, L.M. Pratt, G.L. Andersen, T.C. Hazen, F.J. Brockman, A.P. Arkin, and T.C. Onstott, “Environmental Genomics Reveals a Single-Species Ecosystem Deep Within Earth,” Science 322:275- 278, 2008. 5 . L.J. Rothschild and R.L. Mancinelli, “Life in Extreme Environments,” Nature 409:1092-1101, 2001. 6 . D. Pranghishvili, P. Forterre, and R.A. Garret, “Viruses of the Archaea: A Unifying View,” Nature Reviews Microbiol- ogy 4:837-848, 2006. 7 . J.E. Kyle, K. Pedersen, and F.G. Ferris, “Virus Mineralization at Low pH in the Rio Tinto, Spain,” Geomicrobiology Journal 25:338-345, 2008. 8 . M. Häring, G. Vestergaard, R. Rachel, L. Chen, R.A. Garret, and D. Prangishvili, “Independent Virus Development Outside a Host,” Nature 436:1101-1102, 2005. 9 . Chemoautotrophs are organisms that synthesize all necessary organic molecules from simple carbon compounds (e.g., carbon dioxide) and obtain their energy from chemical reactions. 10 . J.K. Fredrickson and D.L. Balkwill, “Geomicrobial Processes and Biodiversity in the Deep Terrestrial Subsurface,” Geomicrobiology Journal 23:345-356, 2006. 11 . A.P. Teske, “The Deep Subsurface Biosphere is Alive and Well,” Trends in Microbiology 13:402-404, 2005. 12 . R. Larralde, M.P. Robertson, and S.L. Miller, “Rates of Decomposition of Ribose and Other Sugars: Implications for Chemical Evolution,” Proceedings of the National Academy of Sciences 92:8158-8160, 1995. 13 . R.H. Vreeland, W.D. Rosenzweig, and D.W. Powers, “Isolation of a 250 Million-year-old Halotolerant Bacterium from a Primary Salt Crystal,” Nature 407(6806):897-900, 2000. 14 . R.H. Vreeland, “Isolation of Live Cretaceous (121-112 million years old) Halophilic Archaea from Primary Salt Crystals,” Geomicrobiology Journal 24:545-545, 2007.

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 ASSESSMENT OF PLANETARY PROTECTION REQUIREMENTS FOR MARS SAMPLE RETURN MISSIONS 15 . D.A. Gilichinsky, G.S. Wilson, E.I. Friedmann, C.P. McKay, R.S. Sletten, E.M. Rivkina, T.A. Vishnivetskaya, L.G. Erokhina, N.E. Ivanushkina, G.A. Kochkina, V.A. Shcherbakova, V.S. Soina, E.V. Spirina, E.A. Vorobyova, D.G. Fyodorov- Davydov, B. Hallet, S.M. Ozerskaya, V.A. Sorokovikov, K.S. Laurinavichyus, A.V. Shatilovich, J.P. Chanton, V.E. Ostroumov, and J.M. Tiedje, “Microbial Populations in Antarctic Permafrost: Biodiversity, State, Age, and Implication for Astrobiology,” Astrobiology 7:275-311, 2007. 16 . D.E. Sugden, D.R. Marchant, N. Potter, Jr., R.A. Souchez, G.H. Denton, C.C. Swisher III, and J.-L. Tison, “Preserva- tion of Miocene Glacier Ice In East Antarctica,” Nature 376:412-414, 1995. 17 . D.R. Marchant, A.R. Lewis, W.M. Phillips, E.J. Moore, R.A. Souchez, G.H. Denton, D.E. Sugden, N. Potter, Jr., and G.P. Landis, “Formation of Patterned Ground and Sublimation Till Over Miocene Glacier Ice in Beacon Valley, Southern Victoria Land, Antarctica,” Geological Society of America Bulletin 114:718-730, 2002. 18 . John Priscu, personal communication, September 8, 2008. 19 . W.D. Grant, “Life at Low Water Activity,” Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 359(1448):1249-1266, 2004. 20 . L.J. Rothschild and R.L. Mancinelli, “Life in Extreme Environments,” Nature 409:1092-1101, 2001. 21 . V.R. Phoenix, P.C. Bennett, A. Summers Engel, S.W. Tyler, and F.G. Ferris. “Chilean High-altitude Hot Spring Sinters: A Model System for UV Screening Mechanisms by Early Precambrian Cyanobacteria,” Geobiology 4:15-28, 2006. 22 . C.R. Omelon, W.H. Pollard, and F.G. Ferris, “Environmental Controls on Microbial Colonization of High Arctic Cryptoendolithic Habits,” Polar Biology 30:19-29, 2006.