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Nutrient Inputs Stimulate Mercury Methylation by Syntrophs in a Subarctic Peatland

Climate change dramatically impacts Arctic and subarctic regions, inducing shifts in wetland nutrient regimes as a consequence of thawing permafrost. Altered hydrological regimes may drive changes in the dynamics of microbial mercury (Hg) methylation and bioavailability. Important knowledge gaps rem...

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Autores principales: Roth, Spencer, Poulin, Brett A., Baumann, Zofia, Liu, Xiao, Zhang, Lin, Krabbenhoft, David P., Hines, Mark E., Schaefer, Jeffra K., Barkay, Tamar
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8524442/
https://www.ncbi.nlm.nih.gov/pubmed/34675906
http://dx.doi.org/10.3389/fmicb.2021.741523
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author Roth, Spencer
Poulin, Brett A.
Baumann, Zofia
Liu, Xiao
Zhang, Lin
Krabbenhoft, David P.
Hines, Mark E.
Schaefer, Jeffra K.
Barkay, Tamar
author_facet Roth, Spencer
Poulin, Brett A.
Baumann, Zofia
Liu, Xiao
Zhang, Lin
Krabbenhoft, David P.
Hines, Mark E.
Schaefer, Jeffra K.
Barkay, Tamar
author_sort Roth, Spencer
collection PubMed
description Climate change dramatically impacts Arctic and subarctic regions, inducing shifts in wetland nutrient regimes as a consequence of thawing permafrost. Altered hydrological regimes may drive changes in the dynamics of microbial mercury (Hg) methylation and bioavailability. Important knowledge gaps remain on the contribution of specific microbial groups to methylmercury (MeHg) production in wetlands of various trophic status. Here, we measured aqueous chemistry, potential methylation rates (k(meth)), volatile fatty acid (VFA) dynamics in peat-soil incubations, and genetic potential for Hg methylation across a groundwater-driven nutrient gradient in an interior Alaskan fen. We tested the hypotheses that (1) nutrient inputs will result in increased methylation potentials, and (2) syntrophic interactions contribute to methylation in subarctic wetlands. We observed that concentrations of nutrients, total Hg, and MeHg, abundance of hgcA genes, and rates of methylation in peat incubations (k(meth)) were highest near the groundwater input and declined downgradient. hgcA sequences near the input were closely related to those from sulfate-reducing bacteria (SRB), methanogens, and syntrophs. Hg methylation in peat incubations collected near the input source (FPF2) were impacted by the addition of sulfate and some metabolic inhibitors while those down-gradient (FPF5) were not. Sulfate amendment to FPF2 incubations had higher k(meth) relative to unamended controls despite no effect on k(meth) from addition of the sulfate reduction inhibitor molybdate. The addition of the methanogenic inhibitor BES (25 mM) led to the accumulation of VFAs, but unlike molybdate, it did not affect Hg methylation rates. Rather, the concurrent additions of BES and molybdate significantly decreased k(meth), suggesting a role for interactions between SRB and methanogens in Hg methylation. The reduction in k(meth) with combined addition of BES and molybdate, and accumulation of VFA in peat incubations containing BES, and a high abundance of syntroph-related hgcA sequences in peat metagenomes provide evidence for MeHg production by microorganisms growing in syntrophy. Collectively the results suggest that wetland nutrient regimes influence the activity of Hg methylating microorganisms and, consequently, Hg methylation rates. Our results provide key information about microbial Hg methylation and methylating communities under nutrient conditions that are expected to become more common as permafrost soils thaw.
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spelling pubmed-85244422021-10-20 Nutrient Inputs Stimulate Mercury Methylation by Syntrophs in a Subarctic Peatland Roth, Spencer Poulin, Brett A. Baumann, Zofia Liu, Xiao Zhang, Lin Krabbenhoft, David P. Hines, Mark E. Schaefer, Jeffra K. Barkay, Tamar Front Microbiol Microbiology Climate change dramatically impacts Arctic and subarctic regions, inducing shifts in wetland nutrient regimes as a consequence of thawing permafrost. Altered hydrological regimes may drive changes in the dynamics of microbial mercury (Hg) methylation and bioavailability. Important knowledge gaps remain on the contribution of specific microbial groups to methylmercury (MeHg) production in wetlands of various trophic status. Here, we measured aqueous chemistry, potential methylation rates (k(meth)), volatile fatty acid (VFA) dynamics in peat-soil incubations, and genetic potential for Hg methylation across a groundwater-driven nutrient gradient in an interior Alaskan fen. We tested the hypotheses that (1) nutrient inputs will result in increased methylation potentials, and (2) syntrophic interactions contribute to methylation in subarctic wetlands. We observed that concentrations of nutrients, total Hg, and MeHg, abundance of hgcA genes, and rates of methylation in peat incubations (k(meth)) were highest near the groundwater input and declined downgradient. hgcA sequences near the input were closely related to those from sulfate-reducing bacteria (SRB), methanogens, and syntrophs. Hg methylation in peat incubations collected near the input source (FPF2) were impacted by the addition of sulfate and some metabolic inhibitors while those down-gradient (FPF5) were not. Sulfate amendment to FPF2 incubations had higher k(meth) relative to unamended controls despite no effect on k(meth) from addition of the sulfate reduction inhibitor molybdate. The addition of the methanogenic inhibitor BES (25 mM) led to the accumulation of VFAs, but unlike molybdate, it did not affect Hg methylation rates. Rather, the concurrent additions of BES and molybdate significantly decreased k(meth), suggesting a role for interactions between SRB and methanogens in Hg methylation. The reduction in k(meth) with combined addition of BES and molybdate, and accumulation of VFA in peat incubations containing BES, and a high abundance of syntroph-related hgcA sequences in peat metagenomes provide evidence for MeHg production by microorganisms growing in syntrophy. Collectively the results suggest that wetland nutrient regimes influence the activity of Hg methylating microorganisms and, consequently, Hg methylation rates. Our results provide key information about microbial Hg methylation and methylating communities under nutrient conditions that are expected to become more common as permafrost soils thaw. Frontiers Media S.A. 2021-10-04 /pmc/articles/PMC8524442/ /pubmed/34675906 http://dx.doi.org/10.3389/fmicb.2021.741523 Text en Copyright © 2021 Roth, Poulin, Baumann, Liu, Zhang, Krabbenhoft, Hines, Schaefer and Barkay. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Roth, Spencer
Poulin, Brett A.
Baumann, Zofia
Liu, Xiao
Zhang, Lin
Krabbenhoft, David P.
Hines, Mark E.
Schaefer, Jeffra K.
Barkay, Tamar
Nutrient Inputs Stimulate Mercury Methylation by Syntrophs in a Subarctic Peatland
title Nutrient Inputs Stimulate Mercury Methylation by Syntrophs in a Subarctic Peatland
title_full Nutrient Inputs Stimulate Mercury Methylation by Syntrophs in a Subarctic Peatland
title_fullStr Nutrient Inputs Stimulate Mercury Methylation by Syntrophs in a Subarctic Peatland
title_full_unstemmed Nutrient Inputs Stimulate Mercury Methylation by Syntrophs in a Subarctic Peatland
title_short Nutrient Inputs Stimulate Mercury Methylation by Syntrophs in a Subarctic Peatland
title_sort nutrient inputs stimulate mercury methylation by syntrophs in a subarctic peatland
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8524442/
https://www.ncbi.nlm.nih.gov/pubmed/34675906
http://dx.doi.org/10.3389/fmicb.2021.741523
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