Insights into the Arms Race between Prokaryotic Hosts and Their Viruses in Mangrove Ecosystem

The coevolutionary arms race between prokaryotes and viruses has driven the diversification of various microbial immune mechanisms including restriction-modification (RM) and clustered regularly interspaced short palindromic repeats and CRISPR-associated protein (CRISPR-Cas) systems. While recent efforts have expanded the catalog of antiviral systems, their ecological dynamics within complex microbial communities remain underexplored. Here, we analyzed prokaryotic communities, viruses, and defense systems in mangrove habitats from Futian, China, by integrating DNA and RNA sequencing of sediment cores collected across multiple depths and seasons at two sites. Prokaryotic genomes harbored 65 distinct defense system types, representing ∼43% of known systems, with transcriptional activity dominated by <i>Pseudomonadota, Planctomycetota</i>, and <i>Chloroflexiota</i>. The key systems, including abortive infection (AbiD, AbiE, AbiU), Eleos, CRISPR-Cas, MazEF, Retron, and Wadjet, exhibited high transcriptional activity across samples. Strikingly, viruses encoded highly expressed defense systems such as AbiE and RM, despite their co-occurring prokaryotic hosts lacking detectable antiviral systems. The abundance ratio of prokaryotes and viruses with defense systems shows an opposite trend as the depth variation. Heterologous validation confirmed the antiviral efficacy of the selected systems. Our findings suggest that viral-encoded defense systems may functionally augment host immunity in mangrove habitats, revealing a nuanced coevolutionary interplay within these ecosystems. This study advances our understanding of host-virus interactions at the community level in mangrove wetland microbiomes.