Vanadium(V) Reduction by Shewanella oneidensis MR-1 Requires Menaquinone and Cytochromes from the Cytoplasmic and Outer Membranes

Applied and Environmental Microbiology

Volumn 70, Issue 3, 2004, Pages 1405-1412

  Myers, Judith M ^a   Antholine, William E ^a   Myers, Charles R ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; CELL CULTURE; CELL MEMBRANES; ELECTRON TRANSPORT PROPERTIES; PARAMAGNETIC RESONANCE;

CYTOCHROMES;

BACTERIOLOGY;

CYTOCHROME; CYTOCHROME OMCA; MENAQUINONE; UNCLASSIFIED DRUG; VANADIUM;

BACTERIUM;

ANAEROBIC METABOLISM; ARTICLE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL MEMBRANE; BACTERIAL METABOLISM; BACTERIAL STRAIN; CELL MEMBRANE; ELECTRON SPIN RESONANCE; ELECTRON TRANSPORT; GENETIC CODE; NONHUMAN; REDUCTION; RESPIRATORY CHAIN; SHEWANELLA ONEIDENSIS;

BASE SEQUENCE; CELL MEMBRANE; CYTOCHROMES; CYTOPLASM; DNA, BACTERIAL; ELECTRON TRANSPORT; MUTATION; OXIDATION-REDUCTION; SHEWANELLA; VANADIUM; VITAMIN K 2;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; SHEWANELLA; SHEWANELLA ONEIDENSIS MR-1;

EID: 1642364960     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.70.3.1405-1412.2004     Document Type: Article

References (47)

1. Beliaev, A. S., D. K. Thompson, M. W. Fields, L. Wu, D. P. Lies, K. H. Nealson, and J. Zhou. 2002. Microarray transcription profiling of a Shewanella oneidensis etrA mutant. J. Bacteriol. 184:4612-4616.
2. Carpentier, W., K. Sandra, I. De Smet, A. Brigé, L. De Smet, and J. Van Beeumen. 2003. Microbial reduction and precipitation of vanadium by Shewanella oneidensis. Appl. Environ. Microbiol. 69:3636-3639.
3. Costigan, M., R. Cary, and S. Dobson. 2001. Vanadium pentoxide and other inorganic vanadium compounds. World Health Organization, Geneva, Switzerland.
4. Domingo, J. L., J. M. Llobet, and J. Corbella. 1985. Protection of mice against the lethal effects of sodium metavanadate: a quantitative comparison of a number of chelating agents. Toxicol. Lett. 26:95-99.
5. Donaldson, J., R. Hemming, and F. LaBella. 1985. Vanadium exposure enhances lipid peroxidation in the kidney of rats and mice. Can. J. Physiol. Pharmacol. 63:196-199.
6. Gunsalus, R. P. 1992. Control of electron flow in Escherichia coli: coordinated transcription of respiratory pathway genes. J. Bacteriol. 174:7069-7074.
7. Heidelberg, J. F., I. T. Paulsen, K. E. Nelson, E. J. Gaidos, W. C. Nelson, T. D. Read, J. A. Eisen, R. Seshadri, N. Ward, B. Methe, R. A. Clayton, T. Meyer, A. Tsapin, J. Scott, M. Beanan, L. Brinkac, S. Daugherty, R. T. DeBoy, R. J. Dodson, A. S. Durkin, D. H. Haft, J. F. Kolonay, R. Madupu, J. D. Peterson, L. A. Umayam, O. White, A. M. Wolf, J. Vamathevan, J. Weidman, M. Impraim, K. Lee, K. Berry, C. Lee, J. Mueller, H. Khouri, J. Gill, T. R. Utterback, L. A. McDonald, T. V. Feldblyum, H. O. Smith, J. C. Venter, K. H. Nealson, and C. M. Fraser. 2002. Genome sequence of the dissimilatory metal ion-reducing bacterium Shewanella oneidensis. Nat. Biotechnol. 20:1118-1123.
8. Hunke, S., S. Dose, and E. Schneider. 1995. Vanadate and bafilomycin AI are potent inhibitors of the ATPase activity of the reconstituted bacterial ATP-binding cassette transporter for maltose (MalFGK2). Biochem. Biophys. Res. Commun. 216:589-594.
9. Irwin, R. J., M. VanMouwerick, L. Stevens, M. D. Sesse, and W. Basham. 1997. Vanadium. In Environmental contaminants encyclopedia. National Park Service, Water Resources Division, Fort Collins, Colo. [Online.]
10. Knauf, V. C., and E. W. Nester. 1982. Wide host range cloning vectors: cosmid clone bank of Agrobacterium Ti plasmids. Plasmid 8:45-54.
11. Lovley, D. R. 1993. Dissimilatory metal reduction. Annu. Rev. Microbiol. 47:263-290.
12. Lovley, D. R., and E. J. P. Phillips. 1988. Novel mode of microbial energy metabolism: organic carbon oxidation coupled to dissimilatory reduction of iron or manganese. Appl. Environ. Microbiol. 54:1472-1480.
13. Maier, T. M., and C. R. Myers. 2001. Isolation and characterization of a Shewanella putrefaciens MR-1 electron transport regulator etrA mutant: reassessment of the role of EtrA. J. Bacteriol. 183:4918-4926.
14. Maier, T. M., J. M. Myers, and C. R. Myers. 2003. Identification of the gene encoding the sole physiological fumarate reductase of Shewanella putrefaciens MR-1. J. Basic Microbiol. 43:312-327.
15. Mendz, G. L. 1999. Redox and specific effects of vanadium ions on respiratory enzymes. Biometals 12:35-45.
16. Morris, C. J., A. C. Black, S. L. Pealing, F. D. C. Manson, S. K. Chapman, G. A. Reid, D. M. Gibson, and B. F. Ward. 1994. Purification and properties of a novel cytochrome: flavocytochrome c from Shewanella putrefaciens. Biochem. J. 302:587-593.
17. Myers, C. R., and J. M. Myers. 1992. Fumarate reductase is a soluble enzyme in anaerobically grown Shewanella putrefaciens MR-1. FEMS Microbiol. Lett. 98:13-20.
18. Myers, C. R., and J. M. Myers. 1992. Localization of cytochromes to the outer membrane of anaerobically grown Shewanella putrefaciens MR-1. J. Bacteriol. 174:3429-3438.
19. Myers, C. R., and J. M. Myers. 1993. Ferric reductase is associated with the membranes of anaerobically grown Shewanella putrefaciens MR-1. FEMS Microbiol. Lett. 108:15-22.
20. Myers, C. R., and J. M. Myers. 1993. Role of menaquinone in the reduction of fumarate, nitrate, iron(III) and manganese(IV) by Shewanella putrefaciens MR-1. FEMS Microbiol. Lett. 114:215-222.
21. Myers, C. R., and J. M. Myers. 1994. Ferric iron reduction-linked growth yields of Shewanella putrefaciens MR-1. J. Appl. Bacteriol. 76:253-258.
22. Myers, C. R., and J. M. Myers. 1997. Cloning and sequence of cymA, a gene encoding a tetraheme cytochrome c required for reduction of iron(III), fumarate, and nitrate by Shewanella putrefaciens MR-1. J. Bacteriol. 179: 1143-1152.
23. Myers, C. R., and J. M. Myers. 1997. Isolation and characterization of a transposon mutant of Shewanella putrefaciens MR-1 deficient in fumarate reductase. Lett. Appl. Microbiol. 25:162-168.
24. Myers, C. R., and J. M. Myers. 1997. Outer membrane cytochromes of Shewanella putrefaciens MR-1: spectral analysis, and purification of the 83-kDa c-type cytochrome. Biochim. Biophys. Acta 1326:307-318.
25. Myers, C. R., and J. M. Myers. 2002. MtrB is required for proper incorporation of the cytochromes OmcA and OmcB into the outer membrane of Shewanella putrefaciens MR-1. Appl. Environ. Microbiol. 68:5585-5594.
26. Myers, C. R., and J. M. Myers. 2003. Cell surface exposure of the outer membrane cytochromes of Shewanella oneidensis MR-1. Lett. Appl. Microbiol. 37:254-258.
27. Myers, C. R., and K. H. Nealson. 1988. Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor. Science 240: 1319-1321.
28. Myers, C. R., and K. H. Nealson. 1990. Respiration-linked proton translocation coupled to anaerobic reduction of manganese(IV) and iron(III) in Shewanella putrefaciens MR-1. J. Bacteriol. 172:6232-6238.
29. Myers, J. M., and C. R. Myers. 1998. Isolation and sequence of omcA, a gene encoding a decaheme outer membrane cytochrome c of Shewanella putrefaciens MR-1, and detection of omcA homologs in other strains of S. putrefaciens. Biochim. Biophys. Acta 1373:237-251.
30. Myers, J. M., and C. R. Myers. 2000. Role of the tetraheme cytochrome CymA in anaerobic electron transport in cells of Shewanella putrefaciens MR-1 with normal levels of menaquinone. J. Bacteriol. 182:67-75.
31. Myers, J. M., and C. R. Myers. 2001. Role for outer membrane cytochromes OmcA and OmcB of Shewanella putrefaciens MR-1 in reduction of manganese dioxide. Appl. Environ. Microbiol. 67:260-269.
32. Myers, J. M., and C. R. Myers. 2002. Genetic complementation of an outer membrane cytochrome omcB mutant of Shewanella putrefaciens MR-1 requires omcB plus downstream DNA. Appl. Environ. Microbiol. 68:2781-2793.
33. Myers, J. M., and C. R. Myers. 2003. Overlapping role of the outer membrane cytochromes of Shewanella oneidensis MR-1 in the reduction of manganese(IV) oxide. Lett. Appl. Microbiol. 36:21-25.
34. Nealson, K. H., C. R. Myers, and B. B. Wimpee. 1991. Isolation and identification of manganese-reducing bacteria and estimates of microbial Mn(IV)-reducing potential in the Black Sea. Deep-Sea Res. 38(Suppl. 2):S907-S920.
35. Nechay, B. R. 1984. Mechanisms of action of vanadium. Annu. Rev. Pharmacol. Toxicol. 24:501-524.
36. Newman, D. K., and R. Kolter. 2000. A role for excreted quinones in extracellular electron transfer. Nature 405:94-97.
37. Patole, M. S., and T. Ramasarma. 1988. Occurrence of lipid peroxidation in brain microsomes in the presence of NADH and vanadate. J. Neurochem. 51:491-496.
38. Pealing, S. L., A. C. Black, F. D. C. Manson, F. B. Ward, S. K. Chapman, and G. A. Reid. 1992. Sequence of the gene encoding flavocytochrome c from Shewanella putrefaciens: a tetraheme flavoenzyme that is a soluble fumarate reductase related to the membrane-bound enzymes from other bacteria. Biochemistry 31:12132-12140.
39. Quandt, J., and M. F. Hynes. 1993. Versatile suicide vectors which allow direct selection for gene replacement in gram-negative bacteria. Gene 127: 15-21.
40. Rehder, D. 1992. Structure and function of vanadium compounds in living organisms. Biometals 5:3-12.
41. Saffarini, D. A., S. L. Blumerman, and K. J. Mansoorabadi. 2002. Role of menaquinones in Fe(III) reduction by membrane fractions of Shewanella putrefaciens. J. Bacteriol. 184:846-848.
42. Sandell, E. B. 1959. Colorimetric determinations of traces of metals. Interscience, New York, N.Y.
43. Schwalb, C., S. K. Chapman, and G. A. Reid. 2002. The membrane-bound tetrahaem c-type cytochrome CymA interacts directly with the soluble fumarate reductase in Shewanella. Biochem. Soc. Trans. 30:658-662.
44. Schwalb, C., S. K. Chapman, and G. A. Reid. 2003. The tetraheme cytochrome CymA is required for anaerobic respiration with dimethyl sulfoxide and nitrite in Shewanella oneidensis. Biochemistry 42:9491-9497.
45. Shi, X., and N. S. Dalal. 1991. Flavoenzymes reduce vanadium(V) and molecular oxygen and generate hydroxyl radical. Arch. Biochem. Biophys. 289:355-361.
46. Shi, X., and N. S. Dalal. 1993. One-electron reduction of vanadium(V) by flavoenzymes/NADPH. Arch. Biochem. Biophys. 302:300-303.
47. Yurkova, N. A., and N. N. Lyalikova. 1991. New vanadate-reducing facultative chemolithotrophic bacteria. Microbiology 59:672-677.