Periplasmic Cytochrome c3 of Desulfovibrio vulgaris Is Directly Involved in H2-Mediated Metal but Not Sulfate Reduction

Applied and Environmental Microbiology

Volumn 70, Issue 1, 2004, Pages 413-420

  Elias, Dwayne A ^a,b   Suflita, Joseph M ^a   McInerney, Michael J ^a   Krumholz, Lee R ^a  

^a UNIVERSITY OF OKLAHOMA   (United States)

^b PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; BIOASSAY; CELL CULTURE; OXIDATION; REDUCTION; SULFATE MINERALS;

KINETIC PARAMETERS;

MICROBIOLOGY;

CYTOCHROME C; HYDROXIDE; IRON; LACTIC ACID; METAL; OXIDOREDUCTASE; PYRUVIC ACID; SULFATE; URANIUM; CYTOCHROME C(3); FERRIC ION; HYDROGEN;

ARTICLE; BACTERIAL GROWTH; BACTERIUM CULTURE; CELL CULTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOPLASM; DESULFOVIBRIO VULGARIS; ELECTRON; KINETICS; MICHAELIS CONSTANT; NONHUMAN; OXIDATION; OXIDATION REDUCTION REACTION; REDUCTION; ELECTRON TRANSPORT; ENZYMOLOGY; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

BACTERIA (MICROORGANISMS); DESULFOVIBRIO; DESULFOVIBRIO VULGARIS; DESULFOVIBRIO VULGARIS SUBSP. VULGARIS STR. HILDENBOROUGH; NEGIBACTERIA;

CYTOCHROME C GROUP; DESULFOVIBRIO VULGARIS; ELECTRON TRANSPORT; FERRIC COMPOUNDS; HYDROGEN; OXIDATION-REDUCTION; PERIPLASM; SULFATES; URANIUM;

EID: 0346499668     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.70.1.413-420.2004     Document Type: Article

References (64)

1. r 26,000) greatly affects the molecular reactivity. J. Biol. Chem. 272:15128-15134.
2. Badziong, W., and R. K. Thauer. 1980. Vectorial electron transport in Desulfovibrio vulgaris (Marburg) growing on hydrogen plus sulfate as sole energy source. Arch. Microbiol. 125:167-174.
3. Balch, W. E., and R. S. Wolfe. 1976. New approach to the cultivation of methanogenic bacteria: 2-mercaptoethanesulfonic acid (HS-CoM)-dependent growth of Methanobacterium ruminantium in a pressurized atmosphere. Appl. Environ. Microbiol. 32:781-791.
4. Brina, R., and A. G. Miller. 1992. Direct detection of trace levels of uranium by laser-induced kinetic phosphorimetry. Anal. Chem. 64:1413-1418.
5. 3 and Fe-only hydrogenase from Delsulfovibrio vulgaris Hildenborough. Proteins Struct. Funct. Genet. 33:590-600.
6. Bruschi, M., P. Bertrand, C. More, G. Leroy, J. Bonicel, J. Haladjian, G. Chottard, W. B. R. Pollock, and G. Voordouw. 1992. Biochemical and spectroscopic characterization of the high molecular weight cytochrome c from Desulfovibrio vulgaris Hildenborough expressed in Desulfovibrio desulfuricans G200. Biochemistry 31:3281-3288.
7. 3. Biochem. Biophys. Res. Commun. 120:384-389.
8. Cline, J. D. 1969. Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol. Oceanogr. 14:454-458.
9. Cypionka, H. 2000. Oxygen respiration by Desulfovibrio species. Annu. Rev. Microbiol. 54:827-848.
10. Daniels, L., and D. Wessels. 1984. A method for the spectrophotometric assay of anaerobic enzymes. Anal. Biochem. 141:232-237.
11. 2 or nitrate by sulfate-reducing bacteria. Arch. Microbiol. 158:93-99.
12. Dilling, W., and H. Cypionka. 1990. Aerobic respiration in sulfate-reducing bacteria. FEMS Microbiol. Lett. 71:123-128.
13. 3-ferrodoxin electron transfer complex: cross-linking studies. Biochim. Biophys. Acta 932:26-32.
14. Dolla, A., B. K. J. Pohorelic, J. K. Voordouw, and G. Voordouw. 2000. Deletion of the hmc operon of Desulfovibrio vulgaris subsp. vulgaris Hildenborough hampers hydrogen metabolism and low-redox-polential niche establishment. Arch. Microbiol. 174:143-151.
15. 3 at 1.8 Å resolution. J. Mol. Biol. 172:109-139.
16. Kentemich, T., M. Bahnweg, F. Mayer, and H. Bothe. 1989. Localization of the reversible hydrogenase in cyanobacteria. Zeitschr. Naturforsch. C 44:384-391.
17. Keon, R. G., F. Rongdian, and G. Voordouw. 1997. Deletion of the two downstream genes alters expression of the hmc operon of Desulfovibrio vulgaris subsp. vulgaris Hildenborough. Arch. Microbiol. 167:376-383.
18. Lemos, R. S., C. M. Gomes, M. Santana, J. LeGall, A. V. Xavier, and M. Teixeira. 2001. The "strict" anaerobe Desulfovibrio gigas contains a membrane-bound oxygen-reducing respiratory chain. FEBS Lett. 496:40-43.
19. 3 from Desulphovibrio desulphuricans M6. Anaerobe 7:263-269.
20. Liu, C., S. Kota, J. M. Zachara, J. K. Fredrickson, and C. K. Brinkman. 2001. Kinetic analysis of the bacterial reduction of goethite. Environ. Sci. Technol. 35:2482-2490.
21. Liu, C., J. M. Zachara, Y. A. Gorby, J. E. Szecsody, and C. F. Brown. 2001. Microbial reduction of Fe(III) and sorption/precipitation of Fe(II) on Shewanella putrefaciens strain CN32. Environ. Sci. Technol. 35:1385-1393.
22. Lovley, D. R., and E. J. P. Phillips. 1992. Bioremediation of uranium contamination with enzymatic uranium reduction. Environ. Sci. Technol. 26:2228-2234.
23. Lovley, D. R., and E. J. P. Phillips. 1987. Rapid assay for mierobially reducible ferric iron in aquatic sediments. Appl. Environ. Microbiol. 53:1536-1540.
24. 3 cytochrome. Appl. Environ. Microbiol. 60:726-728.
25. Lovley, D. R., and E. J. P. Phillips. 1992. Reduction of uranium by Desulfovibrio desulfuricans. Appl. Environ. Microbiol. 58:850-856.
26. Lovley, D. R., E. E. Roden, E. J. P. Phillips, and J. C. Woodward. 1993. Enzymatic iron and uranium reduction by sulfate-reducing bacteria. Mar. Geol. 113:41-53.
27. 3 of Desulfovibrio vulgaris. Appl. Environ. Microbiol. 59:3572-3576.
28. Marschall, C., P. Frenzel, and H. Cypionka. 1993. Influence of oxygen on sulfate reduction and growth of sulfate-reducing bacteria. Arch. Microbiol. 159:168-173.
29. Masau, R. J. Y., J. K. Oh, and I. Suzuki. 2001. Mechanism of oxidation of inorganic sulfur compounds by thiosulfate-grown Thiobacillus thiooxidans. Can. J. Microbiol. 47:348-358.
30. McKinley, J. P., J. M. Zachara, S. Smith, and G. D. Turner. 1995. The influence of uranyl hydrolysis and multiple site-binding reactions on adsorption of U(VI) to montmorillonite. Clays Clay Min. 43:586-598.
31. 3: a class of electron transfer heme proteins found in both photosynthetic and sulfate-reducing bacteria. Biochim. Biophys. Acta 245:453-464.
32. Noguera, D. R., G. A. Brusseau, B. E. Rittmann, and D. A. Stahl. 1998. A unified model describing the role of hydrogen in the growth in Desulfovibrio vulgaris under different environmental conditions. Biotechnol. Bioeng. 59:732-746.
33. Odom, J. D., and H. D. Peck. 1984. Hydrogenase, electron transfer proteins, and energy coupling in the sulfate-reducing bacteria Desulfovibrio. Annu. Rev. Microbiol. 38:551-592.
34. Odom, J. M., and H. D. Peck. 1981. Hydrogen cycling as a general mechanism for energy coupling in the sulfate-reducing bacteria, Desulfovibrio sp. FEMS Microbiol. Lett. 12:47-50.
35. Odom, J. M., and J. D. Wall. 1987. Properties of a hydrogen-inhibited mutant of Desulfovibrio desulfuricans ATCC 27774. J. Bacteriol. 169:1335-1337.
36. Oremland, R. S., and D. G. Capone. 1988. Use of "specific" inhibitors in biogeochemistry and microbial ecology. Adv. Microb. Ecol. 10:285-383.
37. Pankhania, I. P., L. A. Gow, and W. A. Hamilton. 1986. The effect of hydrogen on the growth of Desulfovibrio vulgaris (Hildenborough) on lactate. J. Gen. Microbiol. 132:3549-3556.
38. 2 in cell suspensions of Desulfovibrio vulgaris (Marburg): indications for the involvement of an energy driven reaction. Arch. Microbiol. 150:26-31.
39. 3 mutant. Appl. Environ. Microbiol. 68:3129-3132.
40. 3. J. Biol. Chem. 257:14341-14348.
41. Pietzsch, K., B. C. Hard, and W. Babel. 1999. A Desulfovibrio sp. capable of growing by reducing U(VI). J. Basic Microbiol. 39:365-372.
42. Pohorelic, B. K. J., J. K. Voordoouw, E. Lojou, A. Dolla, J. Harder, and G. Voordouw. 2002. Effects of deletion of genes encoding Fe-only hydrogenase of Desulfovibrio vulgaris Hildenborough on hydrogen and lactate metabolism. J. Bacteriol. 184:679-686.
43. Pollock, W. B. R., M. Loutfi, M. Bruschi, B. J. Rapp-Giles, J. D. Wall, and G. Voordouw. 1991. Cloning, sequencing, and expression of the gene encoding the high-molecular-weight cytochrome c from Desulfovibrio vulgaris Hildenborough. J. Bacteriol. 173:220-228.
44. 3 and desulphoviridin: pigments of the anaerobe Desulphovibrio desulphuricans. J. Gen. Microbiol. 14:545-572.
45. 3 mutants in Desulfovibrio desulfuricans. Appl. Environ. Microbiol. 66:671-677.
46. Schnell, F. D. (ed.). 1978. Photometric and fluorometric methods of analysis, p. 1351-1416. John Wiley & Sons, Inc., New York, N.Y.
47. Segel, I. H. 1975. Enzyme kinetics: behavior and analysis of rapid equilibrium and steady state enzyme systems. John Wiley & Sons, Inc., New York, N.Y.
48. Senko, J. M., J. D. Istok, J. M. Suflita, and L. R. Krumholz. 2002. In situ evidence for uranium immobilization and remobilization. Environ. Sci. Technol. 36:1491-1496.
49. Spear, J. R., L. A. Figueroa, and B. D. Honeyman. 2000. Modeling reduction of uranium(VI) under variable sulfate concentrations by sulfate-reducing bacteria. Appl. Environ. Microbiol. 66:3711-3721.
50. Spear, J. R., L. A. Figueroa, and B. D. Honeyman. 1999. Modeling the removal of uranium(VI) from aqueous solutions in the presence of sulfate-reducing bacteria. Environ. Sci. Technol. 33:2667-2675.
51. Steger, J. L., C. Vincent, J. D. Ballard, and L. R. Krumholz. 2002. Desulfovibrio sp. genes involved in the respiration of sulfate during metabolism of hydrogen and lactate. Appl. Environ. Microbiol. 68:1932-1937.
52. 3 and hydrogenase. Arch. Microbiol. 162:255-260.
53. Tan, J., and J. A. Cowan. 1990. Coordination and redox properties of a triheme cytochrome from Desulfovibrio vulgaris (Hildenborough). Biochemistry 29:4886-4892.
54. Tebo, B. M., and A. Y. Obraztsova. 1998. Sulfate-reducing bacterium grows with Cr(VI), U(VI), Mn(IV), and Fe(III) as electron acceptors. FEMS Microbiol. Lett. 162:193-198.
55. Thony-Meyer, L. 1997. Biogenesis of respiratory cytochromes in bacteria. Microbiol. Mol. Biol. Rev. 61:337-376.
56. Tucker, M. D., L. L. Barton, and B. M. Thomson. 1996. Kinetic coefficients for simultaneous reduction of sulfate and uranium by Desulfovibrio desulfuricans. Appl. Microbiol. Biotechnol. 46:74-77.
57. Ulrich, G. A., L. R. Krumholz, and J. M. Suflita. 1997. A rapid and simple method for estimating sulfate reduction activity and quantifying inorganic sulfides. Appl. Environ. Microbiol. 63:1627-1630.
58. 3 from Desulfovibrio vulgaris Hildenborough. Chembiochem. 2:895-905.
59. 553 from Desulfovibrio vulgaris (Hildenborough): electrochemical properties and electron transfer with hydrogenase. Eur. J. Biochem. 221:821-829.
60. Voordouw, G. 2002. Carbon monoxide cycling by Desulfovibrio vulgaris Hildenborough. J. Bacteriol. 184:5903-5911.
61. 3 from Desulfovibrio vulgaris (Hildenborough). Eur. J. Biochem. 159:347-351.
62. 3 in Desulfovibrio desulfuricans G200 after conjugational gene transfer from Escherichia coli. J. Bacteriol. 172:6122-6126.
63. + in Methanosphaera stadtmanae. FEMS Microbiol. Lett. 120:285-290.
64. Zellner, G., F. Neudorfer, and H. Diekmann. 1994. Degradation of lactate by an anaerobic mixed culture in a fluidized-bed reactor. Water Res. 28:1337-1340.