A deep-sea hydrothermal vent worm detoxifies arsenic and sulfur by intracellular biomineralization of orpiment (As2S3)
The alvinellid worm Paralvinella hessleri is the only animal that colonizes the hottest part of deep-sea hydrothermal vents in the west pacific. We found P. hessleri accumulates exceptionally high level of toxic element arsenic (>1% of wet weight) and tolerated elevated concentrations hydrogen sulphide. Using advanced microscopy, elementary analysis, and genomics and proteomics approaches, we identified a previously unrecognized arsenic-sulfide biomineralization process in P. hessleri. Our data suggest that arsenic accumulates within epithelial cell granules, where it likely reacts with sulphide diffused inward from the hydrothermal vent fluid, resulting in the intracellular formation of orpiment (As₂S₃) minerals. In this "fighting poison with poison" manner, the highly toxic arsenic and sulphide were simultaneously detoxified in the form of orpiment minerals within the intracellular granules of the single layer of epithelial cells. This process represents a remarkable adaptation to extreme chemical environments. Our study provides new insights into understanding animals' environment adaptation mechanisms and the diversity and plasticity of biomineralization.
Authors
- Chao Lian (ORCID: https://orcid.org/0000-0002-2583-9334)
- Xiaocheng Wang (ORCID: https://orcid.org/0000-0002-5268-1050)
- Minxiao Wang (ORCID: https://orcid.org/0000-0002-6567-3295)
- Chaolun Li (ORCID: https://orcid.org/0000-0003-1890-0587)
- Zhaoshan Zhong (ORCID: https://orcid.org/0000-0003-1643-5407)
- Hao Chen (ORCID: https://orcid.org/0000-0002-9032-8952)
- Huan Zhang (ORCID: https://orcid.org/0000-0001-9339-7999)
- Lei Cao (ORCID: https://orcid.org/0000-0003-4289-4025)
- Hao Wang (ORCID: https://orcid.org/0000-0002-9435-5501)
- Xin Zhang (ORCID: https://orcid.org/0000-0002-0501-3439)
- Li Zhou (ORCID: https://orcid.org/0000-0001-8688-1301)
Institutions
- Chinese Academy of Sciences (CN)
- Institute of Oceanology (CN)
- South China Sea Institute Of Oceanology (CN)
- Qingdao National Laboratory for Marine Science and Technology (CN)
- China National Environmental Monitoring Center (CN)
- University of Chinese Academy of Sciences (CN)
- National Marine Environmental Monitoring Center
Publication Details
- Journal
- PLoS Biology
- Published
- 2025-08-26
- DOI
- https://doi.org/10.1371/journal.pbio.3003291
- Citations
- 2
- Primary Topic
- Selenium in Biological Systems
- Type
- article
- Field-Weighted Citation Impact
- 2.24
Funders
- Innovative Research Group Project of the National Natural Science Foundation of China
- National Natural Science Foundation of China