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.

Virus-induced changes in root volatiles attract soil nematode vectors to infected plants.

Plant-derived volatiles mediate interactions among plants, pathogenic viruses, and viral vectors. These volatile-dependent mechanisms have not been previously demonstrated belowground, despite their likely significant role in soil ecology and agricultural pest impacts. We investigated how the plant virus, tobacco rattle virus (TRV), attracts soil nematode vectors to infected plants. We infected Nicotiana benthamiana with TRV and compared root growth relative to that of uninfected plants. We tested whether TRV-infected N. benthamiana was more attractive to nematodes 7 d post infection and identified a compound critical to attraction. We also infected N. benthamiana with mutated TRV strains to identify virus genes involved in vector nematode attraction. Virus titre and associated impacts on root morphology were greatest 7 d post infection. Tobacco rattle virus infection enhanced 2-ethyl-1-hexanol production. Nematode chemotaxis and 2-ethyl-1-hexanol production correlated strongly with viral load. Uninfected plants were more attractive to nematodes after the addition of 2-ethyl-1-hexanol than were untreated plants. Mutation of TRV RNA2-encoded genes reduced the production of 2-ethyl-1-hexanol and nematode attraction. For the first time, this demonstrates that virus-driven alterations in root volatile emissions lead to increased chemotaxis of the virus's nematode vector, a finding with implications for sustainable management of both nematodes and viral pathogens in agricultural systems.