Viral Communities Suppress the Earthworm Gut Antibiotic Resistome by Lysing Bacteria on a National Scale

Earthworms are critical in regulating soil processes
and act as
filters for antibiotic resistance genes (ARGs). Yet, the geographic
patterns and main drivers of earthworm gut ARGs remain largely unknown.
We collected 52 earthworm and soil samples from arable and forest
ecosystems along a 3000 km transect across China, analyzing the diversity
and abundance of ARGs using shotgun metagenomics. Earthworm guts harbored
a lower diversity and abundance of ARGs compared to soil, resulting
in a stronger distance-decay rate of ARGs in the gut. Greater deterministic
assembly processes of ARGs were found in the gut than in soil. The
earthworm gut had a lower frequency of co-occurrence patterns between
ARGs and mobile genetic elements (MGEs) in forest than in arable systems.
Viral diversity was higher in the gut compared to soil and was negatively
correlated with bacterial diversity. Bacteria such as Streptomyces and Pseudomonas were potential hosts of both viruses
and ARGs. Viruses had negative effects on the diversity and abundance
of ARGs, likely due to the lysis on ARG-bearing bacteria. These findings
provide new insights into the variations of ARGs in the earthworm
gut and highlight the vital role of viruses in the regulation of ARGs
in the soil ecosystem.