Rhizosphere microbiota co-occur with pea root rot disease complex pathogens

Abstract Disease results from interactions between the host, the environment, and the pathogen. However, in complex pathosystems such as the soil-borne pea root rot disease, multiple co-occurring pathogens interact differentially across the host–environment–pathogen triangle, adding additional layers of complexity. The soil microbiome, including beneficial microbes and opportunistic pathogens, adds a fourth dimension of complexity in which microbial communities may either ameliorate or exacerbate disease. Here, using a large-scale field trial of Pisum sativum and naturally occurring root rot disease complexes, we used amplicon-based and shotgun metagenomic sequencing approaches to investigate interactions within the host–environment–pathogen–microbiome disease tetrahedron. Metagenomic analysis identified taxa whose abundance correlated with members of a disease complex dominated by A. euteiches and Fusarium species, including Pseudomonas, Sphingomonas, Bacillus, and Pythium. We also found that pathogen abundance showed a weak correlation with disease severity, and similarly, pea lines exhibited low consistency in disease responses across years. However, we found that disease level affected total prokaryotic and fungal community diversity. We identified microbial taxa that are positively and negatively associated with plant health, suggesting their roles in either disease suppression or exacerbation. Collectively, this work sheds light on the complexity of interactions across plant genotype-environment-pathogen-microbiome interactions to provide insights into multivariate contributors to each disease axis.