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

Abstract

Methylmercury (MeHg), a neurotoxic compound biomagnifying in aquatic food webs, can be a threat to human health via fish consumption. However, the composition and distribution of the microbial communities mediating the methylation of mercury (Hg) to MeHg in marine systems remain largely unknown. In order to fill this knowledge gap, we used the Baltic Sea Reference Metagenome (BARM) dataset to study the abundance and distribution of the genes involved in Hg methylation (the hgcAB gene cluster). We determined the relative abundance of the hgcAB genes and their taxonomic identity in 81 brackish metagenomes that cover spatial, seasonal and redox variability in the Baltic Sea water column. The hgcAB genes were predominantly detected in anoxic water, but some hgcAB genes were also detected in hypoxic and normoxic waters. Phylogenetic analysis identified putative Hg methylators within Deltaproteobacteria, in oxygen-deficient water layers, but also Spirochaetes-like and Kiritimatiellaeota-like bacteria. Higher relative quantities of hgcAB genes were found in metagenomes from marine particles compared to free-living communities in anoxic water, suggesting that such particles are hotspot habitats for Hg methylators in oxygen-depleted seawater. Altogether, our work unveils the diversity of the microorganisms with the potential to mediate MeHg production in the Baltic Sea and pinpoint the important ecological niches for these microorganisms within the marine water column.

Keywords: Baltic Sea; deltaproteobacteria; hgcAB; mercury methylation; spirochaetes-like bacteria.

FIGURE 1

Location of study sites in the Baltic Sea.

FIGURE 2

Alignment of conserved regions for amino acid sequences of the nine hgcAB-like gene clusters, (BARM-01 to 09) 13 hgcA-like genes (BARM-10 to 22), three hgcB-like genes (BARM-23 to 25) detected in the BARM dataset. The corresponding hgcAB amino acid sequences from Desulfovibrio desulfuricans ND132 and Geobacter sulfurreducens PCA were added in the alignment as references.

FIGURE 3

Maximum-likelihood phylogenetic tree of concatenated hgcAB amino acid sequences with collapsed clades. Collapsed clades are discriminated with colors based on their taxonomy. Gene clusters detected in the Baltic Sea water column (BARM) are displayed in bold. Bootstrap values obtained for nodes leading to BARM hgcAB amino acid sequences.

FIGURE 4

Relative abundance of hgcA- and hgcB-like genes in samples from the dataset “Redoxcline 2014” and “Transect 2014”. The dataset “LMO 2012” is not included because only few genes were detected and at low abundances (data shown in Supplementary Datasheet S4). The sampling date is displayed. Samples are ordered based on station locations from Bothnian Bay to Belt Seas (see Figure 1). The sampling depth (m) is color coded based on its respective gradient (darker shade of gray with increasing depth). The water redox zone is color coded based on the O₂ categories defined in the text (light blue for normoxic, beige for hypoxic and brown for anoxic conditions). The abbreviations “Filtr.” and “Pre-filtr.” indicate the pore size of the filters used to obtain each metagenome and if pre-filtration were done prior to filtration, respectively. The composition of microbial communities is described from the dominant bacterial and archaeal lineages in proportion of DNA sequences related to the total number of DNA sequences identified as bacteria and archaea in the metagenomes.