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Evolutionary adaptation of anaerobic and aerobic metabolism to high sulfide and hypoxic hydrothermal vent crab, Xenograpsus testudinatus

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Abstract

The vent crab, Xenograpsus testudinatus (xtcrab), is adapted to inhabit shallow-water, high sulfide and hypoxic hydrothermal vent. Our previous study revealed sulfide tolerance of vent xtcrabs which sulfide: quinone oxidoreductase (xtSQR) paralogs aid in sulfide detoxification. However, the mechanisms of how xtcrab adapts to high sulfide-hypoxic conditions in the vent area remain to be explored. In the present study, we tested the tolerance of xtcrab to sulfide-induced hypoxia, and investigated their aerobic and anaerobic responses in situ and in the laboratory. Comparisons were made to a non-vent, intertidal species, Thranita danae (tdcrab). We analyzed the several factors related to aerobic metabolism (SQR, cytochrome c [CYTC], complex IV [COXIV]), the product of anaerobic metabolism (hemolymph lactate levels) and glucose levels. Our results showed a higher survival tolerance to hypoxia of xtcrabs than tdcrabs. Hemolymph lactate levels increased more rapidly in xtcrabs than tdcrabs exposed to experimental hypoxia, revealing a rapid induction of anaerobic metabolism in hypoxic xtcrabs. Lactate measurement in xtcrabs returned from aquaria to original capture sites (vent habitats), further assessed the remarkable ability of xtcrabs to rapidly switch on and off their anaerobic metabolism. To assess aerobic metabolism, long-term exposure of xtcrabs to hydrothermal vent habitat increased gill xtCYTC transcripts and protein levels together with steadily enzymatic activity of COXIV. This revealed ability of xtcrabs to maintain functional capacity of aerobic respiration in hypoxia. Phylogenetic analysis showed that xtSQR paralogs in xtcrabs were more distant compared to tdSQR paralogs in tdcrabs. The increase of transcripts and enzymatic activity of gill xtSQR, and co-localization of xtSQR and xtCYTC also contribute to maintain aerobic metabolism by preventing sulfide toxicity on mitochondrial respiratory function. Overall, our study suggests that multiple strategies including detoxification of sulfide by gill xtSQR, and a quick/dynamic switch between aerobic and anaerobic metabolisms may play important roles in the metabolic adaptations of xtcrabs to extreme hydrothermal vent environment.

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Data availability

The original data are available from Chi Chen and Ching-Fong Chang upon requests.

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Acknowledgements

This work was supported by the Center of Excellence for the Oceans, NTOU from The Featured Areas Research Center Program within the framework of the Higher Education Sprout Project by the Ministry of Education (MOE), Taiwan, the Yushan Scholar Program (Sylvie Dufour), MOE, Taiwan (MOE-113-YSFAG-0012-001-P2), and the National Science and Technology Council (NSTC 112-2313-B-019-008; 113-2313-B-019-014). We thank to captain Dai-Shiu Lan, SCUBA diving coach Jen-Wei Lu, and Jen-sheng Lu for xtcrabs collection. We thank the staff of Yung-Che Tseng’s laboratory at Academia Sinica for xtcrabs collection. We thank Ying-Syuan Lyu of Ching-Fong Chang’s laboratory at NTOU for xtcrabs collection. We thank Emily Corrigan for the English correction. Thanks to Jie-Lin Guo of Ching-Fong Chang’s laboratory at NTOU for tdcrabs collection.

Funding

This work was supported by the Center of Excellence for the Oceans, NTOU from The Featured Areas Research Center Program within the framework of the Higher Education Sprout Project by the Ministry of Education (MOE), Taiwan, the Yushan Scholar Program (Sylvie Dufour), MOE, Taiwan (MOE-113-YSFAG-0012-001-P2), and the National Science and Technology Council (NSTC 112-2313-B-019-008; 113-2313-B-019-014).

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Authors and Affiliations

  1. Department of Aquaculture, National Taiwan Ocean University, Keelung, Taiwan

    Chi Chen, Guan-Chung Wu & Ching-Fong Chang

  2. Center of Excellence for the Oceans, National Taiwan Ocean University, Keelung, Taiwan

    Chi Chen, Guan-Chung Wu, Sylvie Dufour & Ching-Fong Chang

  3. Institute of Cellular and Organismic Biology, Academia Sinica, Taipei, Taiwan

    Yung-Che Tseng

  4. Biology of Aquatic Organisms and Ecosystems (BOREA), Muséum National d’Histoire Naturelle, Sorbonne Université, CNRS, IRD, Paris, France

    Sylvie Dufour

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  1. Chi Chen
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  5. Ching-Fong Chang
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Contributions

Chi Chen: conducted the sample collection, developed the methodologies in *xt* crab and *td* crab performed the experiments, data curation and analyses of data, and wrote the original draft. Guan-Chung Wu, Yung-Che Tseng and Ching-Fong Chang: developed the concept of the study, guided the experiments, and evaluated the data. Ching-Fong Chang: acquired funding, wrote, reviewed, and edited the paper. Sylvie Dufour: gave important input into conceptual and mechanistic insights, reviewed and edited the paper. All authors approved the paper.

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Chen, C., Wu, GC., Tseng, YC. et al. Evolutionary adaptation of anaerobic and aerobic metabolism to high sulfide and hypoxic hydrothermal vent crab, Xenograpsus testudinatus.
Sci Rep (2025). https://doi.org/10.1038/s41598-025-31968-1

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  • DOI: https://doi.org/10.1038/s41598-025-31968-1

Keywords

  • Aerobic respiration; anaerobic respiration
  • Hydrogen sulfide
  • Cellular energy
  • Extreme environment
  • Adaptation

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