Nutrient factor-dependent performance of bacterial quorum sensing system during population evolution

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ORIGINAL PAPER

Nutrient factor‑dependent performance of bacterial quorum sensing system during population evolution Kelei Zhao1   · Jing Li1 · Yang Yuan1 · Jiafu Lin1 · Xinrong Wang1 · Yidong Guo1 · Yiwen Chu1 Received: 21 June 2019 / Revised: 26 February 2020 / Accepted: 4 June 2020 © Springer-Verlag GmbH Germany, part of Springer Nature 2020

Abstract Bacterial quorum sensing (QS) system regulates the production of most costly but sharable extracellular products (public goods) in a growth-phase-dependent manner, and the development of this energy-intensive process is susceptible to environmental changes. However, the role of nutrient factors in dominating the QS-mediated cooperative interaction and intracellular metabolism still remains less understood. Here we studied the performance of QS system by growing Pseudomonas aeruginosa under different nutrient and culture conditions. The results of comparative-transcriptomic analyses revealed that carbon source-limitation was the main factor suppressing the activation of QS system, and a substantial number of publicgood-encoding genes were induced when phosphorus is limiting in short-term culture. By contrast, although the QS regulation of P. aeruginosa in all the cultures was generally decreased along with the enrichment of QS-deficient individuals during evolution, limitation of different nutrient factors had discrepant effects in directing the formation of population structure by coordinating the production of public goods and primary metabolism, especially the starch and sucrose metabolism. These findings demonstrate the pleiotropy of QS regulation in balancing the development of cooperative behavior and metabolism, and provide a reference for further understanding the role of QS system in causing persistent infections. Keywords  Pseudomonas aeruginosa · Quorum sensing · Nutrient factors · Public goods · Metabolism · Transcriptome

Introduction It is well recognized that many species of Proteobacteria communicate in a common process termed quorum sensing (QS). The development of QS system activates the expression of various extracellular products (public-goods) that can be shared by the local individuals, and thus sets up a form of cooperative interaction in bacterial population (Fuqua Communicated by Erko Stackebrandt. Electronic supplementary material  The online version of this article (https​://doi.org/10.1007/s0020​3-020-01937​-5) contains supplementary material, which is available to authorized users. * Kelei Zhao [email protected] * Yiwen Chu [email protected] 1



Antibiotics Research and Re‑Evaluation Key Laboratory of Sichuan Province, Sichuan Industrial Institute of Antibiotics, Chengdu University, No. 168, Huaguan Road, Chengdu 610052, Sichuan, China

et al. 1994; Diggle et al. 2007; Asfahl and Schuster 2017; Mukherjee and Bassler 2019). However, like in human society, this cooperative system is unstable and vulnerable to the exploitation of public-good non-producers (defectors), which are frequently selected during evolution and may cause a tragedy