Microorganisms Involved in Methylmercury Demethylation and Mercury Reduction are Widely Distributed and Active in the Bathypelagic Deep Ocean Waters

Abstract

The ocean's mercury (Hg) content has tripled due to anthropogenic activities, and although the dark ocean (>200 m) has become an important Hg reservoir, concentrations of the toxic and bioaccumulative methylmercury (MeHg) are low and therefore very difficult to measure. As a consequence, the current understanding of the Hg cycle in the deep ocean is severely data-limited, and the factors controlling MeHg, as well as its transformation rates, remain largely unknown. By analyzing 52 globally distributed bathypelagic deep-ocean metagenomes and 26 new metatranscriptomes from the Malaspina Expedition, our study reveals the widespread distribution and expression of bacterial-coding genes <i>merA</i> and <i>merB</i> in the global bathypelagic ocean (∼4000 m depth). These genes, associated with Hg^II reduction and MeHg demethylation, respectively, are particularly prevalent within the particle-attached fraction. Moreover, our results indicate that water mass age and the organic matter composition shaped the structure of the communities harboring <i>merA</i> and <i>merB</i> genes living in different particle size fractions, their abundance, and their expression levels. Members of the orders <i>Corynebacteriales</i>, <i>Rhodobacterales</i>, <i>Alteromonadales</i>, <i>Oceanospirillales</i>, <i>Moraxellales</i>, and <i>Flavobacteriales</i> were the main taxonomic players containing <i>merA</i> and <i>merB</i> genes in the deep ocean. These findings, together with our previous results of pure culture isolates of the deep bathypelagic ocean possessing the metabolic capacity to degrade MeHg, indicated that both methylmercury demethylation and Hg^II reduction likely occur in the global dark ocean, the largest biome in the biosphere.