Bacterial Nanowires of Shewanella Oneidensis MR-1 are Outer Membrane and Periplasmic Extensions of the Extracellular Electron Transport Components

Abstract

Bacterial nanowires offer a pathway for extracellular electron transfer (EET) by linking the respiratory chain of bacteria to external surfaces, including oxidized metals in the environment and engineered electrodes in renewable energy devices. Specifically, nanowires of the model metal-reducing bacterium Shewanella oneidensis MR-1 were previously shown to be conductive under non-physiological conditions. Despite the global, environmental, and technological consequences of bacterial nanowire-mediated EET, the composition, electron transport mechanism, and physiological relevance of these appendages remain unclear. The nanowires of S. oneidensis MR-1 were previously thought, but never shown, to be bacterial pili. In addition, the transport mechanism through bacterial nanowires has been the subject of intense debate, with ''metallic-like'' band transport and multistep redox hopping between multiheme cytochromes as the two proposed mechanisms. Here we report the first in vivo observations of the formation and respiratory impact of nanowires in S. oneidensis MR-1. Using live fluorescence measurements and quantitative gene expression analysis, we demonstrate that S. oneidensis MR-1 nanowires are extensions of the outer membrane and periplasm, rather than pilin-based structures. We show, through immunolabeling, that multiheme cytochromes localize to nanowires, in turn supporting the multistep redox hopping model as the transport mechanism. Furthermore, these bacterial nanowires are associated with outer membrane vesicles, structures ubiquitous in Gram-negative bacteria, and occasionally appear as membrane vesicle chains that transition to smoother filaments. Redox-functionalized membrane and vesicular extensions may represent a general microbial strategy for electron transport and energy distribution.

Protein bioelectronics: a review of what we do and do not know

“…47,87,151,330 Tunneling can describe protein-mediated solid state ETp over length scales up to a few tens of Å, but it is not clear how it can serve to describe electron transport over longer distances ( 50 Å). 413 Very longrange ( 100 Å) ET in biological systems occurs via redox-active cofactors using chains with close cofactor spacing of typically 15 -20 Å. Transport across photosynthetic and mitochondrial membranes includes protein-protein ET, and, within a protein or protein complex ,is generally described as multi-step hopping between multiple redox cofactors, or via multiple aromatic residues.…”

Electrical signalling in prokaryotes and its convergence with quorum sensing in Bacillus

“…[ 71 ] Interestingly, the “nanowires” of Shewanella oneidensis are actually periplasmic consisting of extensions of the outer membrane and periplasm that can conduct electrons. [ 72,73 ]…”

Different Routes for Direct Interspecies Electron Transfer with Diverse Electron-Accepting Partners

“…Effective extracellular electron transfer by S. oneidensis is limited to soluble electron acceptors such as chelated Fe(III), metal ions, and electron shuttles, such as flavins (27,43,44). S. oneidensis lacks e-pili and primarily reduces extracellular particulate electron acceptors, such as Fe(III) oxides and electrodes, with flavins as an electron shuttle (45)(46)(47). Although soluble electron shuttles have been shown to facilitate interspecies electron transfer between Geobacter species with fumarate serving as the electron acceptor (48), the redox potential of reduced flavins may be too positive to support the reduction of carbon dioxide by methanogens.…”