Nitrospina-Like Bacteria Are Potential Mercury Methylators in the Mesopelagic Zone in the East China Sea

Abstract

In natural environments, the production of neurotoxic and bioaccumulative methylmercury (MeHg) is mediated by microorganisms carrying the genes hgcA and hgcB . However, the contribution of these microorganisms to mercury (Hg) methylation or MeHg accumulation in the ocean is poorly understood. Here we determined the total Hg (THg) and MeHg concentrations in seawater samples and conducted a metagenomic survey of the hgcAB genes and functional modules involved in metabolic pathways in the East China Sea (ECS). In the metagenomic analyses, we used paired-end reads and assembled contigs for hgcAB enumeration and phylogenetic analyses in the seawater column. To evaluate the relative abundance of hgcAB in the metagenomic data, we estimated the abundance of recA (single-copy gene of bacteria) as well and then compared them. Moreover, the profiles of prokaryotic community composition were analyzed by 16S rRNA gene (V4 region) deep-sequencing. In the mesopelagic layers, the hgcA sequences were detected, and there was a positive correlation between hgcA abundance relative to the recA and MeHg concentrations. Thus, the quantification of the hgcA sequences could provide valuable information to evaluate the potential environments of microbial MeHg accumulation in the seawater column. A phylogenetic analysis using the assembled contigs revealed that all of the hgcA sequences in the mesopelagic layers were affiliated with Nitrospina -like sequences. The 16S rRNA gene analysis revealed that Nitrospinae were abundant in the mesopelagic layers. Although the lineages of Deltaproteobacteria, Firmicutes, and Spirochaetes were detected in the seawater column, their hgcAB sequences were not detected in our metagenomes, despite the fact that they are closely related to previously identified Hg methylators. The metabolic pathway analysis revealed that the modules related to sulfur and methane metabolism were prominent in the mesopelagic layers. However, no hgcA sequences affiliated with sulfate-reducing bacteria (SRB) or methanogens were detected in these layers, suggesting that these bacteria could not be strongly involved in the Hg accumulation in the seawater column. Our results indicate that Nitrospina -like bacteria with hgcAB genes could play a critical role in microbial Hg accumulation in the oxygenated mesopelagic layers of the ECS.

Deltaproteobacteria and Spirochaetes-Like Bacteria Are Abundant Putative Mercury Methylators in Oxygen-Deficient Water and Marine Particles in the Baltic Sea

“…Our results thus suggest that Hg methylation is not linked to iron-reduction in the Baltic Sea. Recent studies also identified hgcAB -carrying Nitrospirea/Nitrospinae from several environments including marine systems ( Gionfriddo et al, 2016 ; Tada et al, 2020 ; Villar et al, 2020 ). Despite members of this genus having been detected in open ocean and seas, we did not find any hgcAB -like genes related to Nitrospina sp.…”

“… Podar et al (2015) only detected hgcAB genes in a few metagenomes from marine pelagic waters (seven out of 138 metagenomes) but highlighted that limited sequencing depths of these metagenomes could have hampered detection. While a more recent study did not detect hgcA genes in waters from the Arctic and equatorial Pacific Oceans ( Bowman et al, 2019 ), the presence of hgcAB -like genes was reported in normoxic water from the open ocean in several ocean basins ( Villar et al, 2020 ), the mesopelagic zone of the East China Sea ( Tada et al, 2020 ) and Antarctica sea ice ( Gionfriddo et al, 2016 ), with a fraction of those genes being associated to a microaerophilic nitrite oxidizing bacteria. Further, Blum et al (2013) demonstrated that between 20 and 40 % of MeHg measured in surface mixed layer of the North Pacific Ocean originated from internal production in the surface water.…”

“…Recent advances in metagenomics have yielded new insights into the microbial taxonomic and functional diversity in various aquatic ecosystems (e.g., Mehrshad et al, 2016 ; Haro-Moreno et al, 2018 ; Nowinski et al, 2019 ). The approach has for example been applied to broadly assess the presence and diversity of genes central to biological Hg cycling in marine systems ( Podar et al, 2015 ; Gionfriddo et al, 2016 , 2020 ; Bowman et al, 2019 ; Lin et al, 2020 ; Tada et al, 2020 ; Villar et al, 2020 ). Podar et al (2015) only detected hgcAB genes in a few metagenomes from marine pelagic waters (seven out of 138 metagenomes) but highlighted that limited sequencing depths of these metagenomes could have hampered detection.…”

Mercury methylation by metabolically versatile and cosmopolitan marine bacteria

“…These microorganisms are ubiquitous in soils, sediments, seawater, freshwater, and extreme environments, as well as the digestive tracts of some animals [ 9 ]. A few other hgc carriers, not only from anaerobic but also microaerobic habitats, were discovered using culture-independent approaches, including Chloroflexi, Chrysiogenetes, Spirochaetes [ 9 ] , Nitrospina [ 11 , 12 ], and Verrucomicrobia [ 13 ]. Two more recent studies have expanded the Hg-methylating community [ 14 , 15 ] and revealed the role played by Hg methylators in the context of global biogeochemical cycling.…”

Nitrospina -like Bacteria Are Dominant Potential Mercury Methylators in Both the Oyashio and Kuroshio Regions of the Western North Pacific

“…Thus, the vertical and horizontal distribution of Hg and MeHg in marine environments is critical for understanding MeHg accumulation in marine organisms. Ocean-scale surveys of Hg distribution have highlighted the abundance of MeHg in the mesopelagic layers ( 2 – 5 ). In addition, incubation studies have shown the possibility of MeHg production in seawater columns ( 6 , 7 ).…”