Zhang Qifeng, Li Jie, Tuo Jinhua, Liu Shengnan, Liu Yang, Liu Peng, Ye Lin, Zhang Xu-Xiang
State Key Laboratory of Pollution Control and Resource Reuse, School of Environment, Nanjing University, Nanjing 210023, China.
ISME J. 2025 Jan 2;19(1). doi: 10.1093/ismejo/wraf051.
Bacteria have evolved various antiviral defense systems (DSs) to protect themselves, but how DSs respond to the variation of bacteriophages in complex bacterial communities and whether DSs function effectively in maintaining the stability of bacterial community structure and function remain unknown. Here, we conducted a long-term metagenomic investigation on the composition of bacterial and phage communities of monthly collected activated sludge (AS) samples from two full-scale wastewater treatment plants over 6 years and found that DSs were widespread in AS, with 91.1% of metagenome-assembled genomes (MAGs) having more than one complete DS. The stability of the bacterial community was maintained under the fluctuations of the phage community, and DS abundance and phage abundance were strongly positively correlated; there was a 0-3-month time lag in the responses of DSs to phage fluctuations. The rapid turnover of clustered regularly interspaced short palindromic repeat spacer repertoires further highlighted the dynamic nature of bacterial defense mechanisms. A pan-immunity phenomenon was also observed, with nearly identical MAGs showing significant differences in DS composition, which contributed to community stability at the species level. This study provides novel insights into the complexity of phage-bacteria interactions in complex bacterial communities and reveals the key roles of DSs in stabilizing bacterial community structure and function.
细菌已经进化出多种抗病毒防御系统（DSs）来保护自己，但在复杂的细菌群落中，DSs如何应对噬菌体的变化，以及DSs在维持细菌群落结构和功能的稳定性方面是否有效发挥作用，仍然未知。在这里，我们对来自两个全规模污水处理厂的每月收集的活性污泥（AS）样本的细菌和噬菌体群落组成进行了为期6年的长期宏基因组学调查，发现DSs在AS中广泛存在，91.1%的宏基因组组装基因组（MAGs）拥有不止一个完整的DS。在噬菌体群落的波动下，细菌群落的稳定性得以维持，DS丰度和噬菌体丰度呈强烈正相关；DSs对噬菌体波动的响应存在0至3个月的时间滞后。成簇规律间隔短回文重复序列间隔区文库的快速周转进一步突出了细菌防御机制的动态性质。还观察到一种泛免疫现象，几乎相同的MAGs在DS组成上显示出显著差异，这有助于在物种水平上维持群落稳定性。这项研究为复杂细菌群落中噬菌体 - 细菌相互作用的复杂性提供了新的见解，并揭示了DSs在稳定细菌群落结构和功能中的关键作用。
