title: Kinetics of reduction of Fe(III) complexes by outer membrane cytochromes MtrC and OmcA of Shewanella oneidensis MR-1.
abstract: Because of their cell surface locations, the outer membrane c-type cytochromes MtrC and OmcA of Shewanella oneidensis MR-1 have been suggested to be the terminal reductases for a range of redox-reactive metals that form poorly soluble solids or that do not readily cross the outer membrane. In this work, we determined the kinetics of reduction of a series of Fe(III) complexes with citrate, nitrilotriacetic acid (NTA), and EDTA by MtrC and OmcA using a stopped-flow technique in combination with theoretical computation methods. Stopped-flow kinetic data showed that the reaction proceeded in two stages, a fast stage that was completed in less than 1 s, followed by a second, relatively slower stage. For a given complex, electron transfer by MtrC was faster than that by OmcA. For a given cytochrome, the reaction was completed in the order Fe-EDTA > Fe-NTA > Fe-citrate. The kinetic data could be modeled by two parallel second-order bimolecular redox reactions with second-order rate constants ranging from 0.872 microM(-1) s(-1) for the reaction between MtrC and the Fe-EDTA complex to 0.012 microM(-1) s(-1) for the reaction between OmcA and Fe-citrate. The biphasic reaction kinetics was attributed to redox potential differences among the heme groups or redox site heterogeneity within the cytochromes. The results of redox potential and reorganization energy calculations showed that the reaction rate was influenced mostly by the relatively large reorganization energy. The results demonstrate that ligand complexation plays an important role in microbial dissimilatory reduction and mineral transformation of iron, as well as other redox-sensitive metal species in nature.
authors.affiliation: Pacific Northwest National Laboratory, Richland, WA 99352, USA. Zheming.wang@pnl.gov
authors.forename: Zheming
authors.initials: Z
authors.lastname: Wang
authors.forename: Chongxuan
authors.initials: C
authors.lastname: Liu
authors.forename: Xuelin
authors.initials: X
authors.lastname: Wang
authors.forename: Matthew J
authors.initials: MJ
authors.lastname: Marshall
authors.forename: John M
authors.initials: JM
authors.lastname: Zachara
authors.forename: Kevin M
authors.initials: KM
authors.lastname: Rosso
authors.forename: Michel
authors.initials: M
authors.lastname: Dupuis
authors.forename: James K
authors.initials: JK
authors.lastname: Fredrickson
authors.forename: Steve
authors.initials: S
authors.lastname: Heald
authors.forename: Liang
authors.initials: L
authors.lastname: Shi
mesh_terms: D001425:Bacterial Outer Membrane Proteins / Q000378:metabolism*; D003574:Cytochrome c Group / Q000378:metabolism*; D003580:Cytochromes / Q000378:metabolism; D004492:Edetic Acid / Q000378:metabolism; D005290:Ferric Compounds / Q000378:metabolism*; D007700:Kinetics; D009571:Nitrilotriacetic Acid / Q000031:analogs & derivatives* / Q000378:metabolism; D020592:Shewanella / Q000378:metabolism*
chemical_list: D001425:Bacterial Outer Membrane Proteins; D003574:Cytochrome c Group; D003580:Cytochromes; D005290:Ferric Compounds; C025314:ferric citrate; D004492:Edetic Acid; C433527:MtrC protein, Shewanella; D009571:Nitrilotriacetic Acid; C019179:Fe(III)-EDTA; C020326:ferric nitrilotriacetate
references.citation: Appl Environ Microbiol. 2000 May;66(5):2006-11
references.pmid: 10788374
references.citation: J Biol Chem. 2002 Sep 20;277(38):35703-11
references.pmid: 12080059
references.citation: J Biol Inorg Chem. 2007 Sep;12(7):1083-94
references.pmid: 17701062
references.citation: Nat Biotechnol. 2002 Nov;20(11):1118-23
references.pmid: 12368813
references.citation: Biotechnol Bioeng. 2002 Dec 20;80(6):637-49
references.pmid: 12378605
references.citation: Appl Environ Microbiol. 1993 Nov;59(11):3572-6
references.pmid: 8285665
references.citation: J Am Chem Soc. 2006 Nov 1;128(43):13978-9
references.pmid: 17061851
references.citation: Environ Sci Technol. 2002 Feb 1;36(3):373-80
references.pmid: 11871551
references.citation: Environ Microbiol. 2008 Jan;10(1):125-36
references.pmid: 17888007
references.citation: PLoS Biol. 2006 Sep;4(9):e268
references.pmid: 16875436
references.citation: Environ Sci Technol. 2001 Jun 15;35(12):2482-90
references.pmid: 11432552
references.citation: J Bacteriol. 2006 Jul;188(13):4705-14
references.pmid: 16788180
references.citation: Environ Sci Technol. 2001 Apr 1;35(7):1385-93
references.pmid: 11348071
references.citation: Geobiology. 2008 Jun;6(3):245-53
references.pmid: 18498527
references.citation: Chemistry. 2005 Mar 18;11(7):2207-19
references.pmid: 15719360
references.citation: FEBS J. 2007 Jul;274(14):3728-3738
references.pmid: 17608722
references.citation: Biochim Biophys Acta. 1991 Aug 30;1079(2):182-96
references.pmid: 1911841
references.citation: Environ Sci Technol. 2007 Apr 15;41(8):2764-9
references.pmid: 17533836
references.citation: J Phys Chem B. 2007 Nov 8;111(44):12857-64
references.pmid: 17939701
references.citation: Water Res. 2006 May;40(8):1539-46
references.pmid: 16600324
references.citation: Inorg Chem. 2003 Jun 30;42(13):4098-101
references.pmid: 12817967
references.citation: Biochemistry. 1989 Jul 25;28(15):6318-22
references.pmid: 2551370
references.citation: Mol Microbiol. 2007 Jul;65(1):12-20
references.pmid: 17581116
references.citation: Science. 2005 Nov 25;310(5752):1311-3
references.pmid: 16311331
references.citation: J Bacteriol. 2008 Aug;190(15):5512-6
references.pmid: 18502849
references.citation: Mol Microbiol. 2008 May;68(3):706-19
references.pmid: 18394146
references.citation: Appl Environ Microbiol. 2007 Sep;73(18):5797-808
references.pmid: 17675441
references.citation: J Chem Phys. 2004 Apr 15;120(15):7050-4
references.pmid: 15267606
references.citation: Faraday Discuss. 2000;(116):191-203; discussion 257-68
references.pmid: 11197478
references.citation: J Phys Chem B. 2006 Aug 10;110(31):15582-8
references.pmid: 16884282
references.citation: J Biol Chem. 2000 Mar 24;275(12):8515-22
references.pmid: 10722689
references.citation: Proc Natl Acad Sci U S A. 1972 Jan;69(1):30-3
references.pmid: 4500552
references.citation: Biochim Biophys Acta. 2000 Sep 29;1481(2):265-72
references.pmid: 11018717