Dataset Information

Synergistic Effects of a Chalkophore, Methanobactin, on Microbial Methylation of Mercury.

ABSTRACT: Microbial production of the neurotoxin methylmercury (MeHg) is a significant health and environmental concern, as it can bioaccumulate and biomagnify in the food web. A chalkophore or a copper-binding compound, termed methanobactin (MB), has been shown to form strong complexes with mercury [as Hg(II)] and also enables some methanotrophs to degrade MeHg. It is unknown, however, if Hg(II) binding with MB can also impede Hg(II) methylation by other microbes. Contrary to expectations, MB produced by the methanotroph Methylosinus trichosporium OB3b (OB3b-MB) enhanced the rate and efficiency of Hg(II) methylation more than that observed with thiol compounds (such as cysteine) by the mercury-methylating bacteria Desulfovibrio desulfuricans ND132 and Geobacter sulfurreducens PCA. Compared to no-MB controls, OB3b-MB decreased the rates of Hg(II) sorption and internalization, but increased methylation by 5- to 7-fold, suggesting that Hg(II) complexation with OB3b-MB facilitated exchange and internal transfer of Hg(II) to the HgcAB proteins required for methylation. Conversely, addition of excess amounts of OB3b-MB or a different form of MB from Methylocystis strain SB2 (SB2-MB) inhibited Hg(II) methylation, likely due to greater binding of Hg(II). Collectively, our results underscore the complex roles of microbial exogenous metal-scavenging compounds in controlling net production and bioaccumulation of MeHg in the environment.IMPORTANCE Some anaerobic microorganisms convert inorganic mercury (Hg) into the neurotoxin methylmercury, which can bioaccumulate and biomagnify in the food web. While the genetic basis of microbial mercury methylation is known, factors that control net methylmercury production in the environment are still poorly understood. Here, it is shown that mercury methylation can be substantially enhanced by one form of an exogenous copper-binding compound (methanobactin) produced by some methanotrophs, but not by another. This novel finding illustrates that complex interactions exist between microbes and that these interactions can potentially affect the net production of methylmercury in situ.

SUBMITTER: Yin X

PROVIDER: S-EPMC7237777 | biostudies-literature | 2020 May

REPOSITORIES: biostudies-literature

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Synergistic Effects of a Chalkophore, Methanobactin, on Microbial Methylation of Mercury.

Yin Xixiang X Wang Lihong L Zhang Lijie L Chen Hongmei H Liang Xujun X Lu Xia X DiSpirito Alan A AA Semrau Jeremy D JD Gu Baohua B

Applied and environmental microbiology 20200519 11

Microbial production of the neurotoxin methylmercury (MeHg) is a significant health and environmental concern, as it can bioaccumulate and biomagnify in the food web. A chalkophore or a copper-binding compound, termed methanobactin (MB), has been shown to form strong complexes with mercury [as Hg(II)] and also enables some methanotrophs to degrade MeHg. It is unknown, however, if Hg(II) binding with MB can also impede Hg(II) methylation by other microbes. Contrary to expectations, MB produced by ...[more]

PMID: 32220843

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Project description:Neurotoxic methylmercury (MeHg) is produced by anaerobic Bacteria and Archaea possessing the genes hgcAB, but it is unknown how organic substrate and electron acceptor availability impacts the distribution and abundance of these organisms. We evaluated the impact of organic substrate amendments on mercury (Hg) methylation rates, microbial community structure, and the distribution of hgcAB+ microbes with sediments. Sediment slurries were amended with short-chain fatty acids, alcohols, or a polysaccharide. Minimal increases in MeHg were observed following lactate, ethanol, and methanol amendments, while a significant decrease (∼70%) was observed with cellobiose incubations. Postincubation, microbial diversity was assessed via 16S rRNA amplicon sequencing. The presence of hgcAB+ organisms was assessed with a broad-range degenerate PCR primer set for both genes, while the presence of microbes in each of the three dominant clades of methylators (Deltaproteobacteria, Firmicutes, and methanogenic Archaea) was measured with clade-specific degenerate hgcA quantitative PCR (qPCR) primer sets. The predominant microorganisms in unamended sediments consisted of Proteobacteria, Firmicutes, Bacteroidetes, and Actinobacteria Clade-specific qPCR identified hgcA+Deltaproteobacteria and Archaea in all sites but failed to detect hgcA+Firmicutes Cellobiose shifted the communities in all samples to ∼90% non-hgcAB-containing Firmicutes (mainly Bacillus spp. and Clostridium spp.). These results suggest that either expression of hgcAB is downregulated or, more likely given the lack of 16S rRNA gene presence after cellobiose incubation, Hg-methylating organisms are largely outcompeted by cellobiose degraders or degradation products of cellobiose. These results represent a step toward understanding and exploring simple methodologies for controlling MeHg production in the environment.IMPORTANCE Methylmercury (MeHg) is a neurotoxin produced by microorganisms that bioacummulates in the food web and poses a serious health risk to humans. Currently, the impact that organic substrate or electron acceptor availability has on the mercury (Hg)-methylating microorganisms is unclear. To study this, we set up microcosm experiments exposed to different organic substrates and electron acceptors and assayed for Hg methylation rates, for microbial community structure, and for distribution of Hg methylators. The sediment and groundwater was collected from East Fork Poplar Creek in Oak Ridge, TN. Amendment with cellobiose (a lignocellulosic degradation by-product) led to a drastic decrease in the Hg methylation rate compared to that in an unamended control, with an associated shift in the microbial community to mostly nonmethylating Firmicutes This, along with previous Hg-methylating microorganism identification methods, will be important for identifying strategies to control MeHg production and inform future remediation strategies.

Project description:Periphytic 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.

Dataset Information

Synergistic Effects of a Chalkophore, Methanobactin, on Microbial Methylation of Mercury.

Publications

Synergistic Effects of a Chalkophore, Methanobactin, on Microbial Methylation of Mercury.

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