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Microbial communities employ a variety of complex strategies to compete successfully against competitors sharing their niche, with antibiotic production being a common strategy of aggression. Here, by systematic evaluation of four non-ribosomal peptides/polyketide (NRPs/PKS) antibiotics produced by Bacillus subtilis clade, we revealed that they acted synergistically to effectively eliminate phylogenetically distinct competitors. The production of these antibiotics came with a fitness cost manifested in growth inhibition, rendering their synthesis uneconomical when growing in proximity to a phylogenetically close species, carrying resistance against the same antibiotics. To resolve this conflict and ease the fitness cost, antibiotic production was only induced by the presence of a peptidoglycan cue from a sensitive competitor, a response mediated by the global regulator of cellular competence, ComA. These results experimentally demonstrate a general ecological concept – closely related communities are favoured during competition, due to compatibility in attack and defence mechanisms.

Microbial communities employ a variety of complex strategies to compete successfully against competitors sharing their niche, with antibiotic production being a common strategy of aggression. Here, by systematic evaluation of four non-ribosomal peptides (NRP) produced by B. subtilis clade, we revealed that they acted either synergistically or additively to effectively eliminate phylogenetically distinct competitors. All four major NRP biosynthetic clusters were also imperative for the survival of B. subtilis in a complex community extracted from the rhizosphere. The production of NRP came with a fitness cost manifested in growth inhibition, rendering NRP synthesis uneconomical when growing in proximity to a phylogenetically close species, carrying resistance against the same antibiotics. To resolve this conflict and ease the fitness cost, NRP production was only induced by the presence of peptidoglycan cue from a sensitive competitor. These results experimentally demonstrate a general ecological concept: closely related communities (self) are favoured during competition, due to compatibility in attack and defence mechanisms.

Beneficial and probiotic bacteria play an important role in conferring immunity of their hosts to a wide range of bacterial, viral, and fungal diseases. Bacillus subtilis is a Gram-positive bacterium that protects the plant from various pathogens due to its capacity to produce an extensive repertoire of antibiotics. At the same time, the plant microbiome is a highly competitive niche, with multiple microbial species competing for space and resources, a competition that can be determined by the antagonistic potential of each microbiome member. Therefore, regulating antibiotic production in the rhizosphere is of great importance for the elimination of pathogens and establishing beneficial host-associated communities. In this work, we used B. subtilis as a model to investigate the role of plant colonization in antibiotic production. Flow cytometry and imaging flow cytometry (IFC) analysis supported the notion that Arabidopsis thaliana specifically induced the transcription of the biosynthetic clusters for the non-ribosomal peptides surfactin, bacilysin, plipastatin, and the polyketide bacillaene. IFC was more robust in quantifying the inducing effects of A. thaliana, considering the overall heterogeneity of the population. Our results highlight IFC as a useful tool to study the effect of association with a plant host on bacterial gene expression. Furthermore, the common regulation of multiple biosynthetic clusters for antibiotic production by the plant can be translated to improve the performance and competitiveness of beneficial members of the plant microbiome.