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 Pseudomonadota, Planctomycetota, and Chloroflexiota. 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.