Abstract

ABSTRACTPeriphytic biofilms have the potential to greatly influence the microbial production of the neurotoxicant monomethylmercury in freshwaters although few studies have simultaneously assessed periphyton mercury methylation and demethylation rates and the microbial communities associated with these transformations. We performed a field study on periphyton from a river affected by run-of-river power plants and artificial wetlands in a boreal landscape (Québec, Canada). In situ incubations were performed on three sites using environmental concentrations of isotopically enriched monomethylmercury (MM198Hg) and inorganic mercury (200Hg) for demethylation and methylation rate measurements. Periphytic microbial communities were investigated through 16S rRNA gene analyses and metagenomic screenings for the hgcA gene, involved in mercury methylation. Positive mercury methylation rates ([5.9 ± 3.4] × 10−3 day−1) were observed only in the wetlands, and demethylation rates averaged 1.78 ± 0.21 day−1 for the three studied sites. The 16S rRNA gene analyses revealed Proteobacteria as the most abundant phylum across all sites (36.3% ± 1.4%), from which families associated with mercury methylation were mostly found in the wetland site. Metagenome screening for HgcA identified 24 different hgcA sequences in the constructed wetland site only, associated with 8 known families, where the iron-reducing Geobacteraceae were the most abundant. This work brings new information on mercury methylation in periphyton from habitats of impacted rivers, associating it mostly with putative iron-reducing bacteria.IMPORTANCE Monomethylmercury (MMHg) is a biomagnifiable neurotoxin of global concern with risks to human health mostly associated with fish consumption. Hydroelectric reservoirs are known to be sources of MMHg many years after their impoundment. Little is known, however, on run-of-river dams flooding smaller terrestrial areas, although their numbers are expected to increase considerably worldwide in decades to come. Production of MMHg is associated mostly with anaerobic processes, but Hg methylation has been shown to occur in periphytic biofilms located in oxic zones of the water column. Therefore, in this study, we investigated in situ production of MMHg by periphytic communities in habitats impacted by the construction of a run-of-river dam by combining transformation rate measurements with genomic approaches targeting hgcAB genes, responsible for mercury methylation. These results provide extended knowledge on mercury methylators in river ecosystems impacted by run-of-river dams in temperate habitats.

Highlights

  • IMPORTANCE Monomethylmercury (MMHg) is a biomagnifiable neurotoxin of global concern with risks to human health mostly associated with fish consumption

  • Anoxic sediments have long been considered the primary location of MMHg production [4], but their central role in MMHg production has been recently challenged by studies on Hg transformations in littoral biofilms [5, 6], which consist of heterogeneous communities of photosynthetic and heterotrophic microorganisms attached to a submerged substrate [7]

  • Low oxygen and pH conditions in the wetland site are favorable for anaerobic MMHg production and affect microbial activity and Hg speciation [39]

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Summary

Introduction

IMPORTANCE Monomethylmercury (MMHg) is a biomagnifiable neurotoxin of global concern with risks to human health mostly associated with fish consumption. Production of MMHg is associated mostly with anaerobic processes, but Hg methylation has been shown to occur in periphytic biofilms located in oxic zones of the water column. In this study, we investigated in situ production of MMHg by periphytic communities in habitats impacted by the construction of a run-of-river dam by combining transformation rate measurements with genomic approaches targeting hgcAB genes, responsible for mercury methylation. These results provide extended knowledge on mercury methylators in river ecosystems impacted by run-of-river dams in temperate habitats. The combined activities of microbial methylation and demethylation contribute to the amount of MMHg available for biomagnification in aquatic food webs

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