1887

Abstract

is a metabolically flexible micro-organism. It can use sulfate as an electron acceptor to catabolize a variety of substrates, or in the absence of sulfate can utilize organic acids and alcohols by forming a syntrophic association with a hydrogen-scavenging partner to relieve inhibition by hydrogen. These alternative metabolic types increase the chance of survival for in environments where one of the potential external electron acceptors becomes depleted. In this work, whole-genome microarrays were used to determine relative transcript levels as shifted its metabolism from syntrophic in a lactate-oxidizing dual-culture with to a sulfidogenic metabolism. Syntrophic dual-cultures were grown in two independent chemostats and perturbation was introduced after six volume changes with the addition of sulfate. The results showed that 132 genes were differentially expressed in 2 h after addition of sulfate. Functional analyses suggested that genes involved in cell envelope and energy metabolism were the most regulated when comparing syntrophic and sulfidogenic metabolism. Upregulation was observed for genes encoding ATPase and the membrane-integrated energy-conserving hydrogenase (Ech) when cells shifted to a sulfidogenic metabolism. A five-gene cluster encoding several lipoproteins and membrane-bound proteins was downregulated when cells were shifted to a sulfidogenic metabolism. Interestingly, this gene cluster has orthologues found only in another syntrophic bacterium, , and four recently sequenced strains. This study also identified several novel -type cytochrome-encoding genes, which may be involved in the sulfidogenic metabolism.

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2010-09-01
2019-10-15
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References

  1. Albert, T. J., Norton, J., Ott, M., Richmond, T., Nuwaysir, K., Nuwaysir, E. F., Stengele, K. P. & Green, R. D. ( 2003; ). Light directed 5′→3′ synthesis of complex oligonucleotide microarrays. Nucleic Acids Res 31, e35.[CrossRef]
    [Google Scholar]
  2. Aubert, C., Brugna, M., Dolla, A., Bruschi, M. & Giudici-Orticoni, M. T. ( 2000; ). A sequential electron transfer from hydrogenases to cytochromes in sulfate-reducing bacteria. Biochim Biophys Acta 1476, 85–92.[CrossRef]
    [Google Scholar]
  3. Bender, K. S., Yen, H. C., Hemme, C. L., Yang, Z., He, Z., He, Q., Zhou, J., Huang, K. H., Alm, E. J. & other authors ( 2007; ). Analysis of a ferric uptake regulator (Fur) mutant of Desulfovibrio vulgaris Hildenborough. Appl Environ Microbiol 73, 5389–5400.[CrossRef]
    [Google Scholar]
  4. Benjemini, Y. & Hochberg, Y. ( 1995; ). Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 57, 289–300.
    [Google Scholar]
  5. Bryant, M. P., Wolin, E. A., Wolin, M. J. & Wolfe, R. S. ( 1967; ). Methanobacillus omelianskii, a symbiotic association of two species of bacteria. Arch Mikrobiol 59, 20–31.[CrossRef]
    [Google Scholar]
  6. Bryant, M. P., Campbell, L. L., Reddy, C. A. & Crabill, M. R. ( 1977; ). Growth of Desulfovibrio in lactate or ethanol media low in sulfate in association with H2-utilizing methanogenic bacteria. Appl Environ Microbiol 33, 1162–1169.
    [Google Scholar]
  7. Chhabra, S. R., He, Q., Huang, K. H., Gaucher, S. P., Alm, E. J., He, Z., Hadi, M. Z., Hazen, T. C., Wall, J. D. & other authors ( 2006; ). Global analysis of heat shock response in Desulfovibrio vulgaris Hildenborough. J Bacteriol 188, 1817–1828.[CrossRef]
    [Google Scholar]
  8. Clark, M. E., He, Q., He, Z., Huang, K. H., Alm, E. J., Wan, X. F., Hazen, T. C., Arkin, A. P., Wall, J. D. & other authors ( 2006; ). Temporal transcriptomic analysis as Desulfovibrio vulgaris Hildenborough transitions into stationary phase during electron donor depletion. Appl Environ Microbiol 72, 5578–5588.[CrossRef]
    [Google Scholar]
  9. Culley, D. E., Kovacik, W. P., Jr, Brockman, F. J. & Zhang, W. ( 2006; ). Optimization of RNA isolation from the archaebacterium Methanosarcina barkeri and validation for oligonucleotide microarray analysis. J Microbiol Methods 67, 36–43.[CrossRef]
    [Google Scholar]
  10. Cypionka, H. ( 2000; ). Oxygen respiration in Desulfovibrio species. Annu Rev Microbiol 54, 827–848.[CrossRef]
    [Google Scholar]
  11. Dehal, P. S., Joachimiak, M. P., Price, M. N., Bates, J. T., Baumohl, J. K., Chivian, D., Friedland, G. D., Huang, K. H., Keller, K. & other authors ( 2010; ). MicrobesOnline: an integrated portal for comparative and functional genomics. Nucleic Acids Res 38, D396–D400.[CrossRef]
    [Google Scholar]
  12. Harmsen, H. J., Van Kuijk, B. L., Plugge, C. M., Akkermans, A. D., De Vos, W. M. & Stams, A. J. ( 1998; ). Syntrophobacter fumaroxidans sp. nov., a syntrophic propionate-degrading sulfate-reducing bacterium. Int J Syst Bacteriol 48, 1383–1387.[CrossRef]
    [Google Scholar]
  13. Haveman, S. A., Greene, E. A., Stilwell, C. P., Voordouw, J. K. & Voordouw, G. ( 2004; ). Physiological and gene expression analysis of inhibition of Desulfovibrio vulgaris Hildenborough by nitrite. J Bacteriol 186, 7944–7950.[CrossRef]
    [Google Scholar]
  14. He, Q., Huang, K. H., He, Z., Alm, E. J., Fields, M. W., Hazen, T. C., Arkin, A. P., Wall, J. D. & Zhou, J. ( 2006; ). Energetic consequences of nitrite stress in Desulfovibrio vulgaris Hildenborough inferred from global transcriptional analysis. Appl Environ Microbiol 72, 4370–4381.[CrossRef]
    [Google Scholar]
  15. Heidelberg, J. F., Seshadri, R., Haveman, S. A., Hemme, C. L., Paulsen, I. T., Kolonay, J. F., Eisen, J. A., Ward, N., Methe, B. & other authors ( 2004; ). The genome sequence of the anaerobic sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough. Nat Biotechnol 22, 554–559.[CrossRef]
    [Google Scholar]
  16. Holmer, M. & Kristensen, E. ( 1994; ). Co-existence of sulfate reduction and methane production in an organic-rich sediment. Mar Ecol Prog Ser 107, 177–184.[CrossRef]
    [Google Scholar]
  17. Kammler, M., Schön, C. & Hantke, K. ( 1993; ). Characterization of the ferrous iron uptake system of Escherichia coli. J Bacteriol 175, 6212–6219.
    [Google Scholar]
  18. Kuivila, K.M., Murray, J. W. & Devol, A. H. ( 1990; ). Methane production in the sulfate depleted sediments of two marine basins. Geochim Cosmochim Acta 54, 403–411.[CrossRef]
    [Google Scholar]
  19. Leloup, J., Fossing, H., Kohls, K., Holmkvist, L. & Jørgensen, B. B. ( 2009; ). Sulfate-reducing bacteria in marine sediment (Aarhus Bay, Denmark): abundance and diversity related to geochemical zonation. Environ Microbiol 11, 1278–1291.[CrossRef]
    [Google Scholar]
  20. Livak, K. J. & Schmittgen, T. D. ( 2001; ). Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408.[CrossRef]
    [Google Scholar]
  21. McInerney, M. J., Mackie, R. I. & Bryant, M. P. ( 1981; ). Syntrophic association of a butyrate-degrading bacterium and Methanosarcina enriched from bovine rumen fluid. Appl Environ Microbiol 41, 826–828.
    [Google Scholar]
  22. Meuer, J., Bartoschek, S., Koch, J., Künkel, A. & Hedderich, R. ( 1999; ). Purification and catalytic properties of Ech hydrogenase from Methanosarcina barkeri. Eur J Biochem 265, 325–335.[CrossRef]
    [Google Scholar]
  23. Meuer, J., Kuettner, H. C., Zhang, J. K., Hedderich, R. & Metcalf, W. W. ( 2002; ). Genetic analysis of the archaeon Methanosarcina barkeri Fusaro reveals a central role for Ech hydrogenase and ferredoxin in methanogenesis and carbon fixation. Proc Natl Acad Sci U S A 99, 5632–5637.[CrossRef]
    [Google Scholar]
  24. Mukhopadhyay, A., He, Z., Alm, E. J., Arkin, A. P., Baidoo, E. E., Borglin, S. C., Chen, W., Hazen, T. C., He, Q. & other authors ( 2006; ). Salt stress in Desulfovibrio vulgaris Hildenborough: an integrated genomics approach. J Bacteriol 188, 4068–4078.[CrossRef]
    [Google Scholar]
  25. Mukhopadhyay, A., Redding, A. M., Joachimiak, M. P., Arkin, A. P., Borglin, S. E., Dehal, P. S., Chakraborty, R., Geller, J. T., Hazen, T. C. & other authors ( 2007; ). Cell-wide responses to low-oxygen exposure in Desulfovibrio vulgaris Hildenborough. J Bacteriol 189, 5996–6010.[CrossRef]
    [Google Scholar]
  26. Muyzer, G. & Stams, A. J. M. ( 2008; ). The ecology and biotechnology of sulphate-reducing bacteria. Nat Rev Microbiol 6, 441–454.
    [Google Scholar]
  27. Neretin, L. N., Schippers, A., Pernthaler, A., Hamann, K., Amann, R. & Jørgensen, B. B. ( 2003; ). Quantification of dissimilatory (bi)sulphite reductase gene expression in Desulfobacterium autotrophicum using real-time RT-PCR. Environ Microbiol 5, 660–671.[CrossRef]
    [Google Scholar]
  28. Nuwaysir, E. F., Huang, W., Albert, T. J., Singh, J., Nuwaysir, K., Pitas, A., Richmond, T., Gorski, T., Berg, J. P. & other authors ( 2002; ). Gene expression analysis using oligonucleotide arrays produced by maskless photolithography. Genome Res 12, 1749–1755.[CrossRef]
    [Google Scholar]
  29. Odom, J. M. & Peck, H. D., Jr ( 1981; ). Hydrogen cycling as a general mechanism for energy coupling in the sulfate-reducing bacteria Desulfovibrio sp. FEMS Microbiol Lett 12, 47–50.[CrossRef]
    [Google Scholar]
  30. Oremland, R. S. & Polcin, S. ( 1982; ). Methanogenesis and sulfate reduction: competitive and noncompetitive substrates in estuarine sediments. Appl Environ Microbiol 44, 1270–1276.
    [Google Scholar]
  31. Peck, H. D., Jr ( 1966; ). Phosphorylation coupled with electron transfer in extracts of the sulfate reducing bacterium Desulfovibrio gigas. Biochem Biophys Res Commun 22, 112–118.[CrossRef]
    [Google Scholar]
  32. Pereira, P. M., He, Q., Valente, F. M. A., Xavier, A. V., Zhou, J., Pereira, I. A. C. & Louro, R. O. ( 2008; ). Energy metabolism in Desulfovibrio vulgaris Hildenborough: insights from transcriptome analysis. Antonie van Leeuwenhoek 93, 347–362.[CrossRef]
    [Google Scholar]
  33. Rodionov, D. A., Dubchak, I., Arkin, A., Alm, E. & Gelfand, M. S. ( 2004; ). Reconstruction of regulatory and metabolic pathways in metal-reducing delta-proteobacteria. Genome Biol 5, R90.[CrossRef]
    [Google Scholar]
  34. Rodrigues, R., Valente, F. M., Pereira, I. A., Oliveira, S. & Rodrigues-Pousada, C. ( 2003; ). A novel membrane-bound Ech [NiFe] hydrogenase in Desulfovibrio gigas. Biochem Biophys Res Commun 306, 366–375.[CrossRef]
    [Google Scholar]
  35. Schink, B. ( 1997; ). Energetics of syntrophic cooperation in methanogenic degradation. Microbiol Mol Biol Rev 61, 262–280.
    [Google Scholar]
  36. Schink, B. ( 2002; ). Synergistic interactions in the microbial world. Antonie van Leeuwenhoek 81, 257–261.[CrossRef]
    [Google Scholar]
  37. Scholten, J. C. & Conrad, R. ( 2000; ). Energetics of syntrophic propionate oxidation in defined batch and chemostat cocultures. Appl Environ Microbiol 66, 2934–2942.[CrossRef]
    [Google Scholar]
  38. Scholten, J. C., Culley, D. E., Brockman, F. J., Wu, G. & Zhang, W. ( 2007a; ). Evolution of the syntrophic interaction between Desulfovibrio vulgaris and Methanosarcina barkeri: Involvement of an ancient horizontal gene transfer. Biochem Biophys Res Commun 352, 48–54.[CrossRef]
    [Google Scholar]
  39. Scholten, J. C., Culley, D. E., Nie, L., Munn, K. J., Chow, L., Brockman, F. J. & Zhang, W. ( 2007b; ). Development and assessment of whole-genome oligonucleotide microarrays to analyze an anaerobic microbial community and its responses to oxidative stress. Biochem Biophys Res Commun 358, 571–577.[CrossRef]
    [Google Scholar]
  40. Simon, R. M., Korn, E. L., McShane, L. M., Radmacher, M. D., Wright, G. E. & Zhao, Y. ( 2003; ). Design and Analysis of DNA Microarray Investigations. New York. : Springer.
    [Google Scholar]
  41. Stams, A. J. M. ( 1994; ). Metabolic interactions between anaerobic bacteria in methanogenic environments. Antonie van Leeuwenhoek 66, 271–294.[CrossRef]
    [Google Scholar]
  42. Stams, A. J. M. & Plugge, C. M. ( 2009; ). Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nat Rev Microbiol 7, 568–577.[CrossRef]
    [Google Scholar]
  43. Tang, Y., Pingitore, F., Mukhopadhyay, A., Phan, R., Hazen, T. C. & Keasling, J. D. ( 2007; ). Pathway confirmation and flux analysis of central metabolic pathways in Desulfovibrio vulgaris Hildenborough using gas chromatography-mass spectrometry and Fourier transform-ion cyclotron resonance mass spectrometry. J Bacteriol 189, 940–949.[CrossRef]
    [Google Scholar]
  44. Vignais, P. M., Billoud, B. & Meyer, J. ( 2001; ). Classification and phylogeny of hydrogenases. FEMS Microbiol Rev 25, 455–501.[CrossRef]
    [Google Scholar]
  45. Voordouw, G. ( 1995; ). The genus Desulfovibrio: the centennial. Appl Environ Microbiol 61, 2813–2819.
    [Google Scholar]
  46. Walker, C. B., He, Z., Yang, Z. K., Ringbauer, J. A., Jr, He, Q., Zhou, J., Voordouw, G., Wall, J. D., Arkin, A. P. & other authors ( 2009; ). The electron transfer system of syntrophically grown Desulfovibrio vulgaris. J Bacteriol 191, 5793–5801.[CrossRef]
    [Google Scholar]
  47. Widdel, F. & Hansen, T. A. ( 1991; ). The dissimilatory sulphate and sulphur-reducing bacteria. In The Prokaryotes, 2nd edn, vol. I, pp. 583–624. Edited by Balows, A., Truper, H. G., Dworkin, M., Harder, W. & Schleiter, K. H.. New York. : Springer.
    [Google Scholar]
  48. Winfrey, M. R. & Ward, D. M. ( 1983; ). Substrates for sulfate reduction and methane production in intertidal sediments. Appl Environ Microbiol 45, 193–199.
    [Google Scholar]
  49. Zhang, W., Culley, D. E., Scholten, J. C., Hogan, M., Vitiritti, L. & Brockman, F. J. ( 2006a; ). Global transcriptomic analysis of Desulfovibrio vulgaris on different electron donors. Antonie van Leeuwenhoek 89, 221–237.[CrossRef]
    [Google Scholar]
  50. Zhang, W., Culley, D. E., Hogan, M., Vitiritti, L. & Brockman, F. J. ( 2006b; ). Oxidative stress and heat-shock responses in Desulfovibrio vulgaris by genome-wide transcriptomic analysis. Antonie van Leeuwenhoek 90, 41–55.[CrossRef]
    [Google Scholar]
  51. Zhang, W., Gritsenko, M. A., Moore, R. J., Culley, D. E., Nie, L., Petritis, K., Strittmatter, E., Camp, D. G., II, Smith, R. D. & Brockman, F. J. ( 2006c; ). A proteomic view of Desulfovibrio vulgaris metabolism as determined by liquid chromatography coupled with tandem mass spectrometry. Proteomics 6, 4286–4299.[CrossRef]
    [Google Scholar]
  52. Zhang, W., Culley, D. E., Nie, L. & Brockman, F. J. ( 2006d; ). DNA microarray analysis of anaerobic Methanosarcina barkeri reveals responses to heat shock and air exposure. J Ind Microbiol Biotechnol 33, 784–790.[CrossRef]
    [Google Scholar]
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