Department of Gastroenterology, Ministry of Education Key Laboratory of Combinatorial Biosynthesis and Drug Discovery, Hubei Clinical Center and Key Laboratory of Intestinal and Colorectal Disease, Zhongnan Hospital of Wuhan University, School of Pharmaceutical Sciences, Wuhan University , Wuhan, Hubei, China.
Department of Respiratory Diseases, The Research and Application Center of Precision Medicine, The Second Affiliated Hospital of Zhengzhou University, Zhengzhou University , Zhengzhou, Henan, China.
mBio. 2023 Aug 31;14(4):e0093323. doi: 10.1128/mbio.00933-23. Epub 2023 Jun 1.
DndABCDE-catalyzed DNA phosphorothioation (PT), in which the nonbridging oxygen is swapped with a sulfur atom, was first identified in the bacterial genome. Usually, this modification gene cluster is paired with a restriction module consisting of DndF, DndG, and DndH. Although the mechanisms for the antiphage activity conferred by this Dnd-related restriction and modification (R-M) system have been well characterized, several features remain unclear, including the antiphage spectrum and potential interference with DNA methylation. Recently, a novel PT-related R-M system, composed of the modification module SspABCD paired with a single restriction enzyme, SspE, was revealed to be widespread in the bacterial kingdom, which aroused our interest in the interaction between Dnd- and Ssp-based R-M systems. In this study, we discussed the action of Dnd-related R-M systems against phages and demonstrated that the host could benefit from the protection provided by Dnd-related R-M systems against infection by various lytic phages as well as temperate phages. However, this defense barrier would fail against lysogenic phages. Interestingly, DNA methylation, even in the consensus sequence recognized by the Dnd system, could not weaken the restriction efficiency. Finally, we explored the interaction between Dnd- and Ssp-based R-M systems and found that these two systems were compatible. This study not only expands our knowledge of Dnd-associated R-M systems but also reveals a complex interaction between different defense barriers that coexist in the cell. IMPORTANCE Recently, we decoded the mechanism of Dnd-related R-M systems against genetic parasites. In the presence of exogenous DNA that lacks PT, the macromolecular machine consisting of DndF, DndG, and DndH undergoes conformational changes to perform DNA binding, translocation, and DNA nicking activities and scavenge the foreign DNA. However, several questions remain unanswered, including questions regarding the antiphage spectrum, potential interference by DNA methylation, and interplay with other PT-dependent R-M systems. Here, we revealed that the host could benefit from Dnd-related R-M systems for a broad range of antiphage activities, regardless of the presence of DNA methylation. Furthermore, we demonstrated that the convergence of Dnd- and Ssp-related R-M systems could confer to the host a stronger antiphage ability through the additive suppression of phage replication. This study not only deepens our understanding of PT-related defense barriers but also expands our knowledge of the arms race between bacteria and their predators.
DndABCDE 催化的 DNA 硫代磷酸化 (PT),其中非桥氧被硫原子取代,最初在细菌基因组中被发现。通常,这个修饰基因簇与由 DndF、DndG 和 DndH 组成的限制模块配对。尽管这种 Dnd 相关的限制和修饰 (R-M) 系统赋予的抗噬菌体活性的机制已经得到很好的描述,但仍有几个特征尚不清楚,包括抗噬菌体谱和潜在的对 DNA 甲基化的干扰。最近,一种新型的 PT 相关的 R-M 系统,由修饰模块 SspABCD 与单个限制酶 SspE 组成,被发现广泛存在于细菌王国中,这引起了我们对 Dnd 和 Ssp 为基础的 R-M 系统之间相互作用的兴趣。在这项研究中,我们讨论了 Dnd 相关的 R-M 系统对噬菌体的作用,并证明宿主可以从 Dnd 相关的 R-M 系统对各种裂解噬菌体和温和噬菌体的感染提供的保护中受益。然而,这种防御屏障将无法抵御溶原噬菌体。有趣的是,即使在 Dnd 系统识别的共识序列中进行 DNA 甲基化,也不能削弱限制效率。最后,我们探讨了 Dnd 和 Ssp 为基础的 R-M 系统之间的相互作用,发现这两种系统是兼容的。这项研究不仅扩展了我们对 Dnd 相关的 R-M 系统的认识,还揭示了细胞中同时存在的不同防御屏障之间复杂的相互作用。
最近,我们解码了 Dnd 相关的 R-M 系统对抗遗传寄生虫的机制。在缺乏 PT 的外源 DNA 存在的情况下,由 DndF、DndG 和 DndH 组成的大分子机器经历构象变化,以进行 DNA 结合、易位和 DNA 切口活性,并清除外来 DNA。然而,仍有几个问题没有得到解答,包括抗噬菌体谱、DNA 甲基化的潜在干扰以及与其他依赖 PT 的 R-M 系统的相互作用等问题。在这里,我们揭示了宿主可以从 Dnd 相关的 R-M 系统中受益于广泛的抗噬菌体活性,而不管 DNA 甲基化的存在如何。此外,我们还证明了 Dnd 和 Ssp 相关的 R-M 系统的融合可以通过附加抑制噬菌体复制赋予宿主更强的抗噬菌体能力。这项研究不仅加深了我们对 PT 相关防御屏障的理解,也扩展了我们对细菌和其捕食者之间军备竞赛的认识。