Differential signal sensitivities can contribute to the stability of multispecies bacterial communities
Juhász et al. Biology Direct
Differential signal sensitivities can contribute to the stability of multispecies bacterial communities
János Juhász 0 3
Dóra Bihary 0 2 3
Attila Jády 0 3
Sándor Pongor 0 3
Balázs Ligeti 0 1 3
0 Faculty of Information Technology and Bionics, Pázmány Péter Catholic University , Práter Street 50/A, Budapest H-1085 , Hungary
1 Institute of Medical Microbiology, Semmelweis University , Nagyvárad square 4, Budapest H-1089 , Hungary
2 Present address: RC Cancer Unit, Hutchison/MRC Research Centre, University of Cambridge , Hills Road, Cambridge CB2 0XZ , UK
3 Faculty of Information Technology and Bionics, Pázmány Péter Catholic University , Práter Street 50/A, Budapest H-1085 , Hungary
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.
Microbiome; Quorum sensing; Swarming; Self-restraint; Response threshold; Antibiotic production; Agent-based modelling
Background
Bacteria are the most widespread life forms on Earth that
populate every habitat, including the surfaces of the
human body. [
1–3
]. In most cases bacterial cells live in large
multispecies communities in which they compete for
nutrients and space, but at the same time they also cooperate
with each other via chemical materials secreted into the
environment. One well-studied mechanism whereby
bacterial cells can communicate and cooperate with each
other is quorum sensing (QS) [
4, 5
]. QS is based on the
ability of cells to respond to a chemical signal that they
themselves release into the environment. As the
environmental concentration of the signal will be higher if many
similar cells are present, this simple mechanism allows
cells to indirectly sense population density. In this manner
a population can turn on and off metabolic functions in a
synchronized manner, which enables it to solve problems
that individual cells cannot tackle, such as colonizing
habitats, infecting host organisms etc.
One of the simplest QS systems is the N-acyl
homoserine lactone (AHL) based communication present in Gram
negative bacteria [
6
]. In a typical case, such as present in
Pseudomonas aeruginosa, cells constantly produce a low
level of AHL [
7, 8
]. Just to take a simple hypothetical
example, if the extracellular AHL concentration exceeds a
threshold level, cells turn on the metabolically expensive
production of an enzyme. When the enzyme
concentration reaches a critical level, it will digest protein nutrients
present in the environment, and the liberated amino acids
will allow cells to upgrade their metabolic activities. In
reality, there are over 70 AHL molecular signals known in
various Gram negative bacteria [9], and a typical
bacterium has several QS systems [
10–12
], which makes the
experimental study of QS quite difficult. Also, not only
enzyme production but a large variety of metabolic or
regulatory functions can be activated by QS [
5, 11
], so
general conclusions cannot be easily reached from the
study of individual species.
It is a well-known property of AHL signalling that
bacterial species often react to various chemical signals
emitted by other bacterial species [
13
]. From the protein
structural point of view thi (...truncated)