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Mechanism of electron transport during thiosulfate oxidation in an obligately mixotrophic bacterium Thiomonas bhubaneswarensis strain S10 (DSM 18181T)

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Abstract

This study describes the thiosulfate-supported respiratory electron transport activity of Thiomonas bhubaneswarensis strain S10 (DSM 18181T). Whole-genome sequence analysis revealed the presence of complete sox (sulfur oxidation) gene cluster (soxCDYZAXB) including the sulfur oxygenase reductase (SOR), sulfide quinone reductase (SQR), sulfide dehydrogenase (flavocytochrome c (fcc)), thiosulfate dehydrogenase (Tsd), sulfite dehydrogenase (SorAB), and intracellular sulfur oxidation protein (DsrE/DsrF). In addition, genes encoding respiratory electron transport chain components viz. complex I (NADH dehydrogenase), complex II (succinate dehydrogenase), complex III (ubiquinone-cytochrome c reductase), and various types of terminal oxidases (cytochrome c and quinol oxidase) were identified in the genome. Using site-specific electron donors and inhibitors and by analyzing the cytochrome spectra, we identified the shortest thiosulfate-dependent electron transport chain in T. bhubaneswarensis DSM 18181T. Our results showed that thiosulfate supports the electron transport activity in a bifurcated manner, donating electrons to quinol (bd) and cytochrome c (Caa 3 ) oxidase; these two sites (quinol oxidase and cytochrome c oxidase) also showed differences in their phosphate esterification potential (oxidative phosphorylation efficiency (P/O)). Further, it was evidenced that the substrate-level phosphorylation is the major contributor to the total energy budget in this bacterium.

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Acknowledgements

This work was supported in part by the funding received from the Department of Biotechnology, Government of India (D.O. no. BT/PR9712/NBD/52/91/2007), to SKD. Author KDN acknowledges the Council of Scientific and Industrial Research, Government of India, for providing the research fellowship. Thanks are due to Director, Institute of Life Sciences, for offering an adjunct faculty to SCS. The sequence data used in the study was produced by the US Department of Energy Joint Genome Institute (http://www.jgi.doe.gov/).

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  1. Department of Biotechnology, Institute of Life Sciences, Nalco Square, Bhubaneswar, 751023, India

    Kunwar Digvijay Narayan, Surendra Chandra Sabat & Subrata K Das

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  1. Kunwar Digvijay Narayan
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  2. Surendra Chandra Sabat
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  3. Subrata K Das
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Correspondence to Subrata K Das.

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Narayan, K.D., Sabat, S.C. & Das, S.K. Mechanism of electron transport during thiosulfate oxidation in an obligately mixotrophic bacterium Thiomonas bhubaneswarensis strain S10 (DSM 18181T). Appl Microbiol Biotechnol 101, 1239–1252 (2017). https://doi.org/10.1007/s00253-016-7958-x

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