Geobacteraceae are important members of mercury-methylating microbial communities of sediments impacted by waste water releases

Abstract

Microbial mercury (Hg) methylation in sediments can result in bioaccumulation of the neurotoxin methylmercury (MMHg) in aquatic food webs. Recently, the discovery of the gene hgcA, required for Hg methylation, revealed that the diversity of Hg methylators is much broader than previously thought. However, little is known about the identity of Hg-methylating microbial organisms and the environmental factors controlling their activity and distribution in lakes. Here, we combined high-throughput sequencing of 16S rRNA and hgcA genes with the chemical characterization of sediments impacted by a waste water treatment plant that releases significant amounts of organic matter and iron. Our results highlight that the ferruginous geochemical conditions prevailing at 1–2 cm depth are conducive to MMHg formation and that the Hg-methylating guild is composed of iron and sulfur-transforming bacteria, syntrophs, and methanogens. Deltaproteobacteria, notably Geobacteraceae, dominated the hgcA carrying communities, while sulfate reducers constituted only a minor component, despite being considered the main Hg methylators in many anoxic aquatic environments. Because iron is widely applied in waste water treatment, the importance of Geobacteraceae for Hg methylation and the complexity of Hg-methylating communities reported here are likely to occur worldwide in sediments impacted by waste water treatment plant discharges and in iron-rich sediments in general.

Metabolic potential of microbial communities from ferruginous sediments

“…Altogether, our data suggest that microbial communities in anoxic ferruginous sediments exhibit vertical succession of the putative phenotypes FeRB, SRB, methanogens and methanotrophs (Fig. 5B), forming a microbial community different from those reported from lacustrine environments with ferruginous conditions in the pore water (Norði et al, 2013;Bravo et al, 2018). Although, the metabolic potential to reduce and disproportionate sulfur compounds was present, the absence of monosulfides and rapid increase of disulfides in the sediment suggested that cryptic sulfur cycling is minor, or even absent, compared to methanogenesis.…”

Expanded Phylogenetic Diversity and Metabolic Flexibility of Microbial Mercury Methylation

“…This 86 discovery has allowed for high-throughput identification of microorganisms with the 87 potential to methylate mercury in diverse environmental datasets based upon hgcAB 88 sequence presence (12, 13). 89Currently, the known diversity of mercury methylating microorganisms has been 90 described based on cultured isolates, amplicon sequencing of the 16S rRNA and/or hgcA 91 loci of mercury impacted sites, hgcA quantitative PCR (qPCR) primers targeting specific 92 5 groups, or identification of hgcA on assembled metagenomic contigs (11,(13)(14)(15)(16)(17)(18)(19)(20). 93 However, the complete phylogenetic and metabolic diversity of microorganisms capable 94 of methylating mercury is not fully understood due to previous efforts focusing on a few 95 cultured representatives, and poor predictive power of methylation potential based on 96 16S rRNA phylogenetic signal (8, 10, 21).…”

Periphyton and Flocculent Materials Are Important Ecological Compartments Supporting Abundant and Diverse Mercury Methylator Assemblages in the Florida Everglades

“…Although the Hg could be methylated abiotically in the presence of suitable methyl donors (6), microorganisms are the prime agents responsible for Hg methylation (7)(8)(9). Recent studies using hgcAB (essential genes for Hg methylation) (10) as a biomarker have indicated that the potential for Hg methylation is spread much more broadly across more diverse microbial taxa than previously thought and includes the Deltaproteobacteria, Chloroflexi, Firmicutes, and Euryarchaeota (11)(12)(13)(14)(15). The produced MeHg may flow through food webs and accumulate in top predators through biomagnification (16)(17)(18)(19).…”

“…The difference of Hg methylator assemblages between compartments within each site was also indicated by their diversity within a compartment (referred to as alpha diversity) and between compartments (referred to as beta diversity). The Chao1 richness estimator (an alpha diversity index) indicated that soil harbored the highest diversity of hgcAB OTUs (158 to 162), followed by floc (57 to 103), and periphyton (12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26) (Table S3). This tendency was in good agreement with the Shannon diversity indices, with 3.9 to 4.0 in soil, 3.0 to 3.1 in floc, and 2.1 to 2.8 in periphyton.…”