Coevolution and cross-infection patterns between viruses and their host methanogens in paddy soils

Methanogens play a critical role in global methane (CH₄) emissions from rice paddy ecosystems. Through the integration of metagenomic analysis and meta-analysis, we constructed a CRISPR spacer database comprising 14 475 spacers derived from 351 methanogenic genomes. This enabled the identification of viruses targeting key methanogenic families prevalent in rice paddies, including <i>Methanosarcinaceae</i>, <i>Methanotrichaceae</i>, <i>Methanobacteriaceae</i>, <i>Methanocellaceae</i>, and <i>Methanomassiliicoccaceae</i>. We identified 419 virus-host linkages involving 56 methanogenic host species and 189 viruses, spanning the families <i>Straboviridae</i>, <i>Salasmaviridae</i>, <i>Kyanoviridae</i>, <i>Herelleviridae</i>, and <i>Demerecviridae</i>, along with 126 unclassified viral entities. These findings highlight a virome composition that is markedly distinct from those observed in gut environments. Cross-infection patterns were supported by the presence of specific viruses predicted to infect multiple closely related methanogenic species. Evidence for potential virus-host coevolution was observed in 24 viruses encoding anti-CRISPR proteins, likely facilitating evasion of host CRISPR-mediated immunity. Collectively, this study reveals a complex and dynamic network of virus-host interactions shaping methanogen communities in rice paddy ecosystems.