Microbial mercury methylation in Antarctic sea ice

Abstract

Atmospheric deposition of mercury onto sea ice and circumpolar sea water provides mercury for microbial methylation, and contributes to the bioaccumulation of the potent neurotoxin methylmercury in the marine food web. Little is known about the abiotic and biotic controls on microbial mercury methylation in polar marine systems. However, mercury methylation is known to occur alongside photochemical and microbial mercury reduction and subsequent volatilization. Here, we combine mercury speciation measurements of total and methylated mercury with metagenomic analysis of whole-community microbial DNA from Antarctic snow, brine, sea ice and sea water to elucidate potential microbially mediated mercury methylation and volatilization pathways in polar marine environments. Our results identify the marine microaerophilic bacterium Nitrospina as a potential mercury methylator within sea ice. Anaerobic bacteria known to methylate mercury were notably absent from sea-ice metagenomes. We propose that Antarctic sea ice can harbour a microbial source of methylmercury in the Southern Ocean.

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Figure 1: Sea-ice and sea-water mercury and chlorophyll concentrations.
Figure 2: Fisher's exact test of taxonomic profiles for bulk sea-ice and brine metagenomes.
Figure 3: Maximum likelihood tree of HgcA-like sequences retrieved from polar and marine metagenomes and sequenced PCR products from this study (blue text).
Figure 4: Structural model of the Nitrospina HgcA-like protein complexed with cobalamin.

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Acknowledgements

The authors acknowledge funding support from the Australian Antarctic Division (AAD4032, awarded to R.S., J.W.M., M.T.T. and D.P.K.) and The University of Melbourne Joyce Lambert Antarctic Research Seed Funding Grant (no. 501325, awarded to M.B.S., K.E.H. and J.W.M.). The authors thank K. Meiners for contributions to the sea ice chemistry data and shipboard logistical support as the Chief Scientist of SIPEX II; A. Klekociuk (Australian Antarctic Division, Co-Investigator on AAD4032) for shipboard logistical support; D. Lannuzel and A. Bowie (University of Tasmania) for making trace metal data available and for shipboard sampling and logistical support; K. Westwood at the Australian Antarctic Division for assistance in the biology laboratory and contributions to water chemistry data; and A. Martin, S. Ugalde, F. Chever, C. Schallenberg and J. Janssens (SIPEX II Science Party) for logistical assistance on the ice. The authors also thank J. Banfield and B. Thomas (University of California-Berkeley) for help with ggKbase. The authors thank J. Santillan and C. Gilmour (Smithsonian Environmental Research Center) for their constructive review that helped to improve this manuscript.

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C.M.G. and J.W.M. designed the project and wrote the manuscript with contributions from all co-authors. C.M.G. was the shipboard scientist on the Aurora Australis for SIPEX II, and J.W.M. and R.S. were the research co-supervisors. M.T.T. assisted C.M.G. with the installation of Hg analytical equipment, and C.M.G. performed the laboratory-based Hg analyses with assistance from M.T.T. and under the supervision of D.P.K. and J.W.M. C.M.G., R.R.W. and M.B.S. performed the metagenomic and bioinformatic analyses, supervised by K.E.H. and J.W.M. A.Z. and M.P.T. performed the protein analysis and structural modelling with inputs from C.M.G., J.W.M. and K.E.H.

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Correspondence to John W. Moreau.

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Gionfriddo, C., Tate, M., Wick, R. et al. Microbial mercury methylation in Antarctic sea ice. Nat Microbiol 1, 16127 (2016). https://doi.org/10.1038/nmicrobiol.2016.127

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