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ISME J. 2018 Oct;12(10):2363-2375. doi: 10.1038/s41396-018-0178-x. Epub 2018 Jun 13.

Eavesdropping and crosstalk between secreted quorum sensing peptide signals that regulate bacteriocin production in Streptococcus pneumoniae.

Author information

1
School of Biological Science, Faculty of Biology, Medicine, and Health, Manchester Academic Health Science Centre, University of Manchester, Manchester, M13 9PL, UK.
2
Institute of Biology Leiden, Leiden University, Leiden, 2333 BE, The Netherlands.
3
Molecular Genetics Group, Groningen Biomolecular Sciences and Biotechnology Institute, Centre for Synthetic Biology, University of Groningen, Groningen, 9700 AE, The Netherlands.
4
Faculty of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, 1432, Ås, Norway.
5
Wellcome Trust Sanger Institute, Genome Campus, Cambridge, CB10 1SA, UK.
6
Faculty of Medicine, School of Public Health, Imperial College, London, W2 1PG, UK.
7
School of Biological Science, Faculty of Biology, Medicine, and Health, Manchester Academic Health Science Centre, University of Manchester, Manchester, M13 9PL, UK. i.s.roberts@manchester.ac.uk.
8
Molecular Genetics Group, Groningen Biomolecular Sciences and Biotechnology Institute, Centre for Synthetic Biology, University of Groningen, Groningen, 9700 AE, The Netherlands. Jan-Willem.Veening@unil.ch.
9
Department of Fundamental Microbiology, Faculty of Biology and Medicine, University of Lausanne, Biophore Building, 1015, Lausanne, Switzerland. Jan-Willem.Veening@unil.ch.
10
Institute of Biology Leiden, Leiden University, Leiden, 2333 BE, The Netherlands. d.e.rozen@biology.leidenuniv.nl.

Abstract

Quorum sensing (QS), where bacteria secrete and respond to chemical signals to coordinate population-wide behaviors, has revealed that bacteria are highly social. Here, we investigate how diversity in QS signals and receptors can modify social interactions controlled by the QS system regulating bacteriocin secretion in Streptococcus pneumoniae, encoded by the blp operon (bacteriocin-like peptide). Analysis of 4096 pneumococcal genomes detected nine blp QS signals (BlpC) and five QS receptor groups (BlpH). Imperfect concordance between signals and receptors suggested widespread social interactions between cells, specifically eavesdropping (where cells respond to signals that they do not produce) and crosstalk (where cells produce signals that non-clones detect). This was confirmed in vitro by measuring the response of reporter strains containing six different blp QS receptors to cognate and non-cognate peptides. Assays between pneumococcal colonies grown adjacent to one another provided further evidence that crosstalk and eavesdropping occur at endogenous levels of signal secretion. Finally, simulations of QS strains producing bacteriocins revealed that eavesdropping can be evolutionarily beneficial even when the affinity for non-cognate signals is very weak. Our results highlight that social interactions can mediate intraspecific competition among bacteria and reveal that competitive interactions can be modified by polymorphic QS systems.

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