Differential signal sensitivities can contribute to the stability of multispecies bacterial communities

Abstract

Background: Bacterial species present in multispecies microbial communities often react to the same chemical signal but at vastly different concentrations. The existence of different response thresholds with respect to the same signal molecule has been well documented in quorum sensing which is one of the best studied inter-cellular signalling mechanisms in bacteria. The biological significance of this phenomenon is still poorly understood, and cannot be easily studied in nature or in laboratory models. The aim of this study is to establish the role of differential signal response thresholds in stabilizing microbial communities.

Results: We tested binary competition scenarios using an agent-based model in which competing bacteria had different response levels with respect to signals, cooperation factors or both, respectively. While in previous scenarios fitter species outcompete slower growing competitors, we found that stable equilibria could form if the fitter species responded to a higher chemical concentration level than the slower growing competitor. We also found that species secreting antibiotic could form a stable community with other competing species if antibiotic production started at higher response thresholds.

Conclusions: Microbial communities in nature rely on the stable coexistence of species that necessarily differ in their fitness. We found that differential response thresholds provide a simple and elegant way for keeping slower growing species within the community. High response thresholds can be considered as self-restraint of the fitter species that allows metabolically useful but slower growing species to remain within a community, and thereby the metabolic repertoire of the community will be maintained.

Reviewers: This article was reviewed by Michael Gromiha, Sebastian Maurer-Stroh, István Simon and L. Aravind.

Keywords: Agent-based modelling; Antibiotic production; Microbiome; Quorum sensing; Response threshold; Self-restraint; Swarming.

Fig. 1

Competition phenotypes of two species simulations. a There is no growth if species are unable to grow under the given conditions, e.g. they are incapable of quorum sensing; b stable coexistence of two different cell types; c exclusion of a less fit species by a fitter one; d collapse of a community. Blue lines indicate the cell numbers of the first (in case of b, c, d WT) species and the red lines the cell number of the other species as a function of time (in simulation steps). The small inserts show the population on the two dimensional longitudinal track in the time points indicated by the arrows. Blue and red dots represent the positions of agents from different species

Fig. 2

Competition between WT species 1 (blue) and species 2 with modified threshold values (red). a WT species 1 and higher signal threshold (T_S+) species 2, leads to exclusion of species 2; b WT species 1 and higher factor threshold (T_F+) species 2, leads to exclusion of species 2; c WT species 1 and higher signal and factor threshold (T_S+ T_F+) species 2, leads to exclusion of species 2; d WT species 1 and higher signal threshold and higher fitness (T_S+ T_D-) species 2, leads to coexistence of species 1 and species 2; e WT species 1 and higher factor threshold and higher fitness (T_F+ T_D-) species 2, leads to coexistence of species 1 and species 2; f WT species 1 and higher signal and factor threshold and higher fitness (T_S+ T_F+ T_D-) species 2, leads to coexistence of species 1 and species 2

Fig. 3

Competition between AB sensitive (ABS)(blue) and AB producing (ABP) (red) populations. Raising the response threshold (T_AB) of an antibiotic producing eavesdropping species leads to stable coexistence with the target ABS species (the members of which are activated at threshold T_R). a eavesdropping with equal signal thresholds, leads to exclusion of the eavesdropped species; b eavesdropping after raising the threshold of the eavesdropper for foreign signal leads to coexistence between the species