Host–Symbiont Interactions in Deep-Sea Chemosymbiotic Vesicomyid Clams: Insights From Transcriptome Sequencing
In deep-sea hydrothermal vents and hydrocarbon seeps, chemoautotrophic bacteria use chemical substances as energy resources for primary production, ultimately supporting dense communities of megafauna, including charismatic giant vesicomyid clams. These clams inherit their endosymbionts from their p...
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doaj-ac708f191d1a4d2caed91a9e56b9d50f2020-11-25T02:42:46ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452019-11-01610.3389/fmars.2019.00680487107Host–Symbiont Interactions in Deep-Sea Chemosymbiotic Vesicomyid Clams: Insights From Transcriptome SequencingYi Lan0Jin Sun1Weipeng Zhang2Ting Xu3Yu Zhang4Chong Chen5Dong Feng6Hongbin Wang7Jun Tao8Jian-Wen Qiu9Pei-Yuan Qian10Department of Ocean Science, Division of Life Science and Hong Kong Branch of the Southern Marine Science and Engineering Guangdong Laboratory, The Hong Kong University of Science and Technology, Hong Kong, ChinaDepartment of Ocean Science, Division of Life Science and Hong Kong Branch of the Southern Marine Science and Engineering Guangdong Laboratory, The Hong Kong University of Science and Technology, Hong Kong, ChinaDepartment of Ocean Science, Division of Life Science and Hong Kong Branch of the Southern Marine Science and Engineering Guangdong Laboratory, The Hong Kong University of Science and Technology, Hong Kong, ChinaDepartment of Biology, Hong Kong Baptist University, Kowloon Tong, Hong KongCollege of Life Sciences and Oceanography, Shenzhen University, Shenzhen, ChinaX-STAR, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Yokosuka, JapanCAS Key Laboratory of Ocean and Marginal Sea Geology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, ChinaMLR Key Laboratory of Marine Mineral Resources, Guangzhou Marine Geological Survey, Guangzhou, ChinaMLR Key Laboratory of Marine Mineral Resources, Guangzhou Marine Geological Survey, Guangzhou, ChinaDepartment of Biology, Hong Kong Baptist University, Kowloon Tong, Hong KongDepartment of Ocean Science, Division of Life Science and Hong Kong Branch of the Southern Marine Science and Engineering Guangdong Laboratory, The Hong Kong University of Science and Technology, Hong Kong, ChinaIn deep-sea hydrothermal vents and hydrocarbon seeps, chemoautotrophic bacteria use chemical substances as energy resources for primary production, ultimately supporting dense communities of megafauna, including charismatic giant vesicomyid clams. These clams inherit their endosymbionts from their parents and house them intracellularly in their gills. How these organisms maintain their unique symbiotic relationship at the cellular level, however, remains largely unclear. In the present study, transcriptomes of different organs in Phreagena okutanii collected from a hydrothermal vent and in Archivesica marissinica collected from a methane seep were sequenced in order to decipher their host–symbiont relationships. Expressional analyses of the transcriptomes showed that the tricarboxylic acid (TCA) cycle-related genes, the Rab gene family, and the lysozyme genes were highly expressed in the gills. Furthermore, genes related to vesicle trafficking, lysosomes, and mitochondrial and energy metabolism were positively selected. The endosymbiont genes involved in sulfur oxidation, oxidative phosphorylation, and adenosine triphosphate (ATP) synthesis were highly expressed. The results suggest that the vesicomyid clams provide intermediates to fulfill the metabolic needs of their endosymbionts, and in return the endosymbionts actively generate nutrients for the hosts through being digested by the lysozymes of the host. Furthermore, the positive selection of genes related to vesicle trafficking, lysosomes, and mitochondrial and energy metabolism indicates molecular adaptations of the host in order to benefit from symbiosis. Overall, the present study provides the first set of transcriptomes for deep-sea chemosymbiotic vesicomyid clams, facilitating a better understanding of the host–symbiont relationship that has allowed them to become dominant animals in deep-sea hydrothermal vents and cold seeps.https://www.frontiersin.org/article/10.3389/fmars.2019.00680/fullchemosynthesissymbiosisgene expressionMolluscavertical transmission |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Yi Lan Jin Sun Weipeng Zhang Ting Xu Yu Zhang Chong Chen Dong Feng Hongbin Wang Jun Tao Jian-Wen Qiu Pei-Yuan Qian |
spellingShingle |
Yi Lan Jin Sun Weipeng Zhang Ting Xu Yu Zhang Chong Chen Dong Feng Hongbin Wang Jun Tao Jian-Wen Qiu Pei-Yuan Qian Host–Symbiont Interactions in Deep-Sea Chemosymbiotic Vesicomyid Clams: Insights From Transcriptome Sequencing Frontiers in Marine Science chemosynthesis symbiosis gene expression Mollusca vertical transmission |
author_facet |
Yi Lan Jin Sun Weipeng Zhang Ting Xu Yu Zhang Chong Chen Dong Feng Hongbin Wang Jun Tao Jian-Wen Qiu Pei-Yuan Qian |
author_sort |
Yi Lan |
title |
Host–Symbiont Interactions in Deep-Sea Chemosymbiotic Vesicomyid Clams: Insights From Transcriptome Sequencing |
title_short |
Host–Symbiont Interactions in Deep-Sea Chemosymbiotic Vesicomyid Clams: Insights From Transcriptome Sequencing |
title_full |
Host–Symbiont Interactions in Deep-Sea Chemosymbiotic Vesicomyid Clams: Insights From Transcriptome Sequencing |
title_fullStr |
Host–Symbiont Interactions in Deep-Sea Chemosymbiotic Vesicomyid Clams: Insights From Transcriptome Sequencing |
title_full_unstemmed |
Host–Symbiont Interactions in Deep-Sea Chemosymbiotic Vesicomyid Clams: Insights From Transcriptome Sequencing |
title_sort |
host–symbiont interactions in deep-sea chemosymbiotic vesicomyid clams: insights from transcriptome sequencing |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Marine Science |
issn |
2296-7745 |
publishDate |
2019-11-01 |
description |
In deep-sea hydrothermal vents and hydrocarbon seeps, chemoautotrophic bacteria use chemical substances as energy resources for primary production, ultimately supporting dense communities of megafauna, including charismatic giant vesicomyid clams. These clams inherit their endosymbionts from their parents and house them intracellularly in their gills. How these organisms maintain their unique symbiotic relationship at the cellular level, however, remains largely unclear. In the present study, transcriptomes of different organs in Phreagena okutanii collected from a hydrothermal vent and in Archivesica marissinica collected from a methane seep were sequenced in order to decipher their host–symbiont relationships. Expressional analyses of the transcriptomes showed that the tricarboxylic acid (TCA) cycle-related genes, the Rab gene family, and the lysozyme genes were highly expressed in the gills. Furthermore, genes related to vesicle trafficking, lysosomes, and mitochondrial and energy metabolism were positively selected. The endosymbiont genes involved in sulfur oxidation, oxidative phosphorylation, and adenosine triphosphate (ATP) synthesis were highly expressed. The results suggest that the vesicomyid clams provide intermediates to fulfill the metabolic needs of their endosymbionts, and in return the endosymbionts actively generate nutrients for the hosts through being digested by the lysozymes of the host. Furthermore, the positive selection of genes related to vesicle trafficking, lysosomes, and mitochondrial and energy metabolism indicates molecular adaptations of the host in order to benefit from symbiosis. Overall, the present study provides the first set of transcriptomes for deep-sea chemosymbiotic vesicomyid clams, facilitating a better understanding of the host–symbiont relationship that has allowed them to become dominant animals in deep-sea hydrothermal vents and cold seeps. |
topic |
chemosynthesis symbiosis gene expression Mollusca vertical transmission |
url |
https://www.frontiersin.org/article/10.3389/fmars.2019.00680/full |
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