Mercury Methylation Genes Identified across Diverse Anaerobic Microbial Guilds in a Eutrophic Sulfate-Enriched Lake

Abstract

Mercury (Hg) methylation is a microbially mediated process that converts inorganic Hg into bioaccumulative, neurotoxic methylmercury (MeHg). The metabolic activity of methylating organisms is highly dependent on biogeochemical conditions, which subsequently influences MeHg production. However, our understanding of the ecophysiology of methylators in natural ecosystems is still limited. Here, we identified potential locations of MeHg production in the anoxic, sulfidic hypolimnion of a freshwater lake. At these sites, we used shotgun metagenomics to characterize microorganisms with the Hg-methylation gene hgcA. Putative methylators were dominated by hgcA sequences divergent from those in well-studied, confirmed methylators. Using genome-resolved metagenomics, we identified organisms with hgcA (hgcA+) within the Bacteroidetes and the recently described Kiritimatiellaeota phyla. We identified hgcA+ genomes derived from sulfate-reducing bacteria, but these accounted for only 22% of hgcA+ genome coverage. The most abundant hgcA+ genomes were from fermenters, accounting for over half of the hgcA gene coverage. Many of these organisms also mediate hydrolysis of polysaccharides, likely from cyanobacterial blooms. This work highlights the distribution of the Hg-methylation genes across microbial metabolic guilds and indicate that primary degradation of polysaccharides and fermentation may play an important but unrecognized role in MeHg production in the anoxic hypolimnion of freshwater lakes.

Mercury methylation in oxic aquatic macro-environments: a review

“…The two-gene cluster hgcAB is currently the primary indicator used to detect bacteria capable of methylation (Schaefer et al, 2011;Parks et al, 2013;Podar et al, 2015;Bravo and Cosio, 2019;Regnell and Watras, 2019). Peterson et al (2020) investigated an anoxic sulfidic hypolimnion lake with shotgun metagenomics to determine the presence of the gene cluster hgcAB in the microorgan-ism's population. Surprisingly they found that the wellstudied sulfate-reducing bacteria only account for the 22% of all the genome coverage, whereas fermenters were the most abundant accounting for more than half of the genome coverage.…”

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

“…The methylation of Hg II to MeHg in the environment is governed by two factors: the activities of microbial communities (Bravo et al, 2017) and the availability of Hg II for use by these methylators (Schaefer and Morel, 2009;Jonsson et al, 2014;Mazrui et al, 2016). 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).…”

Microbial Diversity and Mercury Methylation Activity in Periphytic Biofilms at a Run-of-River Hydroelectric Dam and Constructed Wetlands

“…More recently, a combination of methylation assays using metabolic inhibitors and molecular genetic surveys of microbial assemblages broadened the diversity of putative Hg methylators to include iron-reducing bacteria (FeRB) (15) and methanogens (16). The discovery of the genetic basis for Hg methylation (hgcA and hgcB genes that encode a corrinoid iron-sulfur protein and a ferredoxin protein, respectively) (17) has facilitated studies that have expanded the diversity of putative Hg methylators and explored their distributions in the environment (18)(19)(20)(21)(22). Numerous additional bacterial phyla are now known to be implicated in MMHg production, including Actinobacteria, Bacteroidetes, Firmicutes, and Chloroflexi (17,18,(23)(24)(25).…”