Extraordinary solute-stress tolerance contributes to the environmental tenacity of mycobacteria

Environmental Microbiology Reports

Volumn 7, Issue 5, 2015, Pages 746-764

  Santos, Ricardo ^a,b   de Carvalho, Carla C C R ^b   Stevenson, Andrew ^a   Grant, Irene R ^a   Hallsworth, John E ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^b INSTITUTO SUPERIOR TÉCNICO   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

INORGANIC SALT;

CHEMICAL PHENOMENA; CHEMISTRY; DRUG EFFECTS; ISOLATION AND PURIFICATION; MICROBIAL VIABILITY; MICROBIOLOGY; MYCOBACTERIUM; OSMOTIC PRESSURE; PH; PHYSIOLOGICAL STRESS; PHYSIOLOGY; RECREATIONAL PARK; TEMPERATURE; UNITED STATES;

ENVIRONMENTAL MICROBIOLOGY; HYDROGEN-ION CONCENTRATION; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MICROBIAL VIABILITY; MYCOBACTERIUM; OSMOTIC PRESSURE; PARKS, RECREATIONAL; SALTS; STRESS, PHYSIOLOGICAL; TEMPERATURE; UNITED STATES;

EID: 84945186377     PISSN: None     EISSN: 17582229     Source Type: Journal    
DOI: 10.1111/1758-2229.12306     Document Type: Article

References (123)

1. Ahmed, N., Saini, V., Raghuvanshi, S., Khurana, J.P., Tyagi, A.K., Tyagi, A.K., etal. (2007) Molecular analysis of a leprosy immunotherapeutic bacillus provides insights into Mycobacterium evolution. PLoS ONE 2: e968. doi:10.1371/journal.pone.0000968.
2. Alves, F.L., Stevenson, A., Baxter, E., Gillion, J.L.M., Hejazi, F., Morrison, I.E., etal. (2015) Concomitant osmotic and chaotropicity-induced stresses in Aspergillus wentii: compatible solutes determine the biotic window. Curr Genet. doi:10.1007/s00294-015-0496-8.
3. Antolín, E.M., Delange, D.M., and Canavaciolo, V.G. (2008) Evaluation of five methods for derivatization and GC determination of a mixture of very long chain fatty acids (C24:0-C36:0). J Pharm Biomed Anal 46: 194-199.
4. Aston, J.E., and Peyton, B.M. (2007) Response of Halomonas campisalis to saline stress: changes in growth kinetics, compatible solute production and membrane phospholipid fatty acid composition. FEMS Microbiol Lett 274: 196-203.
5. Ball, P., and Hallsworth, J.E. (2015) Water structure and chaotropicity: their uses, abuses and implications for biology. Phys Chem Chem Phys 17: 8297-8305.
6. Ballerstedt, H., Volkers, R.J., Mars, A.E., Hallsworth, J.E., dos Santos, V.A., Puchalka, J., etal. (2007) Genomotyping of Pseudomonas putida strains using P.putida KT2440-based high-density DNA microarrays: implications for transcriptomics studies. Appl Microbiol Biotechnol 75: 1133-1142.
7. Banciu, H., Sorokin, D.Y., Rijpstra, W.I., Sinninghe Damsté, J.S., Galinski, E.A., Takaichi, S., etal. (2005) Fatty acid, compatible solute and pigment composition of obligately chemolithoautotrophic alkaliphilic sulfur-oxidizing bacteria from soda lakes. FEMS Microbiol Lett 243: 181-187.
8. Bell, A.N.W., Magill, E., Hallsworth, J.E., and Timson, D.T. (2013) Effects of alcohols and compatible solutes on the activity of ß-galactosidase. Appl Biochem Biotech 169: 786-796.
9. Bhaganna, P., Volkers, R.J.M., Bell, A.N.W., Kluge, K., Timson, D.J., McGrath, J.W., etal. (2010) Hydrophobic substances induce water stress in microbial cells. Microb Biotechnol 3: 701-716.
10. Bodaker, I., Sharon, I., Suzuki, M.T., Feingersch, R., Shmoish, M., Andreischeva, E., etal. (2010) Comparative community genomics in the Dead Sea: an increasingly extreme environment. ISME J 4: 399-407.
11. Bolhuis, H., te Poele, E.M., and Rodriquez-Valera, F. (2004) Isolation and cultivation of Walsby's square archaeon. Environ Microbiol 6: 1287-1291.
12. Borase, H.P., Salunke, B.K., Salunkhe, R.B., Patil, C.D., Hallsworth, J.E., Kim, B.S., and Patil, S.V. (2014) Plant extract: a promising biomatrix for ecofriendly controlled synthesis of silver nanoparticles. Appl Biochem Biotechnol 173: 1-29.
13. Bronikowski, A.M., Bennett, A.F., and Lenski, R.E. (2001) Evolutionary adaptation to temperature. VIII. Effects of temperature on growth rate in natural isolates of Escherichia coli and Salmonella enterica from different thermal environments. Evolution 55: 33-40.
14. Brown, A.D. (1990) Microbial Water Stress Physiology: Principles and Perspectives. Chichester, England: Wiley.
15. T when subjected to both osmotic and organic solvent stress. FEMS Microbiol Lett 189: 149-154.
16. de Carvalho, C.C.C.R. (2012) Adaptation of Rhodococcus erythropolis cells for growth and bioremediation under extreme conditions. Res Microbiol 163: 125-136.
17. de Carvalho, C.C.C.R., Pons, M.P., and da Fronseca, M.R. (2003) Principal components analysis as a tool to summarise biotransformation data: influence on cells of solvent type and phase ratio. Biocatal Biotransform 21: 305-314.
18. de Carvalho, C.C.C.R., Fatal, V., Alves, S.S., and de Fonseca, M.M.R. (2007) Adaptation of Rhodococcus erythropolis cells to high concentrations of toluene. Appl Microbiol Biotechnol 76: 1423-1430.
19. de Carvalho, C.C.C.R., Marques, M.P., Hachicho, N., and Heipieper, H.J. (2014) Rapid adaptation of Rhodococcus erythropolis cells to salt stress by synthesizing polyunsaturated fatty acids. Appl Microbiol Biotechnol 98: 5599-5606.
20. Cebrián, G., Sagarzazu, N., Pagán, R., Condón, S., and Mañas, P. (2010) Development of stress resistance in Staphylococcus aureus after exposure to sublethal environmental conditions. Int J Food Microbiol 140: 26-33.
21. Chen, P., and Shakhnovich, E.I. (2010) Thermal adaptation of viruses and bacteria. Biophys J 98: 1109-1118.
22. Chin, J.P., Megaw, J., Magill, C.L., Nowotarski, K., Williams, J.P., Bhaganna, P., etal. (2010) Solutes determine the temperature windows for microbial survival and growth. Proc Natl Acad Sci 107: 7835-7840.
23. Cray, J.A., Russell, J.T., Timson, D.J., Singhal, R.S., and Hallsworth, J.E. (2013a) A universal measure of chaotropicity and kosmotropicity. Environ Microbiol 15: 287-296.
24. Cray, J.A., Bell, A.N.W., Bhaganna, P., Mswaka, A.Y., Timson, D.J., and Hallsworth, J.E. (2013b) The biology of habitat dominance; can microbes behave as weeds? Microb Biotechnol 6: 453-492.
25. Cray, J.A., Bhaganna, P., Singhal, R.S., Timson, D.J., and Hallsworth, J.E. (2014) Chaotropic and Hydrophobic Stress Mechanisms of Antifungal Substances, Fungicides and Antifungal Compounds, Vol. VII. Dehne, H.W., Deising, H.B., Fraaije, B., Gisi, U., Hermann, D., Mehl, A., etal. (eds). Braunschweig, Germany: Deutsche Phytomedizinische Gesellschaft.
26. Cray, J.A., Stevenson, A., Ball, P., Bankar, S.B., Eleutherio, E.C.A., Ezeji, T.C., etal. (2015a) Chaotropicity: a key factor in product tolerance of biofuel-producing microorganisms. Curr Opin Biotechnol 33: 228-259.
27. Cray, J.A., Houghton, J.D., Cooke, L.R., and Hallsworth, J.E. (2015b) A simple inhibition coefficient for quantifying potency of biocontrol agents against plant-pathogenic fungi. Biol Control 81: 93-100.
28. Daffonchio, D., Borin, S., Brusa, T., Brusetti, L., van der Wielen, P.W.J.J., Bolhuis, H., etal. (2006) Stratified prokaryote network in the oxic-anoxic transition of a deep sea halocline. Nature 440: 203-207.
29. DeBruyn, J.M., Chewning, C.S., and Sayler, G.S. (2007) Comparative quantitative prevalence of Mycobacteria and functionally abundant nidA, nahAc, and nagAc dioxygenase genes in coal tar contaminated sediments. Environ Sci Technol 41: 5426-5432.
30. Duda, V.I., Danilevich, V.N., Suzina, N.E., Shorokhova, A.P., Dmitriev, V.V., Mokhova, O.N., etal. (2004) Changes in the fine structure of microbial cells induced by chaotropic salts. Mikrobiologiya 73: 341-349.
31. Fajardo-Cavazos, P., Shuerger, A.C., and Nicholson, W.L. (2007) Testing interplanetary transfer of bacteria between Earth and Mars as a result of natural impact phenomena and human spaceflight activities. Acta Astronaut 60: 534-540.
32. Falkinham, J.O., III (2009) The biology of environmental mycobacteria. Environ Microbiol Rep 1: 477-487.
33. Falkinham, J.O., III, George, K.L., Parker, B.C., and Gruft, H. (1984) In vitro susceptibility of human and environmental isolates of Mycobacterium avium, M.intracellulare, and M.scrofulaceum to heavy-metal salts and oxyanions. Antimicrob Agents Chemother 25: 137-139.
34. Ferrer, M., Chernikova, T.N., Yakimov, M.M., Golyshin, P.N., and Timmis, K.N. (2003) Chaperonins govern growth of Escherichia coli at low temperatures. Nat Biotechnol 21: 1266-1267.
35. Flahaut, S., Hartke, A., GIard, J.C., and Auffray, Y. (1997) Alkaline stress response in Enterococcus faecalis: adaptation, cross-protection and changes in protein synthesis. Appl Environ Microbiol 63: 812-814.
36. Golyshina, O.V. (2011) Environmental, biogeographic, and biochemical patterns of Archaea of the family Ferroplasmaceae. Appl Environ Microbiol 77: 5071-5078.
37. Grant, W.D. (2004) Life at low water activity. Philos Trans R Soc Lond B Biol Sci 359: 1249-1266.
38. Guinebretière, M.H., Thompson, F.L., Sorokin, A., Normand, P., Dawyndt, P., Ehling-Schulz, M., etal. (2008) Ecological diversification in the Bacillus cereus group. Environ Microbiol 10: 851-865.
39. Gupta, S., and Chatterji, D. (2005) Stress responses in mycobacteria. IUBMB Life 57: 149-159.
40. Hahn, M.W., and Pöckl, M. (2005) Ecotypes of planktonic actinobacteria with identical 16S rRNA genes adapted to thermal niches in temperate, subtropical, and tropical freshwater habitats. Appl Environ Microbiol 71: 766-773.
41. Hallsworth, J.E. (1998) Ethanol-induced water stress in yeast. J Ferment Bioeng 85: 125-137.
42. Hallsworth, J.E., and Magan, N. (1994a) Improved biological control by changing polyols/ trehalose in conidia of entomopathogens. In Brighton Crop Protection Council - Pests and Diseases 1994. Farnham, England: British Crop Protection Council, pp. 1091-1096.
43. Hallsworth, J.E., and Magan, N. (1994b) Effect of carbohydrate type and concentration on polyols and trehalose in conidia of three entomopathogenic fungi. Microbiology 140: 2705-2713.
44. Hallsworth, J.E., and Magan, N. (1996) Culture age, temperature and pH affect the polyol and trehalose contents of fungal propagules. Appl Environ Microbiol 62: 2435-2442.
45. Hallsworth, J.E., and Nomura, Y. (1999) A simple method to determine the water activity of ethanol-containing samples. Biotechnol Bioeng 20: 242-245.
46. Hallsworth, J.E., Nomura, Y., and Iwahara, M. (1998) Ethanol-induced water stress and fungal growth. J Ferment Bioeng 86: 451-456.
47. Hallsworth, J.E., Heim, S., and Timmis, K.N. (2003a) Chaotropic solutes cause water stress in Pseudomonas putida. Environ Microbiol 5: 1270-1280.
48. Hallsworth, J.E., Prior, B.A., Nomura, Y., Iwahara, M., and Timmis, K.N. (2003b) Compatible solutes protect against chaotrope (ethanol)-induced, nonosmotic water stress. Appl Environ Microbiol 69: 7032-7034.
49. 2-containing environments: chaotropicity defines the window. Environ Microbiol 9: 803-813.
50. Haque, M.A., and Russell, N.J. (2004) Strains of Bacillus cereus vary in the phenotypic adaptation of their membrane lipid composition in response to low water activity, reduced temperature and growth in rice starch. Microbiology 150: 1397-1404.
51. Harrison, J.P., Gheeraert, N., Tsigelnitskiy, D., and Cockell, C.S. (2013) The limits for life under multiple extremes. Trends Microbiol 21: 204-212.
52. Harrison, J.P., Hallsworth, J.E., and Cockell, C.S. (2015) Reduction of the temperature sensitivity of Halomonas hydrothermalis by iron starvation combined with microaerobic conditions. Appl Environ Microbiol 81: 2156-2162.
53. Heim, S., Ferrer, M., Heuer, H., Regenhardt, D., Nimtz, M., and Timmis, K.N. (2003) Proteome reference map of Pseudomonas putida strain KT2440 for genome expression profiling: distinct responses of KT2440 and Pseudomonas aeruginosa strain PAO1 to iron deprivation and a new form of superoxide dismutase. Environ Microbiol 5: 1257-1269.
54. Heinlin, J., Isbary, G., Stolz, W., Morfill, G., Landthaler, M., Shimizu, T., etal. (2011) Plasma applications in medicine with a special focus on dermatology. J Europ Acad Dermatol Venereol 25: 1-11.
55. Hocking, A.D. (1993) Responses of xerophilic fungi to changes in water activity. In Stress Tolerance of Fungi. Jennings, D.H. (ed.). New York, NY, USA: Marcel Decker, pp. 233-256.
56. Hosono, K. (1992) Effect of salt stress on lipid composition and membrane fluidity of the salt tolerant yeast Zygosaccharomyces rouxii. Microbiology 138: 91-96.
57. Hümpel, A., Gebhard, S., Cook, G.M., and Berney, M. (2010) The SigF regulon in Mycobacterium smegmatis reveals roles in adaptation to stationary phase, heat, and oxidative stress. J Bacteriol 192: 2491-2502.
58. van Ingen, J., Boeree, M.J., Dekhuijzen, P.N., and van Soolingen, D. (2009) Environmental sources of rapid growing nontuberculous mycobacteria causing disease in humans. Clin Microbiol Infect 15: 888-893.
59. Jacobs, J., Rhodes, M., Sturgis, B., and Wood, B. (2009) Influence of environmental gradients on the abundance and distribution of Mycobacterium spp. in a coastal lagoon estuary. Appl Environ Microbiol 75: 7378-7384.
60. Jarlier, V., and Nikaido, H. (1994) Mycobacterial cell wall: structure and role in natural resistance to antibiotics. FEMS Microbiol Lett 123: 11-18.
61. Justé, A., Lievans, B., Frans, I., Marsh, T.L., Klingeberg, M., Michiels, C.W., etal. (2008a) Genetic and physiological diversity of Tetragenococcus halophilus strains isolated from sugar- and salt-rich environments. Microbiology 154: 2600-2610.
62. Kar, J.R., Hallsworth, J.E., and Singhal, R.S. (2015) Fermentative production of glycine betaine and trehalose from acid whey using Actinopolyspora halophila (MTCC 263). Environ Technol Innov 3: 68-76.
63. Kashangura, C., Hallsworth, J.E., and Mswaka, A.Y. (2006) Phenotypic diversity amongst strains of Pleurotus sajor-caju: implications for cultivation in arid environments. Mycol Res 110: 312-317.
64. Kazda, J., Pavlik, I., Falkinham, J.O., III, and Hruska, K. (2009) The Ecology of Mycobacteria: Impact on Animal's and Human's Health. Heidelberg, Germany: Springer, pp. 89-95.
65. Kelly, J.J., Minalt, N., Culotti, A., Pryor, M., and Packman, A. (2014) Temporal variations in the abundance and composition of biofilm communities colonizing drinking water distribution pipes. PLoS ONE 9: e98542.
66. Kminek, G., Rummel, J.D., Cockell, C.S., Atlas, R., Barlow, N., Beaty, D., etal. (2010) Report of the COSPAR Mars special regions colloquium. Adv Space Res 46: 811-829.
67. Kminek, G., Conley, C., Allen, C.C., Bartlett, D.H., Beaty, D.W., Benning, D.G., etal. (2014) Report of the workshop for life detection on samples from Mars. Life Sciences in Space Research 2: 1-5.
68. Krenek, S., Petzoldt, T., and Berendonk, T.U. (2012) Coping with temperature at the warm edge - patterns of thermal adaptation in the microbial eukaryote Paramecium caudatum. PLoS ONE 7: e30598. doi:10.1371/journal.pone.0030598.
69. Lievens, B., Hallsworth, J.E., Belgacem, Z.B., Pozo, M.I., Stevenson, A., Willems, K.A., etal. (2015) Microbiology of sugar-rich environments: diversity, ecology, and system constraints. Environ Microbiol 17: 278-298.
70. Lin, D.X., Tang, H., Wang, E.T., and Chen, W.X. (2009) An ABC transporter is required for alkaline stress and potassium transport regulation in Sinorhizobium meliloti. FEMS Microbiol Lett 293: 35-41.
71. McCammick, E.M., Gomase, V.S., Timson, D.J., McGenity, T.J., and Hallsworth, J.E. (2010) Water-hydrophobic compound interactions with the microbial cell. In Handbook of Hydrocarbon and Lipid Microbiology - Hydrocarbons, Oils and Lipids: Diversity, Properties and Formation, Vol. 1. Timmis, K.N. (ed.). Berlin, Germany: Springer-Verlag, pp. 1451-1466.
72. Mesbah, N.M., and Wiegel, J. (2012) Life under multiple extreme conditions: diversity and physiology of the halophilic alkalithermophiles. Appl Environ Microbiol 78: 4074-4082.
73. Moissl, C., Osman, S., La Duc, M.T., Dekas, A., Brodie, E., DeSantis, T., etal. (2007) Molecular bacterial community analysis of cleanrooms where spacecraft are assembled. FEMS Microbiol Ecol 61: 509-521.
74. Moissl-Eichinger, C., Rettberg, P., and Pukall, R. (2012) The first collection of spacecraft-associated microorganisms: a public source of extremotolerant microorganisms from spacecraft assembly clean rooms. Astrobiology 12: 1024-1034.
75. Morris, S., Bai, G.H., Suffys, P., Protillo-Gomez, L., Fairchok, M., and Rouse, D. (1995) Molecular mechanisms of multiple drug resistance in clinical isolates of Mycobacterium tuberculosis. J Infect Dis 171: 954-960.
76. Mukherji, S., and Ghosh, I. (2012) Bacterial degradation of high molecular weight polynuclear aromatic hydrocarbons. In Microbial Degradation of Xenobiotics. Singh, S.N. (ed.). Berlin, Germany: Springer-Verlag, pp. 189-212. Ch. 7.
77. Nelson, K.E., Weinel, C., Paulsen, I.T., Dodson, R.J., Hilbert, H., Martins dos Santos, V.A., etal. (2002) Complete genome sequence and comparative analysis of the metabolically versatile Pseudomonas putida KT2440. Environ Microbiol 4: 799-808.
78. Nicolaus, B., Manca, M.C., Lama, L., Esposito, E., and Gambacorta, A. (2001) Lipid modulation by environmental stresses in two models of extremophiles isolated from Antartica. Polar Biol 24: 1-8.
79. Niederweis, M., Danilchanka, O., Huff, J., Hoffmann, C., and Engelhardt, H. (2010) Mycobacterial outer membranes: in search of proteins. Trends Microbiol 18: 109-116.
80. Nikel, P.I., Martínez-García, E., and de Lorenzo, V. (2014) Biotechnological domestication of pseudomonads using synthetic biology. Nat Rev Microbiol 12: 368-379.
81. Norton, C.D., LeChevallier, M.W., and Falkinham, J.O., III (2004) Survival of Mycobacterium avium in a model distribution system. Water Res 38: 1457-1466.
82. Oren, A. (2010) The dying Dead Sea: the microbiology of an increasingly extreme environment. Lakes Reser: Res Manag 15: 215-222.
83. Oren, A., and Hallsworth, J.E. (2014) Microbial weeds in hypersaline habitats: the enigma of the weed-like Haloferax mediterranei. FEMS Microbiol Lett 359: 134-142.
84. Parro, V., de Diego-Castilla, G., Moreeno-Paz, M., Blanco, Y., Cruz-Gil, P., Rodríguez-Manfredi, J.A., etal. (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.
85. Petroff, S.A. (1915) A new and rapid method for the isolation and cultivation of tubercle bacilli directly from the sputum and feces. J Exp Med 21: 38-42.
86. Pirajno, F., and van Kranendonk, M.J. (2005) Review of hydrothermal processes and systems on Earth and implications for Martian analogues. Aust J Earth Sci 52: 329-351.
87. Pitt, J.I. (1975) Water Relations of Foods. Duckworth, R.B. (ed.). London, England: Academic Press, pp. 273-307.
88. Ponder, M.A., Gilmour, S.J., Bergholz, P.W., Mindock, C.A., Hollingsworth, R., Thomashow, M.F., etal. (2005) Characterization of potential stress responses in ancient Siberian permafrost psychroactive bacteria. FEMS Microbiol Ecol 53: 103-115.
89. Potts, M. (1994) Desiccation tolerance of prokaryotes. Microbiol Rev 58: 755-805.
90. Randall, K., Lever, M., Peddie, B.A., and Chambers, S.T. (1996) Natural and synthetic betaines counter the effects of high NaCl and urea concentrations. Biochim Biophys Acta Gen Subj 1291: 189-194.
91. Rangel, D.E.N., Braga, G.U.L., Fernandes, E.K.K., Keyser, C.A., Hallsworth, J.E., and Roberts, D.W. (2015a) Stress tolerance and virulence of insect-pathogenic fungi are determined by environmental conditions during conidial formation. Curr Genet. doi:10.1007/s00294-015-0477-y.
92. Rangel, D.E.N., Alder-Rangel, A., Dadachova, E., Finlay, R.D., Kupiec, M., Dijksterhuis, J., etal. (2015b) Fungal stress biology: a preface to the Fungal Stress Responses special edition. Curr Genet. doi:10.1007/s00294-015-0500-3.
93. Roth, A., Reischl, U., Streubel, A., Naumann, L., Kroppenstedt, R.M., Habicht, M., etal. (2000) Novel diagnostic algorithm for identification of mycobacteria using genus-specific amplification of the 16S-23S rRNA gene spacer and restriction endonucleases. J Clin Microbiol 38: 1094-1104.
94. Rummel, J.D., Beaty, D.W., Jones, M.A., Bakermans, C., Barlow, N.G., Boston, P., etal. (2014) A new analysis of Mars 'Special Regions', findings of the second MEPAG Special Regions Science Analysis Group (SR-SAG2). Astrobiology 14: 887-968.
95. Santos, R., Fernandes, J., Fernandes, N., Oliveira, F., and Cadete, M. (2007) Mycobacterium parascrofulaceum in acidic hot springs in Yellowstone National Park. Appl Environ Microbiol 73: 5071-5073.
96. Sarathy, J.P., Dartois, V., and Lee, E.J.D. (2012) The role of transport mechanisms in Mycobacterium tuberculosis drug resistance and tolerance. Pharmaceuticals 5: 1210-1235.
97. Segura, A., Molina, L., Fillet, S., Krell, T., Bernal, P., Muñoz-Rojas, J., etal. (2012) Solvent tolerance in Gram-negative bacteria. Curr Opin Biotechnol 24: 415-421.
98. Shi, B., and Xia, X. (2003) Morphological changes of Pseudomonas pseudoalcaligenes in response to temperature selection. Curr Microbiol 46: 120-123.
99. Shin, G.A., Lee, J.K., Freeman, R., and Cangelosi, G.A. (2008) Inactivation of Mycobacterium avium complex by UV irradiation. Appl Environ Microbiol 74: 7067-7069.
100. Sikkema, J., de Bont, J.A., and Poolman, B. (1995) Mechanisms of membrane toxicity of hydrocarbons. Microbiol Mol Biol Rev 59: 201-222.
101. Sikorski, J., and Nevo, E. (2007) Patterns of thermal adaptation of Bacillus simplex to the microclimatically contrasting slopes of 'Evolution Canyons' I and II, Israel. Environ Microbiol 9: 716-726.
102. Stevenson, A., and Hallsworth, J.E. (2014) Water and temperature relations of soil Actinobacteria. Environ Microbiol Rep 6: 744-755.
103. Stevenson, A., Cray, J.A., Williams, J.P., Santos, R., Sahay, R., Neuenkirchen, N., etal. (2015a) Is there a common water-activity limit for the three domains of life? ISME J 9: 1333-1351.
104. Stevenson, A., Burkhardt, J., Cockell, C.S., Cray, J.A., Dijksterhuis, J., Fox-Powell, M., etal. (2015b) Multiplication of microbes below 0.690 water activity: implications for terrestrial and extraterrestrial life. Environ Microbiol 17: 257-277.
105. Suryawanshi, R.K., Patil, C.D., Borase, H.P., Narkhede, C.P., Stevenson, A., Hallsworth, J.E., etal. (2015) Towards an understanding of bacterial metabolites prodigiosin and violacein and their potential for use in commercial sunscreens. Int J Cosmetic Sci 37: 98-107.
106. Timmis, K.N., McGenity, T.J., van der Meer, J.R., and de Lorenzo, V. (2010) Handbook of Hydrocarbon and Lipid Microbiology - Hydrocarbons, Oils and Lipids: Diversity, Properties and Formation. Berlin, Germany: Springer-Verlag.
107. Torvinera, E., Torkko, P., and Nevalainen, A.N. (2010) Real-time PCR detection of environmental mycobacteria in house dust. J Microbiol Methods 82: 78-84.
108. Toungoussova, S., Caugant, D.A., Sandven, P., Mariandyshev, A.O., and Bjune, G. (2002) Drug resistance of Mycobacterium tuberculosis strains isolated from patients with pulmonary tuberculosis in Achangels, Russia. Int J Tuberc Lung Dis 6: 406-414.
109. Venkatswaran, K., La Duc, M.T., and Vaishampayan, P. (2012) Genetic Inventory Task: Final Report, JPL publication, Vol. 1. Pasadena, CA: Jet Propulsion Laboratory, National Aeronautics and Space Administration, Publication 12-12.
110. Voskuil, M.I., Bartek, I.L., Visconti, K., and Schoolnik, G.K. (2011) The response of Mycobacterium tuberculosis to reactive oxygen and nitrogen species. Front Microbiol 2: 105.
111. Walker, J.J., Spear, J.R., and Pace, N.R. (2005) Geobiology of a microbial endolithic community in the Yellowstone geothermal environment. Nature 434: 1011-1014.
112. Wallace, R.J., Steele, L.C., Forrester, G.D., Swenson, J.M., and Hull, S.I. (1984) Susceptibilities of Mycobacterium fortuitum and the unnamed third biovariant complex to heavy-metal salts. Antimicrob Agents Chemother 26: 594-596.
113. Wang, Y., Ogawa, M., Fuduka, K., Miyamoto, H., and Taniguchi, H. (2006) Isolation and Identification of mycobacteria from soils and an illegal dumping site and landfills in Japan. Microbiol Immunol 50: 513-524.
114. Williams, E.S., Snyder, S.P., and Martin, K.L. (1983) Pathology of spontaneous and experimental infection of North American wild ruminants with Mycobacterium paratuberculosis. Vet Pathol 20: 274-290.
115. Williams, J.P., and Hallsworth, J.E. (2009) Limits of life in hostile environments; no limits to biosphere function? Environ Microbiol 11: 3292-3308.
116. Wyatt, T.T., van Leeuwen, M.R., Gerwig, G.J., Golovina, E.A., Hoekstra, F.A., Kuenstner, E.J., etal. (2015a) Functionality and prevalence of trehalose-based oligosaccharides as novel compatible solutes in ascospores of Neosartorya fischeri (Aspergillus fischeri) and other fungi. Environ Microbiol 17: 395-411.
117. Wyatt, T.T., Golovina, E.A., Leeuwen, R., Hallsworth, J.E., Wösten, H.A., and Dijksterhuis, J. (2015b) A decrease in bulk water and mannitol and accumulation of trehalose and trehalose-based oligosaccharides define a two-stage maturation process towards extreme stress resistance in ascospores of Neosartorya fischeri (Aspergillus fischeri). Environ Microbiol 17: 383-394.
118. Wynn-Williams, D.D., and Edwards, H.G.M. (2000) Antarctic ecosystems as models for extraterrestrial surface. Planet Space Sci 48: 1065-1075.
119. Xu, X.Q., and Beardall, J. (1997) Effect of salinity on fatty acid composition of a green microalga from an Antarctic hypersaline lake. Phytochemistry 45: 655-658.
120. Yakimov, M.M., Lo Cono, V., La Spada, G., Bortoluzzi, G., Messina, E., Smedile, F., etal. (2015) Microbial community of seawater-brine interface of the deep-sea brine Lake Kryos as revealed by recovery of mRNA are active below the chaotropicity limit of life. Environ Microbiol 17: 364-382.
121. Zvyagintsev, D.G., Zenova, G.M., Doroshenko, E.A., Gryadunova, A.A., Gracheva, T.A., and Sudnitsyn, I.I. (2007) Actinomycete growth in conditions of low moisture. Biol Bull 34: 242-247.
122. Zvyagintsev, D.G., Zenova, G.M., Sudnitsyn, I.I., Gracheva, T.A., Napol'skaya, K.R., and Belousova, M.A. (2009) Dynamics of spore germination and mycelial growth of streptomycetes under low humidity conditions. Microbiology 78: 440-444.
123. Zvyagintsev, D.G., Zenova, G.M., Sudnitsyn, I.I., Gracheva, T.A., Lapygina, E.E., Napol'skaya, K.R., etal. (2012) Development of actinomycetes in brown semidesert soil under low water pressure. Eursian Soil Sci 45: 717-725.