The antagonists and helpers of plant pathogens: unraveling interactions that determine pathogen success

A range of soil-borne diseases is increasingly threatening agricultural production around the world. As production demands increase, there is a pressing need to reduce the use of environmentally unfriendly pesticides and agrochemicals. To address this need, plant root-associated microbiomes are increasingly being seen as a possible solution to boost natural pathogen resistance and soil microorgniams have become a target for innovative strategies aiming at improving crop protection. However, the ability of rhizosphere microbial communities to keep diseases under control is influenced by many factors, including the microbial interactions within these communities. Unfortunately, we still have relatively little insight into how microbial interactions affect community assembly and how such interactions eventually impact plant health. This thesis seeks to examine how microbial interactions within the rhizosphere microbiome impact the ability of plant pathogens to proliferate and cause plant disease. To this end, this thesis used bacterial wilt disease in tomato plant, which is caused by pathogen Ralstonia solanacearum, as a relevant model system. In Chapter 2, I have combined direct examination of the plant-associated microbiomes from healthy and diseased tomato rhizosphere soils with interaction studies in the laboratory involving bacterial isolates recovered from these soils. Results showed that rhizosphere microbial communities were one of the important factors influencing the manifestation of disease. However, correlation analyses showed discrepancies between co-occurrence patterns and direct strain interactions. This suggests that positive or negative links within co-occurrence networks are poor predictors of actual one-on-one interactions of bacterial populations. I subsequently used controlled systems with synthetic microbial communities to disentangle the role of specific organisms and their interactions in the ecological processes associated with bacterial wilt disease suppression. In these simplified systems, Chapter 3 assessed how interactions among antagonistic strains influenced pathogen invasion, and Chapter 4 tested if control of the pathogen can be achieved indirectly though inhibition of pathogen helpers. Results showed that in addition to the direct interactions between rhizobacterial isolates and the pathogen, indirect effects from interactions among rhizobacterial isolates could also be strong determinants of pathogen success. These results suggest that instead of a purely pathogen-focused view, better solutions for controlling plant disease outbreaks may be achieved by managing the composition of the soil microbiome as a whole. Chapter 5 examined the extent to which microbial interactions were influenced by resource availability. I found that at high resource availability, competitive resident communities produced more antimicrobial compounds, making them less susceptible to invasion compared to more facilitative communities. At low resource availability, facilitative communities reached higher productivity, which in turn was more important for resistance to pathogen invasion than the competitive interactions in such less productive communities. Therefore, in the study of microbial interactions in the rhizosphere, it is important to consider the effects of relevant environmental factors such as nutrient availability. Taken together, the results of this thesis form the basis for more informed management strategies based on knowledge of microbial interactions and community assembly, ultimately aiming to improve soil-borne disease suppressive potential in a targeted fashion without the use of pesticides.