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Eco-evolutionary feedbacks can rescue cooperation in microbial populations

View Article: PubMed Central - PubMed

ABSTRACT

Bacterial populations whose growth depends on the cooperative production of public goods are usually threatened by the rise of cheaters that do not contribute but just consume the common resource. Minimizing cheater invasions appears then as a necessary mechanism to maintain these populations. However, that invasions result instead in the persistence of cooperation is a prospect that has yet remained largely unexplored. Here, we show that the demographic collapse induced by cheaters in the population can actually contribute to the rescue of cooperation, in a clear illustration of how ecology and evolution can influence each other. The effect is made possible by the interplay between spatial constraints and the essentiality of the shared resource. We validate this result by carefully combining theory and experiments, with the engineering of a synthetic bacterial community in which the public compound allows survival to a lethal stress. The characterization of the experimental system identifies additional factors that can matter, like the impact of the lag phase on the tolerance to stress, or the appearance of spontaneous mutants. Our work explains the unanticipated dynamics that eco-evolutionary feedbacks can generate in microbial communities, feedbacks that reveal fundamental for the adaptive change of ecosystems at all scales.

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Influence of secondary effects on the maintenance of public good-based communities under antibiotic stress.(A) Cheater cells in exponential or saturating phase were resuspended in medium with gentamicin (Gm) (Materials and Methods). (Right) Cells in exponential phase experienced less antibiotic tolerance (Gm = 12 μg/ml, dots correspond to N = 45 replicas, box plots indicate associated statistical parameters). (Left) Concentration of quorum-sensing (QS) molecules decays as a function of time of growth (Byers et al.28) (Fig. S9), starting from an initial low-density of cooperators, i.e., “pop 2” density condition in Fig. 3. Bars represent measurement errors associated to QS estimation (Methods). Starting from these “pop 2” initial densities, and after an accumulation time of 15.5 hrs (T1), cells are in exponential phase, and the amount of QS is maximal. Recovery is thus strongly linked to the presence of the public good. (B,C) Emergence of spontaneous mutants to Gm. Initial populations of cooperators and cheaters are subjected to an accumulation and stress protocol under the “pop 1” and “pop 2” conditions (same as Fig. 3; black dots represent replicas, N = 45; box plots represent statistical parameters, color codes as Fig. 3). We repeated the experiment for each strain and dosage, so that one can quantify the typical resulting population, and also the mutant subpopulation (by plating with Gm and without no Gm antibiotic; the specific plating dosage corresponds to that of the matching growing conditions). Emergence of spontaneous mutants is reduced at higher dosage (C), i.e., “pop 2” conditions. Tolerance is most significantly associated in this regime to the presence of the public good.
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f4: Influence of secondary effects on the maintenance of public good-based communities under antibiotic stress.(A) Cheater cells in exponential or saturating phase were resuspended in medium with gentamicin (Gm) (Materials and Methods). (Right) Cells in exponential phase experienced less antibiotic tolerance (Gm = 12 μg/ml, dots correspond to N = 45 replicas, box plots indicate associated statistical parameters). (Left) Concentration of quorum-sensing (QS) molecules decays as a function of time of growth (Byers et al.28) (Fig. S9), starting from an initial low-density of cooperators, i.e., “pop 2” density condition in Fig. 3. Bars represent measurement errors associated to QS estimation (Methods). Starting from these “pop 2” initial densities, and after an accumulation time of 15.5 hrs (T1), cells are in exponential phase, and the amount of QS is maximal. Recovery is thus strongly linked to the presence of the public good. (B,C) Emergence of spontaneous mutants to Gm. Initial populations of cooperators and cheaters are subjected to an accumulation and stress protocol under the “pop 1” and “pop 2” conditions (same as Fig. 3; black dots represent replicas, N = 45; box plots represent statistical parameters, color codes as Fig. 3). We repeated the experiment for each strain and dosage, so that one can quantify the typical resulting population, and also the mutant subpopulation (by plating with Gm and without no Gm antibiotic; the specific plating dosage corresponds to that of the matching growing conditions). Emergence of spontaneous mutants is reduced at higher dosage (C), i.e., “pop 2” conditions. Tolerance is most significantly associated in this regime to the presence of the public good.

Mentions: We examined first the demographic collapse. Both the in silico model and the main attributes of the experimental system predict that a community with different frequency of cooperative and noncooperative strains would accumulate a distinct amount of public good, and thus present different tolerance to stress. To confirm this, we engineered an initial population with density ~104 cells/ml and different composition (Fig. S5), and distributed it as a metapopulation (SI Materials and Methods). Figure 3B confirms the demographic collapse of each well according to composition (left panel; associated inset illustrates the corresponding range of accumulation of QS molecules), while also illustrating the differential collapse of the whole population (right panel). The large initial density ensures homogeneity between the groups when distributed what de-emphasizes spatial effects. Some outliers here are associated to the emergence of spontaneous mutants, see Fig. 4. In this way, the behavior of the full population is equivalent to that of a single group, i.e., every group represents in practice a replica of the same conditions. Moreover, rising the strength of stress, i.e., essentiality of the public good, also impacts on collapse (Fig. 3C, fixed composition of 20% P but increasing antibiotic dosage). Note that the fraction of producers in the collected final populations does not vary substantially in this regime (Fig. S6).


Eco-evolutionary feedbacks can rescue cooperation in microbial populations
Influence of secondary effects on the maintenance of public good-based communities under antibiotic stress.(A) Cheater cells in exponential or saturating phase were resuspended in medium with gentamicin (Gm) (Materials and Methods). (Right) Cells in exponential phase experienced less antibiotic tolerance (Gm = 12 μg/ml, dots correspond to N = 45 replicas, box plots indicate associated statistical parameters). (Left) Concentration of quorum-sensing (QS) molecules decays as a function of time of growth (Byers et al.28) (Fig. S9), starting from an initial low-density of cooperators, i.e., “pop 2” density condition in Fig. 3. Bars represent measurement errors associated to QS estimation (Methods). Starting from these “pop 2” initial densities, and after an accumulation time of 15.5 hrs (T1), cells are in exponential phase, and the amount of QS is maximal. Recovery is thus strongly linked to the presence of the public good. (B,C) Emergence of spontaneous mutants to Gm. Initial populations of cooperators and cheaters are subjected to an accumulation and stress protocol under the “pop 1” and “pop 2” conditions (same as Fig. 3; black dots represent replicas, N = 45; box plots represent statistical parameters, color codes as Fig. 3). We repeated the experiment for each strain and dosage, so that one can quantify the typical resulting population, and also the mutant subpopulation (by plating with Gm and without no Gm antibiotic; the specific plating dosage corresponds to that of the matching growing conditions). Emergence of spontaneous mutants is reduced at higher dosage (C), i.e., “pop 2” conditions. Tolerance is most significantly associated in this regime to the presence of the public good.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC5304172&req=5

f4: Influence of secondary effects on the maintenance of public good-based communities under antibiotic stress.(A) Cheater cells in exponential or saturating phase were resuspended in medium with gentamicin (Gm) (Materials and Methods). (Right) Cells in exponential phase experienced less antibiotic tolerance (Gm = 12 μg/ml, dots correspond to N = 45 replicas, box plots indicate associated statistical parameters). (Left) Concentration of quorum-sensing (QS) molecules decays as a function of time of growth (Byers et al.28) (Fig. S9), starting from an initial low-density of cooperators, i.e., “pop 2” density condition in Fig. 3. Bars represent measurement errors associated to QS estimation (Methods). Starting from these “pop 2” initial densities, and after an accumulation time of 15.5 hrs (T1), cells are in exponential phase, and the amount of QS is maximal. Recovery is thus strongly linked to the presence of the public good. (B,C) Emergence of spontaneous mutants to Gm. Initial populations of cooperators and cheaters are subjected to an accumulation and stress protocol under the “pop 1” and “pop 2” conditions (same as Fig. 3; black dots represent replicas, N = 45; box plots represent statistical parameters, color codes as Fig. 3). We repeated the experiment for each strain and dosage, so that one can quantify the typical resulting population, and also the mutant subpopulation (by plating with Gm and without no Gm antibiotic; the specific plating dosage corresponds to that of the matching growing conditions). Emergence of spontaneous mutants is reduced at higher dosage (C), i.e., “pop 2” conditions. Tolerance is most significantly associated in this regime to the presence of the public good.
Mentions: We examined first the demographic collapse. Both the in silico model and the main attributes of the experimental system predict that a community with different frequency of cooperative and noncooperative strains would accumulate a distinct amount of public good, and thus present different tolerance to stress. To confirm this, we engineered an initial population with density ~104 cells/ml and different composition (Fig. S5), and distributed it as a metapopulation (SI Materials and Methods). Figure 3B confirms the demographic collapse of each well according to composition (left panel; associated inset illustrates the corresponding range of accumulation of QS molecules), while also illustrating the differential collapse of the whole population (right panel). The large initial density ensures homogeneity between the groups when distributed what de-emphasizes spatial effects. Some outliers here are associated to the emergence of spontaneous mutants, see Fig. 4. In this way, the behavior of the full population is equivalent to that of a single group, i.e., every group represents in practice a replica of the same conditions. Moreover, rising the strength of stress, i.e., essentiality of the public good, also impacts on collapse (Fig. 3C, fixed composition of 20% P but increasing antibiotic dosage). Note that the fraction of producers in the collected final populations does not vary substantially in this regime (Fig. S6).

View Article: PubMed Central - PubMed

ABSTRACT

Bacterial populations whose growth depends on the cooperative production of public goods are usually threatened by the rise of cheaters that do not contribute but just consume the common resource. Minimizing cheater invasions appears then as a necessary mechanism to maintain these populations. However, that invasions result instead in the persistence of cooperation is a prospect that has yet remained largely unexplored. Here, we show that the demographic collapse induced by cheaters in the population can actually contribute to the rescue of cooperation, in a clear illustration of how ecology and evolution can influence each other. The effect is made possible by the interplay between spatial constraints and the essentiality of the shared resource. We validate this result by carefully combining theory and experiments, with the engineering of a synthetic bacterial community in which the public compound allows survival to a lethal stress. The characterization of the experimental system identifies additional factors that can matter, like the impact of the lag phase on the tolerance to stress, or the appearance of spontaneous mutants. Our work explains the unanticipated dynamics that eco-evolutionary feedbacks can generate in microbial communities, feedbacks that reveal fundamental for the adaptive change of ecosystems at all scales.

No MeSH data available.


Related in: MedlinePlus