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

Lower, Brian H.; Shi, Liang; Yongsunthon, Ruchirej; Droubay, Timothy C.; McCready, David E.; Lower, Steven K.

doi:10.1128/jb.01518-06

Cited by 127 publications

(138 citation statements)

References 50 publications

(70 reference statements)

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“…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). We suggest that while OmcA plays a small role in electron transfer in vivo, it also is involved in cellular attachment to solid surfaces or other cells.…”

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

confidence: 68%

“…Strains lacking the genes omcA (⌬omcA), mtrC (⌬mtrC), mtrA (⌬mtrA), and mtrB (⌬mtrB), as well as a strain lacking both omcA and mtrC (⌬omcA ⌬mtrC), were tested for their ability to reduce both riboflavin and FMN. Both flavins were tested here, because they have been detected previously in wild-type cultures of electrode (28) and iron-reducing cultures (49) of S. oneidensis strain MR-1. Quantitative RT-PCR confirmed that in all constructed mutants, the expression of the remaining mtr genes was not altered more than twofold compared to that of the wild type (see Table S1 in the supplemental material).…”

Section: Flavin Reduction By Mtr Mutantsmentioning

confidence: 99%

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

confidence: 68%

Section: Flavin Reduction By Mtr Mutantsmentioning

confidence: 99%

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

et al. 2010

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“…Microscopic imaging of cell exteriors labeled with an MtrC-specific antibody showed surface-exposed MtrC colocalized with cell-associated iron precipitates (15). It also has been reported that purified MtrC can bind tightly to hematite (α-Fe 2 O 3 ) (16). In support of electron transfer by direct contact, studies of S. oneidensis grown on an Fe(III) oxyhydroxide mineral surface showed the bacterial cells were associated with Fe(II)-enriched areas (17).…”

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confidence: 88%

Rapid electron exchange between surface-exposed bacterial cytochromes and Fe(III) minerals

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Shi

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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The mineral-respiring bacterium Shewanella oneidensis uses a protein complex, MtrCAB, composed of two decaheme cytochromes, MtrC and MtrA, brought together inside a transmembrane porin, MtrB, to transport electrons across the outer membrane to a variety of mineral-based electron acceptors. A proteoliposome system containing a pool of internalized electron carriers was used to investigate how the topology of the MtrCAB complex relates to its ability to transport electrons across a lipid bilayer to externally located Fe(III) oxides. With MtrA facing the interior and MtrC exposed on the outer surface of the phospholipid bilayer, the established in vivo orientation, electron transfer from the interior electron carrier pool through MtrCAB to solid-phase Fe(III) oxides was demonstrated. The rates were 10 3 times higher than those reported for reduction of goethite, hematite, and lepidocrocite by S. oneidensis, and the order of the reaction rates was consistent with those observed in S. oneidensis cultures. In contrast, established rates for single turnover reactions between purified MtrC and Fe(III) oxides were 10 3 times lower. By providing a continuous flow of electrons, the proteoliposome experiments demonstrate that conduction through MtrCAB directly to Fe(III) oxides is sufficient to support in vivo, anaerobic, solid-phase iron respiration.mineral respiration | multiheme cytochromes | proteoliposome

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“…To determine if MtrA was expressed in each mutant, we attached a His 6 tag at the C terminus of MtrA to facilitate protein detection (see Table S1 in the supplemental material). Previous studies have successfully expressed correctly folded and functional multiheme cytochromes MtrC and MtrA carrying a C-terminal His 6 tag in E. coli and Shewanella MR-1 (14,27,28). MtrA could be detected in soluble preparations from cells grown anaerobically with fumarate and lactate.…”

Section: Reduction Of Terminal Electron Acceptorsmentioning

confidence: 99%

Characterization of Axial and Proximal Histidine Mutations of the Decaheme Cytochrome MtrA from Shewanella sp. Strain ANA-3 and Implications for the Electron Transport System

et al. 2012

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c Extracellular respiration of solid-phase electron acceptors in some microorganisms requires a complex chain of multiheme ctype cytochromes that span the inner and outer membranes. In Shewanella species, MtrA, an ϳ35-kDa periplasmic decaheme c-type cytochrome, is an essential component for extracellular respiration of iron(III). The exact mechanism of electron transport has not yet been resolved, but the arrangement of the polypeptide chain may have a strong influence on the capability of the MtrA cytochrome to transport electrons. The iron hemes of MtrA are bound to its polypeptide chain via proximal (CXXCH) and distal histidine residues. In this study, we show the effects of mutating histidine residues of MtrA to arginine on protein expression and extracellular respiration using Shewanella sp. strain ANA-3 as a model organism. Individual mutations to six out of nine proximal histidines in CXXCH of MtrA led to decreased protein expression. However, distal histidine mutations resulted in various degrees of protein expression. In addition, the effects of histidine mutations on extracellular respiration were tested using ferrihydrite and current production in microbial fuel cells. These results show that proximal histidine mutants were unable to reduce ferrihydrite. Mutations to the distal histidine residues resulted in various degrees of ferrihydrite reduction. These findings indicate that mutations to the proximal histidine residues affect MtrA expression, leading to loss of extracellular respiration ability. In contrast, mutations to the distal histidine residues are less detrimental to protein expression, and extracellular respiration can proceed.

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

Cited by 127 publications

References 50 publications

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

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

Rapid electron exchange between surface-exposed bacterial cytochromes and Fe(III) minerals

Characterization of Axial and Proximal Histidine Mutations of the Decaheme Cytochrome MtrA from Shewanella sp. Strain ANA-3 and Implications for the Electron Transport System

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