Role of outer-membrane cytochromes MtrC and OmcA in the biomineralization of ferrihydrite by Shewanella oneidensis MR-1

Authors

C. L. Reardon, Pacific Northwest National Laboratory
Alice Dohnalkova, Pacific Northwest National LaboratoryFollow
P. Nachimuthu, Pacific Northwest National Laboratory
David Kennedy, Pacific Northwest National LaboratoryFollow
D. A. Saffarini, University of Wisconsin
B. W. Arey, Pacific Northwest National Laboratory
L. Shi, Pacific Northwest National Laboratory
Zheming Wang, Pacific Northwest National LaboratoryFollow
D. Moore, Pacific Northwest National Laboratory
J. S. Mclean, Pacific Northwest National Laboratory
D. Moyles, University of Guelph
M. J. Marshall, Pacific Northwest National Laboratory
John M. Zachara, Pacific Northwest National LaboratoryFollow
James K. Fredrickson, Pacific Northwest National LaboratoryFollow
A. S. Beliaev, Pacific Northwest National LaboratoryFollow

Date of this Version

2010

Citation

Geobiology (2010), 8, 56–68; DOI: 10.1111/j.1472-4669.2009.00226.x

Abstract

In an effort to improve the understanding of electron transfer mechanisms at the microbe–mineral interface, Shewanella oneidensis MR-1 mutants with in-frame deletions of outer-membrane cytochromes (OMCs), MtrC and OmcA, were characterized for the ability to reduce ferrihydrite (FH) using a suite of microscopic, spectroscopic, and biochemical techniques. Analysis of purified recombinant proteins demonstrated that both cytochromes undergo rapid electron exchange with FH in vitro with MtrC displaying faster transfer rates than OmcA. Immunomicroscopy with cytochrome-specific antibodies revealed that MtrC co-localizes with iron solids on the cell surface while OmcA exhibits a more diffuse distribution over the cell surface. After 3-day incubation of MR-1 with FH, pronounced reductive transformation mineral products were visible by electron microscopy. Upon further incubation, the predominant phases identified were ferrous phosphates including vivianite [Fe₃(PO₄)₂•8H₂O] and a switzerite-like phase [Mn₃,Fe₃(PO₄)₂•7H₂O] that were heavily colonized by MR-1 cells with surface-exposed outer-membrane cytochromes. In the absence of both MtrC and OmcA, the cells ability to reduce FH was significantly hindered and no mineral transformation products were detected. Collectively, these results highlight the importance of the outer-membrane cytochromes in the reductive transformation of FH and support a role for direct electron transfer from the OMCs at the cell surface to the mineral.