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The evolution of quorum sensing in bacterial biofilms.

Nadell CD, Xavier JB, Levin SA, Foster KR - PLoS Biol. (2008)

Bottom Line: The benefit of activating polymer secretion at high cell density is relatively straightforward: secretion starts upon biofilm formation, allowing strains to push their lineages into nutrient-rich areas and suffocate neighboring cells.We predict, therefore, that down-regulation of polymer secretion at high cell density will evolve when it can coincide with dispersal events, but it will be disfavored in long-lived (chronic) biofilms with sustained competition among strains.More generally, this work shows that the balance of competition within and among biofilms can be pivotal in the evolution of quorum sensing.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey, United States of America. cnadell@princeton.edu

ABSTRACT
Bacteria have fascinating and diverse social lives. They display coordinated group behaviors regulated by quorum-sensing systems that detect the density of other bacteria around them. A key example of such group behavior is biofilm formation, in which communities of cells attach to a surface and envelope themselves in secreted polymers. Curiously, after reaching high cell density, some bacterial species activate polymer secretion, whereas others terminate polymer secretion. Here, we investigate this striking variation in the first evolutionary model of quorum sensing in biofilms. We use detailed individual-based simulations to investigate evolutionary competitions between strains that differ in their polymer production and quorum-sensing phenotypes. The benefit of activating polymer secretion at high cell density is relatively straightforward: secretion starts upon biofilm formation, allowing strains to push their lineages into nutrient-rich areas and suffocate neighboring cells. But why use quorum sensing to terminate polymer secretion at high cell density? We find that deactivating polymer production in biofilms can yield an advantage by redirecting resources into growth, but that this advantage occurs only in a limited time window. We predict, therefore, that down-regulation of polymer secretion at high cell density will evolve when it can coincide with dispersal events, but it will be disfavored in long-lived (chronic) biofilms with sustained competition among strains. Our model suggests that the observed variation in quorum-sensing behavior can be linked to the differing requirements of bacteria in chronic versus acute biofilm infections. This is well illustrated by the case of Vibrio cholerae, which competes within biofilms by polymer secretion, terminates polymer secretion at high cell density, and induces an acute disease course that ends with mass dispersal from the host. More generally, this work shows that the balance of competition within and among biofilms can be pivotal in the evolution of quorum sensing.

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The Quorum-Sensing Strain Can Invade Non-Quorum-Sensing Strains, but Not Vice VersaInvasiveness of a rare mutant was analyzed for different degrees of mixing among strains in biofilms, reflected in the different initial frequencies of the rare strain in the biofilm. For example, if 10 strains are randomly sampled, then the initial frequency of the rare mutant in its own biofilm will be 0.1; initial relatedness will also be 0.1 (see main text). Each box and whisker plot summarizes the results of 20 replicate simulations, and plus signs (+) denote outliers. All simulations were carried out at α = 0.008 for the QS+ strain.(A) Invasion of a rare quorum-sensing strain (QS+) into a population of unconditional EPS producers (EPS+), and (B) failure of a rare EPS+ strain to invade a population of QS+ bacteria. Biofilms composed entirely of QS+ cells attain higher average fitness than biofilms composed entirely of EPS+ cells.(C) Invasion of a rare QS+ strain into a population of non-EPS producers (EPS−), and (D) failure of a rare EPS− strain to invade a population of QS+ bacteria. Again, the QS+ strain can invade EPS−, whereas EPS− cannot invade QS+. Notably, however, biofilms composed entirely of QS+ cells have a lower average fitness than biofilms composed entirely of EPS− cells. Therefore, if all biofilms contained only a single genotype (no within-biofilm evolutionary competition), the EPS− would invade and resist invasion.
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pbio-0060014-g003: The Quorum-Sensing Strain Can Invade Non-Quorum-Sensing Strains, but Not Vice VersaInvasiveness of a rare mutant was analyzed for different degrees of mixing among strains in biofilms, reflected in the different initial frequencies of the rare strain in the biofilm. For example, if 10 strains are randomly sampled, then the initial frequency of the rare mutant in its own biofilm will be 0.1; initial relatedness will also be 0.1 (see main text). Each box and whisker plot summarizes the results of 20 replicate simulations, and plus signs (+) denote outliers. All simulations were carried out at α = 0.008 for the QS+ strain.(A) Invasion of a rare quorum-sensing strain (QS+) into a population of unconditional EPS producers (EPS+), and (B) failure of a rare EPS+ strain to invade a population of QS+ bacteria. Biofilms composed entirely of QS+ cells attain higher average fitness than biofilms composed entirely of EPS+ cells.(C) Invasion of a rare QS+ strain into a population of non-EPS producers (EPS−), and (D) failure of a rare EPS− strain to invade a population of QS+ bacteria. Again, the QS+ strain can invade EPS−, whereas EPS− cannot invade QS+. Notably, however, biofilms composed entirely of QS+ cells have a lower average fitness than biofilms composed entirely of EPS− cells. Therefore, if all biofilms contained only a single genotype (no within-biofilm evolutionary competition), the EPS− would invade and resist invasion.

Mentions: We investigated whether a quorum-sensing strain that obtains an advantage in single biofilms (Figures 1 and 2) can invade a population of constitutive EPS producers and resist their reinvasion. We therefore focus on parameter values under which the QS+ strain has an advantage in the simple competition simulations. Specifically, we examine invasiveness for a disturbance interval of 9 d (tend = 9), with a QS+ strain α value (QS sensitivity) of 0.008, and we find that the QS+ strain can readily invade populations composed mostly of EPS+ cells, but not vice versa (Figure 3A and 3B). Additionally, biofilms composed entirely of QS+ cells have a higher average fitness than biofilms composed entirely of EPS+ cells.


The evolution of quorum sensing in bacterial biofilms.

Nadell CD, Xavier JB, Levin SA, Foster KR - PLoS Biol. (2008)

The Quorum-Sensing Strain Can Invade Non-Quorum-Sensing Strains, but Not Vice VersaInvasiveness of a rare mutant was analyzed for different degrees of mixing among strains in biofilms, reflected in the different initial frequencies of the rare strain in the biofilm. For example, if 10 strains are randomly sampled, then the initial frequency of the rare mutant in its own biofilm will be 0.1; initial relatedness will also be 0.1 (see main text). Each box and whisker plot summarizes the results of 20 replicate simulations, and plus signs (+) denote outliers. All simulations were carried out at α = 0.008 for the QS+ strain.(A) Invasion of a rare quorum-sensing strain (QS+) into a population of unconditional EPS producers (EPS+), and (B) failure of a rare EPS+ strain to invade a population of QS+ bacteria. Biofilms composed entirely of QS+ cells attain higher average fitness than biofilms composed entirely of EPS+ cells.(C) Invasion of a rare QS+ strain into a population of non-EPS producers (EPS−), and (D) failure of a rare EPS− strain to invade a population of QS+ bacteria. Again, the QS+ strain can invade EPS−, whereas EPS− cannot invade QS+. Notably, however, biofilms composed entirely of QS+ cells have a lower average fitness than biofilms composed entirely of EPS− cells. Therefore, if all biofilms contained only a single genotype (no within-biofilm evolutionary competition), the EPS− would invade and resist invasion.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2214811&req=5

pbio-0060014-g003: The Quorum-Sensing Strain Can Invade Non-Quorum-Sensing Strains, but Not Vice VersaInvasiveness of a rare mutant was analyzed for different degrees of mixing among strains in biofilms, reflected in the different initial frequencies of the rare strain in the biofilm. For example, if 10 strains are randomly sampled, then the initial frequency of the rare mutant in its own biofilm will be 0.1; initial relatedness will also be 0.1 (see main text). Each box and whisker plot summarizes the results of 20 replicate simulations, and plus signs (+) denote outliers. All simulations were carried out at α = 0.008 for the QS+ strain.(A) Invasion of a rare quorum-sensing strain (QS+) into a population of unconditional EPS producers (EPS+), and (B) failure of a rare EPS+ strain to invade a population of QS+ bacteria. Biofilms composed entirely of QS+ cells attain higher average fitness than biofilms composed entirely of EPS+ cells.(C) Invasion of a rare QS+ strain into a population of non-EPS producers (EPS−), and (D) failure of a rare EPS− strain to invade a population of QS+ bacteria. Again, the QS+ strain can invade EPS−, whereas EPS− cannot invade QS+. Notably, however, biofilms composed entirely of QS+ cells have a lower average fitness than biofilms composed entirely of EPS− cells. Therefore, if all biofilms contained only a single genotype (no within-biofilm evolutionary competition), the EPS− would invade and resist invasion.
Mentions: We investigated whether a quorum-sensing strain that obtains an advantage in single biofilms (Figures 1 and 2) can invade a population of constitutive EPS producers and resist their reinvasion. We therefore focus on parameter values under which the QS+ strain has an advantage in the simple competition simulations. Specifically, we examine invasiveness for a disturbance interval of 9 d (tend = 9), with a QS+ strain α value (QS sensitivity) of 0.008, and we find that the QS+ strain can readily invade populations composed mostly of EPS+ cells, but not vice versa (Figure 3A and 3B). Additionally, biofilms composed entirely of QS+ cells have a higher average fitness than biofilms composed entirely of EPS+ cells.

Bottom Line: The benefit of activating polymer secretion at high cell density is relatively straightforward: secretion starts upon biofilm formation, allowing strains to push their lineages into nutrient-rich areas and suffocate neighboring cells.We predict, therefore, that down-regulation of polymer secretion at high cell density will evolve when it can coincide with dispersal events, but it will be disfavored in long-lived (chronic) biofilms with sustained competition among strains.More generally, this work shows that the balance of competition within and among biofilms can be pivotal in the evolution of quorum sensing.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey, United States of America. cnadell@princeton.edu

ABSTRACT
Bacteria have fascinating and diverse social lives. They display coordinated group behaviors regulated by quorum-sensing systems that detect the density of other bacteria around them. A key example of such group behavior is biofilm formation, in which communities of cells attach to a surface and envelope themselves in secreted polymers. Curiously, after reaching high cell density, some bacterial species activate polymer secretion, whereas others terminate polymer secretion. Here, we investigate this striking variation in the first evolutionary model of quorum sensing in biofilms. We use detailed individual-based simulations to investigate evolutionary competitions between strains that differ in their polymer production and quorum-sensing phenotypes. The benefit of activating polymer secretion at high cell density is relatively straightforward: secretion starts upon biofilm formation, allowing strains to push their lineages into nutrient-rich areas and suffocate neighboring cells. But why use quorum sensing to terminate polymer secretion at high cell density? We find that deactivating polymer production in biofilms can yield an advantage by redirecting resources into growth, but that this advantage occurs only in a limited time window. We predict, therefore, that down-regulation of polymer secretion at high cell density will evolve when it can coincide with dispersal events, but it will be disfavored in long-lived (chronic) biofilms with sustained competition among strains. Our model suggests that the observed variation in quorum-sensing behavior can be linked to the differing requirements of bacteria in chronic versus acute biofilm infections. This is well illustrated by the case of Vibrio cholerae, which competes within biofilms by polymer secretion, terminates polymer secretion at high cell density, and induces an acute disease course that ends with mass dispersal from the host. More generally, this work shows that the balance of competition within and among biofilms can be pivotal in the evolution of quorum sensing.

Show MeSH
Related in: MedlinePlus