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Applied and Environmental Microbiology, November 2008, p. 6746-6755, Vol. 74, No. 21
0099-2240/08/$08.00+0     doi:10.1128/AEM.01454-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

Kinetics of Reduction of Fe(III) Complexes by Outer Membrane Cytochromes MtrC and OmcA of Shewanella oneidensis MR-1{triangledown}

Zheming Wang,1* Chongxuan Liu,1 Xuelin Wang,1 Matthew J. Marshall,1 John M. Zachara,1 Kevin M. Rosso,1 Michel Dupuis,1 James K. Fredrickson,1 Steve Heald,2 and Liang Shi1*

Pacific Northwest National Laboratory, Richland, Washington 99354,1 Argonne National Laboratory, 9700 S. Cass Avenue, Argonne, Illinois 604392

Received 29 June 2008/ Accepted 30 August 2008

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 µM–1 s–1 for the reaction between MtrC and the Fe-EDTA complex to 0.012 µM–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.

* Corresponding author. Mailing address for Zheming Wang: Pacific Northwest National Laboratory, 902 Battelle Blvd., Mail Stop K8-96, Richland, WA 99352. Phone: (509) 371-6349. Fax: (509) 371-6354. E-mail: Zheming.wang{at}pnl.gov. Mailing address for Liang Shi: Pacific Northwest National Laboratory, 902 Battelle Blvd., Mail Stop P7-50, Richland, WA 99352. Phone: (509) 376-4834. Fax: (509) 372-1632. E-mail: liang.shi{at}pnl.gov

{triangledown} Published ahead of print on 12 September 2008.

Applied and Environmental Microbiology, November 2008, p. 6746-6755, Vol. 74, No. 21
0099-2240/08/$08.00+0     doi:10.1128/AEM.01454-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.





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