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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
Author(s) -
Chen Hao,
Wang Minxiao,
Li Mengna,
Lian Chao,
Zhou Li,
Zhang Xin,
Zhang Huan,
Zhong Zhaoshan,
Wang Hao,
Cao Lei,
Li Chaolun
Publication year - 2021
Publication title -
molecular ecology
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 2.619
H-Index - 225
eISSN - 1365-294X
pISSN - 0962-1083
DOI - 10.1111/mec.15904
Subject(s) - biology , hydrostatic pressure , dna fragmentation , chemosynthesis , deep sea , dna damage , microbiology and biotechnology , ecology , programmed cell death , hydrothermal vent , dna , apoptosis , genetics , paleontology , hydrothermal circulation , fishery , physics , thermodynamics
Bathymodiolinae 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.