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

ABSTRACT Healthy plant leaves potentially host both commensal bacteria and opportunistic pathogens, which, under some circumstances, may cause disease. The interactions between commensals and opportunistic pathogens are generally poorly understood, but such understanding is crucial for developing effective biocontrol strategies. In Arabidopsis thaliana , isothiocyanates (ITCs) are defense metabolites that suppress most bacteria; commensals are especially affected as they do not express ITC resistance genes. The ITC hydrolase SaxA detoxifies ITCs, making it an important virulence factor for bacterial and fungal pathogens. To investigate pathogen-commensal 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. PS degrades 4-methylsulfinylbutyl-ITC (4MSOB-ITC) with SaxA. We examined commensal growth in the presence of 4MSOB-ITC, both in monoculture and in coculture with PS or a saxA -deficient mutant (PSKO). We used the growth data to develop a generalizable consumer-resource mathematical model incorporating ITC toxicity, ITC degradation, and nutrient use. We predicted and confirmed experimentally that the extent to which SaxA benefits the pathogen depends on its effects on commensals. In some contexts, commensal rescue and the resultant nutrient competition limit pathogen growth. 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 commensal rescue (commensal growth). Our findings suggest that the effects of microbial traits—traditionally viewed as either virulence or plant-beneficial factors—are constrained in the microbiome context. This underscores the need to reconsider how such traits are classified in the context of plant-microbiome interactions. IMPORTANCE Healthy plant leaves host a variety of bacteria; these can be beneficial, but some (opportunistic pathogens) can also be harmful under certain conditions. To design effective biocontrol strategies to sustainably protect plants, it is important to understand how opportunistic pathogens thrive as part of a healthy leaf microbiome. Plant defense metabolites, such as isothiocyanates (ITCs), which kill commensal leaf bacteria, and bacterial ITC resistance mechanisms, such as the ITC hydrolase SaxA, which are often expressed in pathogens and degrade ITCs, may play key roles in the plant microbiome composition. In this study, we explore how SaxA-mediated ITC degradation by a pathogen also benefits diverse ITC-sensitive commensals and how this, in turn, could shape microbiome stability and plant health. Using mathematical modeling based on growth data from Pseudomonas viridiflava with diverse commensals, we find that interaction dynamics can be explained by ITC detoxification and nutrient competition. We predict and experimentally confirm that conditions exist under which SaxA favors commensal growth so strongly that the pathogen is outcompeted for resources, thus not benefiting from its own virulence factor. Our findings suggest that the effects of microbial traits, including virulence factors, are context-dependent, especially when functioning as a public good in a community context like SaxA. Moreover, we propose that this concept, which has been known from antibiotic-degrading microbes, may be worth considering as well when studying plant-pathogen interactions under natural conditions where the commensal microbiome might play an important role in plant disease outcomes.