A model for quorum-sensing mediated stochastic biofilm nucleation

Abstract

Surface-attached bacterial biofilms cause disease and industrial biofouling, as well as being widespread in the natural environment. Density-dependent quorum sensing is one of the mechanisms implicated in biofilm initiation. Here we present and analyse a model for quorum-sensing triggered biofilm initiation. In our model, individual, planktonic bacteria adhere to a surface, proliferate and undergo a collective transition to a biofilm phenotype. This model predicts a stochastic transition between a loosely attached, finite, layer of bacteria near the surface, and a growing biofilm. The transition is governed by two key parameters: the collective transition density relative to the carrying capacity, and the immigration rate relative to the detachment rate. Biofilm initiation is complex, but our model suggests that stochastic nucleation phenomena may be relevant.

A biophysical threshold for biofilm formation

“…That is, we expect the transition specified by the black curve in Figure 4A to be smeared out, similar to what is seen in Figure 4D , though due to a fundamentally different reason—with biofilm formation arising in some cases at lower than predicted by the black curve. Indeed, similar behavior was recently observed in a distinct model of biofilm formation on flat surfaces ( Sinclair et al, 2022 ). Exploring the influence of such variations by using a more probabilistic approach in our theoretical framework will thus be a useful direction for future research.…”

A computational model for microbial colonization of an antifouling surface

“…Density-dependent transition to the biofilm state A major assumption of our model is that the looselyattached community at the surface transitions to biofilm in a density-dependent manner. Following other modeling work (Moore-Ott et al, 2022;Sinclair et al, 2022), this represents a quorum-sensing mechanism, based on extensive evidence for the involvement of quorum-sensing in biofilm initiation in a variety of microorganisms (Davies et al, 1998;Hammer and Bassler, 2003;Yarwood et al, 2004;Koutsoudis et al, 2006). However, it is also clear that other, non-density-dependent signaling pathways, such as cyclic-di-GMP signaling, are also central in biofilm initiation (Valentini and Filloux, 2016).…”

“…In our model, microhabitats can be in one of two possible states: A “pre-biofilm”, in which microbes are loosely attached, with a low population density, and B “biofilm”, in which microbes are more strongly attached (Sinclair et al, 2022 ). A microhabitat transitions from state A to state B when its microbial population reaches a critical value N * .…”

“…When this happens, a new microhabitat (in state A) is created. This model mimics a quorum-sensing-mediated transition from planktonic to biofilm physiology (see Section 4, Moore-Ott et al, 2022 ; Sinclair et al, 2022 ). Our simulations are initialized with one microhabitat ( i = 0, L = 0) in state A, adjacent to the surface.…”

“…For some parameters, further explanation is given in Supplementary material . Importantly, our parameter set is in the “stochastic biofilm initiation regime” identified in previous work (Sinclair et al, 2022 ). This means that the predicted population size in the first microhabitat is below the biofilm threshold N * , even for a microbe that is fully biocide-resistant.…”