Cell-cell contacts confine public goods diffusion inside Pseudomonas aeruginosa clonal microcolonies.
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ABSTRACT:
SUBMITTER: Julou T
PROVIDER: S-EPMC3732961 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Cooperation in nature is ubiquitous, but is susceptible to social cheats who pay little or no cost of cooperation yet reap the benefits. The effect such cheats have on reducing population productivity suggests that there is selection for cooperators to mitigate the adverse effects of cheats. While mechanisms have been elucidated for scenarios involving a direct association between producer and cooperative product, it is less clear how cooperators may suppress cheating in an anonymous public goods scenario, where cheats cannot be directly identified. Here, we investigate the real-time evolutionary response of cooperators to cheats when cooperation is mediated by a diffusible public good: the production of iron-scavenging siderophores by Pseudomonas aeruginosa We find that siderophore producers evolved in the presence of a high frequency of non-producing cheats were fitter in the presence of cheats, at no obvious cost to population productivity. A novel morphotype independently evolved and reached higher frequencies in cheat-adapted versus control populations, exhibiting reduced siderophore production but increased production of pyocyanin-an extracellular toxin that can also increase the availability of soluble iron. This suggests that cooperators may have mitigated the negative effects of cheats by downregulating siderophore production and upregulating an alternative iron-acquisition public good. More generally, the study emphasizes that cooperating organisms can rapidly adapt to the presence of anonymous cheats without necessarily incurring fitness costs in the environment they evolve in.
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Project description:Quorum sensing in Pseudomonas aeruginosa controls the production of costly public goods such as exoproteases. This cooperative behavior is susceptible to social cheating by mutants that do not invest in the exoprotease production but assimilate the amino acids and peptides derived by the hydrolysis of proteins in the extracellular media. In sequential cultures with protein as the sole carbon source, these social cheaters are readily selected and often reach equilibrium with the exoprotease producers. Nevertheless, an excess of cheaters causes the collapse of population growth. In this work, using the reference strain PA14 and a clinical isolate from a burn patient, we demonstrate that the initial amount of public goods (exoprotease) that comes with the inoculum in each sequential culture is essential for maintaining population growth and that eliminating the exoprotease in the inoculum leads to rapid population collapse. Therefore, our results suggest that sequential washes should be combined with public good inhibitors to more effectively combat P. aeruginosa infections.
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Project description:Many bacteria possess cell density-dependent quorum-sensing (QS) systems that often regulate cooperative secretions involved in host-microbe or microbe-microbe interactions. These secretions, or "public goods," are frequently coregulated by stress and starvation responses. Here we provide a physiological rationale for such regulatory complexity in the opportunistic pathogen Pseudomonas aeruginosa. Using minimal-medium batch and chemostat cultures, we comprehensively characterized specific growth rate-limiting macronutrients as key triggers for the expression of extracellular enzymes and metabolites directly controlled by the las and rhl QS systems. Expression was unrelated to cell density, depended on the secreted product's elemental composition, and was induced only when the limiting nutrient was not also a building block of the product; rhl-dependent products showed the strongest response, caused by the largely las-independent induction of the regulator RhlR and its cognate signal. In agreement with the prominent role of the rhl system, slow growth inverted the las-to-rhl signal ratio, previously considered a characteristic distinguishing between planktonic and biofilm lifestyles. Our results highlight a supply-driven, metabolically prudent regulation of public goods that minimizes production costs and thereby helps stabilize cooperative behavior. Such regulation would be beneficial for QS-dependent public goods that act broadly and nonspecifically, and whose need cannot always be accurately assessed by the producing cell. Clear differences in the capacities of the las and rhl systems to integrate starvation signals help explain the existence of multiple QS systems in one cell.
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Project description:In most natural environments, bacteria live in polymicrobial communities where secreted molecules from neighboring species alter bacterial behaviors including motility, but such interactions are understudied. Pseudomonas aeruginosa is a motile opportunistic pathogen that exists in diverse multispecies environments such as the soil and is frequently found in human wound and respiratory tract co-infections with other bacteria including Staphylococcus aureus. Here we show that P. aeruginosa can co-opt secreted surfactants from other species for flagellar-based surface motility. We found that exogenous surfactants from S. aureus, other bacteria, and interkingdom species enabled P. aeruginosa to switch from swarming to an alternative surface spreading motility on semi-solid surfaces and allowed for the emergence of surface motility on hard agar where P. aeruginosa was otherwise unable to move. This motility was distinct from the response of other motile bacteria in the presence of exogenous surfactants. Mutant analysis indicated that this P. aeruginosa motility was similar to a previously described mucin-based motility, 'surfing', albeit with divergent regulation. Thus, our study demonstrates that secreted surfactants from the host as well as neighboring bacterial and interkingdom species act as public goods facilitating P. aeruginosa flagella-mediated surfing-like surface motility, thereby allowing it to access different environmental niches.
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Project description:Adaptation to public goods cheats in Pseudomonas aeruginosa
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Project description:Cancers are the result of eco-evolutionary processes fueled by heritable phenotypic diversification and driven by environmentally dependent selection. Space represents a key growth-limiting ecological resource, the ability to explore this resource is likely under strong selection. Using agent-based modeling, we explored the interplay between phenotypic strategies centered on gaining access to new space through cell-extrinsic degradation of extracellular matrix barriers and the exploitation of this resource through maximizing cell proliferation. While cell proliferation is a cell-intrinsic property, newly accessed space represents a public good, which can benefit both producers and non-producers. We found that this interplay results in ecological succession, enabling emergence of large, heterogeneous, and highly proliferative populations. Even though in our simulations both remodeling and proliferation strategies were under strong positive selection, their interplay led to sub-clonal architecture that could be interpreted as evidence for neutral evolution, warranting cautious interpretation of inferences from sequencing of cancer genomes.
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Project description:The production of costly public goods (as distinct from metabolic byproducts) has largely been understood through the realization that spatial structure can minimize losses to non-producing "cheaters" by allowing for the positive assortment of producers. In well-mixed systems, where positive assortment is not possible, the stable production of public goods has been proposed to depend on lineages that become indispensable as the sole producers of those goods while their neighbors lose production capacity through genome streamlining (the Black Queen Hypothesis). Here, we develop consumer-resource models motivated by nitrogen-fixing, siderophore-producing bacteria that consider the role of colimitation in shaping eco-evolutionary dynamics. Our models demonstrate that in well-mixed environments, single "public goods" can only be ecologically and evolutionarily stable if they are partially privatized (i.e., if producers reserve a portion of the product pool for private use). Colimitation introduces the possibility of subsidy: strains producing a fully public good can exclude non-producing strains so long as the producing strain derives sufficient benefit from the production of a second partially private good. We derive a lower bound for the degree of privatization necessary for production to be advantageous, which depends on external resource concentrations. Highly privatized, low-investment goods, in environments where the good is limiting, are especially likely to be stably produced. Coexistence emerges more rarely in our mechanistic model of the external environment than in past phenomenological approaches. Broadly, we show that the viability of production depends critically on the environmental context (i.e., external resource concentrations), with production of shared resources favored in environments where a partially-privatized resource is scarce.
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Project description:The emergence of cooperation is a central question in evolutionary biology. Microorganisms often cooperate by producing a chemical resource (a public good) that benefits other cells. The sharing of public goods depends on their diffusion through space. Previous theory suggests that spatial structure can promote evolution of cooperation, but the diffusion of public goods introduces new phenomena that must be modeled explicitly. We develop an approach where colony geometry and public good diffusion are described by graphs. We find that the success of cooperation depends on a simple relation between the benefits and costs of the public good, the amount retained by a producer, and the average amount retained by each of the producer's neighbors. These quantities are derived as analytic functions of the graph topology and diffusion rate. In general, cooperation is favored for small diffusion rates, low colony dimensionality, and small rates of decay of the public good. DOI: http://dx.doi.org/10.7554/eLife.01169.001.
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Project description:The production, consumption, and exploitation of common resources ranging from extracellular products in microorganisms to global issues of climate change refer to public goods interactions. Individuals can cooperate and sustain common resources at some cost or defect and exploit the resources without contributing. This generates a conflict of interest, which characterizes social dilemmas: Individual selection favors defectors, but for the community, it is best if everybody cooperates. Traditional models of public goods do not take into account that benefits of the common resource enable cooperators to maintain higher population densities. This leads to a natural feedback between population dynamics and interaction group sizes as captured by "ecological public goods." Here, we show that the spatial evolutionary dynamics of ecological public goods in "selection-diffusion" systems promotes cooperation based on different types of pattern formation processes. In spatial settings, individuals can migrate (diffuse) to populate new territories. Slow diffusion of cooperators fosters aggregation in highly productive patches (activation), whereas fast diffusion enables defectors to readily locate and exploit these patches (inhibition). These antagonistic forces promote coexistence of cooperators and defectors in static or dynamic patterns, including spatial chaos of ever-changing configurations. The local environment of cooperators and defectors is shaped by the production or consumption of common resources. Hence, diffusion-induced self-organization into spatial patterns not only enhances cooperation but also provides simple mechanisms for the spontaneous generation of habitat diversity, which denotes a crucial determinant of the viability of ecological systems.
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Project description:Voluntary participation in public goods games (PGGs) has turned out to be a simple but effective mechanism for promoting cooperation under full anonymity. Voluntary participation allows individuals to adopt a risk-aversion strategy, termed loner. A loner refuses to participate in unpromising public enterprises and instead relies on a small but fixed pay-off. This system leads to a cyclic dominance of three pure strategies, cooperators, defectors and loners, but at the same time, there remain two considerable restrictions: the addition of loners cannot stabilize the dynamics and the time average pay-off for each strategy remains equal to the pay-off of loners. Here, we introduce probabilistic participation in PGGs from the standpoint of diversification of risk, namely simple mixed strategies with loners, and prove the existence of a dynamical regime in which the restrictions ono longer hold. Considering two kinds of mixed strategies associated with participants (cooperators or defectors) and non-participants (loners), we can recover all basic evolutionary dynamics of the two strategies: dominance; coexistence; bistability; and neutrality, as special cases depending on pairs of probabilities. Of special interest is that the expected pay-off of each mixed strategy exceeds the pay-off of loners at some interior equilibrium in the coexistence region.
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