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Ultrastructure of Shewanella oneidensis MR-1 nanowires revealed by electron cryotomography.

ABSTRACT: Bacterial nanowires have garnered recent interest as a proposed extracellular electron transfer (EET) pathway that links the bacterial electron transport chain to solid-phase electron acceptors away from the cell. Recent studies showed that Shewanella oneidensis MR-1 produces outer membrane (OM) and periplasmic extensions that contain EET components and hinted at their possible role as bacterial nanowires. However, their fine structure and distribution of cytochrome electron carriers under native conditions remained unclear, making it difficult to evaluate the potential electron transport (ET) mechanism along OM extensions. Here, we report high-resolution images of S. oneidensis OM extensions, using electron cryotomography (ECT). We developed a robust method for fluorescence light microscopy imaging of OM extension growth on electron microscopy grids and used correlative light and electron microscopy to identify and image the same structures by ECT. Our results reveal that S. oneidensis OM extensions are dynamic chains of interconnected outer membrane vesicles (OMVs) with variable dimensions, curvature, and extent of tubulation. Junction densities that potentially stabilize OMV chains are seen between neighboring vesicles in cryotomograms. By comparing wild type and a cytochrome gene deletion mutant, our ECT results provide the likely positions and packing of periplasmic and outer membrane proteins consistent with cytochromes. Based on the observed cytochrome packing density, we propose a plausible ET path along the OM extensions involving a combination of direct hopping and cytochrome diffusion. A mean-field calculation, informed by the observed ECT cytochrome density, supports this proposal by revealing ET rates on par with a fully packed cytochrome network.

SUBMITTER: Subramanian P

PROVIDER: S-EPMC5889646 | biostudies-literature | 2018 Apr

REPOSITORIES: biostudies-literature

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Ultrastructure of <i>Shewanella oneidensis</i> MR-1 nanowires revealed by electron cryotomography.

Subramanian Poorna P Pirbadian Sahand S El-Naggar Mohamed Y MY Jensen Grant J GJ

Proceedings of the National Academy of Sciences of the United States of America 20180319 14

Bacterial nanowires have garnered recent interest as a proposed extracellular electron transfer (EET) pathway that links the bacterial electron transport chain to solid-phase electron acceptors away from the cell. Recent studies showed that <i>Shewanella oneidensis</i> MR-1 produces outer membrane (OM) and periplasmic extensions that contain EET components and hinted at their possible role as bacterial nanowires. However, their fine structure and distribution of cytochrome electron carriers unde ...[more]

PMID: 29555764

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Project description:Exoelectrogenic bacteria are defined by their ability to respire on extracellular and insoluble electron acceptors and have applications in bioremediation and microbial electrochemical systems (MESs), while playing important roles in biogeochemical cycling. Shewanella oneidensis MR-1, which has become a model organism for the study of extracellular respiration, is known to display taxis toward insoluble electron acceptors, including electrodes. Multiple mechanisms have been proposed for MR-1's tactic behavior, and, here, we report on the role of electrochemical potential by video microscopy cell tracking experiments in three-electrode electrochemical cells. MR-1 trajectories were determined using a particle tracking algorithm and validated with Shannon's entropy method. Tactic response by MR-1 in the electrochemical cell was observed to depend on the applied potential, as indicated by the average velocity and density of motile (>4?µm/s) MR-1 close to the electrode (<50?µm). Tactic behavior was observed at oxidative potentials, with a strong switch between the potentials -0.15 to -0.25?V versus the standard hydrogen electrode (SHE), which coincides with the reduction potential of flavins. The average velocity and density of motile MR-1 close to the electrode increased when riboflavin was added (2?µM), but were completely absent in a ?mtrC/?omcA mutant of MR-1. Besides flavin's function as an electron mediator to support anaerobic respiration on insoluble electron acceptors, we propose that riboflavin is excreted by MR-1 to sense redox gradients in its environment, aiding taxis toward insoluble electron acceptors, including electrodes in MESs.IMPORTANCE Previous hypotheses of tactic behavior of exoelectrogenic bacteria are based on techniques that do not accurately control the electrochemical potential, such as chemical-in-plug assays or microscopy tracking experiments in two-electrode cells. Here, we have revisited previous experiments and, for the first time, performed microscopy cell-tracking experiments in three-electrode electrochemical cells, with defined electrode potentials. Based on these experiments, taxis toward electrodes is observed to switch at about -0.2?V versus standard hydrogen electrode (SHE), coinciding with the reduction potential of flavins.

Dataset Information

Ultrastructure of Shewanella oneidensis MR-1 nanowires revealed by electron cryotomography.

Publications

Ultrastructure of <i>Shewanella oneidensis</i> MR-1 nanowires revealed by electron cryotomography.

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