Kinetics of reduction of Fe(III) complexes by outer membrane cytochromes MtrC and OmcA of Shewanella oneidensis MR-1

Applied and Environmental Microbiology

Volumn 74, Issue 21, 2008, Pages 6746-6755

  Wang, Zheming ^a   Liu, Chongxuan ^a   Wang, Xuelin ^a   Marshall, Matthew J ^a   Zachara, John M ^a   Rosso, Kevin M ^a   Dupuis, Michel ^a   Fredrickson, James K ^a   Heald, Steve ^b   Shi, Liang ^a  

^a PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

^b ARGONNE NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACIDS; CELL MEMBRANES; IRON COMPOUNDS; METAL ANALYSIS; MINERALS; PORPHYRINS; REACTION KINETICS; REACTION RATES; REDOX REACTIONS; SECONDARY BATTERIES; SILICA; SILICATE MINERALS;

BIPHASIC REACTIONS; CELL SURFACES; COMPUTATION METHODS; EDTA COMPLEXES; ELECTRON TRANSFERS; FLOW TECHNIQUES; HEME GROUPS; KINETIC DATUMS; METAL SPECIES; MINERAL TRANSFORMATIONS; NITRILOTRIACETIC ACIDS; OUTER MEMBRANES; REACTIVE METALS; REDOX POTENTIALS; REDOX SITES; REORGANIZATION ENERGIES; SHEWANELLA ONEIDENSIS; SOLUBLE SOLIDS; TWO STAGES;

RATE CONSTANTS;

CITRIC ACID; CYTOCHROME; EDETIC ACID; FERRIC ION; NITRILOTRIACETIC ACID; PROTEIN MTRC; PROTEIN OMCA; UNCLASSIFIED DRUG;

BACTERIUM; COMPLEXATION; CYTOCHROME; ELECTRON; ENZYME ACTIVITY; IRON; LIGAND; REACTION KINETICS; REDOX CONDITIONS; REDUCTION;

ARTICLE; CHEMICAL REACTION KINETICS; CHEMICAL STRUCTURE; COMPLEX FORMATION; CONTROLLED STUDY; ELECTRON TRANSPORT; NONHUMAN; OXIDATION REDUCTION REACTION; PROTEIN FUNCTION; REDUCTION; SHEWANELLA ONEIDENSIS;

BACTERIAL OUTER MEMBRANE PROTEINS; CYTOCHROME C GROUP; CYTOCHROMES; EDETIC ACID; FERRIC COMPOUNDS; KINETICS; NITRILOTRIACETIC ACID; SHEWANELLA;

SHEWANELLA ONEIDENSIS MR-1;

EID: 55149120128     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.01454-08     Document Type: Article

References (64)

1. Allison, J. D., D. S. Brown, and K. J. Novo-Gradac. 1998. MINTEQA2// PRODEFA2, a geochemical assessment model for environmental systems (version 4). Environmental Research Laboratory, U.S. Environmental Protection Agency, Washington, DC.
2. Armstrong, F. A., R. Camba, H. A. Heering, J. Hurst, L. J. C. Jeuken, A. K. Jones, C. Leger, and J. P. McEvoy. 2000. Fast voltammetric studies of the kinetics and energetics of coupled electron-transfer reactions in proteins. Faraday Discuss. 116:191-203.
3. Bakan, D. A., P. Saltman, Y. Theriault, and P. E. Wright. 1991. Kinetics and mechanisms of reduction of Cu(II) and Fe(III) complexes by soybean leghemoglobin-alpha. Biochim. Biophys. Acta 1079:182-196.
4. Bard, A. J., and L. R. Faulkner. 2001. Electrochemical methods: fundamentals and applications, 2nd ed. John Wiley and Sons, Inc., New York, NY.
5. Borloo, J., B. Vergauwen, L. De Smet, A. Brige, B. Motte, and B. Devreese. 2007. A kinetic approach to the dependence of dissimilatory metal reduction by Shewanella oneidensis MR-1 on the outer membrane cytochromes c OmcA and OmcB. FEBS J. 274:3728-3738.
6. Brezonik, P. L. 1990. Principles of linear free-energy and structure-activity relationships and their applications to the fate of chemicals in aquatic systems, p. 113-143. In W. Stumm (ed.), Aquatic chemical kinetics. Reaction rates of processes in natural waters. John Wiley and Sons, Inc., New York, NY.
7. Campbell, J. A., R. W. Stromatt, M. R. Smith, D. W. Koppenaal, R. M. Bean, T. E. Jones, D. M. Strachan, and H. Babad. 1994. Organic analysis at the Hanford nuclear site. Anal. Chem. 66:1208A-1215A.
8. Cheddar, G., T. E. Meyer, M. A. Cusanovich, C. D. Stout, and G. Tollin. 1989. Redox protein electron-transfer mechanisms: electrostatic interactions as a determinant of reaction site in c-type cytochromes. Biochemistry 28:6318-6322.
9. Dawson, J. W., H. B. Gray, R. A. Holwerda, and E. W. Westhead. 1972. Kinetics of the reduction of metalloproteins by chromous ion. Proc. Natl. Acad. Sci. USA 69:30-33.
10. Field, S. J., P. S. Dobbin, M. R. Cheesman, N. J. Watmough, A. J. Thomson, and D. J. Richardson. 2000. Purification and magneto-optical spectroscopic characterization of cytochrome membrane and membrane multiheme c-type cytochromes from Shewanella frigidmarina NCIMB400. J. Biol. Chem. 275:8515-8522.
11. Fredrickson, J. K., H. Kostandarithes, S. Li, A. E. Plymale, and M. J. Daly. 2000. Reduction of Fe(III), Cr(VI), U(VI), and Tc(VII) by Deinococcus radiodurans R1. Appl. Environ. Microbiol. 66:2006-2011.
12. Fredrickson, J. K., and J. M. Zachara. 2008. Electron transfer at the microbe-mineral interface: a grand challenge in biogeochemistry. Geobiology 6:245-253.
13. Fredrickson, J. K., J. M. Zachara, D. W. Kennedy, M. C. Duff, Y. A. Gorby, S.-M. W. Li, and K. M. Krupka. 2000. Reduction of U(VI) in goethite (α-FeOOH) suspensions by a dissimilatory metal-reducing bacterium. Geochim. Cosmichim. Acta 64:3085-3098.
14. - by sediment-associated biogenic Fe(II). Geochim. Cosmochim. Acta 68:3171-3187.
15. Gabricevic, M., and A. L. Crumbliss. 2003. Kinetics and mechanism of iron(III)-nitrilotriacetate complex reactions with phosphate and acetohydroxamic acid. Inorg. Chem. 42:4098-4101.
16. Gautier-Luneau, I., C. Merle, D. Phanon, C. Lebrun, F. Biaso, G. Serratrice, and J.-L. Pierre. 2005. New trends in the chemistry of iron(III) citrate complexes: correlations between X-ray structures and solution species probed by electrospray mass spectrometry and kinetics of iron uptake from citrate by iron chelators. Chem. Eur. J. 11:2207-2219.
17. Gescher, J. S., C. D. Cordova, and A. M. Spormann. 2008. Dissimilatory iron reduction in Escherichia coli: identification of CymA of Shewanella oneidensis and NapC of E. coli as ferric reductases. Mol. Microbiol. 68:706-719.
18. Gibbs, C. R. 1976. Characterization and application of ferrozine iron reagent as a ferrous iron indicator. Anal. Chem. 48:1197-1201.
19. Grant, K. E., G. M. Mong, R. B. Lucke, and J. A. Campbell. 1996. Quantitative determination of chelators and their degradation products in mixed hazardous wastes from tank 241-SY-101 using derivatized GC/MS. J. Radioanal. Nucl. Chem. 211:383-402.
20. Gupta, N., and P. C. Nigam. 1989. Multidentate ligand exchange kinetics: reactions of aminocarboxylato-ferrate(III) complexes with 4-(2-pyridylazo) resorcinol. J. Inorg. Chem. 5:61-72.
21. Haas, J. R., and T. J. DiChristina. 2002. Effects of Fe(III) chemical speciation on dissimilatory Fe(III) reduction by Shewanella putrefaciens. Environ. Sci. Technol. 36:373-380.
22. Hartshorne, R. S., B. N. Jepson, T. A. Clarke, S. J. Field, J. M. Fredrickson, J. M. Zachara, L. Shi, J. N. Butt, and D. J. Richardson. 2007. Characterization of Shewanella oneidensis MtrC: a cell-surface decaheme cytochrome involved in respiratory electron transport to extracellular electron acceptors. J. Biol. Inorg. Chem. 12:1083-1094.
23. Heidelberg, J. F., I. T. Paulsen, K. F. Nelson, E. J. Gaodos, 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.
24. Icopini, G. A., H. Boukhalfa, and M. P. Neu. 2007. Biological reduction of Np(V) and Np(V) citrate by metal-reducing bacteria. Environ. Sci. Technol. 41:2764-2769.
25. Inouye, K., T. Mizokawa, A. Saito, B. Tonomura, and H. Ohkawa. 2000. Biphasic kinetic behavior of rat cytochrome P-4501 A1-dependent monooxygenation in recombinant yeast microsomes. Biochim. Biophys. Acta 1481:265-272.
26. Kerisit, S., K. M. Rosso, M. Dupuis, and M. Valiev. 2007. Molecular computational investigation of electron-transfer kinetics across cytochrome-iron oxide interfaces. J. Phys. Chem. C 111:11363-11375.
27. Leys, D., T. E. Meyer, A. S. Tsapin, K. H. Nealson, M. A. Cusanovich, and J. J. Van Beeumen. 2002. Crystal structures at atomic resolution reveal the novel concept of "electron-harvesting" as a role for the small tetraheme cytochrome c. J. Biol. Chem. 277:35703-35711.
28. Lide, D. R. (ed.). 1991. CRC handbook of chemistry and physics, 72nd ed. CRC Press, Boston, MA.
29. Lin, J. P., I. A. Balabin, and B. D. N. 2005. The nature of aqueous tunneling pathways between electron-transfer proteins. Science 310:1311-1313.
30. 2O. Inorg. Chem. 3:34-43.
31. 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.
32. Liu, C. X., Y. A. Gorby, J. M. Zachara, J. K. Fredrickson, and C. F. Brown. 2002. Reduction kinetics of Fe(III), Co(III), U(VI) Cr(VI) and Tc(VII) in cultures of dissimilatory metal-reducing bacteria. Biotechnol. Bioeng. 80:637-649.
33. Liu, C. X., 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.
34. Lojou, E., P. Bianco, and M. Bruschi. 1998. Kinetic studies on the electron transfer between bacterial c-type cytochromes and metal oxides. J. Electroanal. Chem. 452:167-177.
35. Lovley, D., E. Phillips, Y. Gorby, and E. Landa. 1991. Microbial reduction of uranium. Nature 350:413-416.
36. 3 of Desulfovibrio vulgaris. Appl. Environ. Microbiol. 59:3572-3576.
37. Lovley, D. R., and E. J. P. Phillips. 1992. Bioremediation of uranium contamination with enzymatic uranium reduction. Environ. Sci. Technol. 26:2228-2234.
38. 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.
39. Marcus, R. A. 1956. On the theory of oxidation-reduction reactions involving electron transfer. I. J. Chem. Phys. 24:966-978.
40. Marcus, R. A., and N. Sutin. 1985. Electron transfers in chemistry and biology. Biochim. Biophys. Acta 811:265-322.
41. Marshall, M. J., A. S. Beliaev, A. C. Dohnalkova, D. W. Kennedy, L. Shi, Z. Wang, M. I. Boyanov, B. Lai, K. M. Kemner, J. S. McLean, S. B. Reed, D. E. Culley, V. L. Bailey, D. A. Somonson, M. F. Romaine, J. M. Zachara, and J. K. Fredrickson. 2006. c-Type-cytochrome-dependent formation of U(VI) nanoparticle by Shewanella oneidensis. PLoS Biol. 4:1324-1333.
42. Marshall, M. J., A. E. Plymale, D. W. Kennedy, L. Shi, Z. M. Wang, S. B. Reed, A. C. Dohnalkova, C. J. Simonson, C. X. Liu, D. A. Saffarini, M. F. Romine, J. M. Zachara, A. S. Beliaev, and J. K. Fredrickson. 2008. Hydrogenase-and outer membrane c-type cytochrome-facilitated reduction of technetium(VII) by Shewanella oneidensis MR-1. Environ. Microbiol. 10:125-136.
43. Martell, R. E., and R. M. Smith. 1995. Critical Stability Constants of Metal Complexes database, version 2. NIST Standard Reference Data Program, Gaithersburg, MD.
44. Nancharaiah, Y. V., N. Schwarzenbeck, T. V. K. Mohan, S. V. Narasimhan, P. A. Wilderer, and V. P. Venugopalan. 2006. Biodegradation of nitrilotriacetic acid (NTA) and ferric-NTA complex by aerobic microbial granules. Water Res. 40:1539-1546.
45. 2-. J. Am. Chem. Soc. 104:841-845.
46. Ribas, X., V. Salvado, and M. Valiente. 1989. The chemistry of iron in biosystems. II. A hydroplytic model of the complex formulation between Fe(III), citric acid in aqueous solutions. J. Chem. Res. 1989:2533-2553.
47. Ross, D. E., S. S. Ruebush, S. L. Brantley, R. S. Hartshorne, T. A. Clarke, D. J. Richardson, and M. Tien. 2007. Characterization of protein-protein interactions involved in iron reduction by Shewanella oneidensis MR-1. Appl. Environ. Microbiol. 73:5797-5808.
48. Rosso, K. M., and M. Dupuis. 2006. Electron transfer in environmental systems: a frontier for theoretical chemistry. Theor. Chem. Acc. 116:124-136.
49. Rosso, K. M., and M. Dupuis. 2004. Reorganization energy associated with small polaron mobility in iron oxide. J. Chem. Phys. 120:7050-7054.
50. Rosso, K. M., and J. J. Morgan. 2002. Outer-sphere electron transfer kinetics of metal ion oxidation by molecular oxygen. Geochim. Cosmochim. Acta 66:4223-4233.
51. 3+/2+ redox couples. J. Phys. Chem. A 104:6718-6725.
52. Rosso, K. M., D. M. A. Smith, and M. Dupuis. 2004. Aspects of aqueous iron and manganese(II/III) self-exchange electron transfer reactions. J. Phys. Chem. 108:5242-5248.
53. Rosso, K. M., D. M. A. Smith, Z. Wang, C. C. Ainsworth, and J. K. Fredrickson. 2004. Self-exchange electron transfer kinetics and reduction potentials for anthraquinone disulfonate. J. Phys. Chem. A 108:3292-3303.
54. Sakane, H., I. Watanabe, K. Ono, S. Ikeda, S. Kaizaki, and Y. Kushi. 1990. Structures of Fe(III) complexes with EDTA and EDDDA in aqueous solution by EXAFS and XANES. Inorg. Chim. Acta 178:67-70.
55. Shi, L., B. Chen, Z. Wang, D. A. Elias, M. U. Mayer, Y. A. Gorby, S. Ni, B. H. Lower, D. W. Kennedy, D. S. Wunschel, M. M. Heather, M. J. Marshall, E. A. Hill, A. S. Beliaev, J. M. Zachara, J. K. Fredrickson, and T. C. Squier. 2006. Isolation of a high-affinity functional protein complex between OmcA and MtrC: two outer membrane decaheme c-type cytochromes of Shewanella oneidensis MR-1. J. Bacteriol. 188:4705-4714.
56. Shi, L., S. Deng, M. Marshall, Z. Wang, D. W. Kennedy, A. Dohnalkova, H. M. Mottaz, Y. A. Gorby, A. Beliaev, D. J. Richardson, J. M. Zachara, and J. M. Fredrickson. 2008. Direct involvement of type II secretion system in extracellular translocation of Shewanella oneidensis outer membrane cytochromes MtrC and OmcA J. Bacteriol. 190:5512-5516.
57. Shi, L., T. C. Squier, J. M. Zachara, and J. K. Fredrickson. 2007. Respiration of metal (hydr)oxides by Shewanella and Geobacter: a key role for multihaem c-type cytochromes. Mol. Microbiol. 65:12-20.
58. Smith, D. M. A., K. M. Rosso, M. Dupuis, M. Valiev, and T. P. Straatsma. 2006. Electronic coupling between heme electron-transfer centers and its decay with distance depends strongly on relative orientation. J. Phys. Chem. 110:15582-15588.
59. Stumm, W., and B. Sulzberger. 1992. The cycling of iron in natural environments: considerations based on laboratory studies of heterogeneous redox processes. Geochim. Cosmochim. Acta 56:3233-3257.
60. Walters, M. A., V. Vapnyar, A. Bolour, C. Incarvito, and A. L. Rheingold. 2003. Iron(III) nitrilotriacetate and iron(III) iminodiacetate, their X-ray crystallographic structures and chemical properties. Polyhedron 22:941-946.
61. Wang, Z., A. R. Felmy, Y. X. Xia, and M. J. Mason. 2003. The solubility and speciation of Eu(III) and Cm(III) in the presence of organic chelates in highly basic solutions-a fluorescence spectroscopic study. Radiochim. Acta 91:329-337.
62. Wigginton, N. S., K. M. Rosso, and M. F. Hochella. 2007. Mechanisms of electron transfer in two decaheme cytochromes from a metal-reducing bacterium. J. Phys. Chem. B 111:12857-12864.
63. Wigginton, N. S., K. M. Rosso, B. H. Lower, L. Shi, and M. F. Hochella. 2007. Electron tunneling properties of outer-membrane decaheme cytochromes from Shewanella oneidensis. Geochim. Cosmochim. Acta 71:543-555.
64. Xiong, Y. J., L. Shi, B. W. Chen, M. U. Mayer, B. H. Lower, Y. Londer, S. Bose, M. F. Hochella, J. K. Fredrickson, and T. C. Squier. 2006. High-affinity binding and direct electron transfer to solid metals by the Shewanella oneidensis MR-1 outer membrane c-type cytochrome OmcA. J. Am. Chem. Soc. 128:13978-13979.