Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-24T00:53:48.217Z Has data issue: false hasContentIssue false
  • English
  • Français

Bacterial growth in saturated and eutectic solutions of magnesium sulphate and potassium chlorate with relevance to Mars and the ocean worlds

Published online by Cambridge University Press:  28 January 2019

Jonathan M. Wilks ,
Fei Chen ,
Benton C. Clark  and
Mark A. Schneegurt
Jonathan M. Wilks
Affiliation:
Department of Biological Sciences, Wichita State University, Wichita, KS, USA
Fei Chen
Affiliation:
Planetary Protection Group, Jet Propulsion Laboratory, Pasadena CA, USA;
Benton C. Clark
Affiliation:
Space Science Institute, Boulder CO, USA
Mark A. Schneegurt*
Affiliation:
Department of Biological Sciences, Wichita State University, Wichita, KS, USA
*
Author for correspondence: Mark A. Schneegurt, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Liquid water on Mars might be created by deliquescence of hygroscopic salts or by permafrost melts, both potentially forming saturated brines. Freezing point depression allows these heavy brines to remain liquid in the near-surface environment for extended periods, perhaps as eutectic solutions, at the lowest temperatures and highest salt concentrations where ices and precipitates do not form. Perchlorate and chlorate salts and iron sulphate form brines with low eutectic temperatures and may persist under Mars near-surface conditions, but are chemically harsh at high concentrations and were expected to be incompatible with life, while brines of common sulphate salts on Mars may be more suitable for microbial growth. Microbial growth in saturated brines also may be relevant beyond Mars, to the oceans of Ceres, Enceladus, Europa and Pluto. We have previously shown strong growth of salinotolerant bacteria in media containing 2M MgSO4 heptahydrate (~50% w/v) at 25°C. Here we extend those observations to bacterial isolates from Basque Lake, BC and Hot Lake, WA, that grow well in saturated MgSO4 medium (67%) at 25°C and in 50% MgSO4 medium at 4°C (56% would be saturated). Psychrotolerant, salinotolerant microbes isolated from Basque Lake soils included Halomonas and Marinococcus, which were identified by 16S rRNA gene sequencing and characterized phenetically. Eutectic liquid medium constituted by 43% MgSO4 at −4°C supported copious growth of these psychrotolerant Halomonas isolates, among others. Bacterial isolates also grew well at the eutectic for K chlorate (3% at −3°C). Survival and growth in eutectic solutions increases the possibility that microbes contaminating spacecraft pose a contamination risk to Mars. The cold brines of sulphate and (per)chlorate salts that may form at times on Mars through deliquescence or permafrost melt have now been demonstrated to be suitable microbial habitats, should appropriate nutrients be available and dormant cells become vegetative.

Keywords

AstrobiologydeliquescenceepsotoleranceextremophileshabitabilityhalotoleranceMarsplanetary protectionpsychrotolerantsalinotolerance
Type
Research Article
Information
International Journal of Astrobiology , Volume 18 , Issue 6 , December 2019 , pp. 502 - 509
Copyright
Copyright © Cambridge University Press 2019 

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, AF, Farhat, O, Chen, F, Clark, BC and Schneegurt, MA (2017) Bacterial growth tolerance to concentrations of chlorate and perchlorate salts relevant to Mars. International Journal of Astrobiology 16, 229–235.Google Scholar
Bakermans, C (2017) Determining the limits of microbial life at subzero temperatures. In Margesin, R (ed.) Psychrophiles: From Biodiversity to Biotechnology, 2nd Edn. Basil, Switzerland: Springer, pp. 21–38.Google Scholar
Caton, TM, Witte, LR, Ngyuen, HD, Buchheim, JA, Buchheim, MA and Schneegurt, MA (2004) Halotolerant aerobic heterotrophic bacteria from the Great Salt Plains of Oklahoma. Microbial Ecology 48, 449–462.Google Scholar
Chevrier, VF and Altheide, TS (2008) Low temperature aqueous ferric sulfate solutions on the surface of Mars. Geophysical Research Letters 35, L22101.Google Scholar
Chevrier, VF, Hanley, J and Altheide, TS (2009) Stability of perchlorate hydrates and their liquid solutions at the Phoenix landing site, Mars. Geophysical Research Letters 36, L10202.Google Scholar
Clark, BC and Kounaves, SP (2016) Evidence for the distribution of perchlorates on Mars. International Journal of Astrobiology 15, 311–318.Google Scholar
Clarke, A, Morris, GJ, Fonseca, F, Murray, BJ, Acton, E and Price, HC (2013) A low temperature limit for life on Earth. PLoS ONE 8, e66207.Google Scholar
Crisler, JD, Newville, TM, Chen, F, Clark, BC and Schneegurt, MA (2012) Bacterial growth at the high concentrations of magnesium sulfate found in Martian soils. Astrobiology 12, 98–106.Google Scholar
Crisler, JD, Chen, F, Clark, BC and Schneegurt, MA (2018) Numerical taxonomy and phylogenetic analyses of the microbial community of epsomic Basque Lake, BC. Abstracts and Program, 118th General Meeting of the American Society for Microbiology, Atlanta, June 2018.Google Scholar
Davila, AF, Duport, LG, Melchiorri, R, Jänchen, J, Valea, S, de los Rios, A, Fairén, AG, Möhlmann, D, McKay, CP, Ascaso, C and Wierzchos, J (2010) Hygroscopic salts and the potential for life on Mars. Astrobiology 10, 617–628.Google Scholar
Eberl, TC and Schneegurt, MA (2015) Isolation and characterization of bacterial communities in the clean room environment of NASA's Jet Propulsion Laboratory-spacecraft assembly facility in Pasadena, CA. Proceedings: 11th Annual Research Symposium on Graduate Research and Scholarly Projects, Wichita, KS, April 2015.Google Scholar
Echigo, A, Hino, M, Fukushima, T, Mizuki, T, Kamekura, M and Usami, R (2005) Endospores of halophilic bacteria of the family Bacillaceae isolated from non-saline Japanese soil may be transported by Kosa event (Asian dust storm). Saline Systems 1, 8.Google Scholar
Edwards, U, Rogall, H, Blöcker, H, Emde, M and Böttger, EC (1989) Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Research 17, 7843–7853.Google Scholar
Fonseca, F, Meneghei, J, Cenard, S, Passot, S and Morris, GJ (2016) Determination of intracellular vitrification temperatures for unicellular micro organisms under conditions relevant for cryopreservation. PLoS ONE 11, e0152939.Google Scholar
Fox-Powell, MG and Cockell, CS (2018) Building a geochemical view of microbial salt tolerance: halophilic adaptation of Marinococcus in a natural magnesium sulfate brine. Frontiers in Microbiology 9, 739.Google Scholar
Fredsgaard, C, Moore, DB, Chen, F, Clark, BC and Schneegurt, MA (2017) Prevalence of sucretolerant bacteria in common soils and their isolation and characterization. Antonie van Leeuwenhoek 110, 995–1005.Google Scholar
Gendrin, A, Mangold, N, Bibring, JP and Langevin, Y (2005) Sulfates in Martian layered terrains: the OMEGA/Mars express view. Science 307, 1587–1591.Google Scholar
Grant, WD (2004) Life at low water activity. Philosophical Transactions of the Royal Society of London. Series B 359, 1249–1267.Google Scholar
Hammer, UT (1978) The saline lakes of Saskatchewan. III. Chemical characterization. International Review of Hydrobiology 63, 311–335.Google Scholar
Hammer, UT (1986) Saline Lake Ecosystems of the World. Dordrecht: Junk.Google Scholar
Hanley, J, Chevrier, VF, Berget, DJ and Adams, RD (2012) Chlorate salts and solutions on Mars. Geophysical Research Letters 39, L08201.Google Scholar
Haynes, RC and Hammer, UT (1978) The saline lakes of Saskatchewan. IV. Primary production by phytoplankton in selected saline ecosystems. International Review of Hydrobiology 63, 337–351.Google Scholar
Hecht, MH, Kounaves, SP, Quinn, RC, West, SJ, Young, SMM, Ming, DW, Catling, DC, Clark, BC, Boynton, WV, Hoffman, J, DeFlores, LP, Gospodinova, K, Kapit, J and Smith, PH (2009) Detection of perchlorate and the soluble chemistry of Martian soil at the Phoenix Lander site. Science 325, 64–67.Google Scholar
Hu, R, Bloom, AA, Gao, P, Miller, CE and Yung, YL (2016) Hypotheses for near-surface exchange of methane on Mars. Astrobiology 16, 539–550.Google Scholar
Jackson, WA, Böhlke, JK, Andraski, BJ, Fahlquist, L, Bexfield, L, Eckardt, FD, Gates, JB, Davila, AF, McKay, CP, Rao, B and Sevanthi, R (2015) Global patterns and environmental controls of perchlorate and nitrate co-occurrence in arid and semi-arid environments. Geochimica et Cosmochimica Acta 164, 502–522.Google Scholar
Kezao, C and Bowler, JM (1986) Late Pleistocene evolution of salt lakes in the Qaidam basin, Qinghai province, China. Palaeogeography, Palaeoclimatology, Palaeoecology 54, 87–104.Google Scholar
Kilmer, BR, Eberl, TC, Cunderla, B, Chen, F, Clark, BC and Schneegurt, MA (2014) Molecular and phenetic characterization of the bacterial assemblage of Hot Lake, WA, an environment with high concentrations of magnesium sulphate, and its relevance to Mars. International Journal of Astrobiology 13, 69–80.Google Scholar
Kounaves, SP, Hecht, MH, Kapit, J, Gospodinova, K, DeFlores, L, Quinn, RC, Boynton, WV, Clark, BC, Catling, DC, Hredzak, P, Ming, DW, Moore, Q, Shusterman, J, Stroble, S, West, SJ and Young, SMM (2010) Wet chemistry experiments on the 2007 Phoenix Mars Scout Lander mission: data analysis and results. Journal of Geophysical Research 115, E00E10.Google Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.Google Scholar
Last, WM and Ginn, FM (2005) Saline systems of the Great Plains of western Canada: an overview of the limnogeology and paleolimnology. Saline Systems 1, 10.Google Scholar
Last, WM and Slezak, LA (1988) The salt lakes of western Canada: a paleolimnological overview. Hydrobiologia 158, 310–316.Google Scholar
Litzner, BR, Caton, TM and Schneegurt, MA (2006) Carbon substrate utilization, antibiotic sensitivity, and numerical taxonomy of bacterial isolates from the Great Salt Plains of Oklahoma. Archives of Microbiology 185, 286–296.Google Scholar
Mellon, MT, Feldman, WC and Prettyman, TH (2004) The presence and stability of ground ice in the southern hemisphere of Mars. Icarus 169, 324–340.Google Scholar
Ming, DW, Archer, PD Jr, Glavin, DP, Eigenbrode, JL, Franz, HB, Sutter, B, Brunner, AE, Stern, JC, Freissinet, C, McAdam, AC, Mahaffy, PR, Cabane, M, Coll, P, Campbell, JL, Atreya, SK, Niles, PB, Bell, JF 3rd, Bish, DL, Brinckerhoff, WB, Buch, A, Conrad, PG, Des Marais, DJ, Ehlmann, BL, Fairén, AG, Farley, K, Flesch, GJ, Francois, P, Gellert, R, Grant, JA, Grotzinger, JP, Gupta, S, Herkenhoff, KE, Hurowitz, JA, Leshin, LA, Lewis, KW, McLennan, SM, Miller, KE, Moersch, J, Morris, RV, Navarro-González, R, Pavlov, AA, Perrett, GM, Pradler, I, Squyres, SW, Summons, RE, Steele, A, Stolper, EM, Sumner, DY, Szopa, C, Teinturier, S, Trainer, MG, Treiman, AH, Vaniman, DT, Vasavada, AR, Webster, CR, Wray, JJ, Yingst, RA and MSL Science Team (2014) Volatile and organic compositions of sedimentary rocks in Yellowknife Bay, Gale crater, Mars. Science 343, 1245267.Google Scholar
Nimmo, F and Pappalardo, RT (2016) Ocean worlds in the outer solar system. Journal of Geophysical Research 121, 1378–1399.Google Scholar
Pontefract, A, Zhu, TF, Walker, VK, Hepburn, H, Lui, C, Zuber, MT, Ruvkun, G and Carr, CE (2017) Microbial diversity in a hypersaline sulfate lake: a terrestrial analog of ancient Mars. Frontiers in Microbiology 8, 1819.Google Scholar
Rivera-Valentin, EG, Gough, RV, Chevrier, VF, Primm, KM, Martinez, GM and Tolbert, M (2018) Constraining the potential liquid water environment at Gale Crater, Mars throughout MSL's traverse. Lunar and Planetary Science Conference 2018, 2752.Google Scholar
Rivkina, EM, Friedmann, EI, McKay, CP and Gilichinsky, DA (2000) Metabolic activity of permafrost bacteria below the freezing point. Applied and Environmental Microbiology 66, 3230–3233.Google Scholar
Rivkina, E, Shcherbakova, V, Laurinavichius, K, Petrovskaya, L, Krivushin, K, Kraev, G, Pecheritsina, S and Gilichinsky, D (2007) Biogeochemistry of methane and methanogenic archaea in permafrost. FEMS Microbiology Ecology 61, 1–15.Google Scholar
Rummel, JD, Beaty, DW, Jones, MA, Bakermans, C, Barlow, NG, Boston, PJ, Chevrier, VF, Clark, BC, de Vera, JP, Gough, RV, Hallsworth, JE, Head, JW, Hipkin, VJ, Kieft, TL, McEwen, AS, Mellon, MT, Mikucki, JA, Nicholson, WL, Omelon, CR, Peterson, R, Roden, EE, Sherwood Lollar, B, Tanaka, KL, Viola, D and Wray, JJ (2014) A new analysis of Mars ‘special regions’: findings of the second MEPAG Special Regions Science Analysis Group (SR-SAG2). Astrobiology 14, 887–968.Google Scholar
Schneegurt, MA (2012) Media and conditions for the growth of halophilic and halotolerant bacteria and archaea. In Vreeland, RH (ed.) Advances in Understanding the Biology of Halophilic Microorganisms. Dordrecht: Springer, pp. 35–58.Google Scholar
Schneegurt, MA, Wilks, J, Zayed, H, Joad, MD, Mahdi, A, Zbeeb, H, Chen, F and Clark, BC (2018) Bacterial growth and survival under the extreme chemical and physical conditions of Mars and the icy worlds. Abstracts and Program, 42nd COSPAR Scientific Assembly, Pasadena, CA, July 2018, F3.1-0016-18, 22238.Google Scholar
Toner, JD, Catling, DC 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.Google Scholar
Tosca, NJ, Knoll, AH and McLennan, SM (2008) Water activity and the challenge for life on early Mars. Science 320, 1204–1207.Google Scholar
Vaniman, DT, Bish, DL, Chipera, SJ, Fialips, CI, Carey, JW and Feldman, WC (2004) Magnesium sulphate salts and the history of water on Mars. Nature 431, 663–665.Google Scholar
Wilks, J, Chen, F, Clark, BC and Schneegurt, MA (2017) Bacterial growth at eutectic temperatures and in saturated salt solutions relevant to Mars. Abstracts and Program, 117th Annual Meeting of the American Society for Microbiology, New Orleans, LA, June 2017.Google Scholar
Wilson, C, Caton, TM, Buchheim, JA, Buchheim, MA, Schneegurt, MA and Miller, RV (2004) DNA-Repair potential of Halomonas spp. from the Salt Plains Microbial Observatory of Oklahoma. Microbial Ecology 48, 541–549.Google Scholar