Meloidogyne nematodes reprogram rhizosphere metabolism to suppress antagonistic microbiota and enable bacterial pathogen co-infection

Abstract

SummaryRoot-knot nematodes cause substantial crop losses by compromising plant immunity and facilitating invasion by soil-borne bacterial pathogens, yet the mechanisms underlying nematode-facilitated co-infection remain poorly understood. Here, we quantify the global prevalence of nematode-pathogen co-infection and integrate multi-omic analyses across greenhouse and in vitro experiments. We show that nematode invasion activates plant defense gene expression but concurrently disrupts rhizosphere homeostasis, resulting in microbiome dysbiosis that overrides host resistance. Meloidogyne invasion induces pronounced metabolic reprogramming, characterized by depletion of tomatidine and accumulation of carbohydrate metabolites such as galactose. These shifts selectively suppress Streptomyces-dominated antagonistic microbiota while enriching Acidovorax, which exhibits nutritional synergy with Ralstonia. Using synthetic microbial community transplantation, we demonstrate a functional transition from pathogen-suppressive to pathogen-permissive bacteriomes following nematode invasion. Together, our findings reveal how nematodes and bacterial pathogens cooperatively subvert plant-microbe metabolic signaling to undermine rhizosphere immunity, highlighting actionable targets for microbiome-based disease control.