Bacterial viruses are widespread and abundant across natural and engineered habitats. They influence ecosystem functioning through interactions with their hosts. Laboratory studies of phage–host pairs have advanced our understanding of phenotypic and genetic diversification in bacteria and phages. However, the dynamics of phage–host interactions have been seldom recorded in complex natural environments. We conducted an observational metagenomic study of the dynamics of interaction between Gordonia and their phages using a three-year data series of samples collected from a full-scale wastewater treatment plant. The aim was to obtain a comprehensive picture of the coevolution dynamics in naturally evolving populations at relatively high time resolution. Coevolution was followed by monitoring changes over time in the CRISPR loci of Gordonia metagenome-assembled genome, and reciprocal changes in the viral genome. Genome-wide analysis indicated low strain variability of Gordonia, and almost clonal conservation of the trailer end of the CRISPR loci. Incorporation of newer spacers gave rise to multiple coexisting bacterial populations. The host population carrying a shorter CRISPR locus that contain only ancestral spacers, which has not acquired newer spacers against the coexisting phages, accounted for more than half of the total host abundance in the majority of samples. Phages genome co-evolved by introducing directional changes, with no preference for mutations within the protospacer and PAM regions. Metagenomic reconstruction of time-resolved variants of host and viral genomes revealed how the complexity at the population level has important consequences for bacteria-phage coexistence.

细菌病毒在自然和工程栖息地中广泛存在且数量众多。它们通过与宿主的相互作用影响生态系统的功能。噬菌体-宿主对的实验室研究加深了我们对细菌和噬菌体表型和遗传多样化的理解。然而，很少在复杂的自然环境中记录噬菌体与宿主相互作用的动力学。我们对Gordonia之间相互作用的动力学进行了观察性宏基因组学研究和他们的噬菌体使用从一个全面的废水处理厂收集的三年数据系列的样本。目的是以相对较高的时间分辨率全面了解自然进化种群的共同进化动力学。共同进化之后是监测戈登尼亚宏基因组组装基因组的 CRISPR 位点随时间的变化，以及病毒基因组的相互变化。全基因组分析表明Gordonia的菌株变异性低, 以及 CRISPR 基因座尾端的几乎克隆保护。加入较新的间隔子会产生多个共存的细菌种群。宿主群体携带较短的 CRISPR 基因座，仅包含祖先间隔子，尚未获得针对共存噬菌体的更新间隔子，占大多数样本总宿主丰度的一半以上。噬菌体基因组通过引入定向变化共同进化，不偏好原型间隔区和 PAM 区域内的突变。宿主和病毒基因组的时间分辨变体的宏基因组重建揭示了种群水平的复杂性如何对细菌-噬菌体共存产生重要影响。