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Title: Robust Mercury Methylation across Diverse Methanogenic Archaea

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 uninoculated-medium 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 inmore » 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.« less
Authors:
ORCiD logo [1] ;  [1] ;  [1] ; ORCiD logo [2] ; ORCiD logo [2]
  1. Smithsonian Environmental Research Center, Edgewater, MD (United States)
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division
Publication Date:
Grant/Contract Number:
AC05-00OR22725; Mercury SFA
Type:
Published Article
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online); Journal Volume: 9; Journal Issue: 2; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology
Research Org:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Archaea; methylmercury; bioavailability; complexation; cysteine; hgcAB; mercury; methyltransferase; methylation; thiols
OSTI Identifier:
1461239
Alternate Identifier(s):
OSTI ID: 1435231

Gilmour, Cynthia C., Bullock, Allyson L., McBurney, Alyssa, Podar, Mircea, and Elias, Dwayne A.. Robust Mercury Methylation across Diverse Methanogenic Archaea. United States: N. p., Web. doi:10.1128/mBio.02403-17.
Gilmour, Cynthia C., Bullock, Allyson L., McBurney, Alyssa, Podar, Mircea, & Elias, Dwayne A.. Robust Mercury Methylation across Diverse Methanogenic Archaea. United States. doi:10.1128/mBio.02403-17.
Gilmour, Cynthia C., Bullock, Allyson L., McBurney, Alyssa, Podar, Mircea, and Elias, Dwayne A.. 2018. "Robust Mercury Methylation across Diverse Methanogenic Archaea". United States. doi:10.1128/mBio.02403-17.
@article{osti_1461239,
title = {Robust Mercury Methylation across Diverse Methanogenic Archaea},
author = {Gilmour, Cynthia C. and Bullock, Allyson L. and McBurney, Alyssa and Podar, Mircea and Elias, Dwayne A.},
abstractNote = {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 uninoculated-medium 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.},
doi = {10.1128/mBio.02403-17},
journal = {mBio (Online)},
number = 2,
volume = 9,
place = {United States},
year = {2018},
month = {4}
}

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