TY - JOUR
T1 - Adhesion as a weapon in microbial competition
AU - Schluter, Jonas
AU - Nadell, Carey D.
AU - Bassler, Bonnie Lynn
AU - Foster, Kevin R.
N1 - Publisher Copyright:
© 2015 International Society for Microbial Ecology All rights reserved.
PY - 2015/1/11
Y1 - 2015/1/11
N2 - Microbes attach to surfaces and form dense communities known as biofilms, which are central to how microbes live and influence humans. The key defining feature of biofilms is adhesion, whereby cells attach to one another and to surfaces, via attachment factors and extracellular polymers. While adhesion is known to be important for the initial stages of biofilm formation, its function within biofilm communities has not been studied. Here we utilise an individual-based model of microbial groups to study the evolution of adhesion. While adhering to a surface can enable cells to remain in a biofilm, consideration of within-biofilm competition reveals a potential cost to adhesion: immobility. Highly adhesive cells that are resistant to movement face being buried and starved at the base of the biofilm. However, we find that when growth occurs at the base of a biofilm, adhesion allows cells to capture substratum territory and force less adhesive, competing cells out of the system. This process may be particularly important when cells grow on a host epithelial surface. We test the predictions of our model using the enteric pathogen Vibrio cholerae, which produces an extracellular matrix important for biofilm formation. Flow cell experiments indicate that matrix-secreting cells are highly adhesive and form expanding clusters that remove non-secreting cells from the population, as predicted by our simulations. Our study shows how simple physical properties, such as adhesion, can be critical to understanding evolution and competition within microbial communities.
AB - Microbes attach to surfaces and form dense communities known as biofilms, which are central to how microbes live and influence humans. The key defining feature of biofilms is adhesion, whereby cells attach to one another and to surfaces, via attachment factors and extracellular polymers. While adhesion is known to be important for the initial stages of biofilm formation, its function within biofilm communities has not been studied. Here we utilise an individual-based model of microbial groups to study the evolution of adhesion. While adhering to a surface can enable cells to remain in a biofilm, consideration of within-biofilm competition reveals a potential cost to adhesion: immobility. Highly adhesive cells that are resistant to movement face being buried and starved at the base of the biofilm. However, we find that when growth occurs at the base of a biofilm, adhesion allows cells to capture substratum territory and force less adhesive, competing cells out of the system. This process may be particularly important when cells grow on a host epithelial surface. We test the predictions of our model using the enteric pathogen Vibrio cholerae, which produces an extracellular matrix important for biofilm formation. Flow cell experiments indicate that matrix-secreting cells are highly adhesive and form expanding clusters that remove non-secreting cells from the population, as predicted by our simulations. Our study shows how simple physical properties, such as adhesion, can be critical to understanding evolution and competition within microbial communities.
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U2 - 10.1038/ismej.2014.174
DO - 10.1038/ismej.2014.174
M3 - Article
C2 - 25290505
AN - SCOPUS:84927690116
SN - 1751-7362
VL - 9
SP - 139
EP - 149
JO - ISME Journal
JF - ISME Journal
IS - 1
ER -