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

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, Xiaofen Wu, Da Huo, Bo Ma, Yang Liu, Xin Zhang, Zixuan E, Jingxuan Liang, Hongyan Sun, Lihong Yuan, Xujia Liu, Chuhang Cheng, Hao Long, Jianlong Li, Yanhong Wang, Chaoqun Hu and Ting Chen ()
Additional contact information
Wenjie Pan: Chinese Academy of Sciences
Xuan Wang: Chinese Academy of Sciences
Chunhua Ren: Chinese Academy of Sciences
Xiao Jiang: 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
Jiasheng Huang: Chinese Academy of Sciences
Dingding Fan: Chinese Academy of Sciences
Peng Luo: Chinese Academy of Sciences
Yun Yang: Hainan University
Xinyue Ren: Guangdong Pharmaceutical University
Suzhong Yu: Chinese Academy of Sciences
Zhou Qin: Chinese Academy of Sciences
Xiaofen Wu: Chinese Academy of Sciences
Da Huo: Chinese Academy of Sciences
Bo Ma: Chinese Academy of Sciences
Yang Liu: Chinese Academy of Sciences
Xin Zhang: Chinese Academy of Sciences
Zixuan E: Chinese Academy of Sciences
Jingxuan Liang: 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

Nature Communications, 2024, vol. 15, issue 1, 1-14

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41467-024-53205-5

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