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 language | English |
|---|---|
| Pages (from-to) | 6746-6755 |
| Number of pages | 10 |
| Journal | Applied and Environmental Microbiology |
| Volume | 74 |
| Issue number | 21 |
| DOIs | |
| Publication status | Published - Nov 2008 |
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ASJC Scopus subject areas
- Applied Microbiology and Biotechnology
- Food Science
- Biotechnology
- Ecology
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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 journal › Article
}
TY - JOUR
T1 - Kinetics of reduction of Fe(III) complexes by outer membrane cytochromes MtrC and OmcA of Shewanella oneidensis MR-1
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
PY - 2008/11
Y1 - 2008/11
N2 - 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.
AB - 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.
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U2 - 10.1128/AEM.01454-08
DO - 10.1128/AEM.01454-08
M3 - Article
VL - 74
SP - 6746
EP - 6755
JO - Applied and Environmental Microbiology
JF - Applied and Environmental Microbiology
SN - 0099-2240
IS - 21
ER -