Seasonal variation in the biocontrol efficiency of bacterial wilt is driven by temperature-mediated changes in bacterial competitive interactions

Microbe-based biocontrol applications hold the potential to become an efficient way to control plant pathogen disease outbreaks in the future. However, their efficiency is still very variable, which could be due to their sensitivity to the abiotic environmental conditions. Here, we assessed how environmental temperature variation correlates with ability of Ralstonia pickettii, an endophytic bacterial biocontrol agent, to suppress the Ralstonia solanacearum pathogen during different tomato crop seasons in China. We found that suppression of the pathogen was highest when the seasonal mean temperatures were around 20 °C and rapidly decreased with increasing mean crop season temperatures. Interestingly, low levels of disease incidence did not correlate with low pathogen or high biocontrol agent absolute densities. Instead, the biocontrol to pathogen density ratio was a more important predictor of disease incidence levels between different crop seasons. To understand this mechanistically, we measured the growth and strength of competition between the biocontrol agent and the pathogen over a naturally occurring temperature gradient in vitro. We found that the biocontrol strain grew relatively faster at low temperature ranges, and the pathogen at high temperature ranges, and that similar to field experiments, pathogen suppression peaked at 20 °C. Together, our results suggest that temperature-mediated changes in the strength of bacterial competition could potentially explain the variable R. solanacearum biocontrol outcomes between different crop seasons in China. Synthesis and applications. Our results suggest that abiotic environmental conditions, such as temperature, can affect the efficacy of biocontrol applications. Thus, in order to develop more consistent biocontrol applications in the future, we might need to find and isolate bacterial strains that can retain their functionality regardless of the changing environmental conditions.