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Metabolomic analyses show that electron donor and acceptor ratios control anaerobic electron transfer pathways in Shewanella oneidensis

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Abstract

This study investigated the physiological impact of changing electron donor–acceptor ratios on electron transfer pathways in the metabolically flexible subsurface bacterium Shewanella oneidensis, using batch and chemostat cultures, with an azo dye (ramazol black B) as the model electron acceptor. Altering the growth rate did result in changes in biomass yield, but not in other key physiological parameters including the total cytochrome content of the cells, the production of extracellular flavin redox shuttles or the potential of the organism to reduce the azo dye. Dramatic increases in the ability to reduce the dye were noted when cells were grown under conditions of electron acceptor (fumarate) limitation, although the yields of extracellular redox mediators (flavins) were similar under conditions of electron donor (lactate) or acceptor limitation. FT-IR spectroscopy confirmed shifts in the metabolic fingerprints of cells grown under these contrasting conditions, while spectrophotometric analyses supported a critical role for c-type cytochromes, expressed at maximal concentrations under conditions of electron acceptor limitation. Finally, key intracellular metabolites were quantified in batch experiments at various electron donor and acceptor ratios and analysed using discriminant analysis and a Bayesian network to construct a central metabolic pathway model for cells grown under conditions of electron donor or acceptor limitation. These results have identified key mechanisms involved in controlling electron transfer in Shewanella species, and have highlighted strategies to maximise reductive activity for a range of bioprocesses.

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Acknowledgments

This research was supported by BBSRC grant BBS/B/03718 and a Manchester-CSC PhD scholarship to H Wang. Harald von Canstein and Georgios D. Antoniou are acknowledged for initial discussions on Shewanella physiology. E. C. and R. G. would like to thank the Seventh Framework Programme (CommonSense project—SEC-2010.1.3-3 ref: 261809) for financial support. RG and WD thank BBSRC and EPSRC for financial support of the Manchester Centre for Integrative Systems Biology.

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Authors and Affiliations

  1. School of Earth, Atmospheric and Environmental Sciences and Williamson Research Centre of Molecular Environmental Science, University of Manchester, Manchester, M13 9PL, UK

    Hui Wang & Jonathan R. Lloyd

  2. School of Chemistry, Manchester Institute of Biotechnology, University of Manchester, 131 Princess Street, Manchester, M1 7DN, UK

    Elon Correa & Royston Goodacre

  3. Institute of Human Development, The University of Manchester, Manchester, UK

    Warwick B. Dunn

  4. Centre for Advanced Discovery and Experimental Therapeutics, Central Manchester University Hospitals NHS Foundation Trust, Manchester Academic Health Sciences Centre, Manchester, UK

    Warwick B. Dunn

  5. School of Chemical Engineering and Analytical Science, Manchester Institute of Biotechnology, University of Manchester, 131 Princess Street, Manchester, M1 7DN, UK

    Catherine L. Winder

  6. Faculty of Life Science, University of Manchester, Oxford Road, Manchester, M13 9PT, UK

    Hui Wang

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  1. Hui Wang
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  2. Elon Correa
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  3. Warwick B. Dunn
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Correspondence to Jonathan R. Lloyd.

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Wang, H., Correa, E., Dunn, W.B. et al. Metabolomic analyses show that electron donor and acceptor ratios control anaerobic electron transfer pathways in Shewanella oneidensis . Metabolomics 9, 642–656 (2013). https://doi.org/10.1007/s11306-012-0488-3

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