Bacterial periplasmic nitrate and trimethylamine-N-oxide respiration coupled to menaquinol-cytochrome c reductase (Qcr): implications for electrogenic reduction of alternative electron acceptors

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Garg, N., Taylor, A. J. orcid id iconORCID: https://orcid.org/0000-0003-1006-1205 and Kelly, D. J. (2018) Bacterial periplasmic nitrate and trimethylamine-N-oxide respiration coupled to menaquinol-cytochrome c reductase (Qcr): implications for electrogenic reduction of alternative electron acceptors. Scientific Reports, 8 (1). 15478. ISSN 2045-2322 doi: 10.1038/S41598-018-33857-2

Abstract/Summary

The periplasmic reduction of the electron acceptors nitrate (Em +420 mV) and trimethylamine-N-oxide (TMAO; Em +130 mV) by Nap and Tor reductases is widespread in Gram-negative bacteria and is usually considered to be driven by non-energy conserving quinol dehydrogenases. The Epsilonproteobacterium Campylobacter jejuni can grow by nitrate and TMAO respiration and it has previously been assumed that these alternative pathways of electron transport are independent of the proton-motive menaquinol-cytochrome c reductase complex (QcrABC) that functions in oxygen-linked respiration. Here, we show that a qcrABC deletion mutant is completely deficient in oxygen-limited growth on both nitrate and TMAO and is unable to reduce these oxidants with physiological electron donors. As expected, the mutant grows normally on fumarate under oxygen-limited conditions. Thus, the periplasmic Nap and Tor reductases receive their electrons via QcrABC in C. jejuni, explaining the general absence of NapC and TorC quinol dehydrogenases in Epsilonproteobacteria. Moreover, the specific use of menaquinol (Em -75 mV) coupled with a Qcr complex to drive reduction of nitrate or TMAO against the proton-motive force allows the process to be electrogenic with a H+/2e- ratio of 2. The results have general implications for the role of Qcr complexes in bacterial oxygen-independent respiration and growth.

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Item Type Article
URI https://reading-clone.eprints-hosting.org/id/eprint/110826
Identification Number/DOI 10.1038/S41598-018-33857-2
Refereed Yes
Divisions No Reading authors. Back catalogue items
Uncontrolled Keywords Aidan J Taylor, Campylobacter jejuni / enzymology*, Campylobacter jejuni / growth & development, Campylobacter jejuni / metabolism*, Cytochrome Reductases / deficiency, Cytochrome Reductases / metabolism*, David J Kelly, Electron Transport*, Gene Deletion, MEDLINE, Methylamines / metabolism*, NCBI, NIH, NLM, National Center for Biotechnology Information, National Institutes of Health, National Library of Medicine, Nitanshu Garg, Nitrates / metabolism*, Non-U.S. Gov't, Oxidation-Reduction, PMC6195509, PubMed Abstract, Research Support, doi:10.1038/s41598-018-33857-2, pmid:30341307
Publisher Nature Publishing Group
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