Integrated 16S rRNA Sequencing and Metabolomics Reveals Niche-Specific Microbiome and Metabolome Changes Associated...

Toxoptera aurantii is a globally distributed piercing-sucking pest that severely threatens tea production. While the direct damage caused by aphid feeding is well documented, the systemic effects of infestation on plant-associated and soil microbial communities remain poorly understood. Here, we employed full-length 16S rRNA gene sequencing and untargeted metabolomics to investigate the influence of T. aurantii infestation on the microbiota of tea plants (Camellia sinensis) and rhizosphere soil across four sample compartments: aphid bodies, healthy leaves, aphid-infested leaves, and root-zone soil. Our results revealed pronounced niche-specific microbial assembly patterns. The aphid microbiome exhibited the lowest diversity and was dominated by obligate endosymbionts, including Buchnera aphidicola and the secondary symbiont Serratia symbiotica. Soil harbored the highest microbial diversity with a balanced phylum-level structure. Aphid infestation significantly reduced phyllosphere microbial diversity (Shannon index) and shifted community composition, with a decline in a sequence putatively assigned to Methylobacterium brachiatum and a modest increase in a taxon assigned to the opportunistic plant pathogen OTU assigned to Dickeya chrysanthemi. This pattern suggests a hypothesis that aphid infestation may create conditions permissive for such opportunistic pathogens, although experimental validation is required. Concurrently, infestation was associated with profound metabolic reprograming in tea leaves, including upregulation of defense-related flavonoids and terpenoids and downregulation of several primary metabolites. Notably, the phyllosphere of infested leaves showed reduced microbial diversity and an increased relative abundance of a 16S rRNA sequence assigned to Dickeya chrysanthemi, while certain plant-derived antimicrobial metabolites were decreased. These patterns suggest a possible association between aphid infestation, altered antimicrobial metabolite profiles and increased relative abundance of Dickeya-assigned sequences. These findings demonstrate that T. aurantii infestation triggers a systemic response in the aboveground compartments (aphid and leaf), while the soil compartment maintains a distinct and highly diverse microbial community that serves as a potential reservoir. The study characterizes microbial communities across these three compartments without inferring infestation-driven soil remodeling. This study advances our understanding of tripartite interactions in tea ecosystems and provides a basis for developing microbiome-based strategies for sustainable pest management.