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Transcriptional analysis of Shewanella oneidensis MR-1 with an electrode compared to Fe(III)citrate or oxygen as terminal electron acceptor.

ABSTRACT: Shewanella oneidensis is a target of extensive research in the fields of bioelectrochemical systems and bioremediation because of its versatile metabolic capabilities, especially with regard to respiration with extracellular electron acceptors. The physiological activity of S. oneidensis to respire at electrodes is of great interest, but the growth conditions in thin-layer biofilms make physiological analyses experimentally challenging. Here, we took a global approach to evaluate physiological activity with an electrode as terminal electron acceptor for the generation of electric current. We performed expression analysis with DNA microarrays to compare the overall gene expression with an electrode to that with soluble iron(III) or oxygen as the electron acceptor and applied new hierarchical model-based statistics for the differential expression analysis. We confirmed the differential expression of many genes that have previously been reported to be involved in electrode respiration, such as the entire mtr operon. We also formulate hypotheses on other possible gene involvements in electrode respiration, for example, a role of ScyA in inter-protein electron transfer and a regulatory role of the cbb3-type cytochrome c oxidase under anaerobic conditions. Further, we hypothesize that electrode respiration imposes a significant stress on S. oneidensis, resulting in higher energetic costs for electrode respiration than for soluble iron(III) respiration, which fosters a higher metabolic turnover to cover energy needs. Our hypotheses now require experimental verification, but this expression analysis provides a fundamental platform for further studies into the molecular mechanisms of S. oneidensis electron transfer and the physiologically special situation of growth on a poised-potential surface.

SUBMITTER: Rosenbaum MA

PROVIDER: S-EPMC3271074 | biostudies-literature | 2012

REPOSITORIES: biostudies-literature

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Transcriptional analysis of Shewanella oneidensis MR-1 with an electrode compared to Fe(III)citrate or oxygen as terminal electron acceptor.

Rosenbaum Miriam A MA Bar Haim Y HY Beg Qasim K QK Segrè Daniel D Booth James J Cotta Michael A MA Angenent Largus T LT

PloS one 20120201 2

Shewanella oneidensis is a target of extensive research in the fields of bioelectrochemical systems and bioremediation because of its versatile metabolic capabilities, especially with regard to respiration with extracellular electron acceptors. The physiological activity of S. oneidensis to respire at electrodes is of great interest, but the growth conditions in thin-layer biofilms make physiological analyses experimentally challenging. Here, we took a global approach to evaluate physiological a ...[more]

PMID: 22319591

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Project description:UnlabelledIn limiting oxygen as an electron acceptor, the dissimilatory metal-reducing bacterium Shewanella oneidensis MR-1 rapidly forms nanowires, extensions of its outer membrane containing the cytochromes MtrC and OmcA needed for extracellular electron transfer. RNA sequencing (RNA-Seq) analysis was employed to determine differential gene expression over time from triplicate chemostat cultures that were limited for oxygen. We identified 465 genes with decreased expression and 677 genes with increased expression. The coordinated increased expression of heme biosynthesis, cytochrome maturation, and transport pathways indicates that S. oneidensis MR-1 increases cytochrome production, including the transcription of genes encoding MtrA, MtrC, and OmcA, and transports these decaheme cytochromes across the cytoplasmic membrane during electron acceptor limitation and nanowire formation. In contrast, the expression of the mtrA and mtrC homologs mtrF and mtrD either remains unaffected or decreases under these conditions. The ompW gene, encoding a small outer membrane porin, has 40-fold higher expression during oxygen limitation, and it is proposed that OmpW plays a role in cation transport to maintain electrical neutrality during electron transfer. The genes encoding the anaerobic respiration regulator cyclic AMP receptor protein (CRP) and the extracytoplasmic function sigma factor RpoE are among the transcription factor genes with increased expression. RpoE might function by signaling the initial response to oxygen limitation. Our results show that RpoE activates transcription from promoters upstream of mtrC and omcA The transcriptome and mutant analyses of S. oneidensis MR-1 nanowire production are consistent with independent regulatory mechanisms for extending the outer membrane into tubular structures and for ensuring the electron transfer function of the nanowires.ImportanceShewanella oneidensis MR-1 has the capacity to transfer electrons to its external surface using extensions of the outer membrane called bacterial nanowires. These bacterial nanowires link the cell's respiratory chain to external surfaces, including oxidized metals important in bioremediation, and explain why S. oneidensis can be utilized as a component of microbial fuel cells, a form of renewable energy. In this work, we use differential gene expression analysis to focus on which genes function to produce the nanowires and promote extracellular electron transfer during oxygen limitation. Among the genes that are expressed at high levels are those encoding cytochrome proteins necessary for electron transfer. Shewanella coordinates the increased expression of regulators, metabolic pathways, and transport pathways to ensure that cytochromes efficiently transfer electrons along the nanowires.

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

Transcriptional analysis of Shewanella oneidensis MR-1 with an electrode compared to Fe(III)citrate or oxygen as terminal electron acceptor.

Publications

Transcriptional analysis of Shewanella oneidensis MR-1 with an electrode compared to Fe(III)citrate or oxygen as terminal electron acceptor.

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