Quorum Sensing in Bacterial Biofilms: Regulating Matrix Production through Communication

Abstract

Bacteria grow on surfaces in complex communities known as biofilms. Biofilms are composed of cells embedded in extracellular matrix. Within biofilms, bacteria often communicate, cooperate, and compete within their own species and with other species using Quorum Sensing (QS). QS refers to the process by which bacteria produce, secrete, and subsequently detect small molecules called autoinducers (AIs) to assess the local population density of their species, or of other species. QS is known to regulate the production of extracellular matrix. We investigated the benefit of QS in regulating matrix production to gain access to a nutrient that diffuses from a source far from the biofilm. We employed Agent-Based Modeling (ABM), a simulation framework that allows cells to modify their behavior based on local inputs, e.g. nutrient and AI concentrations. We first determined the optimal fixed strategies (that do not use QS) for simulated pairwise competitions between strains, and identified the conditions that favor matrix production. To understand if QS can provide a competitive advantage, we modified our model to include QS with constitutive AI production. We demonstrated that simple QS-based strategies can be superior to any fixed strategy. However, we found that if AI production is not constitutive but rather depends on nutrient intake, then QS-based strategies fail to provide an advantage. We explain this failure of QS using analytic methods. We derive an expression for the biophysically limited dynamic range of AI concentration detection in nutrient limited environments. This expression implies that for QS to provide an advantage in biofilms, production of AI should be privileged and not limited by overall metabolic rates.