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

Author
item ROSENBAUM, MIRIAM - Cornell University
item BAR, HAIM - Cornell University
item BEG, QASIM - Boston University
item SEGRE, DANIEL - Boston University
item BOOTH, JAMES - Cornell University
item Cotta, Michael
item ANGENENT, LARGUS - Cornell University

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/29/2011
Publication Date: 2/1/2012
Citation: Rosenbaum, M.A., Bar, H.Y., Beg, Q., Segre, D., Booth, J., Cotta, M.A., Angenent, L.T. 2012. Transcriptional analysis of Shewanella oneidensis MR-1 with an electrode compared to Fe(III)citrate or oxygen as terminal electron acceptor. PLoS ONE. 7(2):e30827. DOI: 10.1371/journal.pone.0030827.

Interpretive Summary: Interest in the production of energy from agricultural resources has increased markedly in recent years in response to concerns over the high cost and limited supply of petroleum. Bioelectrochemical systems (BES) such as microbial fuel cells are gaining importance as a means of producing power from a wide variety of feedstocks, but improvements in efficiencies of these systems are needed if they are to gain widespread acceptance. In the current study, we performed gene expression analysis with deoxyribonucleic acid (DNA) microarrays to compare the overall gene expression with the important BES microorganism, Shewanella oneidensis. These analyses gave insight into the physiological state of S. oneidensis when grown with an electrode as an electron acceptor compared to soluble iron (III) or oxygen as the electron acceptors. Besides the confirmation of predicted gene functions, we developed hypotheses for several previously unknown gene functions during electrode respiration. These findings will be useful in advancing the BESs toward practical application.

Technical Abstract: Background. Shewanella oneidensis is a target of extensive research efforts in the fields of bioelectrochemical systems and bioremediation because of its versatile metabolic capabilities, especially in regards to the respiration with extracellular electron acceptors. Here, we took a global approach to evaluate physiological activity with an electrode as electron acceptor for the generation of electric current. We performed expression analysis with deoxyribonucleic acid (DNA) microarrays to compare the overall gene expression with an electrode to that with soluble iron (III) or oxygen as the electron acceptor. Results. 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: i) the role of ScyA in inter-protein electron transfer; ii) an electron transfer pathway through the dimethyl sulfoxide (DSMO) reductase proteins that dissipates electrons away from the mtr pathway; and iii) a regulatory role of the cbb3-type cytochrome c oxidase under anaerobic conditions. Further, we hypothesize that the electrode respiration imposes a significant stress on the microorganisms, resulting in higher energetic costs for electrode respiration than for soluble iron (III) respiration, which fosters a higher metabolic turnover to cover energy needs. Conclusions. Our gene expression analyses gave insight into the physiological state of S. oneidensis when grown with an electrode as electron acceptor. Besides the confirmation of predicted gene functions, we developed hypotheses for several previously unknown gene functions and for a possible stress situation for S. oneidensis during electrode respiration. Our hypotheses now require experimental verification.