1887

Abstract

The genome of the sulfate-reducing bacterium Hildenborough encodes three formate dehydrogenases (FDHs), two of which are soluble periplasmic enzymes (FdhAB and FdhABC) and one that is periplasmic but membrane-associated (FdhM). FdhAB and FdhABC were recently shown to be the main enzymes present during growth with lactate, formate or hydrogen. To address the role of these two enzymes, Δ and Δ, mutants were generated and studied. Different phenotypes were observed in the presence of either molybdenum or tungsten, since both enzymes were important for growth on formate in the presence of Mo, whereas in the presence of W only FdhAB played a role. Both Δ and Δ mutants displayed defects in growth with lactate and sulfate providing the first direct evidence for the involvement of formate cycling under these conditions. In support of this mechanism, incubation of concentrated cell suspensions of the mutant strains with lactate and limiting sulfate also gave elevated formate concentrations, as compared to the wild-type strain. In contrast, both mutants grew similarly to the wild-type with H and sulfate. In the absence of sulfate, the wild-type cells produced formate when supplied with H and CO, which resulted from CO reduction by the periplasmic FDHs. The conversion of H and CO to formate allows the reversible storage of reducing power in a much more soluble molecule. Furthermore, we propose this may be an expression of the ability of some sulfate-reducing bacteria to grow by hydrogen oxidation, in syntrophy with organisms that consume formate, but are less efficient in H utilization.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.067868-0
2013-08-01
2019-10-16
Loading full text...

Full text loading...

/deliver/fulltext/micro/159/8/1760.html?itemId=/content/journal/micro/10.1099/mic.0.067868-0&mimeType=html&fmt=ahah

References

  1. Almendra M. J. , Brondino C. D. , Gavel O. , Pereira A. S. , Tavares P. , Bursakov S. , Duarte R. , Caldeira J. , Moura J. J. , Moura I. . ( 1999; ). Purification and characterization of a tungsten-containing formate dehydrogenase from Desulfovibrio gigas. . Biochemistry 38:, 16366–16372. [CrossRef] [PubMed]
    [Google Scholar]
  2. Badziong W. , Ditter B. , Thauer R. K. . ( 1979; ). Acetate and carbon dioxide assimilation by Desulfovibrio vulgaris (Marburg), growing on hydrogen and sulfate as sole energy source. . Arch Microbiol 123:, 301–305. [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] [PubMed]
    [Google Scholar]
  4. Boddien A. , Mellmann D. , Gärtner F. , Jackstell R. , Junge H. , Dyson P. J. , Laurenczy G. , Ludwig R. , Beller M. . ( 2011; ). Efficient dehydrogenation of formic acid using an iron catalyst. . Science 333:, 1733–1736. [CrossRef] [PubMed]
    [Google Scholar]
  5. 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.[PubMed]
    [Google Scholar]
  6. Caffrey S. M. , Park H. S. , Voordouw J. K. , He Z. , Zhou J. , Voordouw G. . ( 2007; ). Function of periplasmic hydrogenases in the sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough. . J Bacteriol 189:, 6159–6167. [CrossRef] [PubMed]
    [Google Scholar]
  7. Chistoserdova L. , Crowther G. J. , Vorholt J. A. , Skovran E. , Portais J. C. , Lidstrom M. E. . ( 2007; ). Identification of a fourth formate dehydrogenase in Methylobacterium extorquens AM1 and confirmation of the essential role of formate oxidation in methylotrophy. . J Bacteriol 189:, 9076–9081. [CrossRef] [PubMed]
    [Google Scholar]
  8. Costa C. , Teixeira M. , LeGall J. , Moura J. J. G. , Moura I. . ( 1997; ). Formate dehydrogenase from Desulfovibrio desulfuricans ATCC 27774: isolation and spectroscopic characterization of the active sites (heme, iron-sulfur centers and molybdenum). . J Biol Inorg Chem 2:, 198–208. [CrossRef]
    [Google Scholar]
  9. da Silva S. M. , Pimentel C. , Valente F. M. A. , Rodrigues-Pousada C. , Pereira I. A. C. . ( 2011; ). Tungsten and molybdenum regulation of formate dehydrogenase expression in Desulfovibrio vulgaris Hildenborough. . J Bacteriol 193:, 2909–2916. [CrossRef] [PubMed]
    [Google Scholar]
  10. Dolfing J. , Jiang B. , Henstra A. M. , Stams A. J. M. , Plugge C. M. . ( 2008; ). Syntrophic growth on formate: a new microbial niche in anoxic environments. . Appl Environ Microbiol 74:, 6126–6131. [CrossRef] [PubMed]
    [Google Scholar]
  11. Ferry J. G. . ( 1990; ). Formate dehydrogenase. . FEMS Microbiol Rev 7:, 377–382.[PubMed] [CrossRef]
    [Google Scholar]
  12. Fu R. D. , Voordouw G. . ( 1997; ). Targeted gene-replacement mutagenesis of dcrA, encoding an oxygen sensor of the sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough. . Microbiology 143:, 1815–1826. [CrossRef] [PubMed]
    [Google Scholar]
  13. Gonzalez P. J. , Rivas M. G. , Mota C. S. , Brondino C. D. , Moura I. , Moura J. J. G. . ( 2013; ). Periplasmic nitrate reductases and formate dehydrogenases: biological control of the chemical properties of Mo and W for fine tuning of reactivity, substrate specificity and metabolic role. . Coord Chem Rev 257:, 315–331. [CrossRef]
    [Google Scholar]
  14. 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] [PubMed]
    [Google Scholar]
  15. Hoehler T. M. , Alperin M. J. , Albert D. B. , Martens C. S. . ( 2001; ). Apparent minimum free energy requirements for methanogenic archaea and sulfate-reducing bacteria in an anoxic marine sediment. . FEMS Microbiol Ecol 38:, 33–41. [CrossRef]
    [Google Scholar]
  16. Hull J. F. , Himeda Y. , Wang W. H. , Hashiguchi B. , Periana R. , Szalda D. J. , Muckerman J. T. , Fujita E. . ( 2012; ). Reversible hydrogen storage using CO2 and a proton-switchable iridium catalyst in aqueous media under mild temperatures and pressures. . Nat Chem 4:, 383–388. [CrossRef] [PubMed]
    [Google Scholar]
  17. Jones J. B. , Stadtman T. C. . ( 1981; ). Selenium-dependent and selenium-independent formate dehydrogenases of Methanococcus vannielii. Separation of the two forms and characterization of the purified selenium-independent form. . J Biol Chem 256:, 656–663.[PubMed]
    [Google Scholar]
  18. Jormakka M. , Törnroth S. , Byrne B. , Iwata S. . ( 2002; ). Molecular basis of proton motive force generation: structure of formate dehydrogenase-N. . Science 295:, 1863–1868. [CrossRef] [PubMed]
    [Google Scholar]
  19. Kim Y. J. , Lee H. S. , Kim E. S. , Bae S. S. , Lim J. K. , Matsumi R. , Lebedinsky A. V. , Sokolova T. G. , Kozhevnikova D. A. . & other authors ( 2010; ). Formate-driven growth coupled with H(2) production. . Nature 467:, 352–355. [CrossRef] [PubMed]
    [Google Scholar]
  20. Kröger A. , Winkler E. , Innerhofer A. , Hackenberg H. , Schägger H. . ( 1979; ). The formate dehydrogenase involved in electron transport from formate to fumarate in Vibrio succinogenes . . Eur J Biochem 94:, 465–475. [CrossRef] [PubMed]
    [Google Scholar]
  21. Leloup J. , Fossing H. , Kohls K. , Holmkvist L. , Borowski C. , 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] [PubMed]
    [Google Scholar]
  22. Li X. , Luo Q. , Wofford N. Q. , Keller K. L. , McInerney M. J. , Wall J. D. , Krumholz L. R. . ( 2009; ). A molybdopterin oxidoreductase is involved in H2 oxidation in Desulfovibrio desulfuricans G20. . J Bacteriol 191:, 2675–2682. [CrossRef] [PubMed]
    [Google Scholar]
  23. Li X. , McInerney M. J. , Stahl D. A. , Krumholz L. R. . ( 2011; ). Metabolism of H2 by Desulfovibrio alaskensis G20 during syntrophic growth on lactate. . Microbiology 157:, 2912–2921. [CrossRef] [PubMed]
    [Google Scholar]
  24. Lupa B. , Hendrickson E. L. , Leigh J. A. , Whitman W. B. . ( 2008; ). Formate-dependent H2 production by the mesophilic methanogen Methanococcus maripaludis. . Appl Environ Microbiol 74:, 6584–6590. [CrossRef] [PubMed]
    [Google Scholar]
  25. Maden B. E. . ( 2000; ). Tetrahydrofolate and tetrahydromethanopterin compared: functionally distinct carriers in C1 metabolism. . Biochem J 350:, 609–629. [CrossRef] [PubMed]
    [Google Scholar]
  26. Matias P. M. , Pereira I. A. C. , Soares C. M. , Carrondo M. A. . ( 2005; ). Sulphate respiration from hydrogen in Desulfovibrio bacteria: a structural biology overview. . Prog Biophys Mol Biol 89:, 292–329. [CrossRef] [PubMed]
    [Google Scholar]
  27. Matson E. G. , Zhang X. N. , Leadbetter J. R. . ( 2010; ). Selenium controls transcription of paralogous formate dehydrogenase genes in the termite gut acetogen, Treponema primitia. . Environ Microbiol 12:, 2245–2258.[PubMed]
    [Google Scholar]
  28. McInerney M. J. , Sieber J. R. , Gunsalus R. P. . ( 2009; ). Syntrophy in anaerobic global carbon cycles. . Curr Opin Biotechnol 20:, 623–632. [CrossRef] [PubMed]
    [Google Scholar]
  29. Mota C. S. , Valette O. , González P. J. , Brondino C. D. , Moura J. J. G. , Moura I. , Dolla A. , Rivas M. G. . ( 2011; ). Effects of molybdate and tungstate on expression levels and biochemical characteristics of formate dehydrogenases produced by Desulfovibrio alaskensis NCIMB 13491. . J Bacteriol 193:, 2917–2923. [CrossRef] [PubMed]
    [Google Scholar]
  30. Müller V. . ( 2003; ). Energy conservation in acetogenic bacteria. . Appl Environ Microbiol 69:, 6345–6353. [CrossRef] [PubMed]
    [Google Scholar]
  31. Müller N. , Worm P. , Schink B. , Stams A. J. M. , Plugge C. M. . ( 2010; ). Syntrophic butyrate and propionate oxidation processes: from genomes to reaction mechanisms. . Environ Microbiol Rep 2:, 489–499. [CrossRef] [PubMed]
    [Google Scholar]
  32. Muyzer G. , Stams A. J. M. . ( 2008; ). The ecology and biotechnology of sulphate-reducing bacteria. . Nat Rev Microbiol 6:, 441–454.[PubMed]
    [Google Scholar]
  33. 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]
  34. Pankhania I. P. , Spormann A. M. , Hamilton W. A. , Thauer R. K. . ( 1988; ). Lactate conversion to acetate, CO2 and H2 in cell suspensions of Desulfovibrio vulgaris (Marburg): indications for the involvement of an energy driven reaction. . Arch Microbiol 150:, 26–31. [CrossRef]
    [Google Scholar]
  35. Pereira P. M. , He Q. , Valente F. M. A. , Xavier A. V. , Zhou J. Z. , 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] [PubMed]
    [Google Scholar]
  36. Pereira I. A. C. , Ramos A. R. , Grein F. , Marques M. C. , da Silva S. M. , Venceslau S. S. . ( 2011; ). A comparative genomic analysis of energy metabolism in sulfate reducing bacteria and archaea. . Front Microbiol 2:, 69. [CrossRef] [PubMed]
    [Google Scholar]
  37. Pierce E. , Xie G. , Barabote R. D. , Saunders E. , Han C. S. , Detter J. C. , Richardson P. , Brettin T. S. , Das A. . & other authors ( 2008; ). The complete genome sequence of Moorella thermoacetica (f. Clostridium thermoaceticum). . Environ Microbiol 10:, 2550–2573. [CrossRef] [PubMed]
    [Google Scholar]
  38. Plugge C. M. , Zhang W. , Scholten J. C. , Stams A. J. . ( 2011; ). Metabolic flexibility of sulfate-reducing bacteria. . Front Microbiol 2:, 81. [CrossRef] [PubMed]
    [Google Scholar]
  39. Popov V. O. , Lamzin V. S. . ( 1994; ). NAD+-dependent formate dehydrogenase. . Biochem J 301:, 625–643.[PubMed]
    [Google Scholar]
  40. Raaijmakers H. , Macieira S. , Dias J. M. , Teixeira S. , Bursakov S. , Huber R. , Moura J. J. G. , Moura I. , Romão M. J. . ( 2002; ). Gene sequence and the 1.8 Å crystal structure of the tungsten-containing formate dehydrogenase from Desulfovibrio gigas . . Structure 10:, 1261–1272. [CrossRef] [PubMed]
    [Google Scholar]
  41. Ragsdale S. W. . ( 2008; ). Enzymology of the Wood-Ljungdahl pathway of acetogenesis. . Ann N Y Acad Sci 1125:, 129–136. [CrossRef] [PubMed]
    [Google Scholar]
  42. Sawers R. G. . ( 2005; ). Formate and its role in hydrogen production in Escherichia coli. . Biochem Soc Trans 33:, 42–46. [CrossRef] [PubMed]
    [Google Scholar]
  43. Schauer N. L. , Ferry J. G. . ( 1982; ). Properties of formate dehydrogenase in Methanobacterium formicicum. . J Bacteriol 150:, 1–7.[PubMed]
    [Google Scholar]
  44. Schink B. . ( 1997; ). Energetics of syntrophic cooperation in methanogenic degradation. . Microbiol Mol Biol Rev 61:, 262–280.[PubMed]
    [Google Scholar]
  45. Schink B. , Stams A. . ( 2006; ). Syntrophism among Prokaryotes. . In The Prokaryotes, pp. 309–335. Edited by Dworkin M. , Falkow S. , Rosenberg E. , Schleifer K.-H. , Stackebrandt E. . . New York:: Springer-Verlag;. [CrossRef]
    [Google Scholar]
  46. Schweizer H. P. . ( 1992; ). Allelic exchange in Pseudomonas aeruginosa using novel ColE1-type vectors and a family of cassettes containing a portable oriT and the counter-selectable Bacillus subtilis sacB marker. . Mol Microbiol 6:, 1195–1204.[PubMed] [CrossRef]
    [Google Scholar]
  47. Sebban C. , Blanchard L. , Bruschi M. , Guerlesquin F. . ( 1995; ). Purification and characterization of the formate dehydrogenase from Desulfovibrio vulgaris Hildenborough. . FEMS Microbiol Lett 133:, 143–149. [CrossRef] [PubMed]
    [Google Scholar]
  48. Simon J. , van Spanning R. J. M. , Richardson D. J. . ( 2008; ). The organisation of proton motive and non-proton motive redox loops in prokaryotic respiratory systems. . Biochim Biophys Acta 1777:, 1480–1490. [CrossRef] [PubMed]
    [Google Scholar]
  49. 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] [PubMed]
    [Google Scholar]
  50. Stolyar S. , Van Dien S. , Hillesland K. L. , Pinel N. , Lie T. J. , Leigh J. A. , Stahl D. A. . ( 2007; ). Metabolic modeling of a mutualistic microbial community. . Mol Syst Biol 3:, 92. [CrossRef] [PubMed]
    [Google Scholar]
  51. 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] [PubMed]
    [Google Scholar]
  52. Thauer R. K. , Shima S. . ( 2008; ). Methane as fuel for anaerobic microorganisms. . Ann N Y Acad Sci 1125:, 158–170. [CrossRef] [PubMed]
    [Google Scholar]
  53. Venceslau S. S. , Lino R. R. , Pereira I. A. C. . ( 2010; ). The Qrc membrane complex, related to the alternative complex III, is a menaquinone reductase involved in sulfate respiration. . J Biol Chem 285:, 22774–22783. [CrossRef] [PubMed]
    [Google Scholar]
  54. Voordouw G. . ( 2002; ). Carbon monoxide cycling by Desulfovibrio vulgaris Hildenborough. . J Bacteriol 184:, 5903–5911. [CrossRef] [PubMed]
    [Google Scholar]
  55. Vorholt J. A. , Thauer R. K. . ( 2002; ). Molybdenum and tungsten enzymes in C1 metabolism. . In Metal Ions in Biological Systems, pp. 571–619. Edited by Sigel A. , Sigel H. . . New York:: Taylor & Francis;. [CrossRef]
    [Google Scholar]
  56. Wood G. E. , Haydock A. K. , Leigh J. A. . ( 2003; ). Function and regulation of the formate dehydrogenase genes of the methanogenic archaeon Methanococcus maripaludis. . J Bacteriol 185:, 2548–2554. [CrossRef] [PubMed]
    [Google Scholar]
  57. Zhang W. W. , Culley D. E. , Scholten J. C. M. , Hogan M. , Vitiritti L. , Brockman F. J. . ( 2006; ). Global transcriptomic analysis of Desulfovibrio vulgaris on different electron donors. . Antonie van Leeuwenhoek 89:, 221–237. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.067868-0
Loading
/content/journal/micro/10.1099/mic.0.067868-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error