Oxygen‐deficient water zones in the Baltic Sea promote uncharacterized Hg methylating microorganisms in underlying sediments

Abstract

Human‐induced expansion of oxygen‐deficient zones can have dramatic impacts on marine systems and its resident biota. One example is the formation of the potent neurotoxic methylmercury (MeHg) that is mediated by microbial methylation of inorganic divalent Hg (HgII) under oxygen‐deficient conditions. A negative consequence of the expansion of oxygen‐deficient zones could be an increase in MeHg production due to shifts in microbial communities in favor of microorganisms methylating Hg. There is, however, limited knowledge about Hg‐methylating microbes, i.e., those carrying hgc genes critical for mediating the process, from marine sediments. Here, we aim to study the presence of hgc genes and transcripts in metagenomes and metatranscriptomes from four surface sediments with contrasting concentrations of oxygen and sulfide in the Baltic Sea. We show that potential Hg methylators differed among sediments depending on redox conditions. Sediments with an oxygenated surface featured hgc‐like genes and transcripts predominantly associated with uncultured Desulfobacterota (OalgD group) and Desulfobacterales (including Desulfobacula sp.) while sediments with a hypoxic‐anoxic surface included hgc‐carrying Verrucomicrobia, unclassified Desulfobacterales, Desulfatiglandales, and uncharacterized microbes. Our data suggest that the expansion of oxygen‐deficient zones in marine systems may lead to a compositional change of Hg‐methylating microbial groups in the sediments, where Hg methylators whose metabolism and biology have not yet been characterized will be promoted and expand.

Expression Levels of hgcAB Genes and Mercury Availability Jointly Explain Methylmercury Formation in Stratified Brackish Waters

“…Previous metagenomic studies have demonstrated the presence of hgc genes in oxygenated marine pelagic systems, suggesting a potentially important role of certain aerobic lineages, e.g., Nitrospina , in marine Hg II methylation. − So far, less attention has been given to oxygen-deficient marine environments ,, where other Hg II -methylating lineages are expected to thrive. Consistent with other recent findings, our results based on the sequencing of metagenomes and metatranscriptomes (Datasheet 1B) from water samples demonstrated that redox conditions are a major factor controlling the presence and abundance of potential Hg II methylators in the central Baltic Sea water column (Figures and ).…”

Anaerobic mercury methylators inhabit sinking particles of oxic water columns

“…Additionally, two recent studies based on the analysis of metagenomes from sulfate-enriched lakes revealed the presence of other hgc + microbial lineages including Kiritimatiellaeota (from PVC superphylum), Spirochaetes or Aminicenantes (Jones et al, 2019;Peterson et al, 2020). The contrasted diversity between water column and sediments was also recently observed in a brackish ecosystem, the Baltic Sea, in which hgc + Spirochaetes were predominant in sinking particles (Capo et al, 2020) but not in anoxic sediments (Capo et al, 2022a), while certain hgc + Desulfobacterota were abundant in both environments.…”

“…This process, also called Hg methylation, is mediated by microorganisms carrying hgcA and hgcB genes (hgc+ microorganisms) coding respectively for a corrinoid protein and a ferredoxin (Parks et al, 2013;Smith et al, 2015). The discovery of hgc genes opens avenues to unravel the diversity and distribution of putative Hg methylators in the environment in microbial groups recognized well to include Hg methylators (Desulfobacterota, Firmicutes, Methanomicrobia) (Gilmour et al, 2013;Podar et al, 2015) and in newly discovered groups such as Chloroflexota and PVC superphylum (McDaniel et al, 2020;Gionfriddo et al, 2020;Capo et al, 2022a).…”

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

“…The normalization of gene counts from environmental metagenomes and metatranscriptomes is a key aspect of works aiming to study the prevalence of certain microorganisms in specific environments (Pereira et al, 2018; Salazar et al, 2019; Pierella Karlusich et al, 2022). In hgcAB omics studies, the number of mapped reads and the coverage values of marker genes or housekeeping genes is usually used to normalize the coverage values of hgc genes (Lin et al, 2021; Vigneron et al, 2021; Tada et al, 2021; Capo et al, 2022). Tests here revealed that a wide range of contrasting normalization methods all provided reasonable abundance estimates that were significantly correlated with one another with the exception of genome equivalent values (Fig 4).…”