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Phenotypic heterogeneity is a selected trait in natural yeast populations subject to environmental stress.

Holland SL, Reader T, Dyer PS, Avery SV - Environ. Microbiol. (2013)

Bottom Line: We found that cell-to-cell heterogeneity (in resistance to the appropriate principal pollutant) was prevalent in the wild yeast isolates.Indeed, growth assays indicated that isolates with high heterogeneities had a significant competitive advantage during stress.The results showed that environmental stress selects for wild microorganisms with high levels of phenotypic heterogeneity.

View Article: PubMed Central - PubMed

Affiliation: School of Life Sciences, University of Nottingham, University Park, Nottingham, NG7 2RD, UK.

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Related in: MedlinePlus

Schematic showing how the selective pressure of stress favours heterogeneous organisms. Three example strains are illustrated, with the same mean resistances to a given stress (approximating to the peaks in the histograms) but with different heterogeneities (reflected by histogram width). In the low-heterogeneity strain, 12.5% of cells fall above the survival threshold at the indicated stressor dose, whereas the medium- and high-heterogeneity strains comprise 25% and 37.5% survivors at the same dose respectively. For clarity in this example, each round of stress application is followed by a recovery period (of three generations) during which resistant survivors re-seed heterogeneous populations. The scheme illustrates how each successive round of stress followed by recovery amplifies the relative numbers of cells in the more heterogeneous populations. This faster outgrowth of the heterogeneous strains is the same process that will favour any higher heterogeneity mutants that may spontaneously arise in the populations, ultimately leading to increased heterogeneity that is heritably stable.
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fig07: Schematic showing how the selective pressure of stress favours heterogeneous organisms. Three example strains are illustrated, with the same mean resistances to a given stress (approximating to the peaks in the histograms) but with different heterogeneities (reflected by histogram width). In the low-heterogeneity strain, 12.5% of cells fall above the survival threshold at the indicated stressor dose, whereas the medium- and high-heterogeneity strains comprise 25% and 37.5% survivors at the same dose respectively. For clarity in this example, each round of stress application is followed by a recovery period (of three generations) during which resistant survivors re-seed heterogeneous populations. The scheme illustrates how each successive round of stress followed by recovery amplifies the relative numbers of cells in the more heterogeneous populations. This faster outgrowth of the heterogeneous strains is the same process that will favour any higher heterogeneity mutants that may spontaneously arise in the populations, ultimately leading to increased heterogeneity that is heritably stable.

Mentions: As depicted in Fig. 7, the slight fitness advantage of heterogeneous organisms during stress, observed in this study with Pb stress, would be expected to cause high-heterogeneity organisms to outcompete low-heterogeneity organisms over a number of cell generations. Previous laboratory studies have yielded similar conclusions, particularly where the stress is fluctuating or intermittent (Thattai and van Oudenaarden, 2004; Acar et al., 2008; Gaal et al., 2010). By comparison, the pollutants at the various environmental sites sampled here might be thought to give more constant exposure. However, there would be intermittent dilution by rainfall, in addition to changes in direction and intensity of the wind (affecting SO2 deposition). In conjunction with fluctuations in pollutant discharges at the mine or coking-plant sources visited here, there will inevitably have been fluctuations in the intensity of stress to which the native yeast isolates were exposed. Even in the case of our evolution assays, the stress exerted by the Pb supplement would be expected to change during the course of each batch culture because of changes in cell density and parameters that affect metal bioavailability, such as pH and dissolved O2 (Hughes and Poole, 1991; Gadd, 1993). Our study harnesses fluctuations in environmental stress that are not directly controlled by a researcher but that occur naturally. Accordingly, it provides a realistic portrayal of the impact of heterogeneity as it applies to populations under natural conditions. It should be noted that heterogeneity can also be expected to provide some advantage where an environment becomes subject to more constant environmental stress (Fig. 7). It seems less likely that selection for heterogeneity would be greater than for mean stress resistance under such constant conditions, although we cannot discount that the trait of heterogeneity may offer a larger mutational target in cells, i.e. it could be ‘easier’ to evolve heterogeneity.


Phenotypic heterogeneity is a selected trait in natural yeast populations subject to environmental stress.

Holland SL, Reader T, Dyer PS, Avery SV - Environ. Microbiol. (2013)

Schematic showing how the selective pressure of stress favours heterogeneous organisms. Three example strains are illustrated, with the same mean resistances to a given stress (approximating to the peaks in the histograms) but with different heterogeneities (reflected by histogram width). In the low-heterogeneity strain, 12.5% of cells fall above the survival threshold at the indicated stressor dose, whereas the medium- and high-heterogeneity strains comprise 25% and 37.5% survivors at the same dose respectively. For clarity in this example, each round of stress application is followed by a recovery period (of three generations) during which resistant survivors re-seed heterogeneous populations. The scheme illustrates how each successive round of stress followed by recovery amplifies the relative numbers of cells in the more heterogeneous populations. This faster outgrowth of the heterogeneous strains is the same process that will favour any higher heterogeneity mutants that may spontaneously arise in the populations, ultimately leading to increased heterogeneity that is heritably stable.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4231229&req=5

fig07: Schematic showing how the selective pressure of stress favours heterogeneous organisms. Three example strains are illustrated, with the same mean resistances to a given stress (approximating to the peaks in the histograms) but with different heterogeneities (reflected by histogram width). In the low-heterogeneity strain, 12.5% of cells fall above the survival threshold at the indicated stressor dose, whereas the medium- and high-heterogeneity strains comprise 25% and 37.5% survivors at the same dose respectively. For clarity in this example, each round of stress application is followed by a recovery period (of three generations) during which resistant survivors re-seed heterogeneous populations. The scheme illustrates how each successive round of stress followed by recovery amplifies the relative numbers of cells in the more heterogeneous populations. This faster outgrowth of the heterogeneous strains is the same process that will favour any higher heterogeneity mutants that may spontaneously arise in the populations, ultimately leading to increased heterogeneity that is heritably stable.
Mentions: As depicted in Fig. 7, the slight fitness advantage of heterogeneous organisms during stress, observed in this study with Pb stress, would be expected to cause high-heterogeneity organisms to outcompete low-heterogeneity organisms over a number of cell generations. Previous laboratory studies have yielded similar conclusions, particularly where the stress is fluctuating or intermittent (Thattai and van Oudenaarden, 2004; Acar et al., 2008; Gaal et al., 2010). By comparison, the pollutants at the various environmental sites sampled here might be thought to give more constant exposure. However, there would be intermittent dilution by rainfall, in addition to changes in direction and intensity of the wind (affecting SO2 deposition). In conjunction with fluctuations in pollutant discharges at the mine or coking-plant sources visited here, there will inevitably have been fluctuations in the intensity of stress to which the native yeast isolates were exposed. Even in the case of our evolution assays, the stress exerted by the Pb supplement would be expected to change during the course of each batch culture because of changes in cell density and parameters that affect metal bioavailability, such as pH and dissolved O2 (Hughes and Poole, 1991; Gadd, 1993). Our study harnesses fluctuations in environmental stress that are not directly controlled by a researcher but that occur naturally. Accordingly, it provides a realistic portrayal of the impact of heterogeneity as it applies to populations under natural conditions. It should be noted that heterogeneity can also be expected to provide some advantage where an environment becomes subject to more constant environmental stress (Fig. 7). It seems less likely that selection for heterogeneity would be greater than for mean stress resistance under such constant conditions, although we cannot discount that the trait of heterogeneity may offer a larger mutational target in cells, i.e. it could be ‘easier’ to evolve heterogeneity.

Bottom Line: We found that cell-to-cell heterogeneity (in resistance to the appropriate principal pollutant) was prevalent in the wild yeast isolates.Indeed, growth assays indicated that isolates with high heterogeneities had a significant competitive advantage during stress.The results showed that environmental stress selects for wild microorganisms with high levels of phenotypic heterogeneity.

View Article: PubMed Central - PubMed

Affiliation: School of Life Sciences, University of Nottingham, University Park, Nottingham, NG7 2RD, UK.

Show MeSH
Related in: MedlinePlus