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A glimpse of deep-sea adaptation in chemosynthetic holobionts: Depressurization causes DNA fragmentation and cell death of methanotrophic endosymbionts rather than their deep-sea Bathymodiolinae host
Chen, Hao1,2,3; Wang, Minxiao1,2,3; Li, Mengna1,2,3,4; Lian, Chao1,2,3; Zhou, Li1,2,3; Zhang, Xin1,3; Zhang, Huan1,2,3; Zhong, Zhaoshan1,2,3; Wang, Hao1,2,3; Cao, Lei1,2,3; Li, Chaolun1,2,3,4
2021-05-01
Source PublicationMOLECULAR ECOLOGY
ISSN0962-1083
Volume30Issue:10Pages:2298-2312
Corresponding AuthorLi, Chaolun(lcl@qdio.ac.cn)
AbstractBathymodiolinae mussels are typical species in deep-sea cold seeps and hydrothermal vents and an ideal model for investigating chemosynthetic symbiosis and the influence of high hydrostatic pressure on deep-sea organisms. Herein, the potential influence of depressurization on DNA fragmentation and cell death in Bathymodiolinae hosts and their methanotrophic symbionts were surveyed using isobaric and unpressurized samples. As a hallmark of cell death, massive DNA fragmentation was observed in methanotrophic symbionts from unpressurized Bathymodiolinae while several endonucleases and restriction enzymes were upregulated. Additionally, genes involved in DNA repair, glucose/methane metabolism as well as two-component regulatory system were also differentially expressed in depressurized symbionts. DNA fragmentation and programmed cell death, however, were rarely detected in the host bacteriocytes owing to the orchestrated upregulation of inhibitor of apoptosis genes and downregulation of caspase genes. Meanwhile, diverse host immune recognition receptors were promoted during depressurization, probably enabling the regain of symbionts. When the holobionts were subjected to a prolonged acclimation at atmospheric pressure, alternations in both the DNA fragmentation and the expression atlas of aforesaid genes were continuously observed in symbionts, demonstrating the persistent influence of depressurization. Contrarily, the host cells demonstrated certain tolerance against depressurization stress as expression level of some immune-related genes returned to the basal level in isobaric samples. Altogether, the present study illustrates the distinct stress responses of Bathymodiolinae hosts and their methanotrophic symbionts against depressurization, which could provide further insight into the deep-sea adaptation of Bathymodiolinae holobionts while highlighting the necessity of using isobaric sampling methods in deep-sea research.
Keywordbathymodiolinae mussel chemosynthetic symbiosis deep‐ sea adaptation hydrostatic pressure methane‐ oxidizing bacteria
DOI10.1111/mec.15904
Indexed BySCI
Language英语
Funding ProjectKey Research Program of Frontier Sciences, CAS[ZDBS-LY-DQC032] ; Strategic Priority Research Program of the Chinese Academy of Sciences[XDA22050303] ; Strategic Priority Research Program of the Chinese Academy of Sciences[XDB42020401] ; National Key Research and Development Program of China[2018YFC0310800] ; National Natural Science Foundation of China[42030407] ; National Natural Science Foundation of China[42076091] ; National Natural Science Foundation of China[41906103] ; Key Deployment Project of Centre for Ocean Mega-Research of Science, CAS[COMS2020Q02] ; Senior User Project of RV KEXUE[KEXUE2020G03]
WOS Research AreaBiochemistry & Molecular Biology ; Environmental Sciences & Ecology ; Evolutionary Biology
WOS SubjectBiochemistry & Molecular Biology ; Ecology ; Evolutionary Biology
WOS IDWOS:000639363800001
PublisherWILEY
Citation statistics
Cited Times:1[WOS]   [WOS Record]     [Related Records in WOS]
Document Type期刊论文
Identifierhttp://ir.qdio.ac.cn/handle/337002/170613
Collection海洋生态与环境科学重点实验室
Corresponding AuthorLi, Chaolun
Affiliation1.Chinese Acad Sci, Ctr Deep Sea Res, Inst Oceanol, CAS Key Lab Marine Ecol & Environm Sci, Qingdao, Peoples R China
2.Qingdao Natl Lab Marine Sci & Technol, Lab Marine Ecol & Environm Sci, Qingdao, Peoples R China
3.Chinese Acad Sci, Ctr Ocean Megasci, Qingdao, Peoples R China
4.Univ Chinese Acad Sci, Beijing, Peoples R China
First Author AffilicationInstitute of Oceanology, Chinese Academy of Sciences;  Center for Ocean Mega-Science, Chinese Academy of Sciences
Corresponding Author AffilicationInstitute of Oceanology, Chinese Academy of Sciences;  Center for Ocean Mega-Science, Chinese Academy of Sciences
Recommended Citation
GB/T 7714
Chen, Hao,Wang, Minxiao,Li, Mengna,et al. A glimpse of deep-sea adaptation in chemosynthetic holobionts: Depressurization causes DNA fragmentation and cell death of methanotrophic endosymbionts rather than their deep-sea Bathymodiolinae host[J]. MOLECULAR ECOLOGY,2021,30(10):2298-2312.
APA Chen, Hao.,Wang, Minxiao.,Li, Mengna.,Lian, Chao.,Zhou, Li.,...&Li, Chaolun.(2021).A glimpse of deep-sea adaptation in chemosynthetic holobionts: Depressurization causes DNA fragmentation and cell death of methanotrophic endosymbionts rather than their deep-sea Bathymodiolinae host.MOLECULAR ECOLOGY,30(10),2298-2312.
MLA Chen, Hao,et al."A glimpse of deep-sea adaptation in chemosynthetic holobionts: Depressurization causes DNA fragmentation and cell death of methanotrophic endosymbionts rather than their deep-sea Bathymodiolinae host".MOLECULAR ECOLOGY 30.10(2021):2298-2312.
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