A physiological role for HgII during phototrophic growth

Journal name:
Nature Geoscience
Volume:
9,
Pages:
121–125
Year published:
DOI:
doi:10.1038/ngeo2629
Received
Accepted
Published online

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.

At a glance

Figures

  1. HgII reduction by purple non-sulphur bacteria grown phototrophically or chemotrophically on acetate or butyrate.
    Figure 1: HgII reduction by purple non-sulphur bacteria grown phototrophically or chemotrophically on acetate or butyrate.

    ac, Hg0 production normalized for cell density for phototrophically grown R. capsulatus (a), R. palustris (b) and R. sphaeroides (c). d,e, Cumulative production for R. capsulatus (d) and phototrophic autoclaved cells and sterile medium controls (e). fh, Hg0 production normalized for cell density for chemotrophically grown R. capsulatus (f), R. palustris (g) and R. sphaeroides (h). Results are representative cases of replicated experiments, but each data point was recorded once per time step by the instrument and as such no error bars are included.

  2. HgII reduction by R. capsulatus grown phototrophically on butyrate and supplied with competing electron sinks.
    Figure 2: HgII reduction by R. capsulatus grown phototrophically on butyrate and supplied with competing electron sinks.

    The competing electron sinks and the concentrations at which they were supplied are: 100μM, 10 and 20mM of HCO3; 1nM and 20mM DMSO; control indicates no competing electron sink. a,c, Hg0 production normalized for cell density for HCO3 (a) and DMSO (c). b,d, Cumulative production for HCO3 (b) and DMSO (d). These results are representative cases of replicated experiments, but each data point was recorded once per time step by the instrument and as such no error bars are included.

  3. [NADH]/[NAD+] for R. capsulatus grown phototrophically on butyrate or acetate in the presence of HCO3-.
    Figure 3: [NADH]/[NAD+] for R. capsulatus grown phototrophically on butyrate or acetate in the presence of HCO3.

    Cells were supplied with 30mM acetate (n = 6), 15mM butyrate (n = 3), or 15mM butyrate with 10 (n = 3) and 20mM HCO3 (n = 3). The bottom and top of the boxes show the first and third quartiles, respectively, the bar in the middle shows the median and the whiskers show the minimum and maximum for each treatment. Carbon source and HCO3 had a significant effect on [NADH]/[NAD+] (p < 0.01). Letters that are not shared between treatments indicate a significant difference according to the Tukey HSD test (p < 0.05).

  4. Comparison of HgII and HCO3- as electron sinks for R. capsulatus grown phototrophically.
    Figure 4: Comparison of HgII and HCO3 as electron sinks for R. capsulatus grown phototrophically.

    Growth parameters are presented for cells grown on 1mM (a,c,e) and 15mM butyrate (b,d,f) (n = 3). The bottom and top of the boxes show the first and third quartiles, respectively, the bar in the middle shows the median and the whiskers show the minimum and maximum for each treatment. Shaded areas represent toxic but sublethal [Hg]. [Hg] had a significant effect on growth rate (p < 0.05), whereas [HCO3] had a significant effect on growth rate (p < 0.01) and yield (p < 0.001). Letters not shared between treatments indicate a significant (p < 0.05) difference according to the Tukey HSD test.

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Affiliations

  1. Biology Department, University of Ottawa, 30 Marie Curie, Ottawa, Ontario K1N 6N5, Canada

    • D. S. Grégoire &
    • A. J. Poulain

Contributions

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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The authors declare no competing financial interests.

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