Bacterial degradation of a plant toxin and nutrient competition with commensals trade off to constrain pathogen growth

Healthy plant leaves host both commensal bacteria, which usually do not cause harm, and opportunistic pathogens, which under the right circumstances can cause disease. Microbial and plant-derived factors can potentially govern the balance between commensals and pathogens; understanding this dynamic is crucial for developing effective biocontrol strategies. In Arabidopsis thaliana , isothiocyanates (ITCs) are toxic defense metabolites that suppress most bacteria. An important virulence factor for bacterial and fungal pathogens of A. thaliana is the ITC hydrolase SaxA, which detoxifies ITCs. To investigate microbial interactions based on SaxA-mediated ITC degradation, we used five ITC-sensitive bacterial commensals and the opportunistic pathogen Pseudomonas viridiflava 3D9 (PS). All strains were isolated from healthy A. thaliana leaves and PS degrades 4-methylsulfinylbutyl-ITC (4MSOB-ITC) with SaxA. We examined their growth in the presence of 4MSOB-ITC, both in monoculture and in coculture with PS or a saxA -deficient mutant (PSKO). Based on experimental growth data, we developed a generalizable consumer-resource mathematical model incorporating ITC toxicity, ITC degradation, and nutrient use. We predicted conditions and confirmed them experimentally under which SaxA not only benefits the pathogen but also indirectly favors commensal growth, which then can limit pathogen proliferation by competing for nutrients. In addition, we tested in silico how commensal ITC susceptibility, pathogen ITC degradation rates, and growth parameters affect the trade-off between SaxA-mediated virulence (strong pathogen growth) and high commensal rescue (commensal growth). Our findings suggest that the effects of microbial traits - traditionally viewed as either virulence or plant-beneficial factors - are context-dependent. This underscores the need to reconsider how such traits are classified in the context of plant-microbiome interactions.