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.2025 Aug 26;23(8):e3003291.
doi: 10.1371/journal.pbio.3003291. eCollection 2025 Aug.

A deep-sea hydrothermal vent worm detoxifies arsenic and sulfur by intracellular biomineralization of orpiment (As2S3)

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A deep-sea hydrothermal vent worm detoxifies arsenic and sulfur by intracellular biomineralization of orpiment (As2S3)

Hao Wang et al. PLoS Biol..

Abstract

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.

Copyright: © 2025 Wang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Images of the alvinellid worm,Paralvinella hessleri.
A: AP. hessleri colonized hydrothermal vent in Iheya north hydrothermal field. The vent fauna showed apparent variation along the environmental gradients. The areas close to hydrothermal venting were covered with white mucus matt (P. hessleri colonies). The squad lobstersShinkaia crosnieri occupied the areas surrounding theP. hessleri colonies (indicated by black arrowheads).Bathymodiolinae mussels stayed further away (indicated by white arrowhead);A’: Close-up image ofP. hessleri worms close to the hydrothermal venting.B: AP. hessleri specimen with buccal tentacles extroverted, lateral view. Note that the animal has a bright yellow color;C: A close-up image of the notopod;D: A close-up image of the stem of branchial apparatus. Both panelsC and D demonstrate that there are yellow granules in the epidermis ofP. hessleri.
Fig 2
Fig 2. Arsenic speciation and distribution between soluble and insoluble forms inP. hessleri.
A: Percentage of each arsenic species present inP. hessleri.B: soluble and insoluble arsenic inP. hessleri (n = 3). The data underlying Fig 2B can be found in S1 Data.
Fig 3
Fig 3. Microscopy analysis of the yellow granules.
A: A longitudinally sectioned paraffin-embeddedP. hessleri specimen, demonstrating the internal structure of theP. hessleri worm.B: Size distribution of the yellow granules in the major tissues ofP. hessleri.C: Number of yellow granules per cell in the major tissues ofP. hessleri.D: Cross section of branchial apparatus tip.E: Longitudinal section ofP. hessleri branchial apparatus stem.F: Longitudinal section ofP. hessleri body wall.G: Longitudinal section ofP. hessleri buccal tentacles.H: Cross section ofP. hessleri digestive tract. ASW: ambient seawater. ci: cilia. cu: cuticle. The data underlying Fig 3B and 3C can be found in S1 Data.
Fig 4
Fig 4. SEM and TEM analysis of the yellow granules.
A: A SEM image ofP. hessleri branchial apparatus;A’: A magnified region showing the electron-dense intracellular yellow granule.B: A SEM image ofP. hessleri body wall;B’: A magnified region showing the electron-dense intracellular yellow granules.C: A SEM image of the digestive tract yellow granules.D: A TEM image ofP. hessleri branchial apparatus.E: A close-up image of a typical branchial apparatus yellow granule.F: A TEM image ofP. hessleri body wall;F’: A magnified region showing yellow granules and a secretion cell.G: A TEM image of buccal tentacles yellow granules;H: A TEM image of digestive tract yellow granules. ci: cilia; cu: cuticle, mt: mitochondria; gry: yellow granule, nu: cell nuclei.
Fig 5
Fig 5. STEM-EDS mapping and micro-Raman spectrometry analysis of the yellow granules.
A: Bright-field STEM image of yellow granules in the fine tip of branchial apparatus;A’: A close up image of the STEM-EDS mapping scanning area;B–E: EDS mapping of Oxygen, Sulphur, Osmium, and Arsenic elements of the yellow granules;F: Merged image of Oxygen and Osmium EDS mapping;G: Merged image of Sulphur and Arsenic EDS-mapping;H: Optical image of branchial apparatus yellow granules for micro-Raman analysis;I: Raman spectra of yellow granules; Redcross inH micro-Raman spectrometry sampling point; Inset inI: Raman spectra from pure As2S3. The data underlying Fig 5I can be found in S2 Data.
Fig 6
Fig 6. TEM analysis of the NaOH-treatedP. hessleri tissues.
A: TEM image of NaOH-treated branchial apparatus;A’: A close-up image of yellow granules’ membrane structures and intra-membrane vacuoles;B: TEM image of two body wall yellow granules;B’: A close-up image showing the two sets of membranes, and numerous vesicles between the membranes;C: ci: cilia, cu: cuticle; gry: yellow granule; mt: mitochondria; nu: nuclei; black arrowhead: yellow granule; white arrowhead: mitochondria; double line arrowhead: lipid bilayer; white arrow: protrusions on the gut yellow granule.
Fig 7
Fig 7. Analysis of the key genes involved inParalvinella hessleri orpiment biomineralization.
A: Proteins identified in threeP. hessleri yellow granules samples.B: Gene ontology cellular component classification (GO CC) ofP. hessleri yellow granule proteome.C: Subcellular locations analysis ofP. hessleri yellow granule proteome.D: Top 5 most abundantly expressed membrane proteins in theP. hessleri yellow granule proteome.E: Immuno-histochemistry analysis of the 001332F.4 Multidrug resistance-associated protein.F: Sequence alignment analysis of twoP. hessleri intracellular hemoglobins.G: Fluorescent in situ hybridization analysis of gene encodingP. hessleri Intracellular hemoglobin 1 (iHem-1, 000092F.85) in the branchial apparatus.H: Fluorescent in situ hybridization analysis of gene encodingP. hessleri Intracellular hemoglobin 2 (iHem-2, 000481F.41) in theH’ branchial apparatus andH” body wall of theP. hessleri.
Fig 8
Fig 8. The “Fighting poison with poison” arsenic detoxification inParalvinella hessleri.
Fig 9
Fig 9. δ34S% analysis of the four typical animals collected from hydrothermal vent chimneys.
The animals were aligned based on the habitat distance (habitat zones) from the hydrothermal venting. TheParalvinella hessleri which lives close to the hydrothermal venting is on the bottom while theBathymodiolus platifrons which lives further away is at the top. The seawater and hydrothermal venting H2S δ34S% are based on Seal [81] and Gamo [42].
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