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

Wetlands store 20–30% of the world's 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.