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Phylogenetic and ecophysiological novelty of subsurface mercury methylators in mangrove sediments

The ISME Journal volume 17, pages 2313–2325 (2023)Cite this article

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Abstract

Mangrove sediment is a crucial component in the global mercury (Hg) cycling and acts as a hotspot for methylmercury (MeHg) production. Early evidence has documented the ubiquity of well-studied Hg methylators in mangrove superficial sediments; however, their diversity and metabolic adaptation in the more anoxic and highly reduced subsurface sediments are lacking. Through MeHg biogeochemical assay and metagenomic sequencing, we found that mangrove subsurface sediments (20–100 cm) showed a less hgcA gene abundance but higher diversity of Hg methylators than superficial sediments (0–20 cm). Regional-scale investigation of mangrove subsurface sediments spanning over 1500 km demonstrated a prevalence and family-level novelty of Hg-methylating microbial lineages (i.e., those affiliated to Anaerolineae, Phycisphaerae, and Desulfobacterales). We proposed the candidate phylum Zixibacteria lineage with sulfate-reducing capacity as a currently understudied Hg methylator across anoxic environments. Unlike other Hg methylators, the Zixibacteria lineage does not use the Wood–Ljungdahl pathway but has unique capabilities of performing methionine synthesis to donate methyl groups. The absence of cobalamin biosynthesis pathway suggests that this Hg-methylating lineage may depend on its syntrophic partners (i.e., Syntrophobacterales members) for energy in subsurface sediments. Our results expand the diversity of subsurface Hg methylators and uncover their unique ecophysiological adaptations in mangrove sediments.

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Fig. 1: The Hg profiles in mangrove sediments.
Fig. 2: The diversity and prevalence of Hg methylators in mangrove subsurface sediments.
Fig. 3: Maximum-likelihood phylogenetic tree of HgcA protein sequences.
Fig. 4: Exploration of HgcAB proteins in candidate phylum Zixibacteria.
Fig. 5: Phylogeny and environmental sources of candidate phylum Zixibacteria.
Fig. 6: Detailed mechanism of Hg methylation in candidate phylum Zixibacteria.

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Data availability

All data needed to evaluate the conclusions in the paper are present in the paper and/or the Supplementary File 1 and 2. The raw reads of metagenomes and 16 S rRNA amplicon sequencing were submitted to the National Center for Biotechnology Information Short Reads Archive (NCBI SRA) database under the project PRJNA798446, PRJNA894374, PRJNA958041, and the National Omics Data Encyclopedia (NODE) under the project OEX012906. All Zixibacteria genomes from this study or NCBI SRA database were shared in Zenodo (10.5281/zenodo.7998010).

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Acknowledgements

This study was supported by the National Natural Science Foundation of China (32000070, 52070196, 32370113), the Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai) (SML2020SP0004), the Innovation Group Project of Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai) (311022011), the Guangdong Natural Resources Department Contract (GDNRC[2021]62), the Guangdong Basic and Applied Basic Research Foundation (2019A1515011406), and Guangzhou Science and Technology Plan Projects (202002030454).

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  1. Environmental Microbiomics Research Center, School of Environmental Science and Engineering, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Sun Yat-sen University, Guangzhou, 510006, China

    Songfeng Liu, Ruiwen Hu, Nenglong Peng, Zhengyuan Zhou, Ruihan Chen, Zhili He & Cheng Wang

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  1. Songfeng Liu
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  7. Cheng Wang
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Contributions

CW conceived and designed the study. SFL, NLP, RWH, ZYZ, and RHC performed the laboratory work and detailed the sampling. SFL and NLP carried out the bioinformatics and statistical analysis. SFL and CW wrote the first draft of the manuscript. SFL, CW, and ZLH discussed results and edited. All authors read and approved the final version of the manuscript.

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Correspondence to Cheng Wang.

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Liu, S., Hu, R., Peng, N. et al. Phylogenetic and ecophysiological novelty of subsurface mercury methylators in mangrove sediments. ISME J 17, 2313–2325 (2023). https://doi.org/10.1038/s41396-023-01544-4

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