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

Abstract

The potent neurotoxin methylmercury (MeHg) is a major concern due to its negative effects on wildlife and human health. Boreal wetlands play a crucial role in Hg cycling on a global scale, and therefore, it is crucial to understand the biogeochemical processes involved in MeHg formation in this landscape element. By combining high-throughput hgcA amplicon sequencing with molecular barcoding, we reveal diverse clades of potential HgII methylators in a wide range of wetland soils. Among Bacteria, Desulfuromonadota (14% of total reads), Desulfurobacterota_A, and Desulfurobacterota (up to 6% of total reads), previously classified as Deltaproteobacteria, were important members of the hgcA+ microbial community in the studied wetlands. We also identified Actinobacteriota (9.4% of total reads), Bacteroidota (2% of total reads), and Firmicutes (1.2% of total reads) as members of the hgcA+ microbial community. Within Archaea, Methanosarcinales represented up to 2.5% of the total reads. However, up to half of the hgcA+ community could not be resolved beyond domain Bacteria. Our survey also shows that local physicochemical conditions, such as pH, nutrient concentrations, water content, and prevailing redox states, are important for shaping the hgcA+ microbial community structure across the four studied wetlands. Furthermore, we observed a significant correlation between HgII methylation rate constants and the structure of the hgcA+ microbial community. Our findings expand the current knowledge on the hgcA+ microbial community composition in wetlands and the physicochemical factors underpinning spatial heterogeneity in such communities.

Mercury Export From Freshwater to Estuary: Carbocentric Science Elucidates the Fate of a Toxic Compound in Aquatic Boreal Environments

“…The biological processes and bacterial groups involved in mercury methylation in anoxic sediments or in the water column are similar in natural lakes (Morel et al, 1998), reservoirs (Hall et al, 2005) and interestingly also in coastal systems (Skrobonja, 2019). In fact, a variety of anaerobes (particularly iron and sulfate-reducing bacteria) share a common gene pair (hgcAB) that encodes proteins essential for Hg methylation (Regnell and Watras, 2019;Xu et al, 2021). The diversity of the methanogenic bacterial community in streams is positively linked to water temperature (Nagler et al, 2020), which suggests a lower diversity in boreal lakes and reservoirs, but one that should be quite similar throughout the boreal ecozone.…”

“…Finally, wetlands, an important portion of the boreal landscape (e.g., 30% in Ontario, Canada, McLaughlin, 2004;Gingras et al, 2016), represent a source of OM and MeHg for the catchments (St. Louis et al, 2004;Xu et al, 2021). Their hydrology and connectivity with the large watersheds typical of boreal biomes is not addressed here.…”

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

“…Microbes that have yet to be cultivated, and for which successful laboratory growth parameters need to be identified, are often referred to as the “unculturable” (Hug et al, 2016; Steen et al, 2019). 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).…”

Microbial Communities Mediating Net Methylmercury Formation Along a Trophic Gradient in a Peatland Chronosequence

“…These genes are found in sulfate-reducing bacteria (SRB) (Compeau and Bartha, 1985;Gilmour et al, 1992Gilmour et al, , 2013, iron-reducing bacteria (FeRB) (Bravo et al, 2018b;Fleming et al, 2006;Kerin et al, 2006), and methanogens (Hamelin et al, 2011;Wood et al, 1968), but also in some fermentative and syntrophic microbes (Gilmour et al, 2013;Podar et al, 2015;Yu et al, 2018). 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).…”

“…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).…”