The Anna Karenina principle in the assembly of plant microbiome under pathogen stress

The Anna Karenina Principle (AKP) posits that healthy microbiomes converge toward similar compositional states, whereas dysbiotic microbiomes diverge into distinct and system-specific configurations. Despite its broad recognition in microbiome research, systematic evidence remains scarce as to whether pathogen stress drives plant microbiome assembly in accordance with AKP. To address this knowledge gap, we examined 1,410 samples from multiple compartments (bulk soil, rhizosphere soil, roots, stems, and seeds) across a continental-scale, comparing healthy and Fusarium stalk rot-infected maize using 16S rRNA gene sequencing, complemented with metagenomic sequencing of 93 selected rhizosphere and stem samples. By integrating variations of bacterial community diversity, beta dispersion, average variation degree, and a modified stochasticity ratio, we demonstrated that pathogen-induced microbiome shifts conform to AKP predictions. Notably, AKP-conforming stochastic assembly enriched oligotrophic taxa, resulting in microbial communities with higher GC content, smaller average genome size, and reduced 16S rRNA operon copy numbers. Moreover, the selective enrichment of specific functional traits (including peptidoglycan biosynthesis and degradation, chromatin structure and dynamics, and lipid transport and metabolism) was closely associated with AKP. Our findings support AKP as a useful framework for understanding plant microbiome assembly under pathogen pressure and provide new insights into plant-microbiome-pathogen interactions.