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Sea cucumbers and their symbiotic microbiome have evolved to feed on seabed sediments

Author

Listed:
  • Wenjie Pan

    (Chinese Academy of Sciences
    Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Xuan Wang

    (Chinese Academy of Sciences
    Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Chunhua Ren

    (Chinese Academy of Sciences)

  • Xiao Jiang

    (Chinese Academy of Sciences
    Chinese Academy of Sciences)

  • Sanqiang Gong

    (Chinese Academy of Sciences)

  • Zhenyu Xie

    (Hainan University)

  • Nai-Kei Wong

    (Shantou University Medical College)

  • Xiaomin Li

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Jiasheng Huang

    (Chinese Academy of Sciences
    Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Dingding Fan

    (Chinese Academy of Sciences)

  • Peng Luo

    (Chinese Academy of Sciences
    Chinese Academy of Sciences)

  • Yun Yang

    (Hainan University
    South China Agricultural University)

  • Xinyue Ren

    (Guangdong Pharmaceutical University)

  • Suzhong Yu

    (Chinese Academy of Sciences
    Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Zhou Qin

    (Chinese Academy of Sciences
    Chinese Academy of Sciences
    University of Chinese Academy of Sciences
    South China Agricultural University)

  • Xiaofen Wu

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Da Huo

    (Chinese Academy of Sciences)

  • Bo Ma

    (Chinese Academy of Sciences
    Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Yang Liu

    (Chinese Academy of Sciences
    Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Xin Zhang

    (Chinese Academy of Sciences
    Chinese Academy of Sciences)

  • Zixuan E

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Jingxuan Liang

    (Chinese Academy of Sciences
    Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Hongyan Sun

    (South China Agricultural University)

  • Lihong Yuan

    (Guangdong Pharmaceutical University)

  • Xujia Liu

    (Guangxi Academy of Sciences)

  • Chuhang Cheng

    (Guangxi Academy of Sciences)

  • Hao Long

    (Hainan University)

  • Jianlong Li

    (Hainan University)

  • Yanhong Wang

    (Chinese Academy of Sciences)

  • Chaoqun Hu

    (Chinese Academy of Sciences)

  • Ting Chen

    (Chinese Academy of Sciences
    Chinese Academy of Sciences)

Abstract

Sea cucumbers are predominant deposit feeders in benthic ecosystems, providing protective benefits to coral reefs by reducing disease prevalence. However, how they receive sufficient nutrition from seabed sediments remains poorly understood. Here, we investigate Holothuria leucospilota, an ecologically significant tropical sea cucumber, to elucidate digestive mechanisms underlying marine deposit-feeding. Genomic analysis reveals intriguing evolutionary adaptation characterized by an expansion of digestive carbohydrase genes and a contraction of digestive protease genes, suggesting specialization in digesting microalgae. Developmentally, two pivotal dietary shifts, namely, from endogenous nutrition to planktonic feeding, and from planktonic feeding to deposit feeding, induce changes in digestive tract enzyme profiles, with adults mainly expressing carbohydrases and lipases. A nuanced symbiotic relationship exists between gut microbiota and the host, namely, specific resident bacteria supply crucial enzymes for food digestion, while other bacteria are digested and provide assimilable nutrients. Our study further identifies Holothuroidea lineage-specific lysozymes that are restrictedly expressed in the intestines to support bacterial digestion. Overall, this work advances our knowledge of the evolutionary innovations in the sea cucumber digestive system which enable them to efficiently utilize nutrients from seabed sediments and promote food recycling within marine ecosystems.

Suggested Citation

  • Wenjie Pan & Xuan Wang & Chunhua Ren & Xiao Jiang & Sanqiang Gong & Zhenyu Xie & Nai-Kei Wong & Xiaomin Li & Jiasheng Huang & Dingding Fan & Peng Luo & Yun Yang & Xinyue Ren & Suzhong Yu & Zhou Qin & , 2024. "Sea cucumbers and their symbiotic microbiome have evolved to feed on seabed sediments," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-53205-5
    DOI: 10.1038/s41467-024-53205-5
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