Robust mercury methylation across diverse methanogenic Archaea

Cynthia C. Gilmour, Allyson L. Bullock, Alyssa McBurney, Mircea Podar, Dwayne A. Elias

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114 Scopus citations

Abstract

Methylmercury (MeHg) production was compared among nine cultured methanogenic archaea that contain hgcAB, a gene pair that codes for mercury (Hg) methylation. The methanogens tested produced MeHg at inherently different rates, even when normalized to growth rate and Hg availability. Eight of the nine tested were capable of MeHg production greater than that of spent- and uninoculatedmedium controls during batch culture growth. Methanococcoides methylutens, an hgcAB+ strain with a fused gene pair, was unable to produce more MeHg than controls. Maximal conversion of Hg to MeHg through a full batch culture growth cycle for each species (except M. methylutens) ranged from 2 to >50% of the added Hg(II) or between 0.2 and 17 pmol of MeHg/mg of protein. Three of the species produced >10% MeHg. The ability to produce MeHg was confirmed in several hgcAB+ methanogens that had not previously been tested (Methanocella paludicola SANAE, Methanocorpusculum bavaricum, Methanofollis liminatans GKZPZ, and Methanosphaerula palustris E1-9c). Maximal methylation was observed at low sulfide concentrations (<100 µM) and in the presence of 0.5 to 5 mM cysteine. For M. hollandica, the addition of up to 5 mM cysteine enhanced MeHg production and cell growth in a concentration-dependent manner. As observed for bacterial Hg methylators, sulfide inhibited MeHg production. An initial evaluation of sulfide and thiol impacts on bioavailability showed methanogens responding to Hg complexation in the same way as do Deltaproteobacteria. The mercury methylation rates of several methanogens rival those of the better-studied Hg-methylating sulfate- and iron-reducing Deltaproteobacteria. IMPORTANCE Archaea, specifically methanogenic organisms, play a role in mercury methylation in nature, but their global importance to MeHg production and the subsequent risk to ecosystems are not known. Methanogenesis has been linked to Hg methylation in several natural habitats where methylmercury production incurs risk to people and ecosystems, including rice paddies and permafrost. In this study, we confirm that most methanogens carrying the hgcAB gene pair are capable of Hg methylation. We found that methylation rates vary inherently among hgcAB+ methanogens but that several species are capable of MeHg production at rates that rival those of the better-know Hg-methylating sulfate- and iron-reducing bacteria. Methanogens may need to be considered equally with sulfate and iron reducers in evaluations of MeHg production in nature.

Original languageEnglish
Article numbere02403-17
JournalmBio
Volume9
Issue number2
DOIs
StatePublished - Mar 1 2018

Funding

This research was sponsored by the Office of Biological and Environmental Research, Office of Science of the U.S. Department of Energy (DOE), as part of the Mercury Science Focus Area at Oak Ridge National Laboratory, which is managed by UT-Battelle LLC for the DOE under contract DE-AC05-00OR22725, and by NIEHS R01ES024284-01 to Upal Ghosh (University of Maryland Baltimore County), C.C.G., and D.A.E.

Keywords

  • Archaea
  • Bioavailability
  • Complexation
  • Cysteine
  • Mercury
  • Methylation
  • Methylmercury
  • Methyltransferase
  • Thiols
  • hgcAB

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