The Evolution of Quorum Sensing as a Mechanism to Infer Kinship

PLoS Comput Biol. 2016 Apr 27;12(4):e1004848. doi: 10.1371/journal.pcbi.1004848. eCollection 2016 Apr.

Abstract

Bacteria regulate many phenotypes via quorum sensing systems. Quorum sensing is typically thought to evolve because the regulated cooperative phenotypes are only beneficial at certain cell densities. However, quorum sensing systems are also threatened by non-cooperative "cheaters" that may exploit quorum-sensing regulated cooperation, which begs the question of how quorum sensing systems are maintained in nature. Here we study the evolution of quorum sensing using an individual-based model that captures the natural ecology and population structuring of microbial communities. We first recapitulate the two existing observations on quorum sensing evolution: density-dependent benefits favor quorum sensing but competition and cheating will destabilize it. We then model quorum sensing in a dense community like a biofilm, which reveals a novel benefit to quorum sensing that is intrinsically evolutionarily stable. In these communities, competing microbial genotypes gradually segregate over time leading to positive correlation between density and genetic similarity between neighboring cells (relatedness). This enables quorum sensing to track genetic relatedness and ensures that costly cooperative traits are only activated once a cell is safely surrounded by clonemates. We hypothesize that under similar natural conditions, the benefits of quorum sensing will not result from an assessment of density but from the ability to infer kinship.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacteria / genetics
  • Bacterial Physiological Phenomena
  • Biological Evolution*
  • Computer Simulation
  • Microbial Consortia / genetics
  • Microbial Consortia / physiology
  • Models, Biological
  • Quorum Sensing / genetics
  • Quorum Sensing / physiology*

Grant support

JS and KRF are supported by European Research Council Grant 242670 (http://erc.europa.eu/) and SM by a Marie Curie Intra-European Fellowship (http://www.fp7peoplenetwork.eu/marie-curie-actions/) and by an Ambizione fellowship from the Swiss National Science Foundation(http://www.snf.ch/en/funding/careers/ambizione/). JS was also supported by the EPSRC (http://www.epsrc.ac.uk/) through the DTC Systems Biology at the University of Oxford (http://www.sysbiodtc.ox.ac.uk/). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.