Habitability of Mars: How Welcoming Are the Surface and Subsurface to Life on the Red Planet?
Abstract
:1. Introduction
2. Characteristics of the Martian Surface and Subsurface
2.1. Habitability of the Martian Surface
2.1.1. Ice and Water
2.1.2. Organic Compounds
2.1.3. Salts
2.1.4. Radiation
2.1.5. Atmosphere
2.2. Mars Subsurface as a Potential Habitat for Life
3. Mars Analog Sites on Earth
3.1. Dry Valleys of Antarctica
3.2. Atacama Desert
3.3. Lava Tubes
4. Studies on Survival of Organisms in Simulated Martian Conditions
4.1. Microorganisms
4.1.1. Archaea
4.1.2. Bacteria
Martian Soil Analogue Exposure
Exposure of Bacterial Isolates from Spacecraft Assembly Facilities
Survival of Bacteria in Brines
Conclusions on Growth of Bacteria Under Martian Conditions
4.1.3. Fungi
4.2. Lichens
4.3. Bryophytes
5. Considerations for Future Studies
6. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Sagan, C. The search for extraterrestrial life. Scientific American, 1 October 1994; 92–99. [Google Scholar]
- Malin, M.C.; Edgett, K.S. Evidence for recent groundwater seepage and surface runoff on Mars. Science 2000, 288, 2330–2335. [Google Scholar] [CrossRef] [PubMed]
- Malin, M.C.; Edgett, K.S. Evidence for persistent flow and aqueous sedimentation on early Mars. Science 2003, 302, 1931–1934. [Google Scholar] [CrossRef] [PubMed]
- McKay, C.P. What is life—And how do we search for it in other worlds? PLoS Biol. 2004, 2, 1260–1263. [Google Scholar] [CrossRef] [PubMed]
- Rasmussen, B.; Blake, T.S.; Fletcher, I.R.; Kilburn, M.R. Evidence for microbial life in synsedimentary cavities from 2.75 Ga terrestrial environments. Geology 2009, 37, 423–426. [Google Scholar] [CrossRef]
- Merino, N.; Aronson, H.S.; Bojanova, D.P.; Feyhl-Buska, J.; Wong, M.L.; Zhang, S.; Giovannelli, D. Living at the extremes: Extremophiles and the limits of life in a planetary context. Front. Microbiol. 2019, 10, 1–25. [Google Scholar] [CrossRef] [PubMed]
- Bakermans, C.; Tsapin, A.I.; Souza-Egipsy, V.; Gilichinsky, D.A.; Nealson, K.H. Reproduction and metabolism at −10 °C of bacteria isolated from Siberian permafrost. Environ. Microbiol. 2003, 5, 321–326. [Google Scholar] [CrossRef]
- Takai, K.; Nakamura, K.; Toki, T.; Tsunogai, U.; Miyazaki, M.; Miyazaki, J.; Hirayama, H.; Nakagawa, S.; Nunoura, T.; Horikoshi, K. Cell proliferation at 122 °C and isotopically heavy CH4 production by a hyperthermophilic methanogen under high-pressure cultivation. Proc. Natl. Acad. Sci. USA 2008, 105, 10949–10954. [Google Scholar] [CrossRef]
- Fang, J.; Zhang, L.; Bazylinski, D.A. Deep-sea piezosphere and piezophiles: Geomicrobiology and biogeochemistry. Trends Microbiol. 2010, 18, 413–422. [Google Scholar] [CrossRef]
- Barns, S.M.; Fundyga, R.E.; Jeffries, M.W.; Pace, N.R. Remarkable archaeal diversity detected in a Yellowstone National Park hot spring environment. Proc. Natl. Acad. Sci. USA 1994, 91, 1609–1613. [Google Scholar] [CrossRef]
- Barton, H.A.; Northup, D.E. Geomicrobiology in cave environments: Past, current and future perspective. J. Cave Karst Stud. 2007, 69, 163–178. [Google Scholar]
- Rothschild, L.J.; Mancinelli, R.L. Life in extreme environments. Nature 2001, 409, 1092–1101. [Google Scholar] [CrossRef] [PubMed]
- Cockell, C.S.; Bush, T.; Bryce, C.; Direito, S.; Fox-Powell, M.; Harrison, J.P.; Lammer, H.; Landenmark, H.; Martin-Torres, J.; Nicholson, N.; et al. Habitability: A Review. Astrobiology 2016, 16, 89–117. [Google Scholar] [CrossRef] [PubMed]
- National Academies of Sciences, Engineering, and Medicine. Review of the MEPAG Report on Mars Special Regions; The National Academies Press: Washington, DC, USA, 2015. [Google Scholar]
- Ball, P. Water is an active matrix of life for cell and molecular biology. Proc. Natl. Acad. Sci. USA 2017, 114, 13327–13335. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Baker, V.R.; Strom, R.G.; Gulick, V.C.; Kargel, J.S.; Komatsu, G.; Kale, V.S. Ancient oceans, ice sheets and the hydrological cycle on Mars. Nature 1991, 352, 589–594. [Google Scholar] [CrossRef]
- Ramirez, R.M.; Craddock, R.A. The geological and climatological case for a warmer and wetter early Mars. Nat. Geosci. 2018, 11, 230–237. [Google Scholar] [CrossRef] [Green Version]
- Baker, V.R. Mars: Water and the Martian landscape. Nature 2001, 412, 228–236. [Google Scholar] [CrossRef] [PubMed]
- Westall, F.; Loizeau, D.; Foucher, F.; Bost, N.; Betrand, M.; Vago, J.; Kminek, G. Habitability on Mars from a microbial point of view. Astrobiology 2013, 13, 887–897. [Google Scholar] [CrossRef] [PubMed]
- Malin, M.C.; Edgett, K.S. Sedimentary rocks of early Mars. Science 2000, 290, 1927–1937. [Google Scholar] [CrossRef] [PubMed]
- Ehlmann, B.L.; Buz, J. Mineralogy and fluvial history of the watersheds of Gale, Knobel, and Sharp craters: A regional context for the Mars Science Laboratory Curiosity’s exploration. Geophys. Res. Lett. 2015, 42, 264–273. [Google Scholar] [CrossRef]
- Chevrier, V.; Mathé, P.E. Mineralogy and evolution of the surface of Mars: A review. Planet. Space Sci. 2007, 55, 289–314. [Google Scholar] [CrossRef]
- Ehlmann, B.L.; Mustard, J.F. An in-situ record of major environmental transitions on early Mars at Northeast Syrtis Major. Geophys. Res. Lett. 2012, 39, 1–7. [Google Scholar] [CrossRef]
- Michalski, J.R.; Cuadros, J.; Niles, P.B.; Parnell, J.; Rogers, A.D.; Wright, S.P. Groundwater activity on Mars and implications for a deep biosphere. Nat. Geosci. 2013, 6, 133–138. [Google Scholar] [CrossRef]
- Orosei, R.; Lauro, S.E.; Pettinelli, E.; Cicchetti, A.; Coradini, M.; Cosciotti, B.; Di Paolo, F.; Flamini, E.; Mattei, E.; Pajola, M.; et al. Radar evidence of subglacial liquid water on Mars. Science 2018, 6401, 490–493. [Google Scholar] [CrossRef] [PubMed]
- Herkenhoff, K.E.; Byrne, S.; Russell, P.S.; Fishbaugh, K.E.; McEwen, A.S. Meter-scale morphology of the north polar region of Mars. Science 2007, 317, 1711–1715. [Google Scholar] [CrossRef] [PubMed]
- Grima, C.; Kofman, W.; Mouginot, J.; Phillips, R.J.; Hérique, A.; Biccari, D.; Seu, R.; Cutigni, M. North polar deposits of Mars: Extreme purity of the water ice. Geophys. Res. Lett. 2009, 36, 1–4. [Google Scholar] [CrossRef]
- Phillips, R.J.; Davis, B.J.; Tanaka, K.L.; Byrne, S.; Mellon, M.T.; Putzig, N.E.; Haberle, R.M.; Kahre, M.A.; Campbell, B.A.; Carter, L.M.; et al. Massive CO2 ice deposits sequestered in the south polar layered deposits of Mars. Science 2011, 332, 838–841. [Google Scholar] [CrossRef]
- Clifford, S.M.; Lasue, J.; Heggy, E.; Boisson, J.; McGovern, P.; Max, M.D. Depth of the Martian cryosphere: Revised estimates and implications for the existence and detection of subpermafrost groundwater. J. Geophys. Res. 2010, 115, 1–17. [Google Scholar] [CrossRef]
- Haberle, R.M.; McKay, C.P.; Schaeffer, J.; Cabrol, N.A.; Grin, E.A.; Zent, A.P.; Quinn, R. On the possibility of liquid water on present-day Mars. J. Geophys. Res. Planets 2001, 106, 23317–23326. [Google Scholar] [CrossRef]
- Jakosky, B.M.; Phillips, R.J. Mars’ volatile and climate history. Nature 2001, 412, 237–244. [Google Scholar] [CrossRef]
- McEwen, A.S.; Ojha, L.; Dundas, C.M.; Mattson, S.S.; Byrne, S.; Wray, J.J.; Cull, S.C.; Murchie, S.L.; Thomas, N.; Gulick, V.C. Seasonal flows on warm Martian slopes. Science 2011, 333, 740–743. [Google Scholar] [CrossRef]
- Ohja, L.; Wilhelm, M.B.; Murchie, S.L.; McEwen, A.S.; Wray, J.J.; Hanley, J.; Massé, M.; Chojnacki, M. Spectral evidence for hydrated salts in recurring slope lineae on Mars. Nat. Geosci. 2015, 8, 829–835. [Google Scholar] [CrossRef]
- Dundas, C.M.; McEwen, A.S.; Chojnacki, M.; Milazzo, M.P.; Byrne, S.; McElwaine, J.N.; Urso, A. Granular flows at recurring slope lineae on Mars indicate a limited role for liquid water. Nat. Geosci. 2017, 10, 903–908. [Google Scholar] [CrossRef]
- Murray, A.E.; Kenig, F.; Fritsen, C.H.; McKay, C.P.; Cawley, K.M.; Edwards, R.; Kuhn, E.; McKnight, D.M.; Ostrom, N.E.; Peng, V.; et al. Microbial life at −13 °C in the brine of an ice-sealed Antarctic lake. Proc. Natl. Acad. Sci. USA 2012, 109, 20626–20631. [Google Scholar] [CrossRef] [PubMed]
- Martín-Torres, F.J.; Zorzano, M.-P.; Valentín-Serrano, P.; Harri, A.-M.; Genzer, M.; Kemppinen, O.; Rivera-Valentin, E.G.; Jun, I.; Wray, J.; Madsen, M.B.; et al. Transient liquid water and water activity at Gale crater on Mars. Nat. Geosci. 2015, 8, 357–361. [Google Scholar] [CrossRef]
- Bhardwaj, A.; Sam, L.; Martín-Torres, F.J.; Zorzano, M.-P.; Fonseca, R.M. Martian slope streaks as plausible indicators of transient water activity. Sci. Rep. 2017, 7, 1–14. [Google Scholar] [CrossRef] [Green Version]
- Martínez, G.M.; Renno, N.O. Water and brines on Mars: Current evidence and implications for MSL. Space Sci. Rev. 2013, 175, 29–51. [Google Scholar] [CrossRef]
- Nuding, D.L.; Rivera-Valentin, E.G.; Davis, R.D.; Gough, R.V.; Chevrier, V.F.; Tolbert, M.A. Deliquescence and efflorescence of calcium perchlorate: An investigation of stable aqueous solutions relevant to Mars. Icarus 2014, 243, 420–428. [Google Scholar] [CrossRef]
- Gough, R.V.; Chevrier, V.F.; Tolbert, M.A. Formation of liquid water at low temperatures via the deliquescence of calcium chloride: Implications for Antarctica and Mars. Planet. Space Sci. 2016, 131, 79–87. [Google Scholar] [CrossRef]
- Chevrier, V.F.; Hanley, J.; Altheide, T.S. Stability of perchlorate hydrates and their liquid solutions at the Phoenix landing site, Mars. Geophys. Res. Lett. 2009, 36, 1–6. [Google Scholar] [CrossRef]
- Rivera-Valentín, E.G.; Gough, R.V.; Chevrier, V.F.; Primm, K.M.; Martínez, G.M.; Tolbert, M. Constraining the potential liquid water environment at Gale Crater, Mars. J. Geophys. Res. Planets 2018, 123, 1156–1167. [Google Scholar] [CrossRef]
- Davila, A.F.; Duport, L.G.; Melchiorri, R.; Jänchen, J.; Valea, S.; de los Rios, A.; Fairén, A.G.; Möhlmann, D.; McKay, C.P.; Ascaso, C.; et al. Hygroscopic salts and the potential for life on Mars. Astrobiology 2010, 10, 617–628. [Google Scholar] [CrossRef] [PubMed]
- McCollom, T.M. The habitability of Mars: Past and present. In Solar System Update; Blonder, P., Mason, J.W., Eds.; Springer Praxis Books: Berlin Heilderberg, 2006; pp. 159–175. [Google Scholar]
- Freissinet, C.; Glavin, D.P.; Mahaffy, P.R.; Miller, K.E.; Eigenbrode, J.L.; Summons, R.E.; Brunner, A.E.; Buch, A.; Szopa, C.; Archer, P.D.; et al. Organic molecules in the Sheepbed Mudstone, Gale Crater, Mars. J. Geophys. Res. Planets 2015, 120, 495–514. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Eigenbrode, J.L.; Summons, R.E.; Steele, A.; Freissinet, C.; Millan, M.; Navarro-González, R.; Sutter, B.; McAdam, A.C.; Franz, H.B.; Glavin, D.P.; et al. Organic matter preserved in 3-billion-year-old mudstones at Gale crater, Mars. Science 2018, 360, 1096–1101. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Parnell, J.; McMahon, S.; Boyce, A. Demonstrating deep biosphere activity in the geological record of lake sediments, on Earth and Mars. Int. J. Astrobiol. 2019, 17, 380–385. [Google Scholar] [CrossRef]
- Biemann, K.; Oro, J.; Tolumin III, P.; Orgel, L.E.; Nier, A.O.; Anderson, D.M.; Simmonds, P.G.; Flory, D.; Diaz, A.V.; Rushneck, D.R.; et al. The search for organic substances and inorganic volatile compounds in the surface of Mars. J. Geophys. Res. 1977, 82, 4641–4658. [Google Scholar] [CrossRef]
- Navarro-González, R.; Vargas, E.; de la Rosa, J.; Raga, A.C.; McKay, C. Reanalysis of the Viking results suggests perchlorate and organics at midlatitudes on Mars. J. Geophys. Res. Planets 2010, 115, 1–11. [Google Scholar] [CrossRef]
- 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. Detection of perchlorate and the soluble chemistry of Martian soil at the Phoenix lander site. Science 2009, 325, 64–67. [Google Scholar] [CrossRef]
- Rampelotto, P.H. Resistance of microorganisms to extreme environmental conditions and its contribution to astrobiology. Sustainability 2010, 2, 1602–1623. [Google Scholar] [CrossRef]
- Clark, B.C.; Morris, R.V.; McLennan, S.M.; Gellert, R.; Jolliff, B.; Knoll, A.H.; Squyres, S.W.; Lowenstein, T.K.; Ming, D.W.; Tosca, N.J.; et al. Chemistry and mineralogy of outcrops at Meridiani Planum. Earth Planet. Sci. Lett. 2005, 240, 73–94. [Google Scholar] [CrossRef]
- Crisler, J.D.; Newville, T.M.; Chen, F.; Clark, B.C.; Schneegurt, M.A. Bacterial growth at the high concentrations of magnesium sulfate found in Martian soils. Astrobiology 2012, 12, 98–106. [Google Scholar] [CrossRef]
- Hallsworth, J.E.; Yakimov, M.M.; Golyshin, P.N.; Gillion, J.L.M.; D’Auria, G.; de Lima Alves, F.; La Cono, V.; Genovese, M.; McKew, B.A.; Hayes, S.L.; et al. Limits of life in MgCl2-containing environments: Chaotropicity defines the window. Environ. Chem. Lett. 2007, 9, 801–813. [Google Scholar] [CrossRef] [PubMed]
- Grant, W.D. Life at low water activity. Philos. Trans. R. Soc. B Biol. Sci. 2004, 359, 1249–1267. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stevenson, A.; Hamill, P.G.; O’Kane, C.J.; Kminek, G.; Rummel, J.D.; Voytek, M.A.; Dijksterhuis, J.; Hallsworth, J.E. Aspergillus penicillioides differentiation and cell division at 0.585 water activity. Environ. Microbiol. 2017, 19, 687–697. [Google Scholar] [CrossRef] [PubMed]
- Steinle, L.; Knittel, K.; Felber, N.; Casalino, C.; de Lange, G.; Tessarolo, C.; Stadnitskaia, A.; Sinninghe Damsté, J.S.; Zopfi, J.; Lehmann, M.F.; et al. Life on the edge: Active microbial communities in the Kryos MgCl2-brine basin at very low water activity. ISME J. 2018, 12, 1414–1426. [Google Scholar] [CrossRef] [PubMed]
- Tosca, N.J.; Knoll, A.H.; McLennan, S.M. Water activity and the challenge for life on Early Mars. Science 2008, 320, 1204–1207. [Google Scholar] [CrossRef] [PubMed]
- Kounaves, S.P.; Chaniotakis, N.A.; Chevrier, V.F.; Carrier, B.L.; Folds, K.E.; Hansen, V.M.; McElhoney, K.M.; Neil, G.D.O.; Weber, A.W. Identification of the perchlorate parent salts at the Phoenix Mars landing site and possible implications. Icarus 2014, 232, 226–231. [Google Scholar] [CrossRef]
- Coates, J.D.; Achenbach, L.A. Microbial perchlorate reduction: Rocket-fuelled metabolism. Nat. Rev. Microbiol. 2004, 2, 569–580. [Google Scholar] [CrossRef]
- Coates, J.D.; Michaelidou, U.; Bruce, R.A.; O’Connor, S.M.; Crespi, J.N.; Achenbach, L.A. Ubiquity and diversity of dissimilatory (per)chlorate-reducing bacteria. Appl. Environ. Microbiol. 1999, 65, 5234–5241. [Google Scholar]
- Ju, X.; Sierra-Alvarez, R.; Field, J.A.; Byrnes, D.J.; Bentley, H.; Bentley, R. Microbial perchlorate reduction with elemental sulfur and other inorganic electron donors. Chemosphere 2008, 71, 114–122. [Google Scholar] [CrossRef]
- Dartnell, L.R. Ionizing radiation and life. Astrobiology 2011, 11, 551–582. [Google Scholar] [CrossRef]
- Rummel, J.D.; Beaty, D.W.; Jones, M.A.; Bakermans, C.; Barlow, N.G.; Boston, P.J.; Chevrier, V.F.; Clark, B.C.; de Vera, J.-P.P.; Gough, R.V.; et al. A new analysis of Mars “Special Regions”: Findings of the second MEPAG Special Regions Science Analysis Group (SR-SAG2). Astrobiology 2014, 14, 887–968. [Google Scholar] [CrossRef] [PubMed]
- Hassler, D.M.; Zeitlin, C.; Wimmer-Schweingruber, R.F.; Ehresmann, B.; Rafkin, S.; Eigenbrode, J.L.; Brinza, D.E.; Weigle, G.; Böttcher, S.; Böhm, E.; et al. Mars’ surface radiation environment measured with the Mars Science Laboratory’s Curiosity rover. Science 2014, 343, 1–7. [Google Scholar] [CrossRef] [PubMed]
- Cockell, C.S.; Catling, D.C.; Davis, D.L.; Snook, K.; Kepner, R.L.; Lee, P.; McKay, C.P. The ultraviolet environment of Mars: Biological implications past, present, and future. Icarus 2000, 146, 343–359. [Google Scholar] [CrossRef] [PubMed]
- Horneck, G. The microbial case for Mars and its implication for human expeditions to Mars. Acta Astronaut. 2008, 63, 1015–1024. [Google Scholar] [CrossRef]
- Rontó, G.; Bérces, A.; Lammer, H.; Cockell, C.S.; Molina-Cuberos, G.J.; Patel, M.R.; Selsis, F. Solar UV irradiation conditions on the surface of Mars. Photochem. Photobiol. 2003, 77, 34. [Google Scholar] [CrossRef]
- Owen, T.; Biemann, K.; Rushneck, D.R.; Biller, J.E.; Howarth, D.W.; Lafleur, A.L. The composition of the atmosphere at the surface of Mars. J. Geophys. Res. 1977, 82, 4635–4639. [Google Scholar] [CrossRef]
- Mahaffy, P.R.; Webster, C.R.; Atreya, S.K.; Franz, H.; Wong, M.; Conrad, P.G.; Harpold, D.; Jones, J.J.; Leshin, L.A.; Manning, H.; et al. Abundance and isotopic composition of gases in the Martian atmosphere from the Curiosity rover. Science 2013, 341, 263–266. [Google Scholar] [CrossRef]
- Ghosh, S.; Osman, S.; Vaishampayan, P.; Venkateswaran, K. Recurrent isolation of extremotolerant bacteria from the clean room where Phoenix spacecraft components were assembled. Astrobiology 2010, 10, 325–335. [Google Scholar] [CrossRef]
- Probst, A.; Vaishampayan, P.; Osman, S.; Moissl-Eichinger, C.; Andersen, G.L.; Venkateswaran, K. Diversity of anaerobic microbes in spacecraft assembly clean rooms. Appl. Environ. Microbiol. 2010, 76, 2837–2845. [Google Scholar] [CrossRef]
- Stieglmeier, M.; Wirth, R.; Kminek, G.; Moissl-Eichinger, C. Cultivation of anaerobic and facultatively anaerobic bacteria from spacecraft-associated clean rooms. Appl. Environ. Microbiol. 2009, 75, 3484–3491. [Google Scholar] [CrossRef]
- La Duc, M.T.; Dekas, A.; Osman, S.; Moissl, C.; Newcombe, D.; Venkateswaran, K. Isolation and characterization of bacteria capable of tolerating the extreme conditions of clean room environments. Appl. Environ. Microbiol. 2007, 73, 2600–2611. [Google Scholar] [CrossRef] [PubMed]
- Jacobson, K.; van Diepeningen, A.; Evans, S.; Fritts, R.; Gemmel, P.; Marsho, C.; Seely, M.; Wenndt, A.; Yang, X.; Jacobson, P. Non-rainfall moisture activates fungal decomposition of surface litter in the Namib Sand Sea. PLoS ONE 2015, 10, e0126977. [Google Scholar] [CrossRef] [PubMed]
- Jones, E.G.; Lineweaver, C.H.; Clarke, J.D. An extensive phase space for the potential Martian biosphere. Astrobiology 2011, 11, 1017–1033. [Google Scholar] [CrossRef] [PubMed]
- Grocott, M.P.W.; Martin, D.S.; Levett, D.Z.H.; McMorrow, R.; Windsor, J.; Montgomery, H.E. Arterial blood gases and oxygen content in climbers on Mount Everest. N. Engl. J. Med. 2009, 360, 140–149. [Google Scholar] [CrossRef] [PubMed]
- Horneck, G.; Klaus, D.M.; Mancinelli, R.L. Space microbiology. Microbiol. Mol. Biol. Rev. 2010, 74, 121–156. [Google Scholar] [CrossRef]
- Nicholson, W.L.; Krivushin, K.; Gilichinsky, D.; Schuerger, A.C. Growth of Carnobacterium spp. from permafrost under low pressure, temperature, and anoxic atmosphere has implications for Earth microbes on Mars. Proc. Natl. Acad. Sci. USA 2013, 110, 666–671. [Google Scholar] [CrossRef]
- Schuerger, A.C.; Ulrich, R.; Berry, B.J.; Nicholson, W.L. Growth of Serratia liquefaciens under 7 mbar, 0 °C, and CO2-enriched anoxic atmospheres. Astrobiology 2013, 13, 115–131. [Google Scholar] [CrossRef]
- Pavlov, A.K.; Shelegedin, V.N.; Vdovina, M.A.; Pavlov, A.A. Growth of microorganisms in Martian-like shallow subsurface conditions: Laboratory modelling. Int. J. Astrobiol. 2010, 9, 51–58. [Google Scholar] [CrossRef]
- Michalski, J.R.; Onstott, T.C.; Mojzsis, S.J.; Mustard, J.; Chan, Q.H.S.; Niles, P.B.; Johnson, S.S. The Martian subsurface as a potential window into the origin of life. Nat. Geosci. 2018, 11, 21–26. [Google Scholar] [CrossRef]
- Boston, P.J.; Ivanov, M.V.; McKay, C.P. On the possibility of chemosynthetic ecosystems in subsurface habitats on Mars. Icarus 1992, 95, 300–308. [Google Scholar] [CrossRef]
- Edwards, K.J.; Becker, K.; Colwell, F. The deep, dark energy biosphere: Intraterrestrial life on Earth. Annu. Rev. Earth Planet. Sci. 2012, 40, 551–568. [Google Scholar] [CrossRef]
- Fisk, M.R.; Giovannoni, S.J. Sources of nutrients and energy for a deep biosphere on Mars. J. Geophys. Res. 1999, 104, 11805–11815. [Google Scholar] [CrossRef]
- Kashefi, K.; Lovley, D.R. Extending the upper temperature limit for life. Science 2003, 301, 934. [Google Scholar] [CrossRef] [PubMed]
- Cockell, C.S. The subsurface habitability of terrestrial rocky planets: Mars. In Microbial Life of the Deep Biosphere; Kallmeyer, J., Wagner, D., Eds.; Deutsche Nationalbibliothek: Berlin, Germany; Boston, MA, USA, 2014; pp. 225–259. [Google Scholar]
- Ehlmann, B.L.; Mustard, J.F.; Murchie, S.L.; Poulet, F.; Bishop, J.L.; Brown, A.J.; Calvin, W.M.; Clark, R.N.; Des Marais, D.J.; Milliken, R.E.; et al. Orbital identification of carbonate-bearing rocks on Mars. Science 2008, 322, 1828–1832. [Google Scholar] [CrossRef] [PubMed]
- McCollom, T.M.; Seewald, J.S. Serpentinites, hydrogen, and life. Elements 2013, 9, 129–134. [Google Scholar] [CrossRef]
- Onstott, T.C.; McGown, D.; Kessler, J.; Sherwood Lollar, B.; Lehmann, K.K.; Clifford, S.M. Martian CH4: Sources, flux, and detection. Astrobiology 1991, 6, 377–395. [Google Scholar] [CrossRef] [PubMed]
- Stern, J.C.; Sutter, B.; Freissinet, C.; Navarro-González, R.; McKay, C.P.; Archer, P.D., Jr.; Buch, A.; Brunner, A.E.; Coll, P.; Eigenbrode, J.L.; et al. Evidence for indigenous nitrogen in sedimentary and aeolian deposits from the Curiosity rover investigations at Gale crater, Mars. Proc. Natl. Acad. Sci. USA 2015, 112, 4245–4250. [Google Scholar] [CrossRef]
- Usui, T.; McSween, H.Y., Jr.; Clark, B.C., III. Petrogenesis of high-phosphorous Wishstone Class rocks in Gusev Crater, Mars. J. Geophys. Res. E Planets 2008, 113, 1–13. [Google Scholar] [CrossRef]
- McGlynn, I.O.; Fedo, C.M.; McSween, H.Y., Jr. Soil mineralogy at the Mars Exploration Rover landing sites: An assessment of the competing roles of physical sorting and chemical weathering. J. Geophys. Res. E Planets 2012, 117, 1–16. [Google Scholar] [CrossRef]
- Yung, Y.L.; Chen, P. Methane on Mars. J. Astrobiol. Outreach 2015, 3, 3–5. [Google Scholar] [CrossRef]
- Formisano, V.; Atreya, S.; Encrenaz, T.; Ignatiev, N.; Giuranna, M. Detection of meethane in the atmosphere of Mars. Science 2004, 306, 1758–1761. [Google Scholar] [CrossRef] [PubMed]
- Krasnopolsky, V.A.; Maillard, J.P.; Owen, T.C. Detection of methane in the martian atmosphere: Evidence for life? Icarus 2004, 172, 537–547. [Google Scholar] [CrossRef]
- Mumma, M.J.; Novak, R.E.; DiSanti, M.A.; Bonev, B.P.; Dello Russo, N. Detection and mapping of methane and water on Mars. In The Bulletin of the American Astronomical Society; American Astronomical Society: Washington, DC, USA, 2004; p. 1127. [Google Scholar]
- Mumma, M.J.; Villanueva, G.L.; Novak, R.E.; Hewagama, T.; Bonev, B.P.; DiSanti, M.A.; Mandell, A.M.; Smith, M.D. Strong release of methane on Mars in northern summer 2003. Science 2009, 323, 1041–1045. [Google Scholar] [CrossRef] [PubMed]
- Webster, C.R.; Mahaffy, P.R.; Atreya, S.K.; Moores, J.E.; Flesch, G.J.; Malespin, C.; McKay, C.P.; Martinez, G.; Smith, C.L.; Martin-Torres, J.; et al. Background levels of methane in Mars’ atmosphere show strong seasonal variations. Science 2018, 1096, 1093–1096. [Google Scholar] [CrossRef] [PubMed]
- Giuranna, M.; Viscardy, S.; Daerden, F.; Neary, L.; Etiope, G.; Oehler, D.; Formisano, V.; Aronica, A.; Wolkenberg, P.; Aoki, S.; et al. Independent confirmation of a methane spike on Mars and a source region east of Gale Crater. Nat. Geosci. 2019, 12, 326–332. [Google Scholar] [CrossRef]
- Korablev, O.; Vandaele, A.C.; Montmessin, F.; Fedorova, A.A.; Trokhimovskiy, A.; Forget, F.; Lefèvre, F.; Daerden, F.; Thomas, I.R.; Trompet, L.; et al. No detection of methane on Mars from early ExoMars Trace Gas Orbiter observations. Nature 2019, 568, 517–520. [Google Scholar] [CrossRef]
- Kirschke, S.; Bousguet, P.; Ciais, P.; Saunois, M.; Canadell, J.G.; Dlugokencky, E.J.; Bergamaschi, P.; Bergmann, D.; Blake, D.R.; Bruhwiler, L.; et al. Three decades of global methane sources and sinks. Nat. Geosci. 2013, 28, 813–823. [Google Scholar] [CrossRef]
- Yung, Y.L.; Chen, P.; Nealson, K.; Atreya, S.; Beckett, P.; Blank, J.G.; Ehlmann, B.; Eiler, J.; Etiope, G.; Ferry, J.G.; et al. Methane on Mars and habitability: Challenges and responses. Astrobiology 2018, 18, 1221–1242. [Google Scholar] [CrossRef]
- Oehler, D.Z.; Etiope, G. Methane seepage on Mars: Where to look and why. Astrobiology 2017, 17, 1233–1264. [Google Scholar] [CrossRef]
- Lyu, Z.; Shao, N.; Akinyemi, T.; Whitman, W.B. Methanogenesis. Curr. Biol. 2018, 28, R727–R732. [Google Scholar] [CrossRef] [Green Version]
- Schulte, M.; Blake, D.; Hoehler, T.; McCollom, T. Serpentinization and its implications for life on the Early Earth and Mars. Astrobiology 2006, 6, 364–376. [Google Scholar] [CrossRef] [PubMed]
- Tarnas, J.D.; Mustard, J.F.; Sherwood Lollar, B.; Bramble, M.S.; Cannon, K.M.; Palumbo, A.M.; Plesa, A.C. Radiolytic H2 production on Noachian Mars: Implications for habitability and atmospheric warming. Earth Planet. Sci. Lett. 2018, 502, 133–145. [Google Scholar] [CrossRef]
- Dzaugis, M.; Spivack, A.J.; D’Hondt, S. Radiolytic H2 production in Martian environments. Astrobiology 2018, 18, 1137–1146. [Google Scholar] [CrossRef] [PubMed]
- Dzaugis, M.E.; Spivack, A.J.; Dunlea, A.G.; Murray, R.W.; D’Hondt, S. Radiolytic hydrogen production in the subseafloor basaltic aquifer. Front. Microbiol. 2016, 7, 1–12. [Google Scholar] [CrossRef] [PubMed]
- Etiope, G.; Sherwood Lollar, B. Abiotic methane on Earth. Rev. Geophys. 2013, 51, 276–299. [Google Scholar] [CrossRef]
- Léveillé, R. Mars Analogue Sites. In Encyclopedia of Astrobiology; Gargaud, M., Amils, R., Cleaves, H.J., Eds.; Springer: Berlin/Heidelberg, Germany, 2014. [Google Scholar]
- Doran, P.T.; McKay, C.P.; Clow, G.D.; Dana, G.L.; Fountain, A.G.; Nylen, T.; Lyons, W.B. Valley floor climate observations from the McMurdo dry valleys, Antarctica, 1986-2000. J. Geophys. Res. Atmos. 2002, 107, 1–12. [Google Scholar] [CrossRef]
- McKay, C.P. Snow recurrence sets the depth of dry permafrost at high elevations in the McMurdo Dry Valleys of Antarctica. Antarct. Sci. 2009, 21, 89–94. [Google Scholar] [CrossRef]
- Cary, S.C.; McDonald, I.R.; Barrett, J.E.; Cowan, D.A. On the rocks: Microbiology of Anctarctic Dry Valley soils. Nat. Rev. Microbiol. 2010, 8, 129–138. [Google Scholar] [CrossRef] [PubMed]
- Goordial, J.; Davila, A.; Lacelle, D.; Pollard, W.; Marinova, M.M.; Greer, C.W.; DiRuggiero, J.; McKay, C.P.; Whyte, L.G. Nearing the cold-arid limits of microbial life in permafrost of an upper dry valley, Antarctica. ISME J. 2016, 10, 1613–1624. [Google Scholar] [CrossRef]
- Azua-Bustos, A.; Urrejola, C.; Vicuña, R. Life at the dry edge: Microorganisms of the Atacama Desert. FEBS Lett. 2012, 586, 2939–2945. [Google Scholar] [CrossRef] [Green Version]
- Navarro-González, R.; Rainey, F.A.; Molina, P.; Bagaley, D.R.; Hollen, B.J.; de la Rosa, J.; Small, A.M.; Quinn, R.C.; Grunthaner, F.J.; Cáceres, L.; et al. Mars-like soils in the Atacama Desert, Chile, and the dry limit of microbial life. Science 2003, 302, 1018–1021. [Google Scholar] [CrossRef] [PubMed]
- Schulze-Makuch, D.; Wagner, D.; Kounaves, S.P.; Mangelsdorf, K.; Devine, K.G.; de Vera, J.-P.; Schmitt-Kopplin, P.; Grossart, H.-P.; Parro, V.; Kaupenjohann, M.; et al. Transitory microbial habitat in the hyperarid Atacama Desert. Proc. Natl. Acad. Sci. USA 2018, 115, 2670–2675. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Davila, A.F.; Hawes, I.; Ascaso, C.; Wierzchos, J. Salt deliquescence drives photosynthesis in the hyperarid Atacama Desert. Environ. Microbiol. Rep. 2013, 5, 583–587. [Google Scholar] [CrossRef] [PubMed]
- Léveillé, R.J.; Datta, S. Lava tubes and basaltic caves as astrobiological targets on Earth and Mars: A review. Planet. Space Sci. 2010, 58, 592–598. [Google Scholar] [CrossRef]
- Lavoie, K.H.; Winter, A.S.; Read, K.J.H.; Hughes, E.M.; Spilde, M.N.; Northup, D.E. Comparison of bacterial communities from lava cave microbial mats to overlying surface soils from Lava Beds National Monument, USA. PLoS ONE 2017, 12, e0169339. [Google Scholar] [CrossRef] [PubMed]
- Gonzalez-Pimentel, J.L.; Miller, A.Z.; Jurado, V.; Laiz, L.; Pereira, M.F.C.; Saiz-Jimenez, C. Yellow coloured mats from lava tubes of La Palma (Canary Islands, Spain) are dominated by metabolically active Actinobacteria. Sci. Rep. 2018, 8, 1–11. [Google Scholar] [CrossRef]
- Kerney, K.R.; Schuerger, A.C. Survival of Bacillus subtilis endospores on ultraviolet-irradiated rover wheels and Mars regolith under simulated Martian conditions. Astrobiology 2011, 11, 477–485. [Google Scholar] [CrossRef] [PubMed]
- Schuerger, A.C.; Mancinelli, R.L.; Kern, R.G.; Rothschild, L.J.; McKay, C.P. Survival of endospores of Bacillus subtilis on spacecraft surfaces under simulated martian environments: Implications for the forward contamination of Mars. Icarus 2003, 165, 253–276. [Google Scholar] [CrossRef]
- Schuerger, A.C.; Golden, D.C.; Ming, D.W. Biotoxicity of Mars soils: 1. Dry deposition of analog soils on microbial colonies and survival under Martian conditions. Planet. Space Sci. 2012, 72, 91–101. [Google Scholar] [CrossRef]
- Schuerger, A.C.; Ming, D.W.; Golden, D.C. Biotoxicity of Mars soils: 2. Survival of Bacillus subtilis and Enterococcus faecalis in aqueous extracts derived from six Mars analog soils. Icarus 2017, 290, 215–223. [Google Scholar] [CrossRef]
- Smith, S.A.; Benardini III, J.N.; Anderl, D.; Ford, M.; Wear, E.; Schrader, M.; Schubert, W.; DeVeaux, L.; Paszczynski, A.; Childers, S.E. Identification and characterization of early mission phase microorganisms residing on the Mars Science Laboratory and assessment of their potential to survive Mars-like conditions. Astrobiology 2017, 17, 253–265. [Google Scholar] [CrossRef] [PubMed]
- Serrano, P.; Alawi, M.; de Vera, J.-P.; Wagner, D. Response of methanogenic archaea from Siberian permafrost and non-permafrost environments to simulated Mars-like desiccation and the presence of perchlorate. Astrobiology 2019, 19, 197–208. [Google Scholar] [CrossRef] [PubMed]
- Smith, S.A.; Paszczynski, A.; Childers, S.E. Are we alone? The search for life on Mars and other planetary bodies. In Into Space—A Journey of How Humans Adapt and Live in Microgravity; Russomano, T., Rehnber, L., Eds.; IntechOpen: London, UK, 2018; pp. 209–228. [Google Scholar]
- Kral, T.A.; Bekkum, C.R.; McKay, C. Growth of methanogens on a Mars soil simulant. Orig. Life Evol. Biosph. 2004, 34, 615–626. [Google Scholar] [CrossRef] [PubMed]
- Caldwell, S.L.; Laidler, J.R.; Brewer, E.A.; Eberly, J.O.; Sandborgh, S.O.; Colwell, F.S. Anaerobic oxidation of methane: Mechanisms, bioenergetics, and the ecology of associated microorganisms. Environ. Sci. Technol. 2008, 42, 6791–6799. [Google Scholar] [CrossRef] [PubMed]
- Krasnopolsky, V.A.; Feldman, P.D. Detection of molecular hydrogen in the atmosphere of Mars. Science 2001, 294, 1914–1917. [Google Scholar] [CrossRef] [PubMed]
- Kral, T.A.; Altheide, T.S.; Lueders, A.E.; Schuerger, A.C. Low pressure and desiccation effects on methanogens: Implications for life on Mars. Planet. Space Sci. 2011, 59, 264–270. [Google Scholar] [CrossRef]
- Mickol, R.L.; Kral, T.A. Low pressure tolerance by methanogens in an aqueous environment: Implications for subsurface life on Mars. Orig. Life Evol. Biosph. 2017, 47, 511–532. [Google Scholar] [CrossRef] [PubMed]
- Kral, T.A.; Travis Aitheide, S. Methanogen survival following exposure to desiccation, low pressure and martian regolith analogs. Planet. Space Sci. 2013, 89, 167–171. [Google Scholar] [CrossRef]
- Kral, T.A.; Goodhart, T.H.; Harpool, J.D.; Hearnsberger, C.E.; McCracken, G.L.; McSpadden, S.W. Sensitivity and adaptability of methanogens to perchlorates: Implications for life on Mars. Planet. Space Sci. 2016, 120, 87–95. [Google Scholar] [CrossRef]
- Mickol, R.L.; Kral, T.A. Low pressure microenvironments: Methane production at 50 mbar and 100 mbar by methanogens. Planet. Space Sci. 2018, 153, 79–88. [Google Scholar] [CrossRef]
- Moeller, R.; Setlow, P.; Reitz, G.; Nicholson, W.L. Roles of small, acid-soluble spore proteins and core water content in survival of Bacillus subtilis spores exposed to environmental solar UV radiation. Appl. Environ. Microbiol. 2009, 75, 5202–5208. [Google Scholar] [CrossRef] [PubMed]
- Checinska, A.; Paszczynski, A.; Burbank, M. Bacillus and other spore-forming genera: Variations in responses and mechanisms for survival. Annu. Rev. Food Sci. Technol. 2015, 6, 351–369. [Google Scholar] [CrossRef] [PubMed]
- Setlow, P. Spores of Bacillus subtilis: Their resistance to and killing by radiation, heat and chemicals. J. Appl. Microbiol. 2006, 101, 514–525. [Google Scholar] [CrossRef] [PubMed]
- Newcombe, D.A.; Schuerger, A.C.; Benardini, J.N.; Dickinson, D.; Tanner, R.; Venkateswaran, K. Survival of spacecraft-associated microorganisms under simulated Martian UV irradiation. Appl. Environ. Microbiol. 2005, 71, 8147–8156. [Google Scholar] [CrossRef] [PubMed]
- Cortesão, M.; Fuchs, F.M.; Commichau, F.M.; Eichenberger, P.; Schuerger, A.C.; Nicholson, W.L.; Setlow, P.; Moeller, R. Bacillus subtilis spore resistance to simulated Mars surface conditions. Front. Microbiol. 2019, 10, 1–16. [Google Scholar] [CrossRef] [PubMed]
- Berry, B.J.; Jenkins, D.G.; Schuerger, A.C. Effects of simulated Mars conditions on the survival and growth of Escherichia coli and Serratia liquefaciens. Appl. Environ. Microbiol. 2010, 76, 2377–2386. [Google Scholar] [CrossRef]
- Nicholson, W.L.; McCoy, L.E.; Kerney, K.R.; Ming, D.W.; Golden, D.C.; Schuerger, A.C. Aqueous extracts of a Mars analogue regolith that mimics the Phoenix landing site do not inhibit spore germination or growth of model spacecraft contaminants Bacillus subtilis 168 and Bacillus pumilus SAFR-032. Icarus 2012, 220, 904–910. [Google Scholar] [CrossRef]
- Bauermeister, A.; Mahnert, A.; Auerbach, A.; Böker, A.; Flier, N.; Weber, C.; Probst, A.J.; Moissl-Eichinger, C.; Haberer, K. Quantification of encapsulated bioburden in spacecraft polymer materials by cultivation-dependent and molecular methods. PLoS ONE 2014, 9, e94265. [Google Scholar] [CrossRef]
- Schubert, W.W.; Newlin, L.; Chung, S.Y.; Ellyin, R. Assessment of bioburden encapsulated in bulk materials. Adv. Space Res. 2016, 57, 2027–2036. [Google Scholar] [CrossRef]
- Kempf, M.J.; Chen, F.; Kern, R.; Venkateswaran, K. Recurrent isolation of hydrogen peroxide-resistant spores of Bacillus pumilus from a spacecraft assembly facility. Astrobiology 2005, 5, 391–405. [Google Scholar] [CrossRef]
- Schuerger, A.C.; Nicholson, W.L. Interactive effects of hypobaria, low temperature, and CO2 atmospheres inhibit the growth of mesophilic Bacillus spp. under simulated Martian conditions. Icarus 2006, 185, 143–152. [Google Scholar] [CrossRef]
- Al Soudi, A.F.; Farhat, O.; Chen, F.; Clark, B.C.; Schneegurt, M.A. Bacterial growth tolerance to concentrations of chlorate and perchlorate salts relevant to Mars. Int. J. Astrobiol. 2019, 16, 229–235. [Google Scholar] [CrossRef]
- Matsubara, T.; Fujishima, K.; Saltikov, C.W.; Nakamura, S.; Rothschild, L.J. Earth analogues for past and future life on Mars: Isolation of perchlorate resistant halophiles from Big Soda Lake. Int. J. Astrobiol. 2019, 16, 218–228. [Google Scholar] [CrossRef]
- Oren, A.; Bardavid, R.E.; Mana, L. Perchlorate and halophilic prokaryotes: Implications for possible halophilic life on Mars. Extremophiles 2014, 18, 75–80. [Google Scholar] [CrossRef] [PubMed]
- Wadsworth, J.; Cockell, C.S. Perchlorates on Mars enhance the bacteriocidal effects of UV light. Sci. Rep. 2017, 7, 1–8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wilks, J.M.; Chen, F.; Clark, B.C.; Schneegurt, M.A. Bacterial growth in saturated and eutectic solutions of magnesium sulphate and potassium chlorate with relevance to Mars and the ocean worlds. Int. J. Astrobiol. 2019, 1–8. [Google Scholar] [CrossRef]
- La Duc, M.T.; Kern, R.; Venkateswaran, K. Microbial monitoring of spacecraft and associated environments. Microb. Ecol. 2004, 47, 150–158. [Google Scholar] [CrossRef] [PubMed]
- La Duc, M.T.; Vaishampayan, P.; Nilsson, H.R.; Torok, T.; Venkateswaran, K. Pyrosequencing-derived bacterial, archaeal, and fungal diversity of spacecraft hardware destined for Mars. Appl. Environ. Microbiol. 2012, 78, 5912–5922. [Google Scholar] [CrossRef] [PubMed]
- Fox-Powell, M.G.; Hallsworth, J.E.; Cousins, C.R.; Cockell, C.S. Ionic strength is a barrier to the habitability of Mars. Astrobiology 2016, 16, 427–442. [Google Scholar] [CrossRef]
- Gostinčar, C.; Grube, M.; de Hoog, S.; Zalar, P.; Gunde-Cimerman, N. Extremotolerance in fungi: Evolution on the edge. FEMS Microbiol. Ecol. 2010, 71, 2–11. [Google Scholar] [CrossRef]
- Sterflinger, K.; Tesei, D.; Zakharova, K. Fungi in hot and cold deserts with particular reference to microcolonial fungi. Fungal Ecol. 2012, 5, 453–462. [Google Scholar] [CrossRef]
- Schmidt, S.K.; Naff, C.S.; Lynch, R.C. Fungal communities at the edge: Ecological lessons from high alpine fungi. Fungal Ecol. 2012, 5, 443–452. [Google Scholar] [CrossRef]
- Nagano, Y.; Nagahama, T. Fungal diversity in deep-sea extreme environments. Fungal Ecol. 2012, 5, 463–471. [Google Scholar] [CrossRef]
- Zhdanova, N.N.; Tugay, T.; Dighton, J.; Zheltonozhsky, V.; Mcdermott, P. Ionizing radiation attracts soil fungi. Mycol. Res. 2004, 108, 1089–1096. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gostinčar, C.; Muggia, L.; Grube, M. Polyextremotolerant black fungi: Oligotrophism, adaptive potential, and a link to lichen symbioses. Front. Microbiol. 2012, 3, 1–6. [Google Scholar] [CrossRef] [PubMed]
- Selbmann, L.; de Hoog, G.S.; Mazzaglia, A.; Friedmann, E.I.; Onofri, S. Fungi at the edge of life: Cryptoendolithic black fungi from Antarctic desert. Stud. Mycol. 2005, 51, 1–32. [Google Scholar]
- Onofri, S.; de Vera, J.-P.; Zucconi, L.; Selbmann, L.; Scalzi, G.; Venkateswaran, K.J.; Rabbow, E.; de la Torre, R.; Horneck, G. Survival of Antarctic cryptoendolithic fungi in simulated Martian conditions on board the International Space Station. Astrobiology 2015, 15, 1052–1059. [Google Scholar] [CrossRef]
- Onofri, S.; Selbmann, L.; Pacelli, C.; Zucconi, L.; Rabbow, E.; de Vera, J.-P. Survival, DNA, and ultrastructural integrity of a cryptoendolithic Antarctic fungus in Mars and Lunar rock analogs exposed outside the International Space Station. Astrobiology 2019, 19, 170–182. [Google Scholar] [CrossRef]
- Blachowicz, A.; Chiang, A.J.; Elsaesser, A.; Kalkum, M.; Ehrenfreund, P.; Stajich, J.E.; Torok, T.; Wang, C.C.C.; Venkateswaran, K. Proteomic and metabolomic characteristics of extremophilic fungi under simulated Mars conditions. Front. Microbiol. 2019, 10, 1–16. [Google Scholar] [CrossRef]
- Kranner, I.; Beckett, R.; Hochman, A.; Nash III, T.H. Desiccation-tolerance in lichens: A review. Bryologist 2008, 111, 576–593. [Google Scholar] [CrossRef]
- Selbmann, L.; Grube, M.; Onofri, S.; Isola, D.; Zucconi, L. Antarctic epilithic lichens as niches for black meristematic fungi. Biology 2013, 2, 784–797. [Google Scholar] [CrossRef] [PubMed]
- de Vera, J.-P. Lichens as survivors in space and on Mars. Fungal Ecol. 2012, 5, 472–479. [Google Scholar] [CrossRef]
- de Vera, J.-P.; Möhlmann, D.; Butina, F.; Lorek, A.; Wernecke, R.; Ott, S. Survival potential and photosynthetic activity of lichens under Mars-like conditions: A laboratory study. Astrobiology 2010, 10, 215–227. [Google Scholar] [CrossRef]
- Sanchez, F.J.; Mateo-Marti, E.; Raggio, J.; Meeßen, J.; Martínez-Frías, J.; Sancho, L.G.; Ott, S.; de la Torre, R. The resistance of the lichen Circinaria gyrosa (nom. provis.) towards simulated Mars conditions—A model test for the survival capacity of an eukaryotic extremophile. Planet. Space Sci. 2012, 72, 102–110. [Google Scholar] [CrossRef]
- Cockell, C.S.; Raven, J.A. Zones of photosynthetic potential on Mars and the early Earth. Icarus 2004, 169, 300–310. [Google Scholar] [CrossRef]
- Proctor, M.C.F. The bryophyteparadox: Tolerance of desiccation, evasion of drought. Plant Ecol. 2000, 151, 41–49. [Google Scholar] [CrossRef]
- Huwe, B.; Fiedler, A.; Moritz, S.; Rabbow, E.; de Vera, J.P.; Joshi, J. Mosses in Low Earth Orbit: Implications for the limits of life and the habitability of Mars. Astrobiology 2019, 19, 221–233. [Google Scholar] [CrossRef] [PubMed]
- de Vera, J.-P.; Alawi, M.; Backhaus, T.; Baqué, M.; Billi, D.; Böttger, U.; Berger, T.; Bohmeier, M.; Cockell, C.; Demets, R.; et al. Limits of life and the habitability of Mars: The ESA Space Experiment BIOMEX on the ISS. Astrobiology 2019, 19, 145–158. [Google Scholar] [CrossRef] [PubMed]
- Bada, J.L. State-of-the-art instruments for detecting extraterrestrial life. Proc. Natl. Acad. Sci. USA 2001, 98, 797–800. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Williford, K.H.; Farley, K.A.; Stack, K.M.; Allwood, A.C.; Beaty, D.; Beegle, L.W.; Bhartia, R.; Brown, A.J.; de la Torre Juarez, M.; Hamran, S.-E.; et al. The NASA Mars 2020 rover mission and the search for extraterrestrial life. In From Habitability to Life on Mars; Cabrol, N.A., Grin, E.A., Eds.; Elsevier: Amsterdam, The Netherlands, 2018; pp. 275–308. ISBN 9780128099353. [Google Scholar]
- Vago, J.L.; Westall, F.; Teams, P.I.; Group, L.S.S.W.; Contributors, O. Habitability on early Mars and the search for biosignatures with the ExoMars rover. Astrobiology 2017, 17, 471–510. [Google Scholar] [CrossRef]
- Mancinelli, R.L. Accessing the Martian deep subsurface to search for life. Planet. Space Sci. 2000, 48, 1035–1042. [Google Scholar] [CrossRef]
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Checinska Sielaff, A.; Smith, S.A. Habitability of Mars: How Welcoming Are the Surface and Subsurface to Life on the Red Planet? Geosciences 2019, 9, 361. https://doi.org/10.3390/geosciences9090361
Checinska Sielaff A, Smith SA. Habitability of Mars: How Welcoming Are the Surface and Subsurface to Life on the Red Planet? Geosciences. 2019; 9(9):361. https://doi.org/10.3390/geosciences9090361
Chicago/Turabian StyleChecinska Sielaff, Aleksandra, and Stephanie A. Smith. 2019. "Habitability of Mars: How Welcoming Are the Surface and Subsurface to Life on the Red Planet?" Geosciences 9, no. 9: 361. https://doi.org/10.3390/geosciences9090361
APA StyleChecinska Sielaff, A., & Smith, S. A. (2019). Habitability of Mars: How Welcoming Are the Surface and Subsurface to Life on the Red Planet? Geosciences, 9(9), 361. https://doi.org/10.3390/geosciences9090361