Early genome erosion and internal phage-symbiont-host interaction in the endosymbionts of a cold-seep tubeworm
Summary: Endosymbiosis with chemosynthetic Gammaproteobacteria is widely recognized as an adaptive mechanism of siboglinid tubeworms, yet evolution of these endosymbionts and their driving forces remain elusive. Here, we report a finished endosymbiont genome (HMS1) of the cold-seep tubeworm Scleroli...
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| Format: | Article |
| Language: | English |
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Elsevier
2023-07-01
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| Series: | iScience |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2589004223011100 |
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| author | Zhao-Ming Gao Ting Xu Hua-Guan Chen Rui Lu Jun Tao Hong-Bin Wang Jian-Wen Qiu Yong Wang |
| author_facet | Zhao-Ming Gao Ting Xu Hua-Guan Chen Rui Lu Jun Tao Hong-Bin Wang Jian-Wen Qiu Yong Wang |
| author_sort | Zhao-Ming Gao |
| collection | DOAJ |
| description | Summary: Endosymbiosis with chemosynthetic Gammaproteobacteria is widely recognized as an adaptive mechanism of siboglinid tubeworms, yet evolution of these endosymbionts and their driving forces remain elusive. Here, we report a finished endosymbiont genome (HMS1) of the cold-seep tubeworm Sclerolinum annulatum. The HMS1 genome is small in size, with abundant prophages and transposable elements but lacking gene sets coding for denitrification, hydrogen oxidization, oxidative phosphorylation, vitamin biosynthesis, cell pH and/or sodium homeostasis, environmental sensing, and motility, indicative of early genome erosion and adaptive evolution toward obligate endosymbiosis. Unexpectedly, a prophage embedded in the HMS1 genome undergoes lytic cycle. Highly expressed ROS scavenger and LexA repressor genes indicate that the tubeworm host likely activates the lysogenic phage into lytic cycle through the SOS response to regulate endosymbiont population and harvest nutrients. Our findings indicate progressive evolution of Sclerolinum endosymbionts toward obligate endosymbiosis and expand the knowledge about phage-symbiont-host interaction in deep-sea tubeworms. |
| first_indexed | 2024-03-12T22:22:24Z |
| format | Article |
| id | doaj.art-136931f5ab5e47dd9b91bf17b26a7ffa |
| institution | Directory Open Access Journal |
| issn | 2589-0042 |
| language | English |
| last_indexed | 2024-03-12T22:22:24Z |
| publishDate | 2023-07-01 |
| publisher | Elsevier |
| record_format | Article |
| series | iScience |
| spelling | doaj.art-136931f5ab5e47dd9b91bf17b26a7ffa2023-07-23T04:55:15ZengElsevieriScience2589-00422023-07-01267107033Early genome erosion and internal phage-symbiont-host interaction in the endosymbionts of a cold-seep tubewormZhao-Ming Gao0Ting Xu1Hua-Guan Chen2Rui Lu3Jun Tao4Hong-Bin Wang5Jian-Wen Qiu6Yong Wang7Institute of Deep Sea Science and Engineering, Chinese Academy of Sciences, Sanya 572000, China; HKUST-CAS Sanya Joint Laboratory of Marine Science Research, Chinese Academy of Sciences, Sanya 572000, ChinaDepartment of Ocean Science, The Hong Kong University of Science and Technology, Hong Kong, China; Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou 511458, ChinaInstitute of Deep Sea Science and Engineering, Chinese Academy of Sciences, Sanya 572000, China; University of Chinese Academy of Sciences, Beijing 101408, ChinaInstitute of Deep Sea Science and Engineering, Chinese Academy of Sciences, Sanya 572000, China; University of Chinese Academy of Sciences, Beijing 101408, ChinaMLR Key Laboratory of Marine Mineral Resources, Guangzhou Marine Geological Survey, China Geological Survey, Guangzhou 511458, ChinaMLR Key Laboratory of Marine Mineral Resources, Guangzhou Marine Geological Survey, China Geological Survey, Guangzhou 511458, ChinaSouthern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou 511458, China; Department of Biology, Hong Kong Baptist University, Hong Kong, China; Corresponding authorInstitute of Deep Sea Science and Engineering, Chinese Academy of Sciences, Sanya 572000, China; HKUST-CAS Sanya Joint Laboratory of Marine Science Research, Chinese Academy of Sciences, Sanya 572000, China; Institute for Ocean Engineering, Shenzhen International Graduate School, Tsinghua University, Shenzhen 518000, China; Corresponding authorSummary: Endosymbiosis with chemosynthetic Gammaproteobacteria is widely recognized as an adaptive mechanism of siboglinid tubeworms, yet evolution of these endosymbionts and their driving forces remain elusive. Here, we report a finished endosymbiont genome (HMS1) of the cold-seep tubeworm Sclerolinum annulatum. The HMS1 genome is small in size, with abundant prophages and transposable elements but lacking gene sets coding for denitrification, hydrogen oxidization, oxidative phosphorylation, vitamin biosynthesis, cell pH and/or sodium homeostasis, environmental sensing, and motility, indicative of early genome erosion and adaptive evolution toward obligate endosymbiosis. Unexpectedly, a prophage embedded in the HMS1 genome undergoes lytic cycle. Highly expressed ROS scavenger and LexA repressor genes indicate that the tubeworm host likely activates the lysogenic phage into lytic cycle through the SOS response to regulate endosymbiont population and harvest nutrients. Our findings indicate progressive evolution of Sclerolinum endosymbionts toward obligate endosymbiosis and expand the knowledge about phage-symbiont-host interaction in deep-sea tubeworms.http://www.sciencedirect.com/science/article/pii/S2589004223011100ZoologyMolecular biologyEvolutionary biology |
| spellingShingle | Zhao-Ming Gao Ting Xu Hua-Guan Chen Rui Lu Jun Tao Hong-Bin Wang Jian-Wen Qiu Yong Wang Early genome erosion and internal phage-symbiont-host interaction in the endosymbionts of a cold-seep tubeworm iScience Zoology Molecular biology Evolutionary biology |
| title | Early genome erosion and internal phage-symbiont-host interaction in the endosymbionts of a cold-seep tubeworm |
| title_full | Early genome erosion and internal phage-symbiont-host interaction in the endosymbionts of a cold-seep tubeworm |
| title_fullStr | Early genome erosion and internal phage-symbiont-host interaction in the endosymbionts of a cold-seep tubeworm |
| title_full_unstemmed | Early genome erosion and internal phage-symbiont-host interaction in the endosymbionts of a cold-seep tubeworm |
| title_short | Early genome erosion and internal phage-symbiont-host interaction in the endosymbionts of a cold-seep tubeworm |
| title_sort | early genome erosion and internal phage symbiont host interaction in the endosymbionts of a cold seep tubeworm |
| topic | Zoology Molecular biology Evolutionary biology |
| url | http://www.sciencedirect.com/science/article/pii/S2589004223011100 |
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