Genomic sequences used in this study.

Intraspecies interactions shape microbial community structure and evolution, yet the mechanisms determining competitive outcomes among closely related strains remain unclear. The soil bacterium Bacillus subtilis is a model for microbial social interactions, where quorum-sensing systems regulate cooperation and antagonism. Here, we take a multifaceted approach to dissect the role of quorum-sensing regulation in competitive fitness. Isolate NCIB 3610 carries a signal unresponsive RapP-PhrP module that alters quorum-sensing control and promotes faster growth. Modelling and mutant analysis demonstrate that the small differences in growth rate conferred by RapP-PhrP3610 are sufficient to drive competitive exclusion. The importance of quorum sensing control is further exemplified by experimental evolution of distinct wild isolates, which revealed recurrent mutations in the sensor kinase comP, which phenocopy complete comP or comA deletions and confer a growth-linked competitive advantage. Key quorum sensing mechanisms are abandoned even in structured microbial communities, where it might be expected that communal traits are favoured. Furthermore, a phylogenomic survey of 370 B. subtilis genomes identified disruptive comP mutations in ~16% of isolates. However, growth rate alone does not explain all interaction outcomes as even isogenic strains with equivalent doubling times differ in competitiveness. Transcriptomic profiling and validation experiments implicated a type VII secretion system toxin as an additional effector. These findings reveal that disruption of quorum-sensing pathways, whether naturally or through selection, provides a rapid route to competitive advantage, highlighting a fundamental trade-off between communal signalling and individual fitness in microbial populations.

种内相互作用塑造微生物群落的结构与演化，但决定近缘菌株间竞争结局的分子机制仍不明确。土壤细菌枯草芽孢杆菌（Bacillus subtilis）是微生物社会互作研究的模式物种，其群体感应（quorum sensing）系统调控菌群的合作与拮抗作用。本研究采用多维度研究手段，解析群体感应调控在竞争适合度中的作用。菌株NCIB 3610携带一个对信号无响应的RapP-PhrP模块，该模块可改变群体感应调控并促进菌株快速生长。建模与突变体分析表明，由RapP-PhrP3610所赋予的微小生长速率差异，足以驱动竞争排斥过程。群体感应调控的重要性进一步通过不同野生菌株的实验演化研究得到验证：该研究发现传感器激酶comP存在独立反复出现的突变，这类突变可模拟comP或comA完全缺失的表型，并赋予与生长相关的竞争优势。即便在结构化微生物群落中——这类环境本应更利于群落公共性状的保留——核心群体感应机制仍会被弃用。此外，对370株枯草芽孢杆菌基因组的系统发育基因组学（phylogenomic）分析显示，约16%的菌株携带功能受损的comP突变。然而，仅靠生长速率无法解释所有的互作结局：即便倍增时间一致的同基因菌株，其竞争能力也存在差异。转录组分析与验证实验证实，VII型分泌系统（type VII secretion system）毒素可作为额外的竞争效应因子。本研究结果表明，无论是自然发生还是经选择获得的群体感应通路破坏，均可快速赋予菌株竞争优势，这凸显了微生物种群中公共信号传导与个体适合度之间存在根本性的权衡关系。