Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-16T07:29:22.390Z Has data issue: false hasContentIssue false
  • English
  • Français

Survival and growth of soil microbial communities under influence of sodium perchlorates

Published online by Cambridge University Press:  29 October 2020

Vladimir Cheptsov Open the ORCID record for Vladimir Cheptsov [Opens in a new window] ,
Andrey Belov ,
Olga Soloveva ,
Elena Vorobyova ,
George Osipov ,
Natalia Manucharova  and
Michael Gorlenko
Vladimir Cheptsov*
Affiliation:
Lomonosov Moscow State University, Leninskie Gory, 1, 12, Moscow, 119234, Russia Space Research Institute, Russian Academy of Sciences, Profsoyuznaya str., 84/32, Moscow, 117997, Russia Network of Researchers on the Chemical Evolution of Life, Leeds, UK
Andrey Belov
Affiliation:
Lomonosov Moscow State University, Leninskie Gory, 1, 12, Moscow, 119234, Russia Network of Researchers on the Chemical Evolution of Life, Leeds, UK
Olga Soloveva
Affiliation:
Lomonosov Moscow State University, Leninskie Gory, 1, 12, Moscow, 119234, Russia
Elena Vorobyova
Affiliation:
Lomonosov Moscow State University, Leninskie Gory, 1, 12, Moscow, 119234, Russia Network of Researchers on the Chemical Evolution of Life, Leeds, UK
George Osipov
Affiliation:
International Analytical Center, Interlab, N.D. Zelinsky Institute of Organic Chemistry, Leninsky Prospekt, 47, Moscow, 119991, Russia
Natalia Manucharova
Affiliation:
Lomonosov Moscow State University, Leninskie Gory, 1, 12, Moscow, 119234, Russia
Michael Gorlenko
Affiliation:
Lomonosov Moscow State University, Leninskie Gory, 1, 12, Moscow, 119234, Russia
*
Author for correspondence: Vladimir Cheptsov, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Previously conducted space missions revealed the presence of perchlorates, which are known to have a high oxidizing potential in Martian regolith, at the level of 0.5%. Due to hygroscopic properties and crystallization features of perchlorate-containing solutions, assumptions leading to the possibility of the existence of liquid water in the form of brines, which can contribute to the vital activity of microorganisms, have been made. At the same time, high concentrations of perchlorates can inhibit the growth of microorganisms and cause their death. Previously performed studies have discovered the presence of highly diverse microbial communities in terrestrial perchlorate-containing soils and have also demonstrated the stability and activity of some prokaryotes cultured on highly concentrated perchlorates media (over 10%). Nevertheless, the limits of microbial tolerance to perchlorates and whether microbial communities are able to withstand the effects of high concentrations of perchlorates remain uncertain. The aim of this research was to study the reaction of microbial communities of hot-arid and cryo-arid soils and sedimentary rocks to the adding of a highly concentrated solution of sodium perchlorate (5%) in situ. An increase in the total number of prokaryotes, the number of metabolically active Bacteria and Archaea, and the variety of the consumed substrates were revealed. It was observed that in samples incubated with sodium perchlorate, a high taxonomic diversity of the microbial community is preserved at a level comparable to control sample. The study shows that the presence of high concentrations of sodium perchlorate (5%) in the soil does not lead to the death or significant inhibition of microbial communities.

Keywords

Marsmetabolic activitymicroorganismsoxidative stresstolerance
Type
Research Article
Information
International Journal of Astrobiology , Volume 20 , Issue 1 , February 2021 , pp. 36 - 47
Check for updates
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

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

References

Al Soudi, A, Farhat, O, Chen, F, Clark, B and Schneegurt, M (2017) Bacterial growth tolerance to concentrations of chlorate and perchlorate salts relevant to Mars. International Journal of Astrobiology 16, 229–235.CrossRefGoogle Scholar
Amann, R and Ludwig, W (2000) Ribosomal RNA-targeted nucleic acid probes for studies in microbial ecology. FEMS Microbiology Reviews 24, 555–565.CrossRefGoogle ScholarPubMed
Anupama, V, Prajeesh, P, Anju, S, Priya, P and Krishnakumar, B (2015) Diversity of bacteria, archaea and protozoa in a perchlorate treating bioreactor. Microbiological Research 177, 8–14.CrossRefGoogle Scholar
Bardiya, N and Bae, J (2011) Dissimilatory perchlorate reduction: a review. Microbiological Research 166, 237–254.CrossRefGoogle ScholarPubMed
Beblo-Vranesevic, K, Bohmeier, M, Perras, A, Schwendner, P, Rabbow, E, Moissl-Eichinger, C, Cockell, C, Pukall, R, Vannier, P, Marteinsson, V, Monaghan, E, Ehrenfreund, P, Garcia-Descalzo, L, Gómez, F, Malki, M, Amils, R, Gaboyer, F, Westall, F, Cabezas, P, Walter, N and Rettberg, P (2017 a) The responses of an anaerobic microorganism, Yersinia intermedia MASE-LG-1 to individual and combined simulated Martian stresses. PLoS ONE 12, e0185178.CrossRefGoogle ScholarPubMed
Beblo-Vranesevic, K, Huber, H and Rettberg, P (2017 b) High tolerance of Hydrogenothermus marinus to sodium perchlorate. Frontiers in Microbiology 8, 1369.CrossRefGoogle ScholarPubMed
Beblo-Vranesevic, K, Bohmeier, M, Schleumer, S, Rabbow, E, Perras, A, Moissl-Eichinger, C, Schwendner, P, Cockell, C, Vannier, P, Marteinsson, V, Monaghan, E, Riedo, A, Ehrenfreund, P, Garcia-Descalzo, L, Gómez, F, Malki, M, Amils, R, Gaboyer, F, Hickman-Lewis, K, Westall, F, Cabezas, P, Walter, N and Rettberg, P (2020) Impact of simulated Martian conditions on (facultatively) anaerobic bacterial strains from different Mars analogue sites. Current Issues in Molecular Biology 38, 103–122.CrossRefGoogle ScholarPubMed
Belov, AA, Cheptsov, VS and Vorobyova, EA (2018) Soil bacterial communities of Sahara and Gibson deserts: physiological and taxonomical characteristics. AIMS Microbiology 4, 685.CrossRefGoogle ScholarPubMed
Belov, AA, Cheptsov, VS, Vorobyova, EA, Manucharova, NA and Ezhelev, ZS (2019) Stress-tolerance and taxonomy of culturable bacterial communities isolated from a central mojave desert soil sample. Geosciences 9, 166.CrossRefGoogle Scholar
Belov, AA, Cheptsov, VS, Manucharova, NA and Ezhelev, ZS (2020 a) Bacterial communities of Novaya Zemlya archipelago ice and permafrost. Geosciences 10, 67.CrossRefGoogle Scholar
Belov, AA, Cheptsov, VS, Vorobyova, EA, Manucharova, NA and Ezhelev, ZS (2020 b) Culturable bacterial communities isolated from cryo-arid soils: phylogenetic and physiological characteristics. Paleontological Journal 54, 95–104.CrossRefGoogle Scholar
Cabiscol Català, E, Tamarit Sumalla, J and Ros Salvador, J (2000) Oxidative stress in bacteria and protein damage by reactive oxygen species. International Microbiology 3, 3–8.Google Scholar
Calderon, R, Palma, P, Parker, D, Molina, M, Godoy, F and Escudey, M (2014) Perchlorate levels in soil and waters from the Atacama Desert. Archives of Environmental Contamination and Toxicology 66, 155–161.CrossRefGoogle ScholarPubMed
Carrier, B and Kounaves, S (2015) The origins of perchlorate in the Martian soil. Geophysical Research Letters 42, 3739–3745.CrossRefGoogle Scholar
Catling, D, Claire, M, Zahnle, K, Quinn, R, Clark, B, Hecht, M and Kounaves, S (2010) Atmospheric origins of perchlorate on Mars and in the Atacama. Journal of Geophysical Research: Planets 115, E1.CrossRefGoogle Scholar
Chattopadhyay, M, Raghu, G, Sharma, Y, Biju, A, Rajasekharan, M and Shivaji, S (2011) Increase in oxidative stress at low temperature in an Antarctic bacterium. Current Microbiology 62, 544–546.CrossRefGoogle Scholar
Cheptsov, VS, Vorobyova, EA, Manucharova, NA, Gorlenko, MV, Pavlov, AK, Vdovina, MA, Lomasov, VN and Bulat, SA (2017) 100 kGy gamma-affected microbial communities within the ancient Arctic permafrost under simulated Martian conditions. Extremophiles 21, 1057–1067.CrossRefGoogle ScholarPubMed
Cheptsov, VS, Vorobyova, E, Belov, AA, Pavlov, AK, Tsurkov, DA, Lomasov, VN and Bulat, SA (2018 a) Survivability of soil and permafrost microbial communities after irradiation with accelerated electrons under simulated Martian and open space conditions. Geosciences 8, 298.CrossRefGoogle Scholar
Cheptsov, VS, Vorobyova, EA, Osipov, GA, Manucharova, NA, Polyanskaya, LM, Gorlenko, MV, Pavlov, AK, Rosanova, MS and Lomasov, VN (2018 b) Microbial activity in Martian analog soils after ionizing radiation: implications for the preservation of subsurface life on Mars. AIMS Microbiology 4, 541.CrossRefGoogle ScholarPubMed
Cheptsov, VS, Vorobyova, EA, Polyanskaya, LM, Gorlenko, MV, Pavlov, AK and Lomasov, VN (2018 c) Sustainability of extreme microbial ecosystems to the comprehensive impact of physical factors of the Martian regolith. Moscow University Soil Science Bulletin 73, 119–123.CrossRefGoogle Scholar
Cheptsov, VS, Vorobyova, EA, Gorlenko, MV, Manucharova, NA, Pavlov, AK and Lomasov, VN (2018 d) Effect of gamma radiation on viability of a soil microbial community under conditions of Mars. Paleontological Journal 52, 1217–1223.CrossRefGoogle Scholar
Cheptsov, VS, Belov, AA, Vorobyova, EA, Osipov, GA and Bulat, SA (2019) Viability of the soddy–podzolic soil microbial community after 148–1250 kGy gamma irradiation. Planetary and Space Science 172, 8–13.CrossRefGoogle Scholar
Chernov, IY and Lysak, LV (2008) Methodical Materials for Seminars on the Course General Ecology. Russia, Moscow: Maks Press, p. 77.Google Scholar
Chevrier, V and Rivera-Valentin, E (2012) Formation of recurring slope lineae by liquid brines on present-day Mars. Geophysical Research Letters 39, L21202.CrossRefGoogle Scholar
Chevrier, V, Hanley, J and Altheide, T (2009) Stability of perchlorate hydrates and their liquid solutions at the Phoenix landing site, Mars. Geophysical Research Letters 36, L10202.CrossRefGoogle Scholar
Connon, S, Lester, E, Shafaat, H, Obenhuber, D and Ponce, A (2007) Bacterial diversity in hyperarid Atacama Desert soils. Journal of Geophysical Research-Biogeosciences 112, G4.CrossRefGoogle Scholar
Davila, A, Willson, D, Coates, J and McKay, C (2013) Perchlorate on Mars: a chemical hazard and a resource for humans. International Journal of Astrobiology 12, 321–325.CrossRefGoogle Scholar
Diehl, D (2013) Soil water repellency: dynamics of heterogeneous surfaces. Colloids and Surfaces A 432, 8–18.CrossRefGoogle Scholar
DiRuggiero, J, Wierzchos, J, Robinson, C, Souterre, T, Ravel, J, Artieda, O, Souza-Egipsy, V and Ascaso, C (2013) Microbial colonisation of chasmoendolithic habitats in the hyper-arid zone of the Atacama Desert. Biogeosciences (Online) 10, 2439–2450.CrossRefGoogle Scholar
Drees, K, Neilson, J, Betancourt, J, Quade, J, Henderson, D, Pryor, B and Maier, R (2006) Bacterial community structure in the hyperarid core of the Atacama Desert, Chile. Applied and Environmental Microbiology 72, 7902–7908.CrossRefGoogle ScholarPubMed
Dundas, CM, McEwen, AS, Chojnacki, M, Milazzo, MP, Byrne, S, McElwaine, JN and Urso, A (2017) Granular flows at recurring slope lineae on Mars indicate a limited role for liquid water. Nature Geoscience 10, 903–907.CrossRefGoogle Scholar
Fierer, N, Leff, J, Adams, B, Nielsen, U, Bates, S, Lauber, C, Owens, S, Gilbert, J, Wall, D and Caporaso, G (2012) Cross-biome metagenomic analyses of soil microbial communities and their functional attributes. Proceedings of the National Academy of Sciences of the USA 109, 21390–21395.CrossRefGoogle ScholarPubMed
Gilichinsky, D, Wilson, G, Friedmann, E, Mckay, C, Sletten, R, Rivkina, E, Vishnivetskaya, T, Erokhina, L, Ivanushkina, N, Kochkina, G, Shcherbakova, V, Soina, V, Spirina, E, Vorobyova, E, Fyodorov-Davydov, D, Hallet, B, Ozerskaya, S, Sorokovikov, V, Laurinavichyus, K, Shatilovich, A, Chanton, J, Ostroumov, V and Tiedje, J (2007) Microbial populations in Antarctic permafrost: biodiversity, state, age and implication for astrobiology. Astrobiology 7, 275–311.CrossRefGoogle ScholarPubMed
Goordial, J, Davila, A, Greer, C, Cannam, R, DiRuggiero, J, McKay, C and Whyte, L (2017) Comparative activity and functional ecology of permafrost soils and lithic niches in a hyper-arid polar desert. Environmental Microbiology 19, 443–458.CrossRefGoogle Scholar
Grigoriev, A, Vorobyova, E and Cheptsov, V (2017) Application of ATR spectroscopy for astrobiological investigations aboard planetary landers. Moscow University Soil Science Bulletin 72, 136–141.CrossRefGoogle Scholar
Groemer, G, Soucek, A, Frischauf, N, Stumptner, W, Ragonig, C, Sams, S, Bartenstein, T, Häuplik-Meusburger, S, Petrova, P, Evetts, S, Sivenesan, C, Bothe, C, Boyd, A, Dinkelaker, A, Dissertori, M, Fasching, D, Fischer, M, Föger, D, Foresta, L, Fritsch, L, Fuchs, H, Gautsch, C, Gerard, S, Goetzloff, L, Gołębiowska, I, Gorur, P, Groemer, G, Groll, P, Haider, C, Haider, O, Hauth, E, Hauth, S, Hettrich, S, Jais, W, Jones, N, Taj-Eddine, K, Karl, A, Kauerhoff, T, Khan, M, Kjeldsen, A, Klauck, J, Losiak, A, Luger, M, Luger, T, Luger, U, McArthur, J, Moser, L, Neuner, J, Orgel, C, Ori, G, Paternesi, R, Peschier, J, Pfeil, I, Prock, S, Radinger, J, Ramirez, B, Ramo, W, Rampey, M, Sams, A, Sams, E, Sandu, O, Sans, A, Sansone, P, Scheer, D, Schildhammer, D, Scornet, Q, Sejkora, N, Stadler, A, Stummer, F, Taraba, M, Tlustos, R, Toferer, E, Turetschek, T, Winter, E and Zanella-Kux, K (2014) The MARS2013 Mars analog mission. Astrobiology 14, 360–376.CrossRefGoogle ScholarPubMed
Harrison, J, Gheeraert, N, Tsigelnitskiy, D and Cockell, C (2013) The limits for life under multiple extremes. Trends in Microbiology 21, 204–212.CrossRefGoogle ScholarPubMed
Hecht, M, Kounaves, S, Quinn, R, West, S, Young, S, Ming, D, Catling, D, Clark, B, Boynton, W, Hoffman, J, DeFlores, L, Gospodinova, K, Kapit, J and Smith, P (2009) Detection of perchlorate and the soluble chemistry of Martian soil at the Phoenix lander site. Science 325, 64–67.CrossRefGoogle ScholarPubMed
Heinz, J, Waajen, A, Airo, A, Alibrandi, A, Schirmack, J and Schulze-Makuch, D (2019) Bacterial growth in chloride and perchlorate brines: halotolerances and salt stress responses of Planococcus halocryophilus. Astrobiology 19, 1377–1387.CrossRefGoogle ScholarPubMed
Heinz, J, Krahn, T and Schulze-Makuch, D (2020) A new record for microbial perchlorate tolerance: fungal growth in NaClO4 brines and its implications for putative life on mars. Life 10, 53.CrossRefGoogle ScholarPubMed
Hennings, E, Heinz, J, Schmidt, H and Voigt, W (2013) Freezing and hydrate formation in aqueous sodium perchlorate solutions. Zeitschrift für Anorganische und Allgemeine Chemie 639, 922–927.CrossRefGoogle Scholar
Impey, C and Henry, H (2016) Dreams of Other Worlds: the Amazing Story of Unmanned Space Exploration. Princeton, New Jersey, USA: Princeton University Press, p. 449.CrossRefGoogle Scholar
Kral, TA, Goodhart, TH, Harpool, JD, Hearnsberger, CE, McCracken, GL and McSpadden, SW (2016) Sensitivity and adaptability of methanogens to perchlorates: implications for life on Mars. Planetary and Space Science 120, 87–95.CrossRefGoogle Scholar
Liebensteiner, M, Pinkse, M, Schaap, P, Stams, A and Lomans, B (2013) Archaeal (per) chlorate reduction at high temperature: an interplay of biotic and abiotic reactions. Science 340, 85–87.CrossRefGoogle ScholarPubMed
Logan, B, Zhang, H, Mulvaney, P, Milner, M, Head, I and Unz, R (2001) Kinetics of perchlorate- and chlorate-respiring bacteria. Applied and Environmental Microbiology 67, 2499–2506.CrossRefGoogle ScholarPubMed
Lybrand, R, Michalski, G, Graham, R and Parker, D (2013) The geochemical associations of nitrate and naturally formed perchlorate in the Mojave Desert, California, USA. Geochimica et Cosmochimica Acta 104, 136–147.CrossRefGoogle Scholar
Manucharova, N, Vlasenko, A, Men'ko, E and Zvyagintsev, D (2011) Specificity of the chitinolytic microbial complex of soils incubated at different temperatures. Microbiology 80, 205–215.CrossRefGoogle ScholarPubMed
Matsubara, T, Fujishima, K, Saltikov, C, Nakamura, S and Rothschild, L (2017) Earth analogues for past and future life on Mars: isolation of perchlorate resistant halophiles from Big Soda Lake. International Journal of Astrobiology 16, 218–228.CrossRefGoogle Scholar
Mohammadipanah, F and Wink, J (2016) Actinobacteria from arid and desert habitats: diversity and biological activity. Frontiers in Microbiology 6, 1541.CrossRefGoogle ScholarPubMed
Möhlmann, D and Thomsen, K (2011) Properties of cryobrines on Mars. Icarus 212, 123–130.CrossRefGoogle Scholar
Musilova, M, Wright, G, Ward, J and Dartnell, L (2015) Isolation of radiation-resistant bacteria from Mars analog Antarctic Dry Valleys by preselection, and the correlation between radiation and desiccation resistance. Astrobiology 15, 1076–1090.CrossRefGoogle ScholarPubMed
Navarro-Gonzalez, R, Sutter, B, Archer, D, Ming, D, Eigenbrode, J, Franz, H, Glavin, D, McAdam, A, Stern, J, McKay, C, Coll, P, Cabane, M, Conrad, P, Mahaffy, P, Martín-Torres, F, Zorzano-Mier, M and Grotzinger, J (2013) Possible detection of perchlorates by the Sample Analysis at Mars (SAM) Instrument: comparison with previous missions. EGU General Assembly Conference Abstracts 15, 6529.Google Scholar
Neilson, J, Quade, J, Ortiz, M, Nelson, W, Legatzki, A, Tian, F, LaComb, M, Betancourt, J, Wing, R, Soderlund, C and Maier, R (2012) Life at the hyperarid margin: novel bacterial diversity in arid soils of the Atacama Desert, Chile. Extremophiles 16, 553–566.CrossRefGoogle ScholarPubMed
Nicholson, W, McCoy, L, Kerney, K, Ming, D, Golden, D and Schuerger, A (2012) 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 220, 904–910.CrossRefGoogle Scholar
Ojha, L, Wilhelm, M, Murchie, S, McEwen, A, Wray, J, Hanley, J, Masse, M and Chojnacki, M (2015) Spectral evidence for hydrated salts in recurring slope lineae on Mars. Nature Geoscience 8, 829–832.CrossRefGoogle Scholar
Okeke, B, Giblin, T and Frankenberger, W (2002) Reduction of perchlorate and nitrate by salt tolerant bacteria. Environmental Pollution 118, 357–363.CrossRefGoogle ScholarPubMed
Oren, A (2014) Halophilic archaea on Earth and in space: growth and survival under extreme conditions. Philosophical Transactions of the Royal Society A 372, 20140194.CrossRefGoogle ScholarPubMed
Parro, V, de Diego-Castilla, G, Moreno-Paz, M, Blanco, Y, Cruz-Gil, P, Rodríguez-Manfredi, J, Fernández-Remolar, D, Gómez, F, Gómez, M, Rivas, L, Demergasso, C, Echeverría, A, Urtuvia, V, Ruiz-Bermejo, M, García-Villadangos, M, Postigo, M, Sánchez-Román, M, Chong-Díaz, G and Gómez-Elvira, J (2011) A microbial oasis in the hypersaline Atacama subsurface discovered by a life detector chip: implications for the search for life on Mars. Astrobiology 11, 969–996.CrossRefGoogle ScholarPubMed
Preston, L and Dartnell, L (2014) Planetary habitability: lessons learned from terrestrial analogues. International Journal of Astrobiology 13, 81–98.CrossRefGoogle Scholar
Primm, K, Gough, R, Chevrier, V and Tolbert, M (2017) Freezing of perchlorate and chloride brines under Mars-relevant conditions. Geochimica et Cosmochimica Acta 212, 211–220.CrossRefGoogle Scholar
Quinn, R, Martucci, H, Miller, S, Bryson, C, Grunthaner, F and Grunthaner, P (2013) Perchlorate radiolysis on Mars and the origin of Martian soil reactivity. Astrobiology 13, 515–520.CrossRefGoogle ScholarPubMed
Rath, KM, Maheshwari, A, Bengtson, P and Rousk, J (2016) Comparative toxicities of salts on microbial processes in soil. Applied and Environmental Microbiology 82, 2012–2020.CrossRefGoogle ScholarPubMed
Rousk, J, Elyaagubi, FK, Jones, DL and Godbold, DL (2011) Bacterial salt tolerance is unrelated to soil salinity across an arid agroecosystem salinity gradient. Soil Biology & Biochemistry 43, 1881–1887.CrossRefGoogle Scholar
Schmidt, F, Andrieu, F, Costard, F, Kocifaj, M and Meresescu, AG (2017) Formation of recurring slope lineae on Mars by rarified gas-triggered granular flows. Nature Geoscience 10, 270–273.CrossRefGoogle Scholar
Serrano, P, Alawi, M, de Vera, J and Wagner, D (2019) Response of methanogenic archaea from Siberian permafrost and non-permafrost environments to simulated Mars-like desiccation and the presence of perchlorate. Astrobiology 19, 197–208.CrossRefGoogle ScholarPubMed
Shcherbakova, V, Oshurkova, V and Yoshimura, Y (2015) The effects of perchlorates on the permafrost methanogens: implication for autotrophic life on Mars. Microorganisms 3, 518–534.CrossRefGoogle ScholarPubMed
Shekhovtsova, N, Osipov, G, Verkhovtseva, N and Pevzner, L (2003) Analysis of lipid biomarkers in rocks of the Archean crystalline basement. Instruments Methods, and Missions for Astrobiology VI 4939, 160–168.CrossRefGoogle Scholar
Smith, H and McKay, C (2005) Drilling in ancient permafrost on Mars for evidence of a second genesis of life. Planetary and Space Science 53, 1302–1308.CrossRefGoogle Scholar
Soina, VS and Vorobyova, EA (2004) Adaptation of bacteria to the Terrestrial Permafrost Environment, Origins. Dordrecht: Springer, pp. 427–444.Google Scholar
Soina, V, Mulyukin, A, Demkina, E, Vorobyova, E and El-Registan, G (2004 a) The structure of resting bacterial populations in soil and subsoil permafrost. Astrobiology 4, 345–358.CrossRefGoogle ScholarPubMed
Sugden, D, Marchant, D, Potter, N, Souchez, R, Denton, G, Swisher, C and Tison, J (1995) Preservation of Miocene glacier ice in East Antarctica. Nature 376, 412–414.CrossRefGoogle Scholar
Takai, K (2019) Limits of Terrestrial Life and Biosphere, Astrobiology. Singapore: Springer, pp. 323–344.Google Scholar
Toner, J, Catling, D and Light, B (2014) The formation of supercooled brines, viscous liquids, and low-temperature perchlorate glasses in aqueous solutions relevant to Mars. Icarus 233, 36–47.CrossRefGoogle Scholar
Turova, E and Osipov, G (1996) Structure of the microbial community transforming iron minerals contained in kaolin. Microbiology (Reading, England) 65, 682–689.Google Scholar
van der Linde, K, Lim, B, Rondeel, J, Antonissen, L and de Jong, G (1999) Improved bacteriological surveillance of haemodialysis fluids: a comparison between Tryptic soy agar and Reasoner's 2A media. Nephrology, Dialysis, Transplantation 14, 2433–2437.CrossRefGoogle ScholarPubMed
Wadsworth, J and Cockell, C (2017) Perchlorates on Mars enhance the bacteriocidal effects of UV light. Scientific Reports 7, 1–8.CrossRefGoogle ScholarPubMed
Wassmann, M, Moeller, R, Reitz, G and Rettberg, P (2010) Adaptation of Bacillus subtilis cells to Archean-like UV climate: relevant hints of microbial evolution to remarkably increased radiation resistance. Astrobiology 10, 605–615.CrossRefGoogle ScholarPubMed
Wichern, J, Wichern, F and Joergensen, RG (2006) Impact of salinity on soil microbial communities and the decomposition of maize in acidic soils. Geoderma 137, 100–108.CrossRefGoogle Scholar
Wierzchos, J, Ríos, A and Ascaso, C (2012) Microorganisms in desert rocks: the edge of life on Earth. International Microbiology 15, 171–181.Google ScholarPubMed