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化学合成共生体深海适应性一瞥:减压导致甲烷营养型内共生体而非其深海贻贝科宿主的DNA片段化和细胞死亡。

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.

作者信息

Chen Hao, Wang Minxiao, Li Mengna, Lian Chao, Zhou Li, Zhang Xin, Zhang Huan, Zhong Zhaoshan, Wang Hao, Cao Lei, Li Chaolun

机构信息

Center of Deep Sea Research, CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China.

Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao, China.

出版信息

Mol Ecol. 2021 May;30(10):2298-2312. doi: 10.1111/mec.15904. Epub 2021 Apr 12.

DOI:10.1111/mec.15904
PMID:33774874
Abstract

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.

摘要

深海贻贝科贻贝是深海冷泉和热液喷口的典型物种,是研究化学合成共生以及高静水压力对深海生物影响的理想模型。在此,我们使用等压和常压样本,研究了减压对深海贻贝科宿主及其甲烷营养型共生体DNA片段化和细胞死亡的潜在影响。作为细胞死亡的标志,在常压下的深海贻贝科甲烷营养型共生体中观察到大量DNA片段化,同时几种核酸内切酶和限制酶上调。此外,参与DNA修复、葡萄糖/甲烷代谢以及双组分调节系统的基因在减压共生体中也有差异表达。然而,由于凋亡抑制基因的协同上调和半胱天冬酶基因的下调,在宿主含菌细胞中很少检测到DNA片段化和程序性细胞死亡。同时,在减压过程中,多种宿主免疫识别受体被激活,这可能有助于共生体的恢复。当全生物体在大气压下进行长时间适应时,共生体中持续观察到DNA片段化和上述基因表达图谱的变化,这表明减压的持续影响。相反,宿主细胞对减压应激表现出一定的耐受性,因为一些免疫相关基因的表达水平在等压样本中恢复到基础水平。总之,本研究阐明了深海贻贝科宿主及其甲烷营养型共生体对减压的不同应激反应,这可以为深入了解深海贻贝科全生物体的深海适应性提供进一步的见解,同时强调在深海研究中使用等压采样方法的必要性。

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