Qiu Huifang, Dandekar Ajai A, Dai Weijun
Integrative Microbiology Research Center, College of Plant Protection, South China of Agricultural University, Guangzhou, China.
Department of Microbiology, University of Washington, Seattle, WA, United States.
Evol Lett. 2024 Dec 20;9(2):273-281. doi: 10.1093/evlett/qrae067. eCollection 2025 Apr.
Social interactions profoundly shape the dynamics and functionality of microbial populations. However, mechanisms governing the regulation of cooperative or individual traits have remained elusive. Here, we investigated the regulatory mechanisms of social behaviors by characterizing the fitness of transcriptional regulator PsdR mutants in cooperating populations. In a canonical model described previously, PsdR was shown to solely have a nonsocial role in adaptation of these populations by controlling the intracellular uptake and processing of dipeptides. In addition to these known private traits, we found that PsdR mutants also enhanced cooperation by increasing the production of quorum sensing (QS)-regulated public goods. Although private dipeptide utilization promotes individual absolute fitness, it only partially accounts for the growth advantage of PsdR mutants. The absence of the QS master regulator LasR delayed the appearance of PsdR variants in an evolution experiment. We also demonstrated that the growth fitness of PsdR mutants is determined by a combination of the QS-mediated cooperative trait and the dipeptide metabolism-related private trait. This dual trait is co-regulated by PsdR, leading to the rapid spread of PsdR variants throughout the population. In conclusion, we identified a new social model of co-regulating cooperative and private traits in PsdR variants, uncovering the social and nonsocial roles of this transcriptional regulator in cooperating bacterial populations. Our findings advance the fundamental understanding of bacterial social interactions and provide insights into population evolution, pathogen infection control and synthetic biotechnology.
社会互动深刻地塑造了微生物群体的动态变化和功能。然而,调控合作或个体特征的机制仍然难以捉摸。在这里,我们通过表征转录调节因子PsdR突变体在合作群体中的适应性,研究了社会行为的调控机制。在先前描述的一个典型模型中,PsdR被证明仅通过控制二肽的细胞内摄取和加工,在这些群体的适应过程中发挥非社会作用。除了这些已知的个体特征外,我们发现PsdR突变体还通过增加群体感应(QS)调节的公共物品的产生来增强合作。虽然个体对二肽的利用促进了个体的绝对适应性,但它只能部分解释PsdR突变体的生长优势。在一项进化实验中,群体感应主调节因子LasR的缺失延迟了PsdR变体的出现。我们还证明,PsdR突变体的生长适应性由QS介导的合作特征和与二肽代谢相关的个体特征共同决定。这种双重特征由PsdR共同调节,导致PsdR变体在整个群体中迅速传播。总之,我们在PsdR变体中确定了一种共同调节合作和个体特征的新社会模型,揭示了这种转录调节因子在合作细菌群体中的社会和非社会作用。我们的发现推进了对细菌社会互动的基本理解,并为群体进化、病原体感染控制和合成生物技术提供了见解。