Skip to main content
SpringerLink
Log in

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

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

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 public-good-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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Asfahl KL, Schuster M (2017) Social interactions in bacterial cell-cell signaling. FEMS Microbiol Rev 41:92–107

    Article  CAS  Google Scholar 

  • Axelrod R, Hamilton WD (1981) The evolution of cooperation. Science 211:1390–1396

    Article  CAS  Google Scholar 

  • Balasubramanian D, Schneper L, Kumari H, Mathee K (2013) A dynamic and intricate regulatory network determines Pseudomonas aeruginosa virulence. Nucleic Acids Res 41:1–20

    Article  CAS  Google Scholar 

  • Bruger EL, Waters CM (2016) Bacterial quorum sensing stabilizes cooperation by optimizing growth strategies. Appl Environ Microbiol 82:6498–6506

    Article  CAS  Google Scholar 

  • Choi Y, Park HY, Park SJ, Park SJ, Kim SK, Ha C et al (2011) Growth phase-differential quorum sensing regulation of anthranilate metabolism in Pseudomonas aeruginosa. Mol Cells 32:57–65

    Article  CAS  Google Scholar 

  • Dandekar AA, Greenberg EP (2013) Microbiology: plan B for quorum sensing. Nat Chem Biol 9:292–293

    Article  CAS  Google Scholar 

  • Dandekar AA, Chugani S, Greenberg EP (2012) Bacterial quorum sensing and metabolic incentives to cooperate. Science 338:264–266

    Article  CAS  Google Scholar 

  • Darch SE, West SA, Winzer K, Diggle SP (2012) Density-dependent fitness benefits in quorum-sensing bacterial populations. Proc Natl Acad Sci USA 109:8259–8263

    Article  CAS  Google Scholar 

  • Diggle SP, Griffin AS, Campbell GS, West SA (2007) Cooperation and conflict in quorum-sensing bacterial populations. Nature 450:411–414

    Article  CAS  Google Scholar 

  • Duan K, Surette MG (2007) Environmental regulation of Pseudomonas aeruginosa PAO1 Las and Rhl quorum-sensing systems. J Bacteriol 189:4827–4836

    Article  CAS  Google Scholar 

  • Even-Tov E, Bendori SO, Valastyan J, Ke X, Pollak S, Bareia T et al (2016) Social evolution selects for redundancy in bacterial quorum sensing. PLoS Biol 14:e1002386

    Article  Google Scholar 

  • Fuqua WC, Winans SC, Greenberg EP (1994) Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 176:269–275

    Article  CAS  Google Scholar 

  • Goo E, Majerczyk CD, An JH, Chandler JR, Seo YS, Ham H et al (2012) Bacterial quorum sensing, cooperativity, and anticipation of stationary-phase stress. Proc Natl Acad Sci USA 109:19775–19780

    Article  CAS  Google Scholar 

  • Goo E, An JH, Kang Y, Hwang I (2015) Control of bacterial metabolism by quorum sensing. Trends Microbiol 23:567–576

    Article  CAS  Google Scholar 

  • Haney BR, Fewell JH (2018) Ecological drivers and reproductive consequences of non-kin cooperation by ant queens. Oecologia 187:643–655

    Article  Google Scholar 

  • Hardin G (1968) The tragedy of the commons. Science 162:1243–1248

    Article  CAS  Google Scholar 

  • Huang DW, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4:44–57

    Article  CAS  Google Scholar 

  • Köhler T, Buckling A, van Delden C (2009) Cooperation and virulence of clinical Pseudomonas aeruginosa populations. Proc Natl Acad Sci USA 106:6339–6344

    Article  Google Scholar 

  • MacLean RC, Fuentes-Hernandez A, Greig D, Hurst LD, Gudelj I (2010) A mixture of “cheats” and “co-operators” can enable maximal group benefit. PLoS Biol 8:e1000486

    Article  Google Scholar 

  • Martínez-García R, Tarnita CE (2016) Lack of ecological and life history context can create the illusion of social interactions in Dictyostelium discoideum. PLoS Comput Biol 12:e1005246

    Article  Google Scholar 

  • Mellbye B, Schuster M (2014) Physiological framework for the regulation of quorum sensing-dependent public goods in Pseudomonas aeruginosa. J Bacteriol 196:1155–1164

    Article  Google Scholar 

  • Mougous JD, Cuff ME, Raunser S, Shen A, Zhou M, Gifford CA et al (2006) A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312:1526–1530

    Article  CAS  Google Scholar 

  • Mukherjee S, Bassler BL (2019) Bacterial quorum sensing in complex and dynamically changing environments. Nat Rev Microbiol 17:371–382

    Article  CAS  Google Scholar 

  • Reed SC, Palm JD (1951) Social fitness versus reproductive fitness. Science 113:294–296

    Article  CAS  Google Scholar 

  • Sandoz KM, Mitzimberg SM, Schuster M (2007) Social cheating in Pseudomonas aeruginosa quorum sensing. Proc Natl Acad Sci USA 104:15876–15881

    Article  CAS  Google Scholar 

  • Schuster M, Lostroh CP, Ogi T, Greenberg EP (2003) Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J Bacteriol 185:2066–2079

    Article  CAS  Google Scholar 

  • Smith DR, Chapman MR (2010) Economical evolution: microbes reduce the synthetic cost of extracellular proteins. MBio 1:e00131–e210

    PubMed  PubMed Central  Google Scholar 

  • Smith EE, Buckley DG, Wu Z, Saenphimmachak C, Hoffman LR, D'Argenio DA et al (2006) Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci USA 103:8487–8492

    Article  CAS  Google Scholar 

  • Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR et al (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7:562–578

    Article  CAS  Google Scholar 

  • Wang L, Feng Z, Wang X, Zhang X (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26:136–138

    Article  Google Scholar 

  • Waters CM, Bassler BL (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319–346

    Article  CAS  Google Scholar 

  • Wilder CN, Diggle SP, Schuster M (2011) Cooperation and cheating in Pseudomonas aeruginosa: the roles of the las, rhl and pqs quorum-sensing systems. ISME J 5:1332–3143

    Article  CAS  Google Scholar 

  • Williams P, Cámara M (2009) Quorum sensing and environmental adaptation in Pseudomonas aeruginosa: a tale of regulatory networks and multifunctional signal molecules. Curr Opin Microbiol 12:182–191

    Article  CAS  Google Scholar 

  • Xavier JB, Kim W, Foster KR (2011) A molecular mechanism that stabilizes cooperative secretions in Pseudomonas aeruginosa. Mol Microbiol 79:166–179

    Article  CAS  Google Scholar 

  • Zhao K, Zhou X, Li W, Zhang X, Yue B (2016) Nutrient reduction induced stringent responses promote bacterial quorum-sensing divergence for population fitness. Sci Rep 6:34925

    Article  CAS  Google Scholar 

  • Zhao K, Du L, Lin J, Yuan Y, Wang X, Yue B et al (2018) Pseudomonas aeruginosa quorum-sensing and type VI secretion system can direct interspecific coexistence during evolution. Front Microbiol 9:2287

    Article  Google Scholar 

  • Zhao K, Liu L, Chen X, Huang T, Du L, Lin J et al (2019a) Behavioral heterogeneity in quorum sensing can stabilize social cooperation in microbial populations. BMC Biol 17:20

    Article  Google Scholar 

  • Zhao K, Li W, Li J, Ma T, Wang K, Yuan Y et al (2019b) TesG is a type I secretion effector of Pseudomonas aeruginosa that suppresses the host immune response during chronic infection. Nat Microbiol 4:459–469

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31700111), the Sichuan Science and Technology Program (2018HH0007), and the Science and Technology Bureau of Chengdu Municipal Government for “Collaboration and Innovation on New Antibiotic Development and Industrialization” (2016-XT00-00023-GX).

Author information

Authors and Affiliations

  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

    Kelei Zhao, Jing Li, Yang Yuan, Jiafu Lin, Xinrong Wang, Yidong Guo & Yiwen Chu

Authors
  1. Kelei Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jing Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yang Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jiafu Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xinrong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yidong Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yiwen Chu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Kelei Zhao or Yiwen Chu.

Ethics declarations

Conflict of interest

The authors declare that no competing financial interests exists.

Additional information

Communicated by Erko Stackebrandt.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhao, K., Li, J., Yuan, Y. et al. Nutrient factor-dependent performance of bacterial quorum sensing system during population evolution. Arch Microbiol 202, 2181–2188 (2020). https://doi.org/10.1007/s00203-020-01937-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-020-01937-5

Keywords

Search

Navigation