Dispersal, habitat filtering, and eco-evolutionary dynamics as drivers of local and global wetland viral biogeography

Wetlands store 20-30% of the worlds soil carbon, and identifying the microbial controls on these carbon reserves is essential to predicting feedbacks to climate change. Although viral infections likely play important roles in wetland ecosystem dynamics, we lack a basic understanding of wetland viral ecology. Here 63 viral size-fraction metagenomes (viromes) and paired total metagenomes were generated from three time points in 2021 at seven fresh- and saltwater wetlands in the California Bodega Marine Reserve. We recovered 12,826 viral population genomic sequences (vOTUs), 4.4% of which were also detected at the same field site two years prior, indicating a small degree of population stability or recurrence. Viral communities differed most significantly across the seven wetland sites and were also structured by habitat (plant community composition and salinity). Read mapping to a new version of our reference database, PIGEONv2.0 (now with 515,763 vOTUs), revealed 196 vOTUs present over large geographic distances, often reflecting shared habitat characteristics. Wetland vOTU microdiversity was significantly lower locally than globally and lower within than between time points, indicating greater divergence with increasing spatiotemporal distance. Viruses tended to have broad predicted host ranges via CRISPR spacer linkages to metagenome-assembled genomes (whether this reflects true biology remains to be seen), and increased SNP frequencies in CRISPR-targeted major tail protein genes suggest viral eco-evolutionary dynamics, potentially in response to both immune targeting and to changes in host cell receptors involved in viral attachment. Together, these results highlight the importance of dispersal, environmental selection, and eco-evolutionary dynamics as drivers of local and global wetland viral biogeography.