Structure of a bacterial cell surface decaheme electron conduit. Proc Natl Acad Sci USA

Centre for Molecular and Structural Biochemistry, School of Biological Sciences and School of Chemistry, University of East Anglia, Norwich NR4 7TJ, United Kingdom.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 06/2011; 108(23):9384-9. DOI: 10.1073/pnas.1017200108
Source: PubMed


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 trans-outer-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.

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    • "MtrF either evolved to interact with a different class of ligands, structurally different from these electron shuttles, or is not designed to interact with soluble electron shuttles. This agrees with the lack of success in observing bound FMN in MtrF crystals soaked with this electron shuttle (Clarke et al., 2011). "
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    ABSTRACT: Dissimilatory metal reducing organisms play key roles in the biogeochemical cycle of metals as well as in the durability of submerged and buried metallic structures. The molecular mechanisms that support electron transfer across the microbe-metal interface in these organisms remain poorly explored. It is known that outer membrane proteins, in particular multiheme cytochromes, are essential for this type of metabolism, being responsible for direct and indirect, via electron shuttles, interaction with the insoluble electron acceptors. Soluble electron shuttles such as flavins, phenazines, and humic acids are known to enhance extracellular electron transfer. In this work, this phenomenon was explored. All known outer membrane decaheme cytochromes from Shewanella oneidensis MR-1 with known metal terminal reductase activity and a undecaheme cytochrome from Shewanella sp. HRCR-6 were expressed and purified. Their interactions with soluble electron shuttles were studied using stopped-flow kinetics, NMR spectroscopy, and molecular simulations. The results show that despite the structural similarities, expected from the available structural data and sequence homology, the detailed characteristics of their interactions with soluble electron shuttles are different. MtrC and OmcA appear to interact with a variety of different electron shuttles in the close vicinity of some of their hemes, and with affinities that are biologically relevant for the concentrations typical found in the medium for this type of compounds. All data support a view of a distant interaction between the hemes of MtrF and the electron shuttles. For UndA a clear structural characterization was achieved for the interaction with AQDS a humic acid analog. These results provide guidance for future work of the manipulation of these proteins toward modulation of their role in metal attachment and reduction.
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    • "Experimental manipulation revealed that this electrical connection responded immediately (that is, within minutes) to oxygen depletion in the overlying water, and so the connection was too fast to be explained by diffusion of redox-active shuttles (Nielsen et al., 2010). Metal-reducing bacteria are known to transport electrons externally via cell surface cytochromes, redox shuttles or conductive pili (Reguera et al., 2005; Gorby et al., 2006; Lovley, 2008; Clarke et al., 2011), and such extracellular electron transport can bridge B100 micrometer distances in electrode biofilms (Reguera et al., 2006; Logan and Rabaey, 2012). The electron transport associated with this electrogenic sulphur oxidation, by contrast, operates on scales of centimetres , thereby extending the known length scale of microbially mediated electron transport by two orders of magnitude. "
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