Nutrient Inputs Stimulate Mercury Methylation by Syntrophs in a Subarctic Peatland

Abstract

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 (kmeth), 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 (kmeth) 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 kmeth relative to unamended controls despite no effect on kmeth 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 kmeth, suggesting a role for interactions between SRB and methanogens in Hg methylation. The reduction in kmeth 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.

Microbial communities mediating net methylmercury formation along a trophic gradient in a peatland chronosequence

“…It is known that peatland microbial communities are shaped by a wide range of environmental factors, such as pH and nutrient availability (Juottonen et al, 2005;Morales et al, 2006;Urbanová and Bárta, 2014). Accordingly, such environmentally controlled changes in the composition of microbial communities, including non-Hg and Hg methylating microorganisms, would likely result in variable net MeHg formation (Liu et al, 2019;Roth et al, 2021;Xu et al, 2021;Zhou et al, 2020). In agreement with this, our results showed a strong association between peat soil characteristics and microbial community composition and subsequently an indirect effect of peat soil characteristics on net MeHg formation (Fig.…”

“…Recently the wider use of culture-independent methods, such as hgcA gene sequencing, genome-resolved metagenomics and metatranscriptomics, has greatly expanded the known phylogenetic and metabolic diversity of Hg methylating microorganisms (Christensen et al, 2019;McDaniel et al, 2020;Peterson et al, 2020;Xu et al, 2019Xu et al, , 2021. While FeRB, methanogens, syntrophs and Firmicutes have been implicated as putative Hg methylating microorganisms in low-sulfate wetlands, SRB remain the main methylators in the ecosystems where sulfate is not limiting (Liu et al, 2018;Roth et al, 2021;Schaefer et al, 2020;Xu et al, 2021).…”

A consensus protocol for the recovery of mercury methylation genes from metagenomes

“…While directly testing for Hg methylation capacity may not be a viable strategy, pairing these sequencing methods with biogeochemical measurements, Hg methylation assays, and other manipulation studies can connect a Hg-methylating microbiome to MeHg production and metabolic activity and help to elucidate the potential contribution of these novel clades to Hg methylation (Bouchet et al, 2018;Kronberg et al, 2016;Roth et al, 2021;Schaefer et al, 2020).…”

A consensus protocol for the recovery of mercury methylation genes from metagenomes

“…High-throughput meta-omic and targeted amplicon sequencing studies have become the main methods for identifying putative Hg methylating microorganisms of this unculturable fraction (Bravo et al, 2018; Gionfriddo et al, 2020; Xu et al, 2021). While directly testing for Hg methylation capacity may not be a viable strategy, pairing these sequencing methods with biogeochemical measurements, Hg methylation assays, and other manipulation studies can connect a Hg-methylating microbiome to MeHg production and metabolic activity and help to elucidate the potential contribution of these novel clades to Hg methylation (Kronberg et al, 2016; Bouchet et al, 2018; Schaefer et al, 2020; Roth et al, 2021).…”