Metagenomic analysis suggests that tomato root-knot nematode infestation disrupts rhizosphere microbial networks, consistent with reduced disease suppression

Introduction The rhizosphere microbiome serves as a critical line of defense for plant health and soil-borne disease suppression. However, the underlying mechanisms by which root-knot nematodes (RKN), a devastating soil-borne pathogen, undermine putative disease-suppressive function through destabilizing microbial interaction networks remain poorly understood. Methods This study employed metagenomic sequencing coupled with microbial co-occurrence network analysis to systematically compare the community structure, interaction network topology, and functional gene profiles of the rhizosphere microbiome between healthy and RKN-infected tomato plants. Results Our findings revealed that RKN infection significantly altered the community structure of bacteria, fungi, and viruses. This disturbance was associated with a systematic simplification and loss of modularity within microbial interaction networks. Specifically, intra-domain bacterial networks exhibited reduced scale and connectivity, whereas fungal networks showed strengthened internal cohesion. Cross-kingdom interactions (e.g., bacteria-fungi) were severely weakened, resulting in a topological imbalance characterized by “tight within domains, loose between domains.” Functional profiling further indicated a distinct metabolic reprogramming in the infected rhizosphere, with a shift in resource allocation from growth and biosynthesis toward core energy acquisition and stress response. Discussion Collectively, our results suggest that the putative decline in disease-suppressive function following RKN infection may be mechanistically rooted in the destabilization of microbial cooperative networks and the consequent loss of functional redundancy. This study provides a novel network-level ecological framework for understanding plant-microbe-pathogen interactions and lays a theoretical foundation for microbiome-based ecological management strategies against soil-borne diseases.