4.8 Article

A biophysical limit for quorum sensing in biofilms

Publisher

NATL ACAD SCIENCES
DOI: 10.1073/pnas.2022818118

Keywords

quorum sensing; biofilms; agent-based modeling; nutrient-limited communication

Funding

  1. Princeton University Physics Department, Office of the Dean of Research at Princeton University
  2. University of California San Diego (UCSD) Physics Department
  3. NIH [R01-GM082938]
  4. qBio program at UCSD
  5. NSF, through the Center for the Physics of Biological Function [PHY1734030]

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Bacteria form complex immobile communities called biofilms, where they interact and compete via quorum sensing (QS) by producing and detecting small molecules called autoinducers (AIs). A study explored the competitive advantage of QS in biofilms and found that the effectiveness of QS strategies is influenced by nutrient availability and the dynamic range of AI concentrations in biofilms is limited by biophysical constraints.
Bacteria grow on surfaces in complex immobile communities known as biofilms, which are composed of cells embedded in an extracellular matrix. Within biofilms, bacteria often interact with members of their own species and cooperate or compete with members of other species via quorum sensing (QS). QS is a process by which microbes produce, secrete, and subsequently detect small molecules called autoinducers (AIs) to assess their local population density. We explore the competitive advantage of QS through agent-based simulations of a spatial model in which colony expansion via extracellular matrix production provides greater access to a limiting diffusible nutrient. We note a significant difference in results based on whether AI production is constitutive or limited by nutrient availability: If AI production is constitutive, simple QS-based matrix-production strategies can be far superior to any fixed strategy. However, if AI production is limited by nutrient availability, QS-based strategies fail to provide a significant advantage over fixed strategies. To explain this dichotomy, we derive a biophysical limit for the dynamic range of nutrient-limited AI concentrations in biofilms. This range is remarkably small (less than 10-fold) for the realistic case in which a growth-limiting diffusible nutrient is taken up within a narrow active growth layer. This biophysical limit implies that for QS to be most effective in biofilms AI production should be a protected function not directly tied to metabolism.

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