Competition between resident rhizosphere bacteria enhances phytopathogen suppression via emergent antagonism

Resident bacterial interactions can shape the invasion resistance of rhizosphere microbiomes, but whether interactions between weakly antagonistic resident bacteria can generate emergent antagonism against invading pathogens remains poorly understood. Here, we used a systematic pairwise interaction screening to identify Ralstonia pickettii RAL5 and Acinetobacter oleivorans ACI4 bacterial pair, that together provided a strong suppression of the phytopathogenic R. solanacearum Rs1115 strain. Although RAL5 and ACI4 monocultures only weakly inhibited pathogen growth, the RAL5-ACI4 co-cultures strongly suppressed the Rs1115, which was associated with asymmetric competition where the RAL5 dominated the ACI4 species. In line with this competitive asymmetry, broad transcriptional reprogramming was detected in RAL5 and only limited stress- and catabolism-associated responses in ACI4. The increased suppressiveness of co-cultures was associated with clear shifts in the extracellular metabolite profile, including the accumulation of candidate antimicrobial metabolites (e.g., a novobiocin-like feature and 4-aminophenol), and with the release of intracellular contents from ACI4 following RAL5-mediated lysis. The observed emergent antagonism also held in greenhouse experiments with tomato, where the RAL5-ACI4 consortium reduced R. solanacearum abundance and bacterial wilt severity relatively much more compared to when either strain was applied alone. Together, these results suggest that competitive interactions between resident bacteria can activate latent biocontrol potential in rhizosphere microbiomes, providing a new approach to harness resident bacterial interactions for enhanced pathogen suppression and biocontrol.