Reovirus infection results in rice rhizosphere microbial community reassembly through metabolite-mediated recruitment and exclusion.

BACKGROUND: Microbial assembly plays a critical role in ecosystem function and biodiversity. While numerous studies have explored the effect of abiotic factors on the belowground community assembly, much less is known about the role of biotic interactions, particularly viral infections, in shaping microbial communities. Southern rice black-streaked dwarf virus (SRBSDV), a member of the Fijivirus genus in the Reoviridae family, has caused severe yield losses in rice due to its rapid transmission. However, its specific effects on rhizosphere microbiota and the dynamics of microbial community changes have not been fully elucidated. RESULTS: By leveraging metabolomics with amplicon and metagenomics, this study provided a comprehensive understanding of the effect of SRBSDV infection on the rhizosphere microbial community and their functions. The results revealed that SRBSDV invasion led to significant changes in rhizosphere metabolites and microbial assembly processes. Specifically, the estimated overdispersion of cations sharply decreased following viral infection, while anion levels decreased markedly during early infection and then increased rapidly after 15 days. Key taxa, such as methanotrophs (e.g., Methylomicrobium), nitrifiers (e.g., Nitrospira), and iron-cycling bacteria (e.g., Sideroxydans), not only increased in abundance but also showed strong involvement in the microbial assembly processes. These key microbes were closely linked to specific metabolites and organized into two distinct network modules. Both modules predominantly recruited beneficial microbes, but one module also actively excluded potentially harmful taxa (e.g., Salmonella), which could disrupt community stability. Further experiments with exogenous metabolites confirmed the vital role of quercetin in attracting beneficial microbes while repelling harmful ones. CONCLUSION: The findings indicate that arboviruses can strongly influence the belowground rhizosphere microbial assembly processes by modulating metabolite profiles to selectively recruit or exclude key microbial species. These taxa, in turn, play fundamental roles in rhizosphere functions. These insights lay the groundwork for strategies to enhance rice immunity against viral infections by managing the rhizosphere microbial community. Video Abstract.