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High local substrate availability stabilizes a cooperative trait.

Bachmann H, Molenaar D, Kleerebezem M, van Hylckama Vlieg JE - ISME J (2010)

Bottom Line: Cooperative behavior is widely spread in microbial populations.By using multiple experimental approaches, as well as modeling population dynamics, we demonstrate that the persistence of the proteolytic trait is determined by the fraction of the generated peptides that can be captured by the cell before diffusing away from it.The mechanism described is likely to be relevant for the evolutionary stability of many extracellular substrate-degrading enzymes.

View Article: PubMed Central - PubMed

Affiliation: NIZO Food Research, Health Department, Ede, The Netherlands.

ABSTRACT
Cooperative behavior is widely spread in microbial populations. An example is the expression of an extracellular protease by the lactic acid bacterium Lactococcus lactis, which degrades milk proteins into free utilizable peptides that are essential to allow growth to high cell densities in milk. Cheating, protease-negative strains can invade the population and drive the protease-positive strain to extinction. By using multiple experimental approaches, as well as modeling population dynamics, we demonstrate that the persistence of the proteolytic trait is determined by the fraction of the generated peptides that can be captured by the cell before diffusing away from it. The mechanism described is likely to be relevant for the evolutionary stability of many extracellular substrate-degrading enzymes.

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Related in: MedlinePlus

(a) Modeling population dynamics of prt+ and prt− mixed strain cultures. The heat map displays the fractional gain of the prt+ strain after one culturing step. The dependency of this fractional gain on the initial fraction of the prt+ cells in the culture (x axis) and the inoculation density in colony forming units (CFU) (y axis) is shown. With increasing inoculation densities and/or an increasing fraction of the prt+ strains in the culture, the overall advantage of the prt+ strain vanishes. Model and parameters are given in the supplementary information. (b) Relative fitness (y axis) of prt+ strains if propagated at different cell densities. Equal amounts of prt+ and prt− strains were inoculated in milk, and propagated for about 100 generations. The inoculation densities at each propagation event are indicated (x axis). For each condition, three biological replicates were propagated (o). Linear regression shows a highly significant correlation between the fitness of prt+ strains and the inoculation density (R2=0.91, P<0.0001). The prt+ strain could be stabilized in the culture when propagated at low cell densities (W∼1) and their abundance in the culture decreased when propagated at high cell densities (W<1).
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fig2: (a) Modeling population dynamics of prt+ and prt− mixed strain cultures. The heat map displays the fractional gain of the prt+ strain after one culturing step. The dependency of this fractional gain on the initial fraction of the prt+ cells in the culture (x axis) and the inoculation density in colony forming units (CFU) (y axis) is shown. With increasing inoculation densities and/or an increasing fraction of the prt+ strains in the culture, the overall advantage of the prt+ strain vanishes. Model and parameters are given in the supplementary information. (b) Relative fitness (y axis) of prt+ strains if propagated at different cell densities. Equal amounts of prt+ and prt− strains were inoculated in milk, and propagated for about 100 generations. The inoculation densities at each propagation event are indicated (x axis). For each condition, three biological replicates were propagated (o). Linear regression shows a highly significant correlation between the fitness of prt+ strains and the inoculation density (R2=0.91, P<0.0001). The prt+ strain could be stabilized in the culture when propagated at low cell densities (W∼1) and their abundance in the culture decreased when propagated at high cell densities (W<1).

Mentions: Population dynamics of the two competitors were described in a mathematical model, taking into account the influence of cell density and population composition on the growth rates of the two host strains in a mixed culture (Figure 2a and Supplementary Information). Model predictions were confirmed by serial dilution experiments of cultures propagated at different inoculation densities. The relative fitness of the prt+ strain was significantly increased when cells were propagated at low densities (Figure 2b). Although it would be desirable to observe the invasion of the prt+ strains from low frequencies in cultures propagated at low inoculation densities, such an analysis is complicated by the fact that wild-type protease carrying plasmids also harbor other functions such as peptide transporters (Siezen et al., 2005). The fact that the extracellular protease is usually plasmid encoded in lactococci is of interest in the light of a recent analysis, showing that cooperative traits are overrepresented on mobile genetic elements, and suggesting that horizontal gene transfer promotes cooperation (Nogueira et al., 2009).


High local substrate availability stabilizes a cooperative trait.

Bachmann H, Molenaar D, Kleerebezem M, van Hylckama Vlieg JE - ISME J (2010)

(a) Modeling population dynamics of prt+ and prt− mixed strain cultures. The heat map displays the fractional gain of the prt+ strain after one culturing step. The dependency of this fractional gain on the initial fraction of the prt+ cells in the culture (x axis) and the inoculation density in colony forming units (CFU) (y axis) is shown. With increasing inoculation densities and/or an increasing fraction of the prt+ strains in the culture, the overall advantage of the prt+ strain vanishes. Model and parameters are given in the supplementary information. (b) Relative fitness (y axis) of prt+ strains if propagated at different cell densities. Equal amounts of prt+ and prt− strains were inoculated in milk, and propagated for about 100 generations. The inoculation densities at each propagation event are indicated (x axis). For each condition, three biological replicates were propagated (o). Linear regression shows a highly significant correlation between the fitness of prt+ strains and the inoculation density (R2=0.91, P<0.0001). The prt+ strain could be stabilized in the culture when propagated at low cell densities (W∼1) and their abundance in the culture decreased when propagated at high cell densities (W<1).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3105769&req=5

fig2: (a) Modeling population dynamics of prt+ and prt− mixed strain cultures. The heat map displays the fractional gain of the prt+ strain after one culturing step. The dependency of this fractional gain on the initial fraction of the prt+ cells in the culture (x axis) and the inoculation density in colony forming units (CFU) (y axis) is shown. With increasing inoculation densities and/or an increasing fraction of the prt+ strains in the culture, the overall advantage of the prt+ strain vanishes. Model and parameters are given in the supplementary information. (b) Relative fitness (y axis) of prt+ strains if propagated at different cell densities. Equal amounts of prt+ and prt− strains were inoculated in milk, and propagated for about 100 generations. The inoculation densities at each propagation event are indicated (x axis). For each condition, three biological replicates were propagated (o). Linear regression shows a highly significant correlation between the fitness of prt+ strains and the inoculation density (R2=0.91, P<0.0001). The prt+ strain could be stabilized in the culture when propagated at low cell densities (W∼1) and their abundance in the culture decreased when propagated at high cell densities (W<1).
Mentions: Population dynamics of the two competitors were described in a mathematical model, taking into account the influence of cell density and population composition on the growth rates of the two host strains in a mixed culture (Figure 2a and Supplementary Information). Model predictions were confirmed by serial dilution experiments of cultures propagated at different inoculation densities. The relative fitness of the prt+ strain was significantly increased when cells were propagated at low densities (Figure 2b). Although it would be desirable to observe the invasion of the prt+ strains from low frequencies in cultures propagated at low inoculation densities, such an analysis is complicated by the fact that wild-type protease carrying plasmids also harbor other functions such as peptide transporters (Siezen et al., 2005). The fact that the extracellular protease is usually plasmid encoded in lactococci is of interest in the light of a recent analysis, showing that cooperative traits are overrepresented on mobile genetic elements, and suggesting that horizontal gene transfer promotes cooperation (Nogueira et al., 2009).

Bottom Line: Cooperative behavior is widely spread in microbial populations.By using multiple experimental approaches, as well as modeling population dynamics, we demonstrate that the persistence of the proteolytic trait is determined by the fraction of the generated peptides that can be captured by the cell before diffusing away from it.The mechanism described is likely to be relevant for the evolutionary stability of many extracellular substrate-degrading enzymes.

View Article: PubMed Central - PubMed

Affiliation: NIZO Food Research, Health Department, Ede, The Netherlands.

ABSTRACT
Cooperative behavior is widely spread in microbial populations. An example is the expression of an extracellular protease by the lactic acid bacterium Lactococcus lactis, which degrades milk proteins into free utilizable peptides that are essential to allow growth to high cell densities in milk. Cheating, protease-negative strains can invade the population and drive the protease-positive strain to extinction. By using multiple experimental approaches, as well as modeling population dynamics, we demonstrate that the persistence of the proteolytic trait is determined by the fraction of the generated peptides that can be captured by the cell before diffusing away from it. The mechanism described is likely to be relevant for the evolutionary stability of many extracellular substrate-degrading enzymes.

Show MeSH
Related in: MedlinePlus