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A physiological role for HgII during phototrophic growth

Abstract

The bioaccumulation of toxic monomethylmercury is influenced by the redox reactions that determine the amount of mercury (Hg) substrate—HgII or Hg0 (refs 1,2)—that is available for methylation3. Phototrophic microorganisms can reduce HgII to Hg0 (ref. 4). This reduction has been linked to a mixotrophic lifestyle5, in which microbes gain energy photosynthetically but acquire diverse carbon compounds for biosynthesis from the environment. Photomixotrophs must maintain redox homeostasis to disperse excess reducing power due to the accumulation of reduced enzyme cofactors6. Here we report laboratory experiments in which we exposed purple bacteria growing in a bioreactor to HgII and monitored Hg0 concentrations. We show that phototrophs use HgII as an electron sink to maintain redox homeostasis. Hg0 concentrations increased only when bacteria grew phototrophically, and when bacterial enzyme cofactor ratios indicated the presence of an intracellular redox imbalance. Under such conditions, bacterial growth rates increased with increasing HgII concentrations; when alternative electron sinks were added, Hg0 production decreased. We conclude that Hg can fulfil a physiological function in bacteria, and that photomixotrophs can modify the availability of Hg to methylation sites.

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Figure 1: HgII reduction by purple non-sulphur bacteria grown phototrophically or chemotrophically on acetate or butyrate.
Figure 2: HgII reduction by R. capsulatus grown phototrophically on butyrate and supplied with competing electron sinks.
Figure 3: [NADH]/[NAD+] for R. capsulatus grown phototrophically on butyrate or acetate in the presence of HCO3.
Figure 4: Comparison of HgII and HCO3 as electron sinks for R. capsulatus grown phototrophically.

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Acknowledgements

Our work was funded by NSERC Discovery and Accelerator grants as well as CFI funding to A.J.P. and an NSERC CGS D Scholarship to D.S.G. This work was inspired by discussions with M. Amyot, T. Barkay and D. Newman on the photobiology of metals and its evolution through geologic times. We are grateful for all three PNSB strains, which were a gift from D. K. Newman. We thank A. Price-Whelan and S. Kern for help and guidance with [NADH]/[NAD+] assays and we thank E. Yumvihoze and A. Dommergue for their help with Hg analyses.

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A.J.P. initiated the study; A.J.P. and D.S.G. designed the experiments; D.S.G. carried out the experiments; A.J.P. and D.S.G. performed data analyses; A.J.P. and D.S.G. wrote the manuscript.

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Correspondence to A. J. Poulain.

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The authors declare no competing financial interests.

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Grégoire, D., Poulain, A. A physiological role for HgII during phototrophic growth. Nature Geosci 9, 121–125 (2016). https://doi.org/10.1038/ngeo2629

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