High-Affinity Binding and Direct Electron Transfer to Solid Metals by the <i>Shewanella oneidensis</i> MR-1 Outer Membrane <i>c</i>-type Cytochrome OmcA

Xiong, Yijia; Shi, Liang; Chen, Baowei; Mayer, Michael; Lower, Brian H.; Londer, Yuri Y.; Bose, Saumyaditya; Hochella, Michael F.; Fredrickson, James K.; Squier, Thomas C.

doi:10.1021/ja063526d

Cited by 203 publications

(205 citation statements)

References 21 publications

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“…Again, we did not observe sawteeth when 0.2 M free OmcA was added to the AFM experiment. The results of these control experiments are consistent with those obtained previously by Xiong et al (52) in which the authors used dynamic light scattering and fluorescence correlation spectroscopy to show that purified OmcA has a specific preference for binding to hematite particles (52).…”

Section: Measurements Of Force Between Mtrc and Hematitesupporting

confidence: 90%

Specific Bonds between an Iron Oxide Surface and Outer Membrane Cytochromes MtrC and OmcA from Shewanella oneidensis MR-1

et al. 2007

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Shewanella oneidensis MR-1 is purported to express outer membrane cytochromes (e.g., MtrC and OmcA) that transfer electrons directly to Fe(III) in a mineral during anaerobic respiration. A prerequisite for this type of reaction would be the formation of a stable bond between a cytochrome and an iron oxide surface. Atomic force microscopy (AFM) was used to detect whether a specific bond forms between a hematite (Fe 2 O 3 ) thin film, created with oxygen plasma-assisted molecular beam epitaxy, and recombinant MtrC or OmcA molecules coupled to gold substrates. Force spectra displayed a unique force signature indicative of a specific bond between each cytochrome and the hematite surface. The strength of the OmcA-hematite bond was approximately twice that of the MtrC-hematite bond, but direct binding to hematite was twice as favorable for MtrC. Reversible folding/unfolding reactions were observed for mechanically denatured MtrC molecules bound to hematite. The force measurements for the hematite-cytochrome pairs were compared to spectra collected for an iron oxide and S. oneidensis under anaerobic conditions. There is a strong correlation between the whole-cell and pure-protein force spectra, suggesting that the unique binding attributes of each cytochrome complement one another and allow both MtrC and OmcA to play a prominent role in the transfer of electrons to Fe(III) in minerals. Finally, by comparing the magnitudes of binding force for the whole-cell versus pure-protein data, we were able to estimate that a single bacterium of S. oneidensis (2 by 0.5 m) expresses ϳ10 4 cytochromes on its outer surface.

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Section: Measurements Of Force Between Mtrc and Hematitesupporting

confidence: 90%

Specific Bonds between an Iron Oxide Surface and Outer Membrane Cytochromes MtrC and OmcA from Shewanella oneidensis MR-1

et al. 2007

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“…strain SW2 (11), as well as dissimilatory Fe(III) reduction by Shewanella and Geobacter species (4,40,42,43,73). Consistent with this, we found a c-type cytochrome to be upregulated when R. palustris TIE-1 was grown photoautotrophically on Fe(II).…”

Section: Discussionsupporting

confidence: 75%

The pio Operon Is Essential for Phototrophic Fe(II) Oxidation in Rhodopseudomonas palustris TIE-1

2007

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“…These experiments highlighted the importance of accounting for all variables when using electrodes as electron acceptors. OmcA previously was thought to be only a terminal reductase of metals, which was supported by in vitro biochemical evidence that it can reduce various forms of iron (46,47,56). OmcA previously was shown to bind insoluble forms of iron in vitro with a high affinity (56), a greater affinity than that of MtrC (28).…”

Section: Vol 192 2010 Reduction Of Flavins and Electrodes By S Onementioning

confidence: 95%

The Mtr Respiratory Pathway Is Essential for Reducing Flavins and Electrodes in Shewanella oneidensis

et al. 2010

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The Mtr respiratory pathway of Shewanella oneidensis strain MR-1 is required to effectively respire both soluble and insoluble forms of oxidized iron. Flavins (riboflavin and flavin mononucleotide) recently have been shown to be excreted by MR-1 and facilitate the reduction of insoluble substrates. Other Shewanella species tested accumulated flavins in supernatants to an extent similar to that of MR-1, suggesting that flavin secretion is a general trait of the species. External flavins have been proposed to act as both a soluble electron shuttle and a metal chelator; however, at biologically relevant concentrations, our results suggest that external flavins primarily act as electron shuttles for MR-1. Using deletion mutants lacking various Mtr-associated proteins, we demonstrate that the Mtr extracellular respiratory pathway is essential for the reduction of flavins and that decaheme cytochromes found on the outer surface of the cell (MtrC and OmcA) are required for the majority of this activity. Given the involvement of external flavins in the reduction of electrodes, we monitored current production by Mtr respiratory pathway mutants in three-electrode bioreactors under controlled flavin concentrations. While mutants lacking MtrC were able to reduce flavins at 50% of the rate of the wild type in cell suspension assays, these strains were unable to grow into productive electrode-reducing biofilms. The analysis of mutants lacking OmcA suggests a role for this protein in both electron transfer to electrodes and attachment to surfaces. The parallel phenotypes of Mtr mutants in flavin and electrode reduction blur the distinction between direct contact and the redox shuttling strategies of insoluble substrate reduction by MR-1.Shewanella oneidensis strain MR-1 (MR-1) is a facultative anaerobe capable of respiring a variety of substrates, including various metals and metal oxides, a phenotype that is important for bioremediation and metal cycling in natural environments (22,53). At near-neutral pH, Fe(III) and Mn(IV) often are present as insoluble oxide minerals. Dissimilatory metal-reducing bacteria such as MR-1 have developed pathways to transfer electrons from the interior of the cell to these external terminal electron acceptors. In some bacteria, these pathways also can transfer electrons to electrodes, which can be harnessed for renewable energy and remote biosensor applications (23,26,27). Beyond increasing our understanding of this unusual process, applying anaerobic microbial extracellular respiration to new technologies requires a thorough understanding of the molecular dynamics and cellular physiology of electron source utilization (substrate oxidation) and the reduction of insoluble terminal electron acceptor(s). There are four proposed mechanisms to explain how insoluble substrates are reduced by Shewanella: (i) direct contact, (ii) electron shuttling, (iii) chelation, and (iv) electrically conductive appendages (reviewed in reference 18). We will focus on the first three strategies here.Flavins recently ...

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High-Affinity Binding and Direct Electron Transfer to Solid Metals by the Shewanella oneidensis MR-1 Outer Membrane c-type Cytochrome OmcA

Cited by 203 publications

References 21 publications

Specific Bonds between an Iron Oxide Surface and Outer Membrane Cytochromes MtrC and OmcA from Shewanella oneidensis MR-1

Specific Bonds between an Iron Oxide Surface and Outer Membrane Cytochromes MtrC and OmcA from Shewanella oneidensis MR-1

The pio Operon Is Essential for Phototrophic Fe(II) Oxidation in Rhodopseudomonas palustris TIE-1

The Mtr Respiratory Pathway Is Essential for Reducing Flavins and Electrodes in Shewanella oneidensis

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