Metabolically diverse microorganisms mediate methylmercury formation under nitrate-reducing conditions in a dynamic hydroelectric reservoir

Abstract

Brownlee Reservoir is a mercury (Hg)-impaired hydroelectric reservoir that exhibits dynamic hydrological and geochemical conditions and is located within the Hells Canyon Complex in Idaho, USA. Methylmercury (MeHg) contamination in fish is a concern in the reservoir. While MeHg production has historically been attributed to sulfate-reducing bacteria and methanogenic archaea, microorganisms carrying the hgcA gene are taxonomically and metabolically diverse and the major biogeochemical cycles driving mercury (Hg) methylation are not well understood. In this study, Hg speciation and redox-active compounds were measured throughout Brownlee Reservoir across the stratified period in four consecutive years (2016–2019) to identify the location where and redox conditions under which MeHg is produced. Metagenomic sequencing was performed on a subset of samples to characterize the microbial community with hgcA and identify possible links between biogeochemical cycles and MeHg production. Biogeochemical profiles suggested in situ water column Hg methylation was the major source of MeHg. These profiles, combined with genome-resolved metagenomics focused on hgcA-carrying microbes, indicated that MeHg production occurs in this system under nitrate- or manganese-reducing conditions, which were previously thought to preclude Hg-methylation. Using this multidisciplinary approach, we identified the cascading effects of interannual variability in hydrology on the redox status, microbial metabolic strategies, abundance and metabolic diversity of Hg methylators, and ultimately MeHg concentrations throughout the reservoir. This work expands the known conditions conducive to producing MeHg and suggests that the Hg-methylation mitigation efforts by nitrate or manganese amendment may be unsuccessful in some locations.

A genome catalogue of mercury‐methylating bacteria and archaea from sediments of a boreal river facing human disturbances

“…The native function of hgcAB remains unknown (Parks et al, 2013), but its widespread presence across various taxonomic and functional groups suggests that this gene pair must have conferred a competitive advantage to microorganisms at some point. The potential co‐regulation between Hg methylation and arsenic detoxification has been recently proposed (Gionfriddo et al, 2023), and co‐occurrence of hgcA and arsenic detoxification genes in MAGs has also been noted in other studies (Lin et al, 2021; McDaniel et al, 2020; Peterson, Poulin, et al, 2023; Zhang et al, 2023; Zheng et al, 2022), a trend similarly identified in our study. It is plausible that the absence of specific drivers for the structure of Hg‐methylating communities is due to the potential loss of the native function of hgcAB .…”

“…The use of metagenome‐assembled genomes (MAGs) is highly pertinent for studying Hg methylators, as they can reveal microbial diversity (Baker et al, 2021) and inferring the metabolic capacities of microorganisms (Vavourakis et al, 2018). Recent studies recovered hgcA ‐containing MAGs from diverse environments, including lakes (Jones et al, 2019; McDaniel et al, 2020; Peterson et al, 2020), ocean (Capo et al, 2022; Langwig et al, 2022; Lin et al, 2021), mangroves (Peterson, Krabbenhoft, et al, 2023; Zhang et al, 2023), a reservoir (Peterson, Poulin, et al, 2023), contaminated sites (Vigneron et al, 2021; Zheng et al, 2022) and composting sludge (Liu et al, 2022). Two of these studies also mined for hgcA in publicly available MAGs retrieved from diverse environments, encompassing the aforementioned list but also including permafrost (McDaniel et al, 2020; Zhang et al, 2023), wetlands, estuaries, subsurface, hydrothermal vents, endosymbionts, engineered ecosystems and hot springs (McDaniel et al, 2020).…”