Characterization of the Decaheme c-Type Cytochrome OmcA in Solution and on Hematite Surfaces by Small Angle X-Ray Scattering and Neutron Reflectometry

Johs, Alexander; Shi, Liang; Droubay, Timothy C.; Ankner, John F.; Liang, Liyuan

doi:10.1016/j.bpj.2010.03.049

Cited by 52 publications

(57 citation statements)

References 46 publications

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“…At this resolution it was possible to confidently place the heme cofactors, main chain polypeptide, and majority of the side chains. The overall structure of the MtrF resembles an oblate ellipsoid with approximate dimensions of 85 × 70 × 30 Å, similar to those predicted by small angle X-ray scattering for OmcA (13) (Fig. 1).…”

Section: Resultssupporting

confidence: 57%

“…(ii) indirect electron transfer mediated by flavin electron shuttles, or (iii) intercytochrome electron transfer, possibly along "nanowires" (8)(9)(10)(11)(12)(13)(14)(15)(16). Here we present the X-ray crystal structure of a decaheme terminus of an OM conduit, MtrF, and propose models from this structure into how these different types of extracellular electron transfer might occur.…”

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confidence: 99%

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Structure of a bacterial cell surface decaheme electron conduit

Clarke

Edwards

Gates

et al. 2011

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

309

375

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Some bacterial species are able to utilize extracellular mineral forms of iron and manganese as respiratory electron acceptors. In Shewanella oneidensis this involves decaheme cytochromes that are located on the bacterial cell surface at the termini of transouter-membrane electron transfer conduits. The cell surface cytochromes can potentially play multiple roles in mediating electron transfer directly to insoluble electron sinks, catalyzing electron exchange with flavin electron shuttles or participating in extracellular intercytochrome electron exchange along "nanowire" appendages. We present a 3.2-Å crystal structure of one of these decaheme cytochromes, MtrF, that allows the spatial organization of the 10 hemes to be visualized for the first time. The hemes are organized across four domains in a unique crossed conformation, in which a staggered 65-Å octaheme chain transects the length of the protein and is bisected by a planar 45-Å tetraheme chain that connects two extended Greek key split β-barrel domains. The structure provides molecular insight into how reduction of insoluble substrate (e.g., minerals), soluble substrates (e.g., flavins), and cytochrome redox partners might be possible in tandem at different termini of a trifurcated electron transport chain on the cell surface.c-type cytochromes | iron respiration | MtrC | multiheme

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Section: Resultssupporting

confidence: 57%

mentioning

confidence: 99%

Structure of a bacterial cell surface decaheme electron conduit

Clarke

Edwards

Gates

et al. 2011

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

309

375

View full text Add to dashboard Cite

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“…Specific binding between individual cytochromes and solids could be demonstrated via atomic force microscopy measurements between a hematite-coated tip and a cytochromecoated surface, demonstrating bonding of both OmcA and MtrC to the iron oxide with OmcA binding stronger and MtrC bonding more frequently [143]. Some insight into how cytochromes interact with a solid surface could be gained via neutron reflectivity which revealed that in binding to a hematite surface, the ellipsoidal OmcA lies flat on the surface, maximizing the contact area with the mineral [144]. However, in vitro modes of contact do not necessarily translate to the situation in vivo as by virtue of their assembly on the cellular [72] which would imply an erect position on the cell surface, with the opposite end of the octa-haem chain (haem 5) as the likely electron egress site towards solid substrates.…”

Section: Solid Substratesmentioning

confidence: 99%

Multi-haem cytochromes inShewanella oneidensisMR-1: structures, functions and opportunities

Breuer

Rosso

Blumberger

et al. 2015

J. R. Soc. Interface.

225

186

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Multi-haem cytochromes are employed by a range of microorganisms to transport electrons over distances of up to tens of nanometres. Perhaps the most spectacular utilization of these proteins is in the reduction of extracellular solid substrates, including electrodes and insoluble mineral oxides of Fe(III) and Mn(III/IV), by species of Shewanella and Geobacter. However, multihaem cytochromes are found in numerous and phylogenetically diverse prokaryotes where they participate in electron transfer and redox catalysis that contributes to biogeochemical cycling of N, S and Fe on the global scale. These properties of multi-haem cytochromes have attracted much interest and contributed to advances in bioenergy applications and bioremediation of contaminated soils. Looking forward, there are opportunities to engage multi-haem cytochromes for biological photovoltaic cells, microbial electrosynthesis and developing bespoke molecular devices. As a consequence, it is timely to review our present understanding of these proteins and we do this here with a focus on the multitude of functionally diverse multi-haem cytochromes in Shewanella oneidensis MR-1. We draw on findings from experimental and computational approaches which ideally complement each other in the study of these systems: computational methods can interpret experimentally determined properties in terms of molecular structure to cast light on the relation between structure and function. We show how this synergy has contributed to our understanding of multi-haem cytochromes and can be expected to continue to do so for greater insight into natural processes and their informed exploitation in biotechnologies.

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“…Phenotypic analyses of MR-1 mutants reveal that while multiheme c-type cytochromes, such as MtrC and OmcA, are directly involved in reduction of Fe(III) oxides, Tc(VII), U(VI), and Cr(VI), [NiFe]-hydrogenase ([NiFe]-H 2 ase) has also been implicated in Tc(VII) reduction (2,3,6,23,24,31). Biochemical characterization of purified proteins demonstrated that MtrC and/or OmcA could bind to the surface of crystalline Fe(III) oxide hematite (␣-Fe 2 O 3 ) and reduce hematite as well as Tc(VII), U(VI), Cr(VI), and chelated Fe(III), providing direct evidence that MtrC and OmcA can serve as terminal reductases for extracellular reduction of these oxidized metals and metal contaminants (2,10,13,17,19,25,35,36,40,42). MR-1 [NiFe]-H 2 ase is believed to be localized in the periplasm, where it has been implicated in both H 2 formation and oxidation in addition to Tc(VII) reduction (24,26).…”

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confidence: 98%