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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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Related in: MedlinePlus

Direct Competition between QS+ and EPS+ Bacteria Initialized with Equal Numbers of Both StrainsAutoinducer (AI) concentration is shown in the background, where isoconcentration lines represent 0.1-mg/l steps. Both strains behave identically, producing both EPS and biomass, until the autoinducer quorum-sensing threshold is reached. QS+ cells then turn off polymer secretion, devote all resources to biomass production, and achieve a growth burst at locations on the upper surface of the biofilm where substrate availability is highest. A movie for this simulation is provided as Video S1.
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pbio-0060014-g001: Direct Competition between QS+ and EPS+ Bacteria Initialized with Equal Numbers of Both StrainsAutoinducer (AI) concentration is shown in the background, where isoconcentration lines represent 0.1-mg/l steps. Both strains behave identically, producing both EPS and biomass, until the autoinducer quorum-sensing threshold is reached. QS+ cells then turn off polymer secretion, devote all resources to biomass production, and achieve a growth burst at locations on the upper surface of the biofilm where substrate availability is highest. A movie for this simulation is provided as Video S1.

Mentions: Simulations were parameterized with empirically estimated values (Table 3), initialized with 50 cells of each strain placed randomly on the solid substratum, and allowed to run for 14 simulated days (Figure 1), which is close to the maximum duration of a V. cholerae infection [49]. The proportion of energy invested in EPS secretion (f) will determine the extent to which EPS production allows one strain to displace others from a biofilm. As Xavier and Foster have discussed [36], for a given set of simulation parameters, there exists some evolutionarily stable strategy for EPS production, f*, which will out-compete any strain that invests either more or less in EPS. To find this optimum strategy, we performed an evolutionary stability analysis in which EPS+ strains with incrementally larger or smaller f values were competed against each other (see Text S1 and Figure S2). We found that, for our model conditions, the evolutionarily stable strategy for EPS investment independent of quorum sensing is approximately f* = 0.5, which was used for both the EPS+ and the QS+ strains (when below its quorum) in all subsequent simulations.


The evolution of quorum sensing in bacterial biofilms.

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

Direct Competition between QS+ and EPS+ Bacteria Initialized with Equal Numbers of Both StrainsAutoinducer (AI) concentration is shown in the background, where isoconcentration lines represent 0.1-mg/l steps. Both strains behave identically, producing both EPS and biomass, until the autoinducer quorum-sensing threshold is reached. QS+ cells then turn off polymer secretion, devote all resources to biomass production, and achieve a growth burst at locations on the upper surface of the biofilm where substrate availability is highest. A movie for this simulation is provided as Video S1.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2214811&req=5

pbio-0060014-g001: Direct Competition between QS+ and EPS+ Bacteria Initialized with Equal Numbers of Both StrainsAutoinducer (AI) concentration is shown in the background, where isoconcentration lines represent 0.1-mg/l steps. Both strains behave identically, producing both EPS and biomass, until the autoinducer quorum-sensing threshold is reached. QS+ cells then turn off polymer secretion, devote all resources to biomass production, and achieve a growth burst at locations on the upper surface of the biofilm where substrate availability is highest. A movie for this simulation is provided as Video S1.
Mentions: Simulations were parameterized with empirically estimated values (Table 3), initialized with 50 cells of each strain placed randomly on the solid substratum, and allowed to run for 14 simulated days (Figure 1), which is close to the maximum duration of a V. cholerae infection [49]. The proportion of energy invested in EPS secretion (f) will determine the extent to which EPS production allows one strain to displace others from a biofilm. As Xavier and Foster have discussed [36], for a given set of simulation parameters, there exists some evolutionarily stable strategy for EPS production, f*, which will out-compete any strain that invests either more or less in EPS. To find this optimum strategy, we performed an evolutionary stability analysis in which EPS+ strains with incrementally larger or smaller f values were competed against each other (see Text S1 and Figure S2). We found that, for our model conditions, the evolutionarily stable strategy for EPS investment independent of quorum sensing is approximately f* = 0.5, which was used for both the EPS+ and the QS+ strains (when below its quorum) in all subsequent simulations.

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