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University of Chinese Academy of Sciences Hu Ligang/Yin Yongguang Cooperation Latest PNAS

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Methylmercury (MeHg) is a bioaccumulative neurotoxin mainly produced by anaerobic microorganisms, and methanogens are one of the most important methylating microorganisms. The key to understanding the mechanism of microbial mercury (Hg) methylation lies in the source of methyl groups. However, the origin of the methyl group during methanogen-mediated mercury methylation is unclear.

On October 9, 2024, Hu Ligang and Yin Yongguang of the University of Chinese Academy of Sciences jointly communicated inPNAS(IF = 9.4) published online entitled“The origin of methyl groups in methanogen-mediated mercury methylation： From the Wolfe cycle”of research papers.The study showed that mercury methylation of Hungate (Methanospirillum hungatei JF-1) is closely related to methanogenesis, which was verified by proteomic studies and substrate limitation experiments.

Next, through 13C labeling experiments, the authors demonstrated that almost all of the methyl groups of MeHg in this species originate from the Wolf cycle, rather than the acetyl-CoA pathway proposed in previous studies.Based on these results, the authors propose a mechanism of mercury methylation based on the Wolf cycle in this species. Further genomic analysis and 13C labeling experiments suggest that the involvement of the Wolff cycle in mercury methylation may be a ubiquitous property in mercury methylating methanogens.These findings reveal a unique mercury methylation mechanism in methanogens and extend the range of carbon substrates and controlling factors for MeHg synthesis in the environment. This helps to predict the production potential of MeHg and provides a reference for the remediation strategy of MeHg pollution.

 

Methylmercury (MeHg) is an environmental pollutant known for its neurotoxicity and bioaccumulation, posing risks to human health and ecosystems.The main source of MeHg is microbial methylation of inorganic mercury (Hg) in anaerobic environments, which is mainly driven by sulfate-reducing bacteria, iron-reducing bacteria, and methanogens. Understanding the mechanism of Hg methylation in mercury-methylating microorganisms can help to assess the production potential of MeHg and understand the environmental pathways of MeHg at the molecular level. Intracellular Hg methylation is an enzyme-catalyzed reaction in which methyltransferases promote the addition of methyl groups. Thus, in addition to Hg itself, the Hg methylation mechanism includes two key components: methyl groups and methyltransferases.
The hgcAB gene is essential for Hg methylation, encoding the methyltransferase of Hg methylation (HgcAB).However, the copy number of the hgcAB gene does not always correlate with MeHg production rate, suggesting that the methyltransfer process alone is not sufficient to fully explain MeHg formation. On the other hand, it is important to identify the metabolic pathway of the methyl group in this process. This not only affects the availability of methyl-containing substrates for HgcAB, but also helps to understand how MeHg is generated from carbon compounds and Hg.

Methanogens are the main MeHg-producing microorganisms in aquatic ecosystems, including lake epiphytes, wetlands and estuarine sediments.Methanogens have been shown to contribute to Hg methylation in almost all MeHg production hotspots, including paddy soils, lakes, peatlands, and permafrost. Clarifying the source of methyl groups in methanogen-mediated Hg methylation can enhance the authors' understanding of the source and production potential of MeHg in the environment, especially where methanogens are the predominant Hg-methylating microorganisms.

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However, the source of the methyl group of MeHg in methanogens remains unclear. Radioisotope labeling experiments and proteomic analysis revealed that Hg methylated methyl groups originated from the acetyl-CoA (acetyl-CoA) pathway of sulfate-reducing and iron-reducing bacteria.The methionine cycle and dimethylthiopropionic acid (DMSP) degradation pathways have been proposed as possible sources of methyl groups, but the role of these two pathways in Hg methylation requires more direct and specific evidence. Thus, the currently established mechanism for Hg methylation suggests that the methyl group is derived from methyltetrahydrofolate (CH3-THF) in the acetyl-CoA pathway, while HgcAB acts as a methyltransferase. However, this mechanism is mainly based on the study of sulfate reducing bacteria and iron reducing bacteria, and does not include the study of methanogens. In addition, there are other potential methyl carriers in methanogens, such as methyltetrahydromethane precursor (CH3-H4 MPT), which may serve as a methyl donor for Hg methylation. This suggests that the methyl groups of Hg methylation in methanogens may come from different metabolic pathways.

In order to determine the source of methyl groups of Hg methylation in methanogens, the authors investigated the source of methyl groups of MeHg in Helicobacter Hungate (Methanospirillum hungatei JF-1), known as Hg-methylating microorganisms and possessing the hgcAB gene pair.Subsequently, the authors explored whether the Hg methylation mechanism in this species could be extended to other Hg methylation methanogens. The authors performed a proteomic analysis to identify processes associated with Hg methylation JF-1 M.hungatei. The authors then studied the effect of carbon-containing substance concentration on MeHg production to identify the metabolic pathways responsible for MeHg synthesis. 13C labeling experiments were subsequently performed to elucidate the origin of the methyl groups.After proposing the Hg methylation mechanism JF-1 by M. hungatei, the authors performed genomic analysis and further 13C labeling experiments on hgcAB methanogens to determine the prevalence of this mechanism in Hg methylation methanogens.

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