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

(2025) 13:214 Li et al. Microbiome https://doi.org/10.1186/s40168-025-02188-6 Microbiome Open Access RESEARCH Reovirus infection results in rice rhizosphere microbial community reassembly through metabolite‑mediated recruitment and exclusion Zhanbiao Li1†, Wandi Luo1,2†, Huiting Xie1†, Cuiping Mo1, Bixia Qin1, Yige Zhao3, Xiao Chen3, Songbai Zhang2, Yaling Zhao9, Mengcen Wang4, Yu Yang5, Jianhe Cai1, Baozhan Wang6*, Xu Liu6,7,8* and Yu Shi3* Abstract 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. † Zhanbiao Li, Wandi Luo, and Huiting Xie contributed equally to this work *Correspondence: Baozhan Wang Xu Liu Yu Shi Full list of author information is available at the end of the article © The Author(s) 2025. 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To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/. Li et al. Microbiome (2025) 13:214 Page 2 of 19 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. Keywords Southern rice black-streaked dwarf virus, Rice rhizosphere, Microbes, Assembly mechanisms, Metabolites, Ecological network Background Southern rice black-streaked dwarf virus (SRBSDV), first reported in 2008, is an arthropod-borne virus belonging to the genus Fijivirus in the family Reoviridae [1, 2]. It is exclusively transmitted by white-backed planthoppers, which are capable of long-distance migration, and it causes severe damage to rice crops across East and Southeast Asia [3]. Rice, an important staple food for over half the global population [4], is particularly susceptible to arthropod-borne viral diseases [3]. Plants naturally coexist with a variety of microbes [5] that are essential for their health and overall fitness [6]. When plants are infected by viruses, their immune systems are activated, leading to the release of defense compounds and changes in root exudates [7, 8], which in turn alter the microbial community and its functional groups both within the plant and in the rhizosphere. Previous reports have confirmed that SRBSDV infection significantly increases the diversity and richness of the microbial community in the rice rhizosphere within 30 days of infection [9]. However, to date, comprehensive studies on the effects of SRBSDV infection on the rice-microbial ecosystem, particularly on rhizosphere microbial assembly, remain limited. The process of microbial assembly is a key topic in microbial ecology, with significant implications for biodiversity and ecosystem functioning [10, 11]. Research exploring the factors shaping soil microbial communities has highlighted two basic categories: (1) deterministic processes, which drive microbial colonization when distinct ecological niches allow species to coexist despite competition. This includes heterogeneous selection, where the selective environment presents high spatial heterogeneity [12, 13], and homogeneous selection, which is prevalent in spatially uniform environments. (2) Stochastic processes, which enable multiple species to coexist in similar or overlapping niches without competitive exclusion. These include dispersal limitation caused by spatial isolation [14], homogenizing dispersal characterized by high rates of dispersal between communities [15], and ecological drift, which involves random fluctuations and undominated cases [16]. To quantify the relative importance of the abovementioned five processes in microbial assembly, Ning et al. constructed a phylogenetic bin-based null model analysis called iCAMP, which allows the identification of the contribution of individual species in these processes [17]. This method helps pinpoint key microbial species that have a greater role in microbial assembly. Typically, highly connected taxa within a microbial network are considered keystone species; these species occupy crucial topological positions and contribute significantly to important ecological functions [18] (...truncated)