Foliar pathogen and drought impose reproducible but community-dependent influence on the root microbiome

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Abstract Plant microbiomes are assembled from environmental pools that differ substantially in composition, yet whether their responses to stress follow general rules or depend on the resident community remains unclear. We tested the generality of root microbiome responses to stress by growing three tomato ( Solanum lycopersicum ) genotypes in 20 independently sourced microbial communities under controlled abiotic and biotic stress. Microbial communities were transferred into a common sterile substrate, allowing to vary microbial community identity independently of soil physicochemical properties, and plants were exposed to drought, the foliar pathogen Pseudomonas syringae pv. tomato , or no stress. We analyzed the root microbiota using 16S rRNA amplicon sequencing. Stressor identity explained more variation in bacterial community composition than inoculum identity or plant genotype. Hierarchical models showed that many bacterial taxa responded consistently across distinct starting communities, with taxon identity contributing far more variation in stress response than microbial community of origin. Both stressors shifted between-community dissimilarity from taxon turnover toward nestedness, indicating increasingly similar patterns of taxon loss, but the pathogen produced stronger effects and increased variability among replicate plants. Drought reduced phylogenetic redundancy, whereas pathogen increased dispersal limitation. Together, these results show that stress imposes reproducible ecological filters across diverse starting microbiomes, while the magnitude and resulting community state remain contingent on the resident microbial community. This provides a basis for identifying transferable microbial targets for microbiome-based crop stress management, while also managing the local microbiome to maximize their beneficial effects.

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