Characterization of NaCl tolerance in Desulfovibrio vulgaris Hildenborough through experimental evolution

ISME Journal

Volumn 7, Issue 9, 2013, Pages 1790-1802

  Zhou, Aifen ^a   Baidoo, Edward ^b   He, Zhili ^a   Mukhopadhyay, Aindrila ^b   Baumohl, Jason K ^b   Benke, Peter ^b   Joachimiak, Marcin P ^b   Xie, Ming ^a   Song, Rong ^a   Arkin, Adam P ^b   Hazen, Terry C ^c,d   Keasling, Jay D ^b   Wall, Judy D ^e   Stahl, David A ^f   Zhou, Jizhong ^a,b,g  

^a UNIVERSITY OF OKLAHOMA   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c University of Tennessee Knoxville   (United States)

^d OAK RIDGE NATIONAL LABORATORY   (United States)

^e UNIVERSITY OF MISSOURI   (United States)

^f University of Washington   (United States)

^g TSINGHUA UNIVERSITY   (China)

Author keywords

D. vulgaris; experimental evolution; metabolites assay; PLFA analysis; salt adaptation; transcriptomics

Indexed keywords

FATTY ACID; SODIUM CHLORIDE;

ACCUMULATION; ADAPTATION; BACTERIUM; BIOASSAY; EVOLUTION; FATTY ACID; METABOLITE; MOTILITY; PHOSPHOLIPID; STRAIN;

ADAPTATION; ARTICLE; DESULFOVIBRIO VULGARIS; ENERGY METABOLISM; EVOLUTION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; MEMBRANE FLUIDITY; METABOLISM; PHYSIOLOGY;

ADAPTATION, PHYSIOLOGICAL; BIOLOGICAL EVOLUTION; DESULFOVIBRIO VULGARIS; ENERGY METABOLISM; FATTY ACIDS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; MEMBRANE FLUIDITY; SODIUM CHLORIDE;

DESULFOVIBRIO VULGARIS; DESULFOVIBRIO VULGARIS SUBSP. VULGARIS STR. HILDENBOROUGH;

EID: 84883161070     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2013.60     Document Type: Article

References (42)

1. Baidoo EEK, Benke PI, Neususs C, Pelzing M, Kruppa G, Leary JA et al. (2008). Capillary electrophoresis-fourier transform ion cyclotron resonance mass spectrometry for the identification of cationic metabolites via a pH-mediated stacking-transient isotachophoretic method. Anal Chem 80: 3112-3122
2. Bender KS, Yen H-CB, Hemme CL, Yang Z, He Z, He Q et al. (2007). Analysis of a ferric uptake regulator (Fur) mutant of Desulfovibrio vulgaris Hildenborough. Appl Environ Microbiol 73: 5389-5400
3. Botsford JL, Alvarez M, Hernandez R, Nichols R. (1994). Accumulation of glutamate by Salmonella typhimurium in response to osmotic stress. Appl Environ Microbiol 60: 2568-2574
4. Botsford JL, Lewis TA. (1990). Osmoregulation in Rhizobium meliloti: Production of glutamic acid in response to osmotic stress. Appl Environ Microbiol 56: 488-494
5. Cameron A, Frirdich E, Huynh S, Parker CT, Gaynor EC. (2012). Hyperosmotic stress response of Campylobacter jejuni. J Bacteriol 194: 6116-6130
6. Chang YJ, Peacock AD, Long PE, Stephen JR, McKinley JP, Macnaughton SJ et al. (2001). Diversity and characterization of sulfate-reducing bacteria in groundwater at a uranium mill tailings site. Appl Environ Microbiol 67: 3149-3160
7. Chhabra SR, He Q, Huang KH, Gaucher SP, Alm EJ, He Z et al. (2006). Global analysis of heat shock response in Desulfovibrio vulgaris Hildenborough. J Bacteriol 188: 1817-1828
8. Dhar R, SÄ Gesser R, Weikert C, Yuan J, Wagner A. (2011). Adaptation of Saccharomyces cerevisiae to saline stress through laboratory evolution. J Evol Biol 24: 1135-1153
9. Dolla A, Pohorelic BKJ, Voordouw JK, Voordouw G. (2000). Deletion of the hmc operon of Desulfovibrio vulgaris subsp. vulgaris Hildenborough hampers hydrogen metabolism and low-redoxpotential niche establishment. Arch Microbiol 174: 143-151
10. Elena SF, Lenski RE. (2003). Evolution experiments with microorganisms: The dynamics and genetic bases of adaptation. Nat Rev Genet 4: 457-469
11. Elias DA, Suflita JM, McInerney MJ, Krumholz LR. (2004). Periplasmic cytochrome c3 of Desulfovibrio vulgaris is directly involved in H2-mediated metal but not sulfate reduction. Appl Environ Microbiol 70: 413-420
12. Gancz H, Merrell DS. (2011). The Helicobacter pylori ferric uptake regulator (Fur) is essential for growth under sodium chloride stress. J Microbiol 49: 294-298
13. Goude R, Renaud S, Bonnassie S, Bernard T, Blanco C. (2004). Glutamine, glutamate, and {alpha}-glucosylglycerate are the major osmotic solutes accumulated by Erwinia chrysanthemi strain 3937. Appl Environ Microbiol 70: 6535-6541
14. He Q, Huang KH, He Z, Alm EJ, Fields MW, Hazen TC et al. (2006). Energetic consequences of nitrite stress in Desulfovibrio vulgaris Hildenborough, inferred from global transcriptional analysis. Appl Environ Microbiol 72: 4370-4381
15. He Z, Zhou A, Baidoo E, He Q, Joachimiak MP, Benke P et al. (2010). Global transcriptional, physiological, and metabolite analyses of the responses of Desulfovibrio vulgaris Hildenborough to salt adaptation. Appl Environ Microbiol 76: 1574-1586
16. Hoffmann T, Schutz A, Brosius M, Volker A, Volker U, Bremer E. (2002). High-salinity-induced iron limitation in Bacillus subtilis. J Bacteriol 184: 718-727
17. Jebbar M, Talibart R, Gloux K, Bernard T, Blanco C. (1992). Osmoprotection of Escherichia coli by ectoine: Uptake and accumulation characteristics. J Bacteriol 174: 5027-5035
18. Kates M. (1986). Influence of salt concentration on the membrane lipids of halophilic bacteria. FEMS Microbiol Rev 39: 95-101
19. Kawecki TJ, Lenski RE, Ebert D, Hollis B, Olivieri I, Whitlock MC. (2012). Experimental evolution. Trends Ecol Evol 27: 547-560
20. Ko R, Smith LT, Smith GM. (1994). Glycine betaine confers enhanced osmotolerance and cryotolerance on Listeria monocytogenes. J Bacteriol 176: 426-431
21. Liu Y, Gao W, Wang Y, Wu L, Liu X, Yan T et al. (2005). Transcriptome analysis of Shewanella oneidensis MR-1 in response to elevated salt conditions. J Bacteriol 187: 2501-2507
22. Los DA, Murata N. (2004). Membrane fluidity and its roles in the perception of environmental signals. Biochim Biophys Acta 1666: 142-157
23. Lovley DR, Phillips EJP. (1994). Reduction of chromate by Desulfovibrio vulgaris and its c3 cytochrome. Appl Environ Microbiol 60: 726-728
24. Lovley DR, Widman PK, Woodward JC, Phillips EJ. (1993). Reduction of uranium by cytochrome c3 of Desulfovibrio vulgaris. Appl Environ Microbiol 59: 3572-3576
25. López CS, Heras H, Garda H, Ruzal S, Sánchez-Rivas C, Rivas E. (2000). Biochemical and biophysical studies of Bacillus subtilis envelopes under hyperosmotic stress. Int J Food Microbiol 55: 137-142
26. McLaggan D, Naprstek J, Buurman ET, Epstein W. (1994). Interdependence of K and glutamate accumulation during osmotic adaptation of Escherichia coli. J Biol Chem 269: 1911-1917
27. Mukhopadhyay A, He Z, Alm EJ, Arkin AP, Baidoo EE, Borglin SC et al. (2006). Salt stress in Desulfovibrio vulgaris Hildenborough: An integrated genomics approach. J Bacteriol 188: 4068-4078
28. Muyzer G, Stams AJM. (2008). The ecology and biotechnology of sulphate-reducing bacteria. Nat Rev Micro 6: 441-454
29. Postgate Jr. (1984). The Sulfate-Reducing Bacteria. Cambridge University Press: Cambridge, U.K.
30. Roberts M. (2005). Organic compatible solutes of halotolerant and halophilic microorganisms. Saline Syst 1: 5
31. Ruess L, Schütz K, Migge-Kleian S, Häggblom MM, Kandeler E, Scheu S. (2007). Lipid composition of collembola and their food resources in deciduous forest stands-implications for feeding strategies. Soil Biol Biochem 39: 1990-2000
32. Russell N. (1989). Adaptive modifications in membranes of halotolerant and halophilic microorganisms. J Bioenerg Biomembr 21: 93-113
33. Sleator RD, Hill C. (2002). Bacterial osmoadaptation: The role of osmolytes in bacterial stress and virulence. FEMS Microbiol Rev 26: 49-71
34. Steil L, Hoffmann T, Budde I, Volker U, Bremer E. (2003). Genome-wide transcriptional profiling analysis of adaptation of Bacillus subtilis to high salinity. J Bacteriol 185: 6358-6370
35. Strøm AR, Kaasen I. (1993). Trehalose metabolism in Escherichia coli: Stress protection and stress regulation of gene expression. Mol Microbiol 8: 205-210
36. Thomas SP, Shanmugasundaram S. (1991). Osmoregulatory role of alanine during salt stress in the nitrogen fixing cyanobacterium Anabaena sp. 287. Biochem Int 23: 93-102
37. Warringer J, Ericson E, Fernandez L, Nerman O, Blomberg A. (2003). High-resolution yeast phenomics resolves different physiological features in the saline response. Proc Natl Acad Sci USA 100: 15724-15729
38. Welsh DT, Lindsay YE, Caumette P, Herbert RA, Hannan J. (1996). Identification of trehalose and glycine betaine as compatible solutes in the moderately halophilic sulfate reducing bacterium, Desulfovibrio halophilus. FEMS Microbiol Lett 140: 203-207
39. Whatmore AM, Chudek JA, Reed RH. (1990). The effects of osmotic upshock on the intracellular solute pools of Bacillus subtilis. J Gen Microbiol 136: 2527-2535
40. Zhou A, He Z, Redding-Johanson AM, Mukhopadhyay A, Hemme CL, Joachimiak MP et al. (2010). Hydrogen peroxide-induced oxidative stress responses in Desulfovibrio vulgaris Hildenborough. Environ Microbiol 12: 2645-2657
41. Zhou J, Bruns MA, Tiedje JM. (1996). DNA recovery from soils of diverse composition. Appl Environ Microbiol 62: 316-322
42. Zhou J, He Q, Hemme CL, Mukhopadhyay A, Hillesland K, Zhou A et al. (2011). How sulfate reducing microorganisms cope with stress: Lessons from systems biology. Nat Rev Microbiol 9: 452-466