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

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 ecologic...

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Published inNature communications Vol. 15; no. 1; pp. 8825 - 14
Main Authors Pan, Wenjie, Wang, Xuan, Ren, Chunhua, Jiang, Xiao, Gong, Sanqiang, Xie, Zhenyu, Wong, Nai-Kei, Li, Xiaomin, Huang, Jiasheng, Fan, Dingding, Luo, Peng, Yang, Yun, Ren, Xinyue, Yu, Suzhong, Qin, Zhou, Wu, Xiaofen, Huo, Da, Ma, Bo, Liu, Yang, Zhang, Xin, E, Zixuan, Liang, Jingxuan, Sun, Hongyan, Yuan, Lihong, Liu, Xujia, Cheng, Chuhang, Long, Hao, Li, Jianlong, Wang, Yanhong, Hu, Chaoqun, Chen, Ting
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 12.10.2024
Nature Publishing Group
Nature Portfolio
Subjects
38/32
45/22
45/23
45/47
45/71
45/77
45/88
45/90
45/91
631/158/857
631/181/2474
631/601/1737
64
Animals
Bacteria
Bacteria - classification
Bacteria - genetics
Bacteria - isolation & purification
Biological Evolution
Carbohydrases
Coral reefs
Digestion
Digestive system
Ecological adaptation
Ecosystem
Ecosystems
Feeding
Feeding Behavior - physiology
Food
Gastrointestinal Microbiome - genetics
Gastrointestinal Microbiome - physiology
Gastrointestinal tract
Genes
Genomic analysis
Geologic Sediments - microbiology
Glycoside Hydrolases - genetics
Glycoside Hydrolases - metabolism
Holothuria - genetics
Holothuria - microbiology
Holothuria - physiology
Humanities and Social Sciences
Intestinal microflora
Intestine
Marine ecosystems
Microbiomes
Microbiota - genetics
Microbiota - physiology
multidisciplinary
Nutrients
Nutrition
Ocean bottom
Ocean floor
Phylogeny
Science
Science (multidisciplinary)
Sea Cucumbers - genetics
Sea Cucumbers - microbiology
Sediments
Symbiosis
Vegetables
Online AccessGet full text

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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. Sea cucumbers are predominant deposit feeders in benthic ecosystems. This study elucidates the mechanisms within the sea cucumber digestive system and their symbiotic microbiome which enable them to efficiently utilize nutrients from seabed sediments.
AbstractList 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.
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.Sea cucumbers are predominant deposit feeders in benthic ecosystems. This study elucidates the mechanisms within the sea cucumber digestive system and their symbiotic microbiome which enable them to efficiently utilize nutrients from seabed sediments.
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. Sea cucumbers are predominant deposit feeders in benthic ecosystems. This study elucidates the mechanisms within the sea cucumber digestive system and their symbiotic microbiome which enable them to efficiently utilize nutrients from seabed sediments.
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.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.
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.
ArticleNumber 8825
Author Jiang, Xiao
Gong, Sanqiang
Wong, Nai-Kei
Cheng, Chuhang
Ma, Bo
Huang, Jiasheng
Li, Xiaomin
Xie, Zhenyu
Pan, Wenjie
Ren, Xinyue
Sun, Hongyan
Li, Jianlong
Yuan, Lihong
Liu, Xujia
Fan, Dingding
Zhang, Xin
Luo, Peng
Hu, Chaoqun
Yu, Suzhong
Wang, Xuan
Liu, Yang
Huo, Da
Qin, Zhou
Wang, Yanhong
Wu, Xiaofen
Ren, Chunhua
E, Zixuan
Yang, Yun
Liang, Jingxuan
Long, Hao
Chen, Ting
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Snippet Sea cucumbers are predominant deposit feeders in benthic ecosystems, providing protective benefits to coral reefs by reducing disease prevalence. However, how...
Abstract Sea cucumbers are predominant deposit feeders in benthic ecosystems, providing protective benefits to coral reefs by reducing disease prevalence....
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Animals
Bacteria
Bacteria - classification
Bacteria - genetics
Bacteria - isolation & purification
Biological Evolution
Carbohydrases
Coral reefs
Digestion
Digestive system
Ecological adaptation
Ecosystem
Ecosystems
Feeding
Feeding Behavior - physiology
Food
Gastrointestinal Microbiome - genetics
Gastrointestinal Microbiome - physiology
Gastrointestinal tract
Genes
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Geologic Sediments - microbiology
Glycoside Hydrolases - genetics
Glycoside Hydrolases - metabolism
Holothuria - genetics
Holothuria - microbiology
Holothuria - physiology
Humanities and Social Sciences
Intestinal microflora
Intestine
Marine ecosystems
Microbiomes
Microbiota - genetics
Microbiota - physiology
multidisciplinary
Nutrients
Nutrition
Ocean bottom
Ocean floor
Phylogeny
Science
Science (multidisciplinary)
Sea Cucumbers - genetics
Sea Cucumbers - microbiology
Sediments
Symbiosis
Vegetables
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Title Sea cucumbers and their symbiotic microbiome have evolved to feed on seabed sediments
URI https://link.springer.com/article/10.1038/s41467-024-53205-5
https://www.ncbi.nlm.nih.gov/pubmed/39394205
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Volume 15
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