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

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

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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 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.

Original languageEnglish
Pages (from-to)6746-6755
Number of pages10
JournalApplied and Environmental Microbiology
Volume74
Issue number21
DOIs
Publication statusPublished - Nov 2008

Fingerprint

Shewanella oneidensis
Shewanella
EDTA (chelating agent)
Cytochromes
cytochromes
nitrilotriacetic acid
EDTA
citrates
Oxidation-Reduction
cytochrome
redox potential
membrane
kinetics
Membranes
Nitrilotriacetic Acid
metals
Edetic Acid
Citric Acid
redox reactions
reaction kinetics

ASJC Scopus subject areas

  • Applied Microbiology and Biotechnology
  • Food Science
  • Biotechnology
  • Ecology

Cite this

Kinetics of reduction of Fe(III) complexes by outer membrane cytochromes MtrC and OmcA of Shewanella oneidensis MR-1. / Wang, Zheming; Liu, Chongxuan; Wang, Xuelin; Marshall, Matthew J.; Zachara, John M.; Rosso, Kevin M.; Dupuis, Michel; Fredrickson, James K.; Heald, Steve; Shi, Liang.

In: Applied and Environmental Microbiology, Vol. 74, No. 21, 11.2008, p. 6746-6755.

Research output: Contribution to journalArticle

Wang, Z, Liu, C, Wang, X, Marshall, MJ, Zachara, JM, Rosso, KM, Dupuis, M, Fredrickson, JK, Heald, S & Shi, L 2008, 'Kinetics of reduction of Fe(III) complexes by outer membrane cytochromes MtrC and OmcA of Shewanella oneidensis MR-1', Applied and Environmental Microbiology, vol. 74, no. 21, pp. 6746-6755. https://doi.org/10.1128/AEM.01454-08
Wang, Zheming ; Liu, Chongxuan ; Wang, Xuelin ; Marshall, Matthew J. ; Zachara, John M. ; Rosso, Kevin M. ; Dupuis, Michel ; Fredrickson, James K. ; Heald, Steve ; Shi, Liang. / Kinetics of reduction of Fe(III) complexes by outer membrane cytochromes MtrC and OmcA of Shewanella oneidensis MR-1. In: Applied and Environmental Microbiology. 2008 ; Vol. 74, No. 21. pp. 6746-6755.
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AU - Wang, Zheming

AU - Liu, Chongxuan

AU - Wang, Xuelin

AU - Marshall, Matthew J.

AU - Zachara, John M.

AU - Rosso, Kevin M.

AU - Dupuis, Michel

AU - Fredrickson, James K.

AU - Heald, Steve

AU - Shi, Liang

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