Department of Ocean Science and Hong Kong Branch of the Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Hong Kong University of Science and Technology, Hong Kong, China.
Shenzhen University-HKUST Joint Marine Science Ph.D. Program, Shenzhen University, Shenzhen, 518060, China.
Microbiome. 2021 Sep 3;9(1):182. doi: 10.1186/s40168-021-01099-6.
Deep-sea animals in hydrothermal vents often form endosymbioses with chemosynthetic bacteria. Endosymbionts serve essential biochemical and ecological functions, but the prokaryotic viruses (phages) that determine their fate are unknown.
We conducted metagenomic analysis of a deep-sea vent snail. We assembled four genome bins for Caudovirales phages that had developed dual endosymbiosis with sulphur-oxidising bacteria (SOB) and methane-oxidising bacteria (MOB). Clustered regularly interspaced short palindromic repeat (CRISPR) spacer mapping, genome comparison, and transcriptomic profiling revealed that phages Bin1, Bin2, and Bin4 infected SOB and MOB. The observation of prophages in the snail endosymbionts and expression of the phage integrase gene suggested the presence of lysogenic infection, and the expression of phage structural protein and lysozyme genes indicated active lytic infection. Furthermore, SOB and MOB appear to employ adaptive CRISPR-Cas systems to target phage DNA. Additional expressed defence systems, such as innate restriction-modification systems and dormancy-inducing toxin-antitoxin systems, may co-function and form multiple lines for anti-viral defence. To counter host defence, phages Bin1, Bin2, and Bin3 appear to have evolved anti-restriction mechanisms and expressed methyltransferase genes that potentially counterbalance host restriction activity. In addition, the high-level expression of the auxiliary metabolic genes narGH, which encode nitrate reductase subunits, may promote ATP production, thereby benefiting phage DNA packaging for replication.
This study provides new insights into phage-bacteria interplay in intracellular environments of a deep-sea vent snail. Video Abstract.
深海热液喷口的动物通常与化学合成细菌形成内共生关系。内共生体具有重要的生化和生态功能，但决定它们命运的原核病毒（噬菌体）尚不清楚。
我们对深海喷口蜗牛进行了宏基因组分析。我们组装了四个与硫氧化菌（SOB）和甲烷氧化菌（MOB）形成双重内共生关系的 Caudovirales 噬菌体的基因组框。聚类规律间隔短回文重复（CRISPR）间隔区映射、基因组比较和转录组分析表明，噬菌体 Bin1、Bin2 和 Bin4 感染了 SOB 和 MOB。在蜗牛内共生体中观察到前噬菌体和噬菌体整合酶基因的表达表明存在溶原性感染，噬菌体结构蛋白和溶菌酶基因的表达表明存在活跃的裂解性感染。此外，SOB 和 MOB 似乎利用适应性 CRISPR-Cas 系统来靶向噬菌体 DNA。其他表达的防御系统，如先天限制修饰系统和休眠诱导毒素-抗毒素系统，可能共同发挥作用，形成多条抗病毒防御线。为了对抗宿主防御，噬菌体 Bin1、Bin2 和 Bin3 似乎进化出了抗限制机制，并表达了甲基转移酶基因，可能抵消宿主的限制活性。此外，辅助代谢基因 narGH 的高水平表达，其编码硝酸盐还原酶亚基，可能促进 ATP 的产生，从而有利于噬菌体 DNA 的复制包装。
本研究为深海喷口蜗牛细胞内环境中噬菌体-细菌相互作用提供了新的见解。视频摘要。
