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Physical and chemical mechanisms that impact the detection, identification, and quantification of organic matter and the survival of microorganisms on the Martian surface – a review

Published online by Cambridge University Press:  31 January 2022

Ebbe Norskov Bak
Affiliation:
Department of Biology, Microbiology Section, Aarhus University, Ny Munkegade 114–116, DK-8000 Aarhus C, Denmark
Per Nørnberg
Affiliation:
Department of Biology, Microbiology Section, Aarhus University, Ny Munkegade 114–116, DK-8000 Aarhus C, Denmark
Svend J. Knak Jensen
Affiliation:
Department of Chemistry, Aarhus University, Langelandsgade 140, DK-8000 Aarhus C, Denmark
Jan Thøgersen
Affiliation:
Department of Chemistry, Aarhus University, Langelandsgade 140, DK-8000 Aarhus C, Denmark
Kai Finster*
Affiliation:
Department of Biology, Microbiology Section, Aarhus University, Ny Munkegade 114–116, DK-8000 Aarhus C, Denmark Stellar Astrophysics Centre, Department of Physics and Astronomy, Aarhus University, Ny Munkegade 120, DK-8000 Aarhus C, Denmark
*
Author for correspondence: Kai Finster, E-mail: Kai.Finster@bio.au.dk

Abstract

The iconic Viking Landers that landed on Mars in 1976 demonstrated that the Martian surface is an extreme place, dominated by high UV fluxes and regolith chemistry capable of oxidizing organic molecules. From follow-on missions, we have learned that Mars was much warmer and wetter in its early history, and even some areas of Mars (such as crater lakes, possibly with sustained hydrothermal activity) were habitable places (e.g. Grotzinger et al. (2014). Science (New York, N.Y.) 343; Mangold et al. (2021). Science (New York, N.Y.). However, based on the Viking results we have learnt that the search for life and its remains is challenged by abiotic breakdown and alteration of organic material. In particular, the harsh radiation climate at the Martian surface that directly and indirectly could degrade organics has been held accountable for the lack of organics in the Martian regolith. Recent work simulating wind-driven erosion of basalts under Mars-like conditions has shown that this process, comparable to UV- and ionizing radiation, produces reactive compounds, kills microbes and removes methane from the atmosphere. and thereby could equally jeopardize the success of life-seeking missions to Mars. In this review, we summarize and discuss previous work on the role of physical and chemical mechanisms that affect the persistence of organics, and their consequences for the detection of life and/or its signatures in the Martian regolith and in the atmosphere.

Type
Review Article
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Anjem, A and Imlay, JA (2012) Mononuclear iron enzymes are primary targets of hydrogen peroxide stress. Journal of Biological Chemistry 287, 1554415556.CrossRefGoogle ScholarPubMed
Anjem, A, Varghese, S and Imlay, JA (2009) Manganese import is a key element of the OxyR response to hydrogen peroxide in Escherichia coli. Molecular Microbiology 72, 844858.CrossRefGoogle ScholarPubMed
Apak, R (2008) Life detection experiments of the Viking mission on Mars can be best interpreted with a Fenton oxidation reaction composed of H2O2 and Fe2+ and iron-catalyzed decomposition of H2O2. International Journal of Astrobiology 7, 187192.CrossRefGoogle Scholar
Atreya, SK, Mahaffy, PR and Wong, AS (2007) Methane and related trace species on Mars: origin, loss, implications for life, and habitability. Planetary and Space Science 55, 358369.CrossRefGoogle Scholar
Atreya, SK et al. (2006) Oxidant enhancement in Martian dust devils and storms: implications for life and habitability. Astrobiology 6, 439450.CrossRefGoogle ScholarPubMed
Audourd, J, Piqueux, S, Poulet, F, Vincendon, M, Arvidson, RE and Rogers, AD (2015) Analysis of Curiosity GTS/REMS surface temperature measurements. 46th Lunar and Planetary Science Conference.Google Scholar
Bak, EN, Jensen, SJK, Nørnberg, P and Finster, K (2016) Methylated silicates may explain the release of chlorinated methane from Martian regolith. Earth and Planetary Science Letters 433, 226231.CrossRefGoogle Scholar
Bak, EN, Zafirov, K, Merrison, J, Jensen, SJK, Nørnberg, P, Gunnlaugsson, HP and Finster, K (2017 a) Production of reactive oxygen species from abraded silicates. Implications for the reactivity of the Martian regolith. Earth and Planetary Science Letters 473, 13121.CrossRefGoogle Scholar
Bak, EN, Larsen, MG, Moeller, R, Nissen, SB, Jensen, LR, Nørnberg, P, Jensen, SJK and Finster, K (2017 b) Silicates eroded under simulated Martian conditions effectively kill bacteria – a challenge for life on Mars. Frontiers of Microbiology 8, 1709.CrossRefGoogle ScholarPubMed
Bak, EN, Larsen, MG, Jensen, SJK, Nørnberg, P, Moeller, R and Finster, K (2019) Wind-driven saltation: an overlooked challenge for life on Mars. Astrobiology 19, 497505.CrossRefGoogle ScholarPubMed
Ballou, EV, Wood, PC, Wydeven, T, Lehwalt, ME and Mack, RE (1978) Chemical interpretation of Viking lander 1 life-detection experiment. Nature 271, 644645.CrossRefGoogle Scholar
Banh, A et al. (2013) Manganese (Mn) oxidation increases intracellular Mn in Pseudomonas putida GB-1. PLoS One 8, e77835.CrossRefGoogle ScholarPubMed
Benardini, JN, La Duc, MT, Beaudet, RA and Koukol, R (2014) Implementing planetary protection measures on the Mars science laboratory. Astrobiology 14, 2732.CrossRefGoogle ScholarPubMed
Benner, SA, Devine, KG, Matveeva, LN and Powell, DH (2000) The missing organic molecules on Mars. PNAS 97, 24252430.CrossRefGoogle ScholarPubMed
Biemann, K and Bada, JL (2011) Comment on “Reanalysis of the Viking results suggests perchlorate and organics at midlatitudes on Mars” by Rafael Navarro-Gonzalez et al. Journal of Geophysical Research-Planets 116, E12001.CrossRefGoogle Scholar
Biemann, K et al. (1977) The search for organic substances and inorganic volatile compounds in the surface of Mars. Journal of Geophysical Research 82, 46414658.CrossRefGoogle Scholar
Bjelland, S and Seeberg, E (2003) Mutagenicity, toxicity and repair of DNA base damage induced by oxidation. Mutation Research-Fundamental and Molecular Mechanisms of Mutagenesis 531, 3780.CrossRefGoogle ScholarPubMed
Blake, DF, et al. (2013) Curiosity at Gale crater, Mars: characterization and analysis of the rocknest sand shadow. Science 341, 18.CrossRefGoogle ScholarPubMed
Boston, PJ et al. (2001) Cave biosignature suites: microbes, minerals and Mars. Astrobiology 1, 2555.CrossRefGoogle ScholarPubMed
Boynton, WV et al. (2001) Thermal and evolved gas analyzer: part of the Mars volatile and climate surveyor integrated payload. Journal of Geophysical Research-Planets 106, 1768317698.CrossRefGoogle Scholar
Bradley, AS and Summons, RE (2010) Multiple origins of methane at the Lost City hydrothermal field. Earth and Planetary Science Letters 297, 3441.CrossRefGoogle Scholar
Brinckerhoff, WB et al. (2013) Mars Organic Molecule Analyzer (MOMA) mass spectrometer for ExoMars 2018 and beyond. 2013 IEEE Aerospace Conference.CrossRefGoogle Scholar
Buege, JA and Aust, SD (1978) Microsomal lipid peroxidation. Methods in Enzymology 52, 302310.CrossRefGoogle ScholarPubMed
Buxton, GV, Greenstock, CL, Helman, WP and Ross, AB (1988) Critical-review of rate constants for reactions of hydrated electrons, hydrogen-atoms and hydroxyl radicals (.Oh/.O) in aqueous-solution. Journal of Physical and Chemical Reference Data 17, 513886.CrossRefGoogle Scholar
Chastain, BK and Chevrier, V (2007) Methane clathrate hydrates as a potential source for Martian atmospheric methane. Planetary and Space Science 55, 12461256.CrossRefGoogle Scholar
Clancy, RT, Sandor, BJ and Moriarty-Schieven, GH (2004) A measurement of the 362 GHz absorption line of Mars atmospheric H2O2. Icarus 168, 116121.CrossRefGoogle Scholar
Clark, B and Kounaves, S (2016) Evidence for the distribution of perchlorates on Mars. International Journal of Astrobiology 15, 311318.CrossRefGoogle Scholar
Cockell, CS, Catling, DC, Davis, WL, Snook, K, Kepner, RL, Lee, P and McKay, CP (2000) The ultraviolet environment of Mars: biological implications past, present, and future. Icarus 146, 343359.CrossRefGoogle ScholarPubMed
Conrad, R (2009) The global methane cycle: recent advances in understanding the microbial processes involved. Environmental Microbiology Reports 1, 285292.CrossRefGoogle ScholarPubMed
Cortezzo, DE and Setlow, P (2005) Analysis of factors that influence the sensitivity of spores of Bacillus subtilis to DNA damaging chemicals. Journal of Applied Microbiology 98, 606617.CrossRefGoogle ScholarPubMed
COSPAR Planetary Protection Policy (2002) COSPAR/IAU workshop on planetary protection. pp.1–13.Google Scholar
Daly, MJ, Gaidamakova, EK, Matrosova, VY et al. (2010) Small-molecule antioxidant proteome-shields in Deinococcus radiodurans. PLoS One 5, e12570.CrossRefGoogle ScholarPubMed
de La Vega, UP, Rettberg, P and Reitz, G (2007) Simulation of the environmental climate conditions on Martian surface and its effect on Deinococcus radiodurans. Advances in Space Research 40, 16721677.CrossRefGoogle Scholar
Delory, GT et al. (2006) Oxidant enhancement in Martian dust devils and storms: storm electric fields and electron dissociative attachment. Astrobiology 6, 451462.CrossRefGoogle ScholarPubMed
D'Hondt, S et al. (2015) Presence of oxygen and aerobic communities from seafloor to basement in deep-sea sediments. Nature Geoscience 8, 299304.CrossRefGoogle Scholar
Diaz, B and Schulze-Makuch, D (2006) Microbial survival rates of Escherichia coli and Deinococcus radiodurans under low temperature, low pressure, and UV-irradiation conditions, and their relevance to possible Martian life. Astrobiology 6, 332347.CrossRefGoogle ScholarPubMed
Eden, HF and Vonnegut, B (1973) Electrical breakdown caused by dust motion in low-pressure atmospheres-considerations for Mars. Science (New York, N.Y.) 180, 962963.CrossRefGoogle ScholarPubMed
Eigenbrode, JL et al. (2018) Organic matter preserved in 3-billion-year-old mudstones at Gale crater, Mars. Science (New York, N.Y.) 360, 10961101.CrossRefGoogle ScholarPubMed
Encrenaz, T, Greathouse, TK, Lefevre, F and Atreya, SK (2012) Hydrogen peroxide on Mars: observations, interpretation and future plans. Planetary and Space Science 68, 317.CrossRefGoogle Scholar
Encrenaz, T et al. (2008) Simultaneous mapping of H2O and H2O2 on Mars from infrared high-resolution imaging spectroscopy. Icarus 195, 547556.CrossRefGoogle Scholar
Farley, KA et al. (2014) In Situ radiometric and exposure age dating of the Martian surface. Science (New York, N.Y.) 343, 1247166.CrossRefGoogle ScholarPubMed
Farrell, WM, Delory, GT and Atreya, SK (2006) Martian dust storms as a possible sink of atmospheric methane. Geophysical Research Letters 33. doi: 10.1029/2006gl027210CrossRefGoogle Scholar
Farrell, WM, McLain, JL, Collier, MR, Keller, JW, Jackson, TJ and Delory, GT (2015) Is the electron avalanche process in a Martian dust devil self-quenching? Icarus 254, 333337.CrossRefGoogle Scholar
Flint, DH, Tuminello, JF and Emptage, MH (1993) The inactivation of Fe-S cluster containing hydro-lyases by superoxide. Journal of Biological Chemistry 268, 2236922376.CrossRefGoogle ScholarPubMed
Flynn, GJ (1996) The delivery of organic matter from asteroids and comets to the early surface of Mars. Earth Moon and Planets 72, 469474.CrossRefGoogle Scholar
Formisano, V, Atreya, S, Encrenaz, T, Ignatiev, N and Giuranna, M (2004) Detection of methane in the atmosphere of Mars. Science (New York, N.Y.) 306, 17581761.CrossRefGoogle ScholarPubMed
Fox, AC, Eigenbrode, JL and Freeman, KH (2019) Radiolysis of macromolecular organic material in Mars relevant mineral matrices. Journal of Geophysical Research: Planets 124, 3257–3266.Google Scholar
Freissinet, C et al. (2015 a) First in situ chemistry experiments on Mars using the SAM instrument: MTBSTFA derivatization on a Martian mudstone. 46th Lunar and Planetary Science Conference.Google Scholar
Freissinet, C et al. (2015 b) Organic molecules in the Sheepbed Mudstone, Gale Crater, Mars. Journal of Geophysical Research-Planets 120, 495514.CrossRefGoogle ScholarPubMed
Fubini, B and Hubbard, A (2003) Reactive oxygen species (ROS) and reactive nitrogen species (RNS) generation by silica in inflammation and fibrosis. Free Radical Biology and Medicine 34, 15071516.CrossRefGoogle ScholarPubMed
Glasner, A and Weidenfeld, L (1952) The thermal decomposition of potassium perchlorate and perchlorate halogenide mixtures – a study in the pyrolysis of solids. Journal of the American Chemical Society 74, 24672472.CrossRefGoogle Scholar
Glavin, D et al. (2013 a) Investigating the origin of chlorohydrocarbons detected by the Sample Analysis at Mars (SAM) instrument at Rocknest. 44th Lunar and Planetary Science Conference (2013).Google Scholar
Glavin, DP et al. (2013 b) Evidence for perchlorates and the origin of chlorinated hydrocarbons detected by SAM at the Rocknest aeolian deposit in Gale Crater. Journal of Geophysical Research-Planets 118, 19551973.CrossRefGoogle Scholar
Goetz, W et al. (2016) MOMA: the challenge to search for organics and biosignatures on Mars. International Journal of Astrobiology 15, 239250.CrossRefGoogle Scholar
Gough, RV et al. (2011) Can rapid loss and high variability of Martian methane be explained by surface H2O2? Planetary and Space Science 59, 238246.CrossRefGoogle Scholar
Grotzinger, JP et al. (2012) Mars science laboratory mission and science investigation. Space Science Reviews 170, 556.CrossRefGoogle Scholar
Grotzinger, J et al. (2014) A habitable fluvio-lacustrine environment at Yellowknife Bay, Gale Crater, Mars. Science (New York, N.Y.) 343. doi: 10.1126/science.1242777.CrossRefGoogle ScholarPubMed
Hansen, AA (2007) Mars simulations – past studies on the biological response to simulated Martian conditions. In Walker, C and Fletcher, K (eds), Response of Organisms to the Martian Environment. Noordwijk, The Netherlands: ESA Communications, ESTEC, pp. 118.Google Scholar
Hansen, AA, Jensen, LL, Kristoffersen, T, Mikkelsen, K, Merrison, J, Finster, KW and Lomstein, BA (2009) Effects of long-term simulated Martian conditions on a freeze-dried and homogenized bacterial permafrost community. Astrobiology 9, 229240.CrossRefGoogle ScholarPubMed
Hartford, OM and Dowds, BCA (1994) Isolation and characterization of hydrogen-peroxide resistant mutant of Bacillus subtilis. Microbiology-Sgm 140, 297304.CrossRefGoogle ScholarPubMed
Hassler, DM et al. (2014) Mars’ surface radiation environment measured with the Mars science laboratory's curiosity rover. Science (New York, N.Y.) 343, 1244797.CrossRefGoogle ScholarPubMed
Hecht, MH et al. (2009) Detection of perchlorate and the soluble chemistry of Martian regolith at the Phoenix lander site. Science (New York, N.Y.) 325, 6467.CrossRefGoogle Scholar
Horowitz, NH, Hobby, GL and Hubbard, JS (1977) Viking on Mars – the carbon assimilation experiments. Journal of Geophysical Research 82, 46594662.CrossRefGoogle Scholar
Horsburgh, MJ, Wharton, SJ, Karavolos, M and Foster, SJ (2002) Manganese: elemental defence for a life with oxygen? Trends in Microbiology 10, 496501.CrossRefGoogle ScholarPubMed
Hu, R, Bloom, AA, Gao, P, Miller, CE and Yung, YL (2016) Hypotheses for near-surface exchange of methane on Mars. Astrobiology 16, 539550.CrossRefGoogle ScholarPubMed
Hurowitz, JA, Tosca, NJ, McLennan, SM and Schoonen, MAA (2007) Production of hydrogen peroxide in Martian and lunar regoliths. Earth and Planetary Science Letters 255, 4152.CrossRefGoogle Scholar
Inaoka, T, Matsumura, Y and Tsuchido, T (1999) SodA and manganese are essential for resistance to oxidative stress in growing and sporulating cells of Bacillus subtilis. Journal of Bacteriology 181, 19391943.CrossRefGoogle ScholarPubMed
Jang, SJ and Imlay, JA (2007) Micromolar intracellular hydrogen peroxide disrupts metabolism by damaging iron-sulfur enzymes. Journal of Biological Chemistry 282, 929937.CrossRefGoogle ScholarPubMed
Jensen, SJK et al. (2014) A sink for methane on Mars? The answer is blowing in the wind. Icarus 236, 2427.CrossRefGoogle Scholar
Keller, JM et al. (2006) Equatorial and midlatitude distribution of chlorine measured by Mars Odyssey GRS. Journal of Geophysical Research-Planets 111. https://doi.org/10.1029/2006JE002679.Google Scholar
Keppler, F, Vigano, I, McLeod, A, Ott, U, Fruchtl, M and Rockmann, T (2012) Ultraviolet-radiation-induced methane emissions from meteorites and the Martian atmosphere. Nature 486, 9396.CrossRefGoogle ScholarPubMed
Kereszturi, A and Appere, T (2014) Searching for springtime zonal liquid interfacial water on Mars. Icarus 238, 6676.CrossRefGoogle Scholar
Kereszturi, A and Gobi, S (2014) Possibility of H2O2 decomposition in thin liquid films on Mars. Planetary and Space Science 103, 153166.CrossRefGoogle Scholar
Kim, J and Park, W (2014) Oxidative stress response in Pseudomonas putida. Applied Microbiology and Biotechnology 98, 69336946.CrossRefGoogle ScholarPubMed
Klein, HP (1977) Viking biological experiments. Abstracts of Papers of the American Chemical Society 173, 5858.Google Scholar
Klein, HP (1978) Viking biological experiments on Mars. Icarus 34, 666674.CrossRefGoogle Scholar
Klein, HP (1979) Simulation of the Viking biology experiments – overview. Journal of Molecular Evolution 14, 161165.CrossRefGoogle ScholarPubMed
Klein, HP, Lederberg, J, Rich, A, Horowitz, NH, Oyama, VI and Levin, GV (1976) Viking mission search for life on Mars. Nature 262, 2427.CrossRefGoogle Scholar
Klotz, MG and Anderson, AJ (1994) The role of catalase isozymes in the culturability of the root colonizer Pseudomonas putida after exposure to hydrogen peroxide and antibiotics. Canadian Journal of Microbiology 40, 382387.CrossRefGoogle Scholar
Kminek, G and Bada, J (2006) The effect of ionizing radiation on the preservation of amino acids on Mars. Earth and Planetary Science Letters 245, 15.CrossRefGoogle Scholar
Kok, JF and Renno, NO (2009) Electrification of wind-blown sand on Mars and its implications for atmospheric chemistry. Geophysical Research Letters 36, https://doi.org/10.1029/2008GL036691.CrossRefGoogle Scholar
Korablev, O et al. (2019) No detection of methane on Mars from early ExoMars trace Gas orbiter observations. Nature 568, 517520.CrossRefGoogle ScholarPubMed
Korshunov, S and Imlay, JA (2010) Two sources of endogenous hydrogen peroxide in Escherichia coli. Molecular Microbiology 75, 13891401.CrossRefGoogle ScholarPubMed
Krashnopolsky, VA, Maillard, JP and Owen, TC (2004) Detection of methane in the Martian atmosphere: evidence for life? Icarus 172, 537547.CrossRefGoogle Scholar
La Duc, MT, Osman, S, Vaishampayan, P, Piceno, Y, Andersen, G, Spry, JA and Venkateswaran, K (2009) Comprehensive census of bacteria in clean rooms by using DNA microarray and cloning methods. Applied and Environmental Microbiology 75, 65596567.CrossRefGoogle ScholarPubMed
Lefevre, F and Forget, F (2009) Observed variations of methane on Mars unexplained by known atmospheric chemistry and physics. Nature 460, 720723.CrossRefGoogle ScholarPubMed
Lefevre, F et al. (2008) Heterogeneous chemistry in the atmosphere of Mars. Nature 454, 971975.CrossRefGoogle ScholarPubMed
Lenhart, JS, Schroeder, JW, Walsh, BW and Simmons, LA (2012) DNA repair and genome maintenance in Bacillus subtilis. Microbiology and Molecular Biology Reviews 76, 530564.CrossRefGoogle ScholarPubMed
Leshin, LA et al. (2013) Volatile, isotope, and organic analysis of Martian fines with the Mars curiosity rover. Science (New York, N.Y.) 341. doi: 10.1126/science.1238937CrossRefGoogle ScholarPubMed
Levin, GV and Straat, PA (1976) Labeled release – experiment in radiorespirometry. Origins of Life and Evolution of the Biosphere 7, 293311.CrossRefGoogle ScholarPubMed
Levin, GV and Straat, PA (1977 a) Life on Mars – Viking labeled release experiment. Biosystems 9, 165174.CrossRefGoogle ScholarPubMed
Levin, GV and Straat, PA (1977 b) Recent results from the Viking labeled release experiment on Mars. Journal of Geophysical Research 82, 46634667.CrossRefGoogle Scholar
Levin, GV and Straat, PA (1979) Completion of the Viking labeled release experiment on Mars. Journal of Molecular Evolution 14, 167183.CrossRefGoogle ScholarPubMed
Levin, GV and Straat, PA (1981) A search for a nonbiological explanation of the Viking Labeled Release life detection experiment. Icarus 45, 494516.CrossRefGoogle Scholar
Levin, GV and Straat, PA (2016) The case for extant life on Mars and its possible detection by the viking labeled release experiment. Astrobiology 16, 798810.CrossRefGoogle ScholarPubMed
Lewis, JMT et al. (2021) Pyrolysis of oxalate, acetate, and perchlorate mixtures and the implications for organic salts on Mars. Journal of Geophysical Research-Planets, 126, e2020JE006803.CrossRefGoogle Scholar
Mahaffy, PR et al. (2013) Abundance and isotopic composition of gases in the Martian atmosphere from the curiosity rover. Science (New York, N.Y.) 341, 263266.CrossRefGoogle ScholarPubMed
Mancinelli, RL and Klovstad, M (2000) Martian regolith and UV radiation: microbial viability assessment on spacecraft surfaces. Planetary and Space Science 48, 10931097.CrossRefGoogle Scholar
Mangold, N et al. (2021) Perseverance rover reveals an ancient delta-lake system and flood deposits at Jezero crater, Mars. Science (New York, N.Y.) 6568, 711–717.Google Scholar
Martin-Torres, FJ et al. (2015) Transient liquid water and water activity at Gale crater on Mars. Nature Geoscience 8, 357361.CrossRefGoogle Scholar
Mattimore, V and Battista, JR (1996) Radioresistance of Deinococcus radiodurans: functions necessary to survive ionizing radiation are also necessary to survive prolonged desiccation. Journal of Bacteriology 178, 633637.CrossRefGoogle ScholarPubMed
Melly, E, Cowan, AE and Setlow, P (2002) Studies on the mechanism of killing of Bacillus subtilis spores by hydrogen peroxide. Journal of Applied Microbiology 93, 316325.CrossRefGoogle ScholarPubMed
Melnik, O and Parrot, M (1998) Electrostatic discharge in Martian dust storms. Journal of Geophysical Research-Space Physics 103, 2910729117.CrossRefGoogle Scholar
Merrison, J et al. (2012) Factors affecting the electrification of wind-driven dust studied with laboratory simulations. Planetary and Space Science 60, 328335.CrossRefGoogle Scholar
Mielecki, D et al. (2013) Pseudomonas putida AlkA and AlkB proteins comprise different defense systems for the repair of alkylation damage to DNA – in vivo, in vitro, and in silico studies. PLoS One 8, e76198.CrossRefGoogle ScholarPubMed
Mills, AA (1977) Dust clouds and frictional generation of glow discharges on Mars. Nature 268, 614614.CrossRefGoogle Scholar
Ming, DW et al. (2014) Volatile and organic compositions of sedimentary rocks in Yellowknife Bay, Gale Crater, Mars. Science (New York, N.Y.) 343, 1245267.CrossRefGoogle ScholarPubMed
Moeller, R, Reitz, G, Berger, T, Okayasu, R, Nicholson, WL and Horneck, G (2010) Astrobiological aspects of the mutagenesis of cosmic radiation on bacterial spores. Astrobiology 10, 509521.CrossRefGoogle ScholarPubMed
Moissl-Eichinger, C, Rettberg, P and Pukall, R (2012) The first collection of spacecraft-associated microorganisms: a public source for extremotolerant microorganisms from spacecraft assembly clean rooms. Astrobiology 12, 10241034.CrossRefGoogle ScholarPubMed
Moseley, BE and Mattingly, A (1971) Repair of irradiated transforming deoxyribonu-cleic acid in wild type and a radiation- sensitive mutant of Micrococcus radiodu- rans. Journal of Bacteriology 105, 976983.CrossRefGoogle Scholar
Mumma, MJ et al. (2009) Strong release of methane on Mars in Northern summer 2003. Science (New York, N.Y.) 323, 10411045.CrossRefGoogle ScholarPubMed
Navarro-Gonzalez, R, Vargas, E, de la Rosa, J, Raga, AC and McKay, CP (2010) Reanalysis of the Viking results suggests perchlorate and organics at midlatitudes on Mars. Journal of Geophysical Research-Planets 115, E12010.CrossRefGoogle Scholar
Ojha, L et al. (2015) Spectral evidence for hydrated salts in recurring slope Lineae on Mars. Nature Geoscience 8, 829832.CrossRefGoogle Scholar
Oyama, VI and Berdahl, BJ (1977) The Viking gas exchange experiment results from Chryse and Utopia surface samples. Journal of Geophysical Research 82, 46694676.CrossRefGoogle Scholar
Oyama, VI and Berdahl, BJ (1979) Model of Martian surface-chemistry. Journal of Molecular Evolution 14, 199210.CrossRefGoogle ScholarPubMed
Oyama, VI, Berdahl, BJ, Carle, GC, Lehwalt, ME and Ginoza, HS (1976) Search for life on Mars – Viking 1976 gas changes as indicators of biological-activity. Origins of Life and Evolution of the Biosphere 7, 313333.CrossRefGoogle ScholarPubMed
Oyama, VI, Berdahl, BJ and Carle, GC (1977) Preliminary findings of Viking gas-exchange experiment and a model for Martian surface-chemistry. Nature 265, 110114.CrossRefGoogle Scholar
Paulino-Lima, IG, Pilling, S, Janot-Pacheco, E, de Brito, AN, Barbosa, J, Leitao, AC and Lage, CDS (2010) Laboratory simulation of interplanetary ultraviolet radiation (broad spectrum) and its effects on Deinococcus radiodurans. Planetary and Space Science 58, 11801187.CrossRefGoogle Scholar
Paulino-Lima, IG et al. (2011) Survival of Deinococcus radiodurans against laboratory simulated solar wind charged particles. Astrobiology 11, 875882.CrossRefGoogle ScholarPubMed
Pavlov, AA, Vasilyev, G, Ostryakov, VM, Pavlov, AK and Mahaffy, P (2012) Degradation of the organic molecules in the shallow subsurface of Mars due to irradiation by cosmic rays. Geophysical Research Letters 39, 5–9.CrossRefGoogle Scholar
Ponnamperuma, C, Shimoyama, A, Yamada, M, Hobo, T and Pal, R (1977) Possible surface-reactions on Mars – implications for Viking biology results. Science (New York, N.Y.) 197, 455457.CrossRefGoogle ScholarPubMed
Prousek, J (2007) Fenton chemistry in biology and medicine. Pure and Applied Chemistry 79, 23252338.CrossRefGoogle Scholar
Puleo, JR, Fields, ND, Bergstrom, SL, Oxborrow, GS, Stabekis, PD and Koukol, RC (1977) Microbiological profiles of Viking spacecraft. Applied and Environmental Microbiology 33, 379384.CrossRefGoogle ScholarPubMed
Quinn, RC and Zent, AP (1999) Peroxide-modified titanium dioxide: a chemical analog of putative Martian regolith oxidants. Origins of Life and Evolution of the Biosphere 29, 5972.CrossRefGoogle Scholar
Quinn, RC, Martucci, HF, Miller, SR, Bryson, CE, Grunthaner, FJ and Grunthaner, PJ (2013) Perchlorate radiolysis on Mars and the origin of martian soil reactivity. Astrobiology 13, 515520.CrossRefGoogle ScholarPubMed
Riesenman, PJ and Nicholson, WL (2000) Role of the spore coat layers in Bacillus subtilis spore resistance to hydrogen peroxide, artificial UV-C, UV-B, and solar UV radiation. Applied and Environmental Microbiology 66, 620626.CrossRefGoogle ScholarPubMed
Sagan, C and Coleman, S (1965) Spacecraft sterilization standards and contamination of Mars. Astronautics and Aeronautics 3, 2227.Google Scholar
Schuerger, AC, Mancinelli, RL, Kern, RG, Rothschild, LJ and McKay, CP (2003) Survival of endospores of Bacillus subtilis on spacecraft surfaces under simulated Martian environments: implications for the forward contamination of Mars. Icarus 165, 253276.CrossRefGoogle ScholarPubMed
Schuerger, AC, Moores, JE, Clausen, CA, Barlow, NG and Britt, DT (2012) Methane from UV-irradiated carbonaceous chondrites under simulated Martian conditions. Journal of Geophysical Research-Planets 117, E08007.CrossRefGoogle Scholar
Schulze-Makuch, D et al. (2012) The Biological Oxidant and Life Detection (BOLD) mission: a proposal for a mission to Mars. Planetary and Space Science 67, 5769.CrossRefGoogle Scholar
Seaver, LC and Imlay, JA (2004) Are respiratory enzymes the primary sources of intracellular hydrogen peroxide? Journal of Biological Chemistry 279, 4874248750.CrossRefGoogle ScholarPubMed
Setlow, B and Setlow, P (1993) Binding of small, acid-soluble spore proteins to DNA plays a significant role in the resistance of Bacillus subtilis spores to hydrogen-peroxide. Applied and Environmental Microbiology 59, 34183423.CrossRefGoogle Scholar
Setlow, B, Atluri, S, Kitchel, R, Koziol-Dube, K and Setlow, P (2006) Role of dipicolinic acid in resistance and stability of spores of Bacillus subtilis with or without DNA-protective alpha/beta-type small acid-soluble proteins. Journal of Bacteriology 188, 37403747.CrossRefGoogle ScholarPubMed
Slade, D and Radman, M (2011) Oxidative stress resistance in Deinococcus radiodurans. Microbiology and Molecular Biology Reviews 75, 133191.CrossRefGoogle ScholarPubMed
Soffen, GA and Young, AT (1972) Viking missions to Mars. Icarus 16, 116.CrossRefGoogle Scholar
Steele, A et al. (2012) A reduced organic carbon component in Martian basalts. Science (New York, N.Y.) 337, 212215.CrossRefGoogle ScholarPubMed
Steininger, H, Goesmann, F and Goetz, W (2012) Influence of magnesium perchlorate on the pyrolysis of organic compounds in Mars analog regoliths. Planetary and Space Science 71, 917.CrossRefGoogle Scholar
Stieglmeier, M, Rettberg, P, Barczyk, S, Bohmeier, M, Pukal, P, Wirt, R and Moissl-Eichinger, C (2012) Abundance and diversity of microbial inhabitance of European space-craft associated clean rooms. Astrobiology 12, 572585.CrossRefGoogle Scholar
Stillman, DE (2018) Chapter 2 – unraveling the mysteries of recurring slope lineae. In Soare, RJ, Conway, SJ and Clifford, SM (eds), Dynamic Mars. Elsevier, pp. 5185, ISBN 9780128130186. https://doi.org/10.1016/B978-0-12-813018-6.00002-9.CrossRefGoogle Scholar
Sutter, B, Ming, DB, Boynton, WV, Niles, PB, Hoffman, J, Lauer, HV and Golden, DC (2009) Summary of results from the Mars Phoenic Lander's thermal evolved gas analyzer. The New Martian Chemistry Workshop.Google Scholar
Sutter, B et al. (2017) Evolved gas analyses of sedimentary rocks and eolian sediment in Gale Crater, Mars: results of the curiosity rover's sample analysis at Mars instrument from Yellowknife Bay to the Namib Dune. Journal of Geophysical Research-Planets 122, 2574–2609.CrossRefGoogle Scholar
Szopa, C et al. (2020) First detections of dichlorobenzene isomers and trichloromethylpropane from organic matter indigenous to Mars mudstone in Gale Crater, Mars: results from the sample analysis at Mars instrument onboard the curiosity rover. Astrobiology 20, 292306.CrossRefGoogle ScholarPubMed
ten Kate, IL (2010) Organics on Mars? Astrobiology 10, 589603.CrossRefGoogle ScholarPubMed
Thøgersen, J, Bak, EN, Finster, K, Nørnberg, P, Jakobsen, HL and Jensen, SJK (2019) Light on a windy night on Mars: a study of saltation-mediated ionization of argon in a Marslike atmosphere. Icarus 332, 1418.CrossRefGoogle Scholar
Thomson, BJ and Schultz, PH (2007) The geology of the Viking lander 2 site revisited. Icarus 191, 505523.CrossRefGoogle Scholar
Tian, B, Xu, ZJ, Sun, ZT, Lin, J and Hua, YJ (2007) Evaluation of the antioxidant effects of carotenoids from Deinococcus radiodurans through targeted mutagenesis, chemiluminescence, and DNA damage analyses. Biochimica Biophysica Acta-General Subjects 1770, 902911.CrossRefGoogle ScholarPubMed
Tuleta, M, Gabla, L and Szkarlat, A (2005) Low-energy ion bombardment of frozen bacterial spores and its relevance to interplanetary space. Europhysics Letters 70, 123128.CrossRefGoogle Scholar
Vandaele, AC et al. (2019) Martian dust storm impact on atmospheric H2O and D/H observed by ExoMars trace gas orbiter. Nature 568, 521525.CrossRefGoogle Scholar
Villanueva, GL et al. (2013) A sensitive search for organics (CH4, CH3OH, H2CO, C2H6, C2H2, C2H4), hydroperoxyl (HO2), nitrogen compounds (N2O, NH3, HCN) and chlorine species (HCl, CH3Cl) on Mars using ground-based high-resolution infrared spectroscopy. Icarus 223, 1127.CrossRefGoogle Scholar
Wadsworth, J and Cockell, CS (2017) The Janus face of iron on anoxic worlds: iron oxides are both protective and destructive to life on the early Earth and present-day Mars. FEMS Microbiology Ecology 93, fix056.CrossRefGoogle ScholarPubMed
Watts, RJ, Washington, D, Howsawkeng, J, Loge, FJ and Teel, AL (2003) Comparative toxicity of hydrogen peroxide, hydroxyl radicals, and superoxide anion to Escherichia coli. Advances in Environmental Research 7, 961968.CrossRefGoogle Scholar
Webster, CR et al. (2015) Mars atmosphere. Mars methane detection and variability at Gale crater. Science (New York, N.Y.) 347, 415417.CrossRefGoogle ScholarPubMed
Withers, P (2012) Empirical estimates of Martian surface pressure in support of the landing of Mars science laboratory. Space Science Reviews 170, 837860.CrossRefGoogle Scholar
Yen, AS, Kim, SS, Hecht, MH, Frant, MS and Murray, B (2000) Evidence that the reactivity of the Martian regolith is due to superoxide ions. Science (New York, N.Y.) 289, 19091912.CrossRefGoogle Scholar
Yung, YL et al. (2018) Methane on Mars and habitability: challenges and responses. Astrobiology 18, 12211242.CrossRefGoogle ScholarPubMed
Zent, AP and McKay, CP (1994) The chemical-reactivity of the Martian regolith and implications for future missions. Icarus 108, 146157.CrossRefGoogle Scholar
Zent, AP, Ichimura, AS, Quinn, RC and Harding, HK (2008) The formation and stability of the superoxide radical (O2) on rock-forming minerals: band gaps, hydroxylation state, and implications for Mars oxidant chemistry. Journal of Geophysical Research 113, E09001.CrossRefGoogle Scholar
Zhai, Y, Cummer, SA and Farrell, WM (2006) Quasi-electrostatic field analysis and simulation of Martian and terrestrial dust devils. Journal of Geophysical Research 111, E06016.CrossRefGoogle Scholar