Li Pengwei, Wu Zongzhi, Liu Tang, Deng Chunfang, Liu Quan, Ni Jinren
Environmental Microbiome and Innovative Genomics Laboratory, College of Environmental Sciences and Engineering, Peking University, Beijing, 100871, P. R. China.
College of Environmental Sciences and Engineering, Key Laboratory of Water and Sediment Sciences, Ministry of Education, Peking University, Beijing, 100871, P. R. China.
Nat Commun. 2025 Jul 14;16(1):6482. doi: 10.1038/s41467-025-61467-w.
Groundwater harbors a pristine biosphere where microbes co-evolve with less human interference, yet the ancient and ongoing arms race between prokaryotes and viruses remains largely unknown in such ecosystems. Based on our recent nationwide groundwater monitoring campaign across China, we construct a metagenomic groundwater prokaryotic defensome catalogue (GPDC), encompassing 190,810 defense genes, 90,824 defense systems, 139 defense families, and 669 defense islands from 141 prokaryotic phyla. Over 94% of the defense genes in GPDC are novel and contribute vast microbial immune resources in groundwater. We find that candidate phyla radiation (CPR) bacteria possess higher defense system density and diversity against intense phage infection, while microbes as a whole exhibit an inverse relationship between defense systems and adaptive traits like resistance genes in groundwater. We further identify five first-line defense families covering 69.2% of the total defense systems, and high-turnover accessory immune genes are mostly conveyed to defense islands by mobile genetic elements. Our study also reveals viral resistance to microbial defense through co-localized anti-defense genes and interactions between CRISPR-Cas9 and anti-CRISPR protein. These findings expand our understanding of microbial immunity in pristine ecosystems and offer valuable immune resources for potential biotechnological applications.
地下水蕴藏着一个原始的生物圈，微生物在较少受到人类干扰的情况下共同进化，然而在这样的生态系统中，原核生物与病毒之间古老且持续的军备竞赛在很大程度上仍不为人知。基于我们近期在中国开展的全国性地下水监测活动，我们构建了一个宏基因组地下水原核生物防御组目录（GPDC），其中包含来自141个原核生物门的190,810个防御基因、90,824个防御系统、139个防御家族以及669个防御岛。GPDC中超过94%的防御基因是新发现的，为地下水中的微生物免疫资源做出了巨大贡献。我们发现候选门辐射（CPR）细菌针对强烈的噬菌体感染拥有更高的防御系统密度和多样性，而地下水中的微生物整体上在防御系统与诸如抗性基因等适应性特征之间呈现出反比关系。我们进一步鉴定出五个覆盖了69.2%的总防御系统的一线防御家族，并且高周转率的辅助免疫基因大多通过移动遗传元件被传递到防御岛。我们的研究还通过共定位的抗防御基因以及CRISPR-Cas9与抗CRISPR蛋白之间的相互作用揭示了病毒对微生物防御的抗性。这些发现扩展了我们对原始生态系统中微生物免疫的理解，并为潜在的生物技术应用提供了宝贵的免疫资源。
