Hologenome analysis reveals independent evolution to chemosymbiosis by deep-sea bivalves
Abstract Background Bivalves have independently evolved a variety of symbiotic relationships with chemosynthetic bacteria. These relationships range from endo- to extracellular interactions, making them ideal for studies on symbiosis-related evolution. It is still unclear whether there are universal...
| Main Authors: | , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2023-03-01
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| Series: | BMC Biology |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12915-023-01551-z |
| _version_ | 1797863546665566208 |
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| author | Yang Guo Lingfeng Meng Minxiao Wang Zhaoshan Zhong Denghui Li Yaolei Zhang Hanbo Li Huan Zhang Inge Seim Yuli Li Aijun Jiang Qianyue Ji Xiaoshan Su Jianwei Chen Guangyi Fan Chaolun Li Shanshan Liu |
| author_facet | Yang Guo Lingfeng Meng Minxiao Wang Zhaoshan Zhong Denghui Li Yaolei Zhang Hanbo Li Huan Zhang Inge Seim Yuli Li Aijun Jiang Qianyue Ji Xiaoshan Su Jianwei Chen Guangyi Fan Chaolun Li Shanshan Liu |
| author_sort | Yang Guo |
| collection | DOAJ |
| description | Abstract Background Bivalves have independently evolved a variety of symbiotic relationships with chemosynthetic bacteria. These relationships range from endo- to extracellular interactions, making them ideal for studies on symbiosis-related evolution. It is still unclear whether there are universal patterns to symbiosis across bivalves. Here, we investigate the hologenome of an extracellular symbiotic thyasirid clam that represents the early stages of symbiosis evolution. Results We present a hologenome of Conchocele bisecta (Bivalvia: Thyasiridae) collected from deep-sea hydrothermal vents with extracellular symbionts, along with related ultrastructural evidence and expression data. Based on ultrastructural and sequencing evidence, only one dominant Thioglobaceae bacteria was densely aggregated in the large bacterial chambers of C. bisecta, and the bacterial genome shows nutritional complementarity and immune interactions with the host. Overall, gene family expansions may contribute to the symbiosis-related phenotypic variations in different bivalves. For instance, convergent expansions of gaseous substrate transport families in the endosymbiotic bivalves are absent in C. bisecta. Compared to endosymbiotic relatives, the thyasirid genome exhibits large-scale expansion in phagocytosis, which may facilitate symbiont digestion and account for extracellular symbiotic phenotypes. We also reveal that distinct immune system evolution, including expansion in lipopolysaccharide scavenging and contraction of IAP (inhibitor of apoptosis protein), may contribute to the different manners of bacterial virulence resistance in C. bisecta. Conclusions Thus, bivalves employ different pathways to adapt to the long-term co-existence with their bacterial symbionts, further highlighting the contribution of stochastic evolution to the independent gain of a symbiotic lifestyle in the lineage. |
| first_indexed | 2024-04-09T22:37:14Z |
| format | Article |
| id | doaj.art-842fd21218b84985b4f6a90591945d22 |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-04-09T22:37:14Z |
| publishDate | 2023-03-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-842fd21218b84985b4f6a90591945d222023-03-22T12:23:12ZengBMCBMC Biology1741-70072023-03-0121112010.1186/s12915-023-01551-zHologenome analysis reveals independent evolution to chemosymbiosis by deep-sea bivalvesYang Guo0Lingfeng Meng1Minxiao Wang2Zhaoshan Zhong3Denghui Li4Yaolei Zhang5Hanbo Li6Huan Zhang7Inge Seim8Yuli Li9Aijun Jiang10Qianyue Ji11Xiaoshan Su12Jianwei Chen13Guangyi Fan14Chaolun Li15Shanshan Liu16Center of Deep-Sea Research, Institute of Oceanology, Chinese Academy of SciencesBGI-Qingdao, BGI-ShenzhenCenter of Deep-Sea Research, Institute of Oceanology, Chinese Academy of SciencesCenter of Deep-Sea Research, Institute of Oceanology, Chinese Academy of SciencesBGI-Qingdao, BGI-ShenzhenBGI-Qingdao, BGI-ShenzhenBGI-Qingdao, BGI-ShenzhenCenter of Deep-Sea Research, Institute of Oceanology, Chinese Academy of SciencesIntegrative Biology Laboratory, College of Life Sciences, Nanjing Normal UniversityCollege of Marine Life Sciences, Ocean University of ChinaBGI-Qingdao, BGI-ShenzhenBGI-Qingdao, BGI-ShenzhenBGI-Qingdao, BGI-ShenzhenBGI-Qingdao, BGI-ShenzhenBGI-Qingdao, BGI-ShenzhenCenter of Deep-Sea Research, Institute of Oceanology, Chinese Academy of SciencesBGI-Qingdao, BGI-ShenzhenAbstract Background Bivalves have independently evolved a variety of symbiotic relationships with chemosynthetic bacteria. These relationships range from endo- to extracellular interactions, making them ideal for studies on symbiosis-related evolution. It is still unclear whether there are universal patterns to symbiosis across bivalves. Here, we investigate the hologenome of an extracellular symbiotic thyasirid clam that represents the early stages of symbiosis evolution. Results We present a hologenome of Conchocele bisecta (Bivalvia: Thyasiridae) collected from deep-sea hydrothermal vents with extracellular symbionts, along with related ultrastructural evidence and expression data. Based on ultrastructural and sequencing evidence, only one dominant Thioglobaceae bacteria was densely aggregated in the large bacterial chambers of C. bisecta, and the bacterial genome shows nutritional complementarity and immune interactions with the host. Overall, gene family expansions may contribute to the symbiosis-related phenotypic variations in different bivalves. For instance, convergent expansions of gaseous substrate transport families in the endosymbiotic bivalves are absent in C. bisecta. Compared to endosymbiotic relatives, the thyasirid genome exhibits large-scale expansion in phagocytosis, which may facilitate symbiont digestion and account for extracellular symbiotic phenotypes. We also reveal that distinct immune system evolution, including expansion in lipopolysaccharide scavenging and contraction of IAP (inhibitor of apoptosis protein), may contribute to the different manners of bacterial virulence resistance in C. bisecta. Conclusions Thus, bivalves employ different pathways to adapt to the long-term co-existence with their bacterial symbionts, further highlighting the contribution of stochastic evolution to the independent gain of a symbiotic lifestyle in the lineage.https://doi.org/10.1186/s12915-023-01551-zSymbiosisHydrothermal ventBivalviaConchocele bisectaGenomeStochastic evolution |
| spellingShingle | Yang Guo Lingfeng Meng Minxiao Wang Zhaoshan Zhong Denghui Li Yaolei Zhang Hanbo Li Huan Zhang Inge Seim Yuli Li Aijun Jiang Qianyue Ji Xiaoshan Su Jianwei Chen Guangyi Fan Chaolun Li Shanshan Liu Hologenome analysis reveals independent evolution to chemosymbiosis by deep-sea bivalves BMC Biology Symbiosis Hydrothermal vent Bivalvia Conchocele bisecta Genome Stochastic evolution |
| title | Hologenome analysis reveals independent evolution to chemosymbiosis by deep-sea bivalves |
| title_full | Hologenome analysis reveals independent evolution to chemosymbiosis by deep-sea bivalves |
| title_fullStr | Hologenome analysis reveals independent evolution to chemosymbiosis by deep-sea bivalves |
| title_full_unstemmed | Hologenome analysis reveals independent evolution to chemosymbiosis by deep-sea bivalves |
| title_short | Hologenome analysis reveals independent evolution to chemosymbiosis by deep-sea bivalves |
| title_sort | hologenome analysis reveals independent evolution to chemosymbiosis by deep sea bivalves |
| topic | Symbiosis Hydrothermal vent Bivalvia Conchocele bisecta Genome Stochastic evolution |
| url | https://doi.org/10.1186/s12915-023-01551-z |
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