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. 1981 Jul;147(1):161–169. doi: 10.1128/jb.147.1.161-169.1981

Localization of dehydrogenases, reductases, and electron transfer components in the sulfate-reducing bacterium Desulfovibrio gigas.

J M Odom, H D Peck Jr
PMCID: PMC216020  PMID: 7240092

Abstract

Various dehydrogenases, reductases, and electron transfer proteins involved in respiratory sulfate reduction by Desulfovibrio gigas have been localized with respect to the periplasmic space, membrane, and cytoplasm. This species was grown on a lactate-sulfate medium, and the distribution of enzyme activities and concentrations of electron transfer components were determined in intact cells, cell fractions prepared with a French press, and lysozyme spheroplasts. A significant fraction of formate dehydrogenase was demonstrated to be localized in the periplasmic space in addition to hydrogenase and some c-type cytochrome. Cytochrome b, menaquinone, fumarate reductase, and nitrite reductase were largely localized on the cytoplasmic membrane. Fumarate reductase was situated on the inner aspect on the membrane, and the nitrite reductase appeared to be transmembraneous. Adenylylsulfate reductase, bisulfite reductase (desulfoviridin), pyruvate dehydrogenase, and succinate dehydrogenase activities were localized in the cytoplasm. Significant amounts of hydrogenase and c-type cytochromes were also detected in the cytoplasm. Growth of D. gigas on a formate-sulfate medium containing acetate resulted in a 10-fold increase in membrane-bound formate dehydrogenase and a doubling of c-type cytochromes. Growth on fumarate with formate resulted in an additional increase in b-type cytochrome compared with lactate-sulfate-grown cells.

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Selected References

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  1. Barton L. L., Le Gall J., Peck H. D., Jr Phosphorylation coupled to oxidation of hydrogen with fumarate in extracts of the sulfate reducing bacterium, Desulfovibrio gigas. Biochem Biophys Res Commun. 1970 Nov 25;41(4):1036–1042. doi: 10.1016/0006-291x(70)90189-0. [DOI] [PubMed] [Google Scholar]
  2. Beacham I. R. Periplasmic enzymes in gram-negative bacteria. Int J Biochem. 1979;10(11):877–883. doi: 10.1016/0020-711x(79)90117-4. [DOI] [PubMed] [Google Scholar]
  3. Bell G. R., LeGall L., Peck H. D. Evidence for the periplasmic location of hydrogenase in Desulfovibrio gigas. J Bacteriol. 1974 Nov;120(2):994–997. doi: 10.1128/jb.120.2.994-997.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bell G. R., Lee J. P., Peck H. D., Jr, Gall J. L. Reactivity of Desulfovibrio gigas hydrogenase toward artificial and natural electron donors or acceptors. Biochimie. 1978;60(3):315–320. doi: 10.1016/s0300-9084(78)80828-1. [DOI] [PubMed] [Google Scholar]
  5. Bramlett R. N., Peck H. D., Jr Some physical and kinetic properties of adenylyl sulfate reductase from Desulfovibrio vulgaris. J Biol Chem. 1975 Apr 25;250(8):2979–2986. [PubMed] [Google Scholar]
  6. Bryant M. P., Campbell L. L., Reddy C. A., Crabill M. R. Growth of desulfovibrio in lactate or ethanol media low in sulfate in association with H2-utilizing methanogenic bacteria. Appl Environ Microbiol. 1977 May;33(5):1162–1169. doi: 10.1128/aem.33.5.1162-1169.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dorn M., Andreesen J. R., Gottschalk G. Fumarate reductase of Clostridium formicoaceticum. A peripheral membrane protein. Arch Microbiol. 1978 Oct 4;119(1):7–11. doi: 10.1007/BF00407920. [DOI] [PubMed] [Google Scholar]
  8. Drake H. L., Akagi J. M. Dissimilatory reduction of bisulfite by Desulfovibrio vulgaris. J Bacteriol. 1978 Dec;136(3):916–923. doi: 10.1128/jb.136.3.916-923.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fauque G., Herve D., Le Gall J. Structure-function relationship in hemoproteins: the role of cytochrome c3 in the reduction of colloidal sulfur by sulfate-reducing bacteria. Arch Microbiol. 1979 Jun;121(3):261–264. doi: 10.1007/BF00425065. [DOI] [PubMed] [Google Scholar]
  10. Futai M. Orientation of membrane vesicles from Escherichia coli prepared by different procedures. J Membr Biol. 1974;15(1):15–28. doi: 10.1007/BF01870079. [DOI] [PubMed] [Google Scholar]
  11. Glenn A. R. Production of extracellular proteins by bacteria. Annu Rev Microbiol. 1976;30:41–62. doi: 10.1146/annurev.mi.30.100176.000353. [DOI] [PubMed] [Google Scholar]
  12. Harold F. M. Conservation and transformation of energy by bacterial membranes. Bacteriol Rev. 1972 Jun;36(2):172–230. doi: 10.1128/br.36.2.172-230.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hatchikian E. C., Bruschi M., Le Gall J. Characterization of the periplasmic hydrogenase from Desulfovibrio gigas. Biochem Biophys Res Commun. 1978 May 30;82(2):451–461. doi: 10.1016/0006-291x(78)90896-3. [DOI] [PubMed] [Google Scholar]
  14. Hatchikian E. C., Le Gall J., Bruschi M., Dubourdieu M. Regulation of the reduction of sulfite and thiosulfate by ferredoxin, flavodoxin and cytochrome cc' 3 in extracts of the sulfate reducer Desulfovibrio gigas. Biochim Biophys Acta. 1972 Mar 8;258(3):701–708. doi: 10.1016/0005-2744(72)90171-4. [DOI] [PubMed] [Google Scholar]
  15. Hatchikian E. C., Le Gall J. Evidence for the presence of a b-type cytochrome in the sulfate-reducing bacterium Desulfovibrio gigas, and its role in the reduction of fumarate by molecular hydrogen. Biochim Biophys Acta. 1972 Jun 23;267(3):479–484. doi: 10.1016/0005-2728(72)90175-2. [DOI] [PubMed] [Google Scholar]
  16. Hatchikian E. C. On the role of menaquinone-6 in the electron transport of hydrogen: fumarate reductase system in the strict anaerobe Desulfovibrio gigas. J Gen Microbiol. 1974 Mar;81(1):261–266. doi: 10.1099/00221287-81-1-261. [DOI] [PubMed] [Google Scholar]
  17. Jones H. E., Skyring G. W. Effect of enzymic assay conditions on sulfite reduction catalysed by desulfoviridin from Desulfovibrio gigas. Biochim Biophys Acta. 1975 Jan 23;377(1):52–60. doi: 10.1016/0005-2744(75)90285-5. [DOI] [PubMed] [Google Scholar]
  18. Jones R. W., Garland P. B. Sites and specificity of the reaction of bipyridylium compounds with anaerobic respiratory enzymes of Escherichia coli. Effects of permeability barriers imposed by the cytoplasmic membrane. Biochem J. 1977 Apr 15;164(1):199–211. doi: 10.1042/bj1640199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Klingenberg M. Localization of the glycerol-phosphate dehydrogenase in the outer phase of the mitochondrial inner membrane. Eur J Biochem. 1970 Apr;13(2):247–252. doi: 10.1111/j.1432-1033.1970.tb00924.x. [DOI] [PubMed] [Google Scholar]
  20. Kobayashi K., Morisawa Y., Ishituka T., Ishimoto M. Biochemical studies on sulfate-reducing bacteria. XIV. Enzyme levels of adenylylsulfate reductase, inorganic pyrophosphatase, sulfite reductase, hydrogenase, and adenosine triphosphatase in cells grown on sulfate, sulfite, and thiosulfate. J Biochem. 1975 Nov;78(5):1079–1085. doi: 10.1093/oxfordjournals.jbchem.a130985. [DOI] [PubMed] [Google Scholar]
  21. Kröger A. Fumarate as terminal acceptor of phosphorylative electron transport. Biochim Biophys Acta. 1978 Oct 23;505(2):129–145. doi: 10.1016/0304-4173(78)90010-1. [DOI] [PubMed] [Google Scholar]
  22. LEGALL J., MAZZA G., DRAGONI N. LE CYTOCHROME C3 DE DESULFOVIBRIO GIGAS. Biochim Biophys Acta. 1965 May 18;99:385–387. [PubMed] [Google Scholar]
  23. Le Gall J., Dragoni N. Dependance of sulfite reduction on a crystallized ferredoxin from Desulfovibrio gigas. Biochem Biophys Res Commun. 1966 Apr 19;23(2):145–149. doi: 10.1016/0006-291x(66)90519-5. [DOI] [PubMed] [Google Scholar]
  24. Lee J. P., LeGall J., Peck H. D., Jr Isolation of assimilatroy- and dissimilatory-type sulfite reductases from Desulfovibrio vulgaris. J Bacteriol. 1973 Aug;115(2):529–542. doi: 10.1128/jb.115.2.529-542.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Maroc J., Azerad R., Kamen M. D., Le Gall J. Menaquinone (MK-6) in the sulfate-reducing obligate anaerobe, Desulfovibrio. Biochim Biophys Acta. 1970 Jan 13;197(1):87–89. doi: 10.1016/0005-2728(70)90012-5. [DOI] [PubMed] [Google Scholar]
  26. PECK H. D., Jr Evidence for oxidative phosphorylation during the reduction of sulfate with hydrogen by Desulfovibrio desulfuricans. J Biol Chem. 1960 Sep;235:2734–2738. [PubMed] [Google Scholar]
  27. PECK H. D., Jr The role of adenosine-5'-phosphosulfate in the reduction of sulfate to sulfite by Desulfovibrio desulfuricans. J Biol Chem. 1962 Jan;237:198–203. [PubMed] [Google Scholar]
  28. Peck H. D., Jr Phosphorylation coupled with electron transfer in extracts of the sulfate reducing bacterium, Desulfovibrio gigas. Biochem Biophys Res Commun. 1966 Jan 4;22(1):112–118. doi: 10.1016/0006-291x(66)90611-5. [DOI] [PubMed] [Google Scholar]
  29. Shipp W. S. Cytochromes of Escherichia coli. Arch Biochem Biophys. 1972 Jun;150(2):459–472. doi: 10.1016/0003-9861(72)90063-x. [DOI] [PubMed] [Google Scholar]
  30. Steenkamp D. J., Peck H. D., Jr The association of hydrogenase and dithionite reductase activities with the nitrite reductase of Desulfovibrio desulfuricans. Biochem Biophys Res Commun. 1980 May 14;94(1):41–48. doi: 10.1016/s0006-291x(80)80184-7. [DOI] [PubMed] [Google Scholar]
  31. Van de Bogart M., Beinert H. Micro methods for the quantitative determination of iron and copper in biological material. Anal Biochem. 1967 Aug;20(2):325–334. doi: 10.1016/0003-2697(67)90038-3. [DOI] [PubMed] [Google Scholar]
  32. Wanner B. L., Sarthy A., Beckwith J. Escherichia coli pleiotropic mutant that reduces amounts of several periplasmic and outer membrane proteins. J Bacteriol. 1979 Oct;140(1):229–239. doi: 10.1128/jb.140.1.229-239.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Weber M. M., Matschiner J. T., Peck H. D. Menaquinone-6 in the strict anaerobes Desulfovibrio vulgaris and Desulfovibrio gigas. Biochem Biophys Res Commun. 1970 Jan 23;38(2):197–204. doi: 10.1016/0006-291x(70)90696-0. [DOI] [PubMed] [Google Scholar]
  34. Wood P. M. A chemiosmotic model for sulphate respiration. FEBS Lett. 1978 Nov 1;95(1):12–18. doi: 10.1016/0014-5793(78)80042-8. [DOI] [PubMed] [Google Scholar]
  35. Yagi T. Formate: cytochrome oxidoreductase of Desulfovibrio vulgaris. J Biochem. 1969 Oct;66(4):473–478. doi: 10.1093/oxfordjournals.jbchem.a129171. [DOI] [PubMed] [Google Scholar]
  36. Yagi T. Purification and properties of cytochrome c-553, an electron acceptor for formate dehydrogenase of Desulfovibrio vulgaris, Miyazaki. Biochim Biophys Acta. 1979 Oct 10;548(1):96–105. doi: 10.1016/0005-2728(79)90190-7. [DOI] [PubMed] [Google Scholar]
  37. van der Westen H. M., Mayhew S. G., Veeger C. Separation of hydrogenase from intact cells of Desulfovibrio vulgaris. Purification and properties. FEBS Lett. 1978 Feb 1;86(1):122–126. doi: 10.1016/0014-5793(78)80112-4. [DOI] [PubMed] [Google Scholar]

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