The social biology of quorum sensing in a naturalistic host pathogen system
- PMID: 25308072
- DOI: 10.1016/j.cub.2014.08.049
The social biology of quorum sensing in a naturalistic host pathogen system
Abstract
Many microorganisms cooperate by secreting products that are commonly available to neighboring cells. These "public goods" include autoinduced, quorum-sensing (QS) molecules and the virulence factors activated by these signals. Public goods cooperation is exploitable by cheaters, cells that avoid the costs of production but gain an advantage by freeloading on the products of others. QS signals and responses can be cooperative under artificial laboratory conditions, but it remains unclear whether QS is cooperative in nature: little is known about the frequency of cheaters in natural populations, and cheaters may do poorly because of the importance of QS in major transcriptional networks. Here, we investigate the cooperative nature of QS in a natural system: the Gram-positive insect pathogen Bacillus thuringiensis and the larvae of the diamondback moth, Plutella xylostella. Although we find evidence of cooperation, QS null mutants are not effective cheats in vivo and cannot outcompete wild-type strains. We show that spatial structure limits mutant fitness and that well-separated microcolonies occur in vivo because of the strong population bottlenecks occurring during natural infection. We argue that spatial structure and low densities are the norm in early-stage infections, and this can explain why QS cheaters are rare in B. thuringiensis and its relatives. These results contrast with earlier experiments describing the high fitness of Gram-negative QS cheaters and suggest that QS suppression ("quorum quenching") can be clinically effective without having negative impacts on the evolution of virulence.
Copyright © 2014 The Authors. Published by Elsevier Inc. All rights reserved.
Similar articles
-
Optimal Response to Quorum-Sensing Signals Varies in Different Host Environments with Different Pathogen Group Size.mBio. 2020 Jun 2;11(3):e00535-20. doi: 10.1128/mBio.00535-20. mBio. 2020. PMID: 32487754 Free PMC article.
-
Cooperation, quorum sensing, and evolution of virulence in Staphylococcus aureus.Infect Immun. 2014 Mar;82(3):1045-51. doi: 10.1128/IAI.01216-13. Epub 2013 Dec 16. Infect Immun. 2014. PMID: 24343650 Free PMC article.
-
The Fitness of Pseudomonas aeruginosa Quorum Sensing Signal Cheats Is Influenced by the Diffusivity of the Environment.mBio. 2017 May 2;8(3):e00353-17. doi: 10.1128/mBio.00353-17. mBio. 2017. PMID: 28465424 Free PMC article.
-
Janus-headed communication promotes bacterial cooperation and cheating: is quorum sensing useful against infections?Virulence. 2010 Sep-Oct;1(5):402-3. doi: 10.4161/viru.1.5.12549. Virulence. 2010. PMID: 21178478 Review.
-
Cooperation and the evolutionary ecology of bacterial virulence: the Bacillus cereus group as a novel study system.Bioessays. 2013 Aug;35(8):706-16. doi: 10.1002/bies.201300028. Epub 2013 May 23. Bioessays. 2013. PMID: 23702950 Review.
Cited by
-
Bacterial-excreted small volatile molecule 2-aminoacetophenone induces oxidative stress and apoptosis in murine skeletal muscle.Int J Mol Med. 2016 Apr;37(4):867-78. doi: 10.3892/ijmm.2016.2487. Epub 2016 Feb 12. Int J Mol Med. 2016. PMID: 26935176 Free PMC article.
-
Bacillus thuringiensis Spores and Vegetative Bacteria: Infection Capacity and Role of the Virulence Regulon PlcR Following Intrahaemocoel Injection of Galleria mellonella.Insects. 2019 May 5;10(5):129. doi: 10.3390/insects10050129. Insects. 2019. PMID: 31060274 Free PMC article.
-
Facultative cheating supports the coexistence of diverse quorum-sensing alleles.Proc Natl Acad Sci U S A. 2016 Feb 23;113(8):2152-7. doi: 10.1073/pnas.1520615113. Epub 2016 Jan 19. Proc Natl Acad Sci U S A. 2016. PMID: 26787913 Free PMC article.
-
A common evolutionary pathway for maintaining quorum sensing in Pseudomonas aeruginosa.J Microbiol. 2018 Feb;56(2):83-89. doi: 10.1007/s12275-018-7286-1. Epub 2018 Feb 2. J Microbiol. 2018. PMID: 29392560
-
Bacterial Cooperation Causes Systematic Errors in Pathogen Risk Assessment due to the Failure of the Independent Action Hypothesis.PLoS Pathog. 2015 Apr 24;11(4):e1004775. doi: 10.1371/journal.ppat.1004775. eCollection 2015 Apr. PLoS Pathog. 2015. PMID: 25909384 Free PMC article.
Publication types
MeSH terms
LinkOut - more resources
Full Text Sources
Other Literature Sources