Diverse Communities of hgcAB⁺ Microorganisms Methylate Mercury in Freshwater Sediments Subjected to Experimental Sulfate Loading

Abstract

Methylmercury (MeHg) is a bioaccumulative neurotoxin produced by certain sulfate-reducing bacteria and other anaerobic microorganisms. Because microorganisms differ in their capacity to methylate mercury, the abundance and distribution of methylating populations may determine MeHg production in the environment. We compared rates of MeHg production and the distribution of hgcAB genes in epilimnetic sediments from a freshwater lake that were experimentally amended with sulfate levels from 7 to 300 mg L–1. The most abundant hgcAB sequences were associated with clades of Methanomicrobia, sulfate-reducing Deltaproteobacteria, Spirochaetes, and unknown environmental sequences. The hgcAB + communities from higher sulfate amendments were less diverse and had relatively more Deltaproteobacteria, whereas the communities from lower amendments were more diverse with a larger proportion of hgcAB sequences affiliated with other clades. Potential methylation rate constants varied 52-fold across the experiment. Both potential methylation rate constants and % MeHg were the highest in sediments from the lowest sulfate amendments, which had the most diverse hgcAB + communities and relatively fewer hgcAB genes from clades associated with sulfate reduction. Although pore water sulfide concentration covaried with hgcAB diversity across our experimental sulfate gradient, major changes in the community of hgcAB + organisms occurred prior to a significant buildup of sulfide in pore waters. Our results indicate that methylating communities dominated by diverse anaerobic microorganisms that do not reduce sulfate can produce MeHg as effectively as communities dominated by sulfate-reducing populations.

Mercury Methylating Microbial Community Structure in Boreal Wetlands Explained by Local Physicochemical Conditions

“…In particular, we show that more diverse hgcA+ communities are related to higher Hg II methylation rates in wetlands. This has also been suggested by a recent study performed with freshwater lake sediments amended with different sulfate concentrations (Jones et al, 2020). Our study, therefore, emphasizes the relevance of describing the diversity of hgcA+ microbial communities in order to better understand the processes controlling MeHg formation in the environment.…”

“…Some members of sulfate-reducing bacteria (SRB) (Gilmour et al, 1992;King et al, 2001;Gilmour et al, 2013), iron-reducing bacteria (FeRB) (Fleming et al, 2006;Kerin et al, 2006;Bravo et al, 2018b), methanogens (Hamelin et al, 2011;Yu et al, 2013), Firmicutes (Gilmour et al, 2013), acetogens, and recently also obligate fermenting lineages (McDaniel et al, 2020b;Peterson et al, 2020) have so far been implicated in Hg II methylation. The identification of two genes (hgcAB) essential for Hg II methylation (Parks et al, 2013) provides the means to more directly characterize the diversity of potential Hg II methylators in contrasting environmental niches, such as soils (Liu et al, 2014;Liu et al, 2018;Vishnivetskaya et al, 2018;Xu et al, 2019), lakes, reservoirs (Bravo et al, 2018a;Bravo et al, 2018b;Jones et al, 2019;Jones et al, 2020), coastal sediments, animal guts, extremes of pH, salinity environments (Gilmour et al, 2013), the global ocean (Podar et al, 2015;Villar et al, 2020), Baltic Sea (Capo et al, 2020), and even in the Southern Ocean (Gionfriddo et al, 2016). However, for most of the recently discovered microorganisms carrying the hgcA gene (hgcA+), their role in the environment and their capacity to actually methylate Hg II has yet to be demonstrated.…”

“…However, still little is known on the factors influencing the structure and function of hgcA+ microbial communities in the environment or the effect of the hgcA+ microbial community composition on Hg II methylation rate constants. Jones et al (2020) amended freshwater lake sediments with different sulfate concentrations and observed that the experimental plots with the lowest sulfate concentrations presented the highest hgcA+ diversity and the highest Hg II methylation rate, highlighting that diverse hgcA+ communities that do not reduce sulfate can methylate Hg II as effectively as communities dominated by sulfatereducing populations (Jones et al, 2020). Although this study emphasizes that the hgcA+ microbial community structure is relevant for the Hg II methylation rate, further evidence is needed to confirm the effect of compositional changes of hgcA+ communities in Hg II methylation rates.…”

Unravelling biogeochemical drivers of methylmercury production in an Arctic fen soil and a bog soil

“…MeHg is produced by a small group of anaerobic microorganisms carrying a two-gene cluster hgcAB essential for Hg(II) methylation (Parks et al, 2013). These microbes may include, but are not limited to, sulfate-reducing bacteria (SRB), iron-reducing bacteria (FeRB), methanogens, and fermenters (Bravo et al, 2018;Gilmour et al, 2013;Jones et al, 2020;Liu et al, 2018;Yu et al, 2013), although their contributions to MeHg production vary with geochemical conditions in different environmental systems. Several studies reported that methanogens and FeRB were dominant members of Hg(II) methylating community in rice paddy soils and in boreal lakes (Bravo et al, 2018;Liu et al, 2018), while others found that SRB were the principal Hg(II) methylators in some freshwater sediments or boreal wetlands (Jones et al, 2020;Schaefer et al, 2020).…”

Nutrient Inputs Stimulate Mercury Methylation by Syntrophs in a Subarctic Peatland

“…More recently, the discovery of the hgcAB genes encoding for the Hg methylase and associated ferredoxin (Parks et al, 2013) has revealed that several additional guilds of anaerobic microorganisms can methylate Hg, including methanogens (Gilmour et al, 2013(Gilmour et al, , 2018Yu et al, 2013Yu et al, , 2018, fermenters (Gilmour et al, 2013) and syntrophs (Gilmour et al, 2013;Yu et al, 2018). This advancement has provided an important gene marker for identifying environments and microbial taxa with a potential for Hg methylation (Bae et al, 2014;Schaefer J. K. et al, 2014;Christensen et al, 2016;Jones et al, 2020;McDaniel et al, 2020;Peterson et al, 2020). However, the contribution of newly identified methylating guilds to MeHg production in the environment remains to be demonstrated.…”