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Is bacterial persistence a social trait?

Gardner A, West SA, Griffin AS - PLoS ONE (2007)

Bottom Line: Persistence has a direct benefit to cells because it allows survival during catastrophes-a form of bet-hedging.However, persistence can also provide an indirect benefit to other individuals, because the reduced growth rate can reduce competition for limiting resources.More generally, our results clarify the links between persistence and other bet-hedging or social behaviours.

View Article: PubMed Central - PubMed

Affiliation: St John's College, Oxford University, Oxford, United Kingdom. andy.gardner@ed.ac.uk

ABSTRACT
The ability of bacteria to evolve resistance to antibiotics has been much reported in recent years. It is less well-known that within populations of bacteria there are cells which are resistant due to a non-inherited phenotypic switch to a slow-growing state. Although such 'persister' cells are receiving increasing attention, the evolutionary forces involved have been relatively ignored. Persistence has a direct benefit to cells because it allows survival during catastrophes-a form of bet-hedging. However, persistence can also provide an indirect benefit to other individuals, because the reduced growth rate can reduce competition for limiting resources. This raises the possibility that persistence is a social trait, which can be influenced by kin selection. We develop a theoretical model to investigate the social consequences of persistence. We predict that selection for persistence is increased when: (a) cells are related (e.g. a single, clonal lineage); and (b) resources are scarce. Our model allows us to predict how the level of persistence should vary with time, across populations, in response to intervention strategies and the level of competition. More generally, our results clarify the links between persistence and other bet-hedging or social behaviours.

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Related in: MedlinePlus

An illustration of the basic model, defining the three dimensionless model parameters (T, z0 and p0).Two lineages compete for resources during the growth interval before catastrophe occurs at time T. The initial size of the focal lineage is x0, expressed as a proportion of the total carrying capacity. The initial size of the total population is z0 = x0+y0, where y0 is the initial size of the competitor lineage. The initial frequency of the focal lineage is p0 = x0/z0. Persister cells are represented by the shaded areas, and non-persister cells are unshaded. Upon the catastrophe occurring, all persister cells survive and all non-persister cells are destroyed.
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pone-0000752-g001: An illustration of the basic model, defining the three dimensionless model parameters (T, z0 and p0).Two lineages compete for resources during the growth interval before catastrophe occurs at time T. The initial size of the focal lineage is x0, expressed as a proportion of the total carrying capacity. The initial size of the total population is z0 = x0+y0, where y0 is the initial size of the competitor lineage. The initial frequency of the focal lineage is p0 = x0/z0. Persister cells are represented by the shaded areas, and non-persister cells are unshaded. Upon the catastrophe occurring, all persister cells survive and all non-persister cells are destroyed.

Mentions: We consider a large metapopulation of bacteria structured into many separate patches (representing, for example, host individuals), and we investigate reproductive and survival success within a focal patch. Bacterial growth in the context of resource competition is captured by the standard logistic growth model, where the local population moves from exponential growth phase towards stationary phase as it increases in size and resources are exhausted (Figure 1). The model notation is summarized in Table 1. At any time t the local population size zt is expressed as a proportion of the patch carrying capacity, and the initial size of the population (z0, at time t = 0) provides the first parameter for our model. The local population comprises two lineages, X and Y, and the size of the lineages are denoted xt and yt, such that xt+yt = zt. It is helpful to denote the proportion of the population that belongs to lineage X as pt = xt/zt, and the initial proportion (p0, at time t = 0) provides the second parameter of the model.


Is bacterial persistence a social trait?

Gardner A, West SA, Griffin AS - PLoS ONE (2007)

An illustration of the basic model, defining the three dimensionless model parameters (T, z0 and p0).Two lineages compete for resources during the growth interval before catastrophe occurs at time T. The initial size of the focal lineage is x0, expressed as a proportion of the total carrying capacity. The initial size of the total population is z0 = x0+y0, where y0 is the initial size of the competitor lineage. The initial frequency of the focal lineage is p0 = x0/z0. Persister cells are represented by the shaded areas, and non-persister cells are unshaded. Upon the catastrophe occurring, all persister cells survive and all non-persister cells are destroyed.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC1937027&req=5

pone-0000752-g001: An illustration of the basic model, defining the three dimensionless model parameters (T, z0 and p0).Two lineages compete for resources during the growth interval before catastrophe occurs at time T. The initial size of the focal lineage is x0, expressed as a proportion of the total carrying capacity. The initial size of the total population is z0 = x0+y0, where y0 is the initial size of the competitor lineage. The initial frequency of the focal lineage is p0 = x0/z0. Persister cells are represented by the shaded areas, and non-persister cells are unshaded. Upon the catastrophe occurring, all persister cells survive and all non-persister cells are destroyed.
Mentions: We consider a large metapopulation of bacteria structured into many separate patches (representing, for example, host individuals), and we investigate reproductive and survival success within a focal patch. Bacterial growth in the context of resource competition is captured by the standard logistic growth model, where the local population moves from exponential growth phase towards stationary phase as it increases in size and resources are exhausted (Figure 1). The model notation is summarized in Table 1. At any time t the local population size zt is expressed as a proportion of the patch carrying capacity, and the initial size of the population (z0, at time t = 0) provides the first parameter for our model. The local population comprises two lineages, X and Y, and the size of the lineages are denoted xt and yt, such that xt+yt = zt. It is helpful to denote the proportion of the population that belongs to lineage X as pt = xt/zt, and the initial proportion (p0, at time t = 0) provides the second parameter of the model.

Bottom Line: Persistence has a direct benefit to cells because it allows survival during catastrophes-a form of bet-hedging.However, persistence can also provide an indirect benefit to other individuals, because the reduced growth rate can reduce competition for limiting resources.More generally, our results clarify the links between persistence and other bet-hedging or social behaviours.

View Article: PubMed Central - PubMed

Affiliation: St John's College, Oxford University, Oxford, United Kingdom. andy.gardner@ed.ac.uk

ABSTRACT
The ability of bacteria to evolve resistance to antibiotics has been much reported in recent years. It is less well-known that within populations of bacteria there are cells which are resistant due to a non-inherited phenotypic switch to a slow-growing state. Although such 'persister' cells are receiving increasing attention, the evolutionary forces involved have been relatively ignored. Persistence has a direct benefit to cells because it allows survival during catastrophes-a form of bet-hedging. However, persistence can also provide an indirect benefit to other individuals, because the reduced growth rate can reduce competition for limiting resources. This raises the possibility that persistence is a social trait, which can be influenced by kin selection. We develop a theoretical model to investigate the social consequences of persistence. We predict that selection for persistence is increased when: (a) cells are related (e.g. a single, clonal lineage); and (b) resources are scarce. Our model allows us to predict how the level of persistence should vary with time, across populations, in response to intervention strategies and the level of competition. More generally, our results clarify the links between persistence and other bet-hedging or social behaviours.

Show MeSH
Related in: MedlinePlus