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.

Download full-text


Available from: Julea N Butt, Oct 08, 2015
90 Reads
  • Source
    • "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). "
    [Show abstract] [Hide abstract]
    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.
    Frontiers in Microbiology 06/2014; 5:318. DOI:10.3389/fmicb.2014.00318 · 3.99 Impact Factor
  • Source
    • "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. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Recently, a novel mode of sulphur oxidation was described in marine sediments, in which sulphide oxidation in deeper anoxic layers was electrically coupled to oxygen reduction at the sediment surface. Subsequent experimental evidence identified that long filamentous bacteria belonging to the family Desulfobulbaceae likely mediated the electron transport across the centimetre-scale distances. Such long-range electron transfer challenges some long-held views in microbial ecology and could have profound implications for sulphur cycling in marine sediments. But, so far, this process of electrogenic sulphur oxidation has been documented only in laboratory experiments and so its imprint on the seafloor remains unknown. Here we show that the geochemical signature of electrogenic sulphur oxidation occurs in a variety of coastal sediment environments, including a salt marsh, a seasonally hypoxic basin, and a subtidal coastal mud plain. In all cases, electrogenic sulphur oxidation was detected together with an abundance of Desulfobulbaceae filaments. Complementary laboratory experiments in intertidal sands demonstrated that mechanical disturbance by bioturbating fauna destroys the electrogenic sulphur oxidation signal. A survey of published geochemical data and 16S rRNA gene sequences identified that electrogenic sulphide oxidation is likely present in a variety of marine sediments with high sulphide generation and restricted bioturbation, such as mangrove swamps, aquaculture areas, seasonally hypoxic basins, cold sulphide seeps and possibly hydrothermal vent environments. This study shows for the first time that electrogenic sulphur oxidation occurs in a wide range of marine sediments and that bioturbation may exert a dominant control on its natural distribution.The ISME Journal advance online publication, 27 March 2014; doi:10.1038/ismej.2014.41.
    The ISME Journal 03/2014; 8(9). DOI:10.1038/ismej.2014.41 · 9.30 Impact Factor
  • Source
    • "To illustrate the proposed mechanism for the observed phenomena of microbial responses to the graphene film on conductor Cu, semiconductor Ge and insulator SiO2 substrates, the energy band diagrams of these graphene-on-substrate junctions are depicted in Figure 6b–d. Some data in early works272829303132, as well as some calculated values here, are used to draw the band structures, as listed in Table 1. Figure 6b gives the band structure of the Membrane@Graphene@Cu contact. From this figure, it can be seen that the electrons are easily transferred from microbial membrane to graphene film and then to the underlying conductor Cu substrate, which forms a circuit for electron transfer. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Graphene has attracted increasing attention for potential applications in biotechnology due to its excellent electronic property and biocompatibility. Here we use both Gram-positive Staphylococcus aureus (S. aureus) and Gram-negative Escherichia coli (E. coli) to investigate the antibacterial actions of large-area monolayer graphene film on conductor Cu, semiconductor Ge and insulator SiO2. The results show that the graphene films on Cu and Ge can surprisingly inhibit the growth of both bacteria, especially the former. However, the proliferation of both bacteria cannot be significantly restricted by the graphene film on SiO2. The morphology of S. aureus and E. coli on graphene films further confirms that the direct contact of both bacteria with graphene on Cu and Ge can cause membrane damage and destroy membrane integrity, while no evident membrane destruction is induced by graphene on SiO2. From the viewpoint of charge transfer, a plausible mechanism is proposed here to explain this phenomenon. This study may provide new insights for the better understanding of antibacterial actions of graphene film and for the better designing of graphene-based antibiotics or other biomedical applications.
    Scientific Reports 03/2014; 4:4359. DOI:10.1038/srep04359 · 5.58 Impact Factor
Show more