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Relationships between sucretolerance and salinotolerance in bacteria from hypersaline environments and their implications for the exploration of Mars and the icy worlds

Published online by Cambridge University Press:  22 June 2016

Casper Fredsgaard
Affiliation:
Department of Biological Sciences, Wichita State University, Wichita, KS, USA
Donald B. Moore
Affiliation:
Department of Biological Sciences, Wichita State University, Wichita, KS, USA
Amer F. Al Soudi
Affiliation:
Department of Biological Sciences, Wichita State University, Wichita, KS, USA
James D. Crisler
Affiliation:
Department of Biological Sciences, Wichita State University, Wichita, KS, USA
Fei Chen
Affiliation:
Planetary Protection Group, Jet Propulsion Laboratory, NASA, 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

Abstract

The most extremely osmotolerant microbial isolates are fungi from high-sugar environments that tolerate the lowest water activity (0.61) for growth yet reported. Studies of osmotolerant bacteria have focused on halotolerance rather than sucretolerance (ability to grow in high sugar concentrations). A collection of salinotolerant (≥10% NaCl or ≥50% MgSO4) bacterial isolates from the Great Salt Plains of Oklahoma and Hot Lake in Washington were screened for sucretolerance in medium supplemented with ≥50% fructose, glucose or sucrose. Tolerances significantly differed between solutes, even though water activities for saline media (0.92 and 0.85 for 10 and 20% NaCl Salt Plains media, respectively) were comparable or lower than water activities for high-sugar media (0.93 and 0.90 for 50 and 70% sucrose artificial nectar media, respectively). These specific solute effects were differentially expressed among individual isolates. Extrapolating the results of earlier food science studies with yeasts at high sugar concentrations to bacteria in salty environments with low water activity should be done with caution. Furthermore, the discussion of habitable Special Regions on Mars and the icy worlds should reflect an understanding of specific solute effects.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2016 

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References

Belamri, M., Mekkaoui, A.K. & Tantaoui-Elaraki, A. (1991). Saccharolytic bacteria in beet juices. Int. Sugar J. 93, 210212.Google Scholar
Beuchat, L.R. (1981). Microbial stability as affected by water activity. Cereal Foods World 26, 345349.Google Scholar
Beuchat, L.R. & Pitt, J.I. (1990). Influence of water activity and temperature on survival of and colony formation by heat-stressed Chrysosporium farinicola aleuriospores. Appl. Environ. Microbiol. 56, 29512956.Google Scholar
Buchanan, R.L. & Bagi, L.K. (1994). Expansion of response surface models for the growth of Escherichia coli O157:H7 to include sodium nitrate as a variable. Int. J. Food Microbiol. 23, 317332.CrossRefGoogle Scholar
Caton, T.M., Witte, L.R., Ngyuen, H.D., Buchheim, J.A., Buchheim, M.A. & Schneegurt, M.A. (2004). Halotolerant aerobic heterotrophic bacteria from the Great Salt Plains of Oklahoma. Microb. Ecol. 48, 449462.CrossRefGoogle ScholarPubMed
Chevrier, V.F. & Altheide, T.S. (2008). Low temperature aqueous ferric sulfate solutions on the surface of Mars. Geophys. Res. Lett. 35, 15.CrossRefGoogle Scholar
Chevrier, V.F., Hanley, J. & Altheide, T.S. (2009). Stability of perchlorate hydrates and their liquid solutions at the Phoenix landing site, Mars. Geophys. Res. Lett. 36, L10202.Google Scholar
Chirife, J. (1994). Specific solute effects with special reference to Staphylococcus aureus . J. Food Eng. 22, 409419.Google Scholar
Chirife, J. & Buera, M.P. (1994). Water activity, glass transition and microbial stability in concentrated/semimoist food systems. J. Food Sci. 59, 921927.Google Scholar
Chirife, J. & Buera, M.P. (1996). Water activity, water glass dynamics, and the control of microbiological growth in foods. Crit. Rev. Food Sci. Nutr. 36, 465513.Google Scholar
Chirife, J., González, H.H.L. & Resnik, S.L. (1995). On water dynamics and germination time of mold spores in concentrated sugar and polyol solutions. Food Res. Int. 28, 531535.CrossRefGoogle Scholar
Clark, B.C. & Kounaves, S.P. (2015). Evidence for the distribution of perchlorates on Mars. Int. J. Astrobiol. doi: http://dx.doi.org/10.1017/S1473550415000385.Google Scholar
Clark, B.C. et al. (2005). Chemistry and mineralogy of outcrops at Meridiani Planum. Earth Planet. Sci. Lett. 240, 7394.CrossRefGoogle Scholar
Cornillon, P., Andrieu, J., Duplan, J.C. & Laurent, M. (1995). Use of nuclear-magnetic-resonance to model thermophysical properties of frozen and unfrozen model food gels. J. Food Eng. 25, 119.Google Scholar
Cray, J.A., Russell, J.T., Timson, D.J., Singhal, R.S. & Hallsworth, J.E. (2013). A universal measure of chaotropicity and kosmotropicity. Environ. Microbiol. 15, 287296.CrossRefGoogle ScholarPubMed
Crisler, J.D., Newville, T.M., Chen, F., Clark, B.C. & Schneegurt, M.A. (2012). Bacterial growth at the high concentrations of magnesium sulfate found in Martian soils. Astrobiology 12, 98106.Google Scholar
Davila, A.F. et al. (2010). Hygroscopic salts and the potential for life on Mars. Astrobiology 10, 617628.Google Scholar
Fredsgaard, C., Moore, D.B., Kurz, T.L. & Schneegurt, M.A. (2013). Sucretolerant microbes from oligoosmotic turf and prairie soils. 145th Annual Meeting of the Kansas Academy of Science, Overland Park, KS. Trans. KS Acad. Sci. 116, 7475.Google Scholar
Fredsgaard, C., Moore, D.B. & Schneegurt, M.A. (2014). Comparison of sucretolerance and salinotolerance in bacterial isolates from oligosaline and hypersaline soils. 146th Annual Meeting of the Kansas Academy of Science, Emporia, KS. Trans. KS Acad. Sci. 117, 116117.Google Scholar
Gendrin, A. et al. (2005). Sulfates in Martian layered terrains: the OMEGA/Mars Express view. Science 307, 15871591.Google Scholar
Gough, R.V., Chevrier, V.F., Baustian, K.J., Wise, M.E. & Tolbert, M.A. (2011). Laboratory studies of perchlorate phase transitions: support for metastable aqueous perchlorate solutions on Mars. Earth Planet. Sci. Lett. 312, 371377.CrossRefGoogle Scholar
Grant, W.D. (2004). Life at low water activity. Phil. Trans. R. Soc. Lond. B 359, 12491267.CrossRefGoogle ScholarPubMed
Hallsworth, J.E., Heim, S. & Timmis, K.N. (2003). Chaotropic solutes cause water stress in Pseudomonas putida . Environ. Microbiol. 5, 12701280.Google Scholar
Hand, K.P. & Carlson, R.W. (2015). Europa's surface color suggests an ocean rich with sodium chloride. Geophys. Res. Lett. 42, 31743178.CrossRefGoogle Scholar
Harris, R.F. (1981). Effect of water potential on microbial growth and activity. In Water Potential Relations in Soil Microbiology, eds. Parr, J.F., Gardner, W.R., & Elliott, L.F., pp. 2395. SSSA Special Publication 9, Soil Science Society of America, Madison, WI.Google Scholar
Hofmeister, F. (1888). Zur Lehre von der Wirkung der Salze. Arch. Exp. Pathol. Pharmakol. 24, 247260.CrossRefGoogle Scholar
Hsu, H.-W. et al. (2015). Ongoing hydrothermal activities within Enceladus. Nature 519, 207210.Google Scholar
Kilmer, B.R., Eberl, T.C., Cunderla, B., Chen, F., Clark, B.C. & Schneegurt, M.A. (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. Int. J. Astrobiol. 13, 6980.Google Scholar
Lewith, S. (1888). Zur Lehre der Wirkung der Salze. Arch. Exp. Pathol. Pharmakol. 24, 16.Google Scholar
Lievens, B., Hallsworth, J.E., Pozo, M.I., Belgacem, Z.B., Stevenson, A., Willems, K.A. & Jacquemyn, H. (2015). Microbiology of sugar-rich environments: diversity, ecology and system constraints. Environ. Microbiol. 17, 278298.CrossRefGoogle ScholarPubMed
Litzner, B.R., Caton, T.M. & Schneegurt, M.A. (2006). Carbon substrate utilization, antibiotic sensitivity, and numerical taxonomy of bacterial isolates from the Great Salt Plains of Oklahoma. Arch. Microbiol. 185, 286296.CrossRefGoogle ScholarPubMed
Marshall, B.J., Ohye, D.F. & Christian, J.H.B. (1971). Tolerance of bacteria to high concentrations of NaCl and glycerol in the growth medium. Appl. Microbiol. 21, 363364.Google Scholar
McCord, T.B., Hansen, G.B. & Hibbitts, C.A. (2001). Hydrated salt minerals on Ganymede's surface: evidence of an ocean below. Science 292, 15231525.Google Scholar
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. (2011). Seasonal flows on warm Martian slopes. Science 333, 740743.Google Scholar
Muñoz-Iglesias, V., Prieto-Ballesteros, O. & Bonales, L.J. (2014). Conspicuous assemblages of hydrated minerals from the H2O–MgSO4–CO2 system on Jupiter's Europa satellite. Geochim. Cosmochim. Acta 125, 466475.Google Scholar
Osterloo, M.M., Hamilton, V.E., Bandfield, J.L., Glotch, T.D., Baldridge, A.M., Christensen, P.R., Tornabene, L.L. & Anderson, F.S. (2008). Chloride-bearing materials in the southern highlands of Mars. Science 319, 16511654.CrossRefGoogle ScholarPubMed
Pitt, J.I. & Christian, J.H.B. (1968). Water relations of xerophilic fungi isolated from prunes. Appl. Microbiol. 16, 18531858.Google Scholar
Porazka, T., Kilmer, B.R., Wichita High School Northwest Team, Wichita Northeast Magnet High School Team & Schneegurt, M.A. (2011). Inland oligohaline soils as a habitat for culturable halotolerant bacteria. 143rd Annual Meeting of the Kansas Academy of Science, Baldwin City, KS. Trans. KS Acad. Sci. 115, 170.Google Scholar
Rummel, J.D. et al. (2014). A new analysis of Mars ‘Special Regions’: findings of the second MEPAG Special Regions Analysis Group (SR-SAG2). Astrobiology 14, 887968.Google Scholar
Scott, W.J. (1953). Water relations of Staphylococcus aureus at 30°C. Aust. J. Biol. Sci. 6, 549556.CrossRefGoogle Scholar
Williams, J.P. & Hallsworth, J.E. (2009). Limits of life in hostile environments: no barriers to biosphere function? Environ . Microbiol. 11, 32923308.Google Scholar