Interactions mediated by a public good transiently increase cooperativity in growing Pseudomonas putida metapopulations.
ABSTRACT: Bacterial communities have rich social lives. A well-established interaction involves the exchange of a public good in Pseudomonas populations, where the iron-scavenging compound pyoverdine, synthesized by some cells, is shared with the rest. Pyoverdine thus mediates interactions between producers and non-producers and can constitute a public good. This interaction is often used to test game theoretical predictions on the "social dilemma" of producers. Such an approach, however, underestimates the impact of specific properties of the public good, for example consequences of its accumulation in the environment. Here, we experimentally quantify costs and benefits of pyoverdine production in a specific environment, and build a model of population dynamics that explicitly accounts for the changing significance of accumulating pyoverdine as chemical mediator of social interactions. The model predicts that, in an ensemble of growing populations (metapopulation) with different initial producer fractions (and consequently pyoverdine contents), the global producer fraction initially increases. Because the benefit of pyoverdine declines at saturating concentrations, the increase need only be transient. Confirmed by experiments on metapopulations, our results show how a changing benefit of a public good can shape social interactions in a bacterial population.
Project description:Cooperation can be maintained if cooperative behaviours are preferentially directed towards other cooperative individuals. Tag-based cooperation (greenbeards) - where cooperation benefits individuals with the same tag as the actor - is one way to achieve this. Tag-based cooperation can be exploited by individuals who maintain the specific tag but do not cooperate, and selection to escape this exploitation can result in the evolution of tag diversity. We tested key predictions crucial for the evolution of cheat-mediated tag diversity using the production of iron-scavenging pyoverdine by the opportunistic pathogen, Pseduomonas aeruginosa as a model system. Using two strains that produce different pyoverdine types and their respective cheats, we show that cheats outcompete their homologous pyoverdine producer, but are outcompeted by the heterologous producer in well-mixed environments. As a consequence, co-inoculating two types of pyoverdine producer and one type of pyoverdine cheat resulted in the pyoverdine type whose cheat was not present having a large fitness advantage. Theory suggests that in such interactions, cheats can maintain tag diversity in spatially structured environments, but that tag-based cooperation will be lost in well-mixed populations, regardless of tag diversity. We saw that when all pyoverdine producers and cheats were co-inoculated in well-mixed environments, both types of pyoverdine producers were outcompeted, whereas spatial structure (agar plates and compost microcosms), rather than maintaining diversity, resulted in the domination of one pyoverdine producer. These results suggest cheats may play a more limited role in the evolution of pyoverdine diversity than predicted.
Project description:Many natural populations are spatially distributed, forming a network of subpopulations linked by migration. Migration patterns are often asymmetric and heterogeneous, with important consequences on the ecology and evolution of the species. Here we investigate experimentally how asymmetric migration and heterogeneous structure affect a simple metapopulation of budding yeast, formed by one strain that produces a public good and a non-producer strain that benefits from it. We study metapopulations with star topology and asymmetric migration, finding that all their subpopulations have a higher fraction of producers than isolated populations. Furthermore, the metapopulations have lower tolerance to challenging environments but higher resilience to transient perturbations. This apparent paradox occurs because tolerance to a constant challenge depends on the weakest subpopulations of the network, while resilience to a transient perturbation depends on the strongest ones.
Project description:Mobile genetic elements in bacteria are enriched in genes participating in social behaviors, suggesting an evolutionary link between gene mobility and social evolution. Cooperative behaviors, like the production of secreted public good molecules, are susceptible to the invasion of non-cooperative individuals, and their evolutionary maintenance requires mechanisms ensuring that benefits are directed preferentially to cooperators. In order to investigate the reasons for the mobility of public good genes, we designed a synthetic bacterial system where we control and quantify the transfer of public good production genes. In our recent study, we have experimentally shown that horizontal transfer helps maintain public good production in the face of both non-producer organisms and non-producer plasmids. Transfer spreads genes to neighboring cells, thus increasing relatedness and directing a higher proportion of public good benefits to producers. The effect is the strongest when public good genes undergo epidemics dynamics, making horizontal transfer especially relevant for pathogenic bacteria that repeatedly infect new hosts and base their virulence on costly public goods. The promotion of cooperation may be a general consequence of horizontal gene transfer in prokaryotes. Our work has an intriguing parallel, cultural transmission, where horizontal transfer, such as teaching, may preferentially promote cooperative behaviors.
Project description:The growth and virulence of bacteria depends upon a number of factors that are secreted into the environment. These factors can diffuse away from the producing cells, to be either lost or used by cells that do not produce them (cheats). Mechanisms that act to reduce the loss of secreted factors through diffusion are expected to be favoured. One such mechanism may be the production of Fap fibrils, needle-like fibres on the cell surface observed in P. aeruginosa, which can transiently bind several secreted metabolites produced by cells. We test whether Fap fibrils help retain a secreted factor, the iron-scavenging molecule pyoverdine, and hence reduce the potential for exploitation by non-producing, cheating cells. We found that: (i) wild-type cells retain more iron-chelating metabolites than fibril non-producers; (ii) purified Fap fibrils can prevent the loss of the iron-chelators PQS ( Pseudomonas quinolone signal) and pyoverdine; and (iii) pyoverdine non-producers have higher fitness in competition with fibril non-producers than with wild-type cells. Our results suggest that by limiting the loss of a costly public good, Fap fibrils may play an important role in stabilizing cooperative production of secreted factors.
Project description:Multi-agent models often describe populations segregated either in the physical space, i.e. subdivided in metapopulations, or in the ecology of opinions, i.e. partitioned in echo chambers. Here we show how both kinds of segregation can emerge from the interplay between homophily and social influence in a simple model of mobile agents endowed with a continuous opinion variable. In the model, physical proximity determines a progressive convergence of opinions but differing opinions result in agents moving away from each others. This feedback between mobility and social dynamics determines the onset of a stable dynamical metapopulation scenario where physically separated groups of like-minded individuals interact with each other through the exchange of agents. The further introduction of confirmation bias in social interactions, defined as the tendency of an individual to favor opinions that match his own, leads to the emergence of echo chambers where different opinions coexist also within the same group. We believe that the model may be of interest to researchers investigating the origin of segregation in the offline and online world.
Project description:Many organisms-notably microbes-are embedded within complex communities where cooperative behaviors in the form of excreted public goods can benefit other species. Under such circumstances, intraspecific interactions are likely to be less important in driving the evolution of cooperation. We first illustrate this idea with a simple theoretical model, showing that relatedness-the extent to which individuals with the same cooperative alleles interact with each other-has a reduced impact on the evolution of cooperation when public goods are shared between species. We test this empirically using strain of Pseudomonas aeruginosa that vary in their production of metal-chelating siderophores in copper contaminated compost (an interspecific public good). We show that nonsiderophore producers grow poorly relative to producers under high relatedness, but this cost can be alleviated by the presence of the isogenic producer (low relatedness) and/or the compost microbial community. Hence, relatedness can become unimportant when public goods provide interspecific benefits.
Project description:Bacteria secrete a variety of compounds important for nutrient scavenging, competition mediation and infection establishment. While there is a general consensus that secreted compounds can be shared and therefore have social consequences for the bacterial collective, we know little about the physical limits of such bacterial social interactions. Here, we address this issue by studying the sharing of iron-scavenging siderophores between surface-attached microcolonies of the bacterium Pseudomonas aeruginosa Using single-cell fluorescence microscopy, we show that siderophores, secreted by producers, quickly reach non-producers within a range of 100 µm, and significantly boost their fitness. Producers in turn respond to variation in sharing efficiency by adjusting their pyoverdine investment levels. These social effects wane with larger cell-to-cell distances and on hard surfaces. Thus, our findings reveal the boundaries of compound sharing, and show that sharing is particularly relevant between nearby yet physically separated bacteria on soft surfaces, matching realistic natural conditions such as those encountered in soft tissue infections.
Project description:The co-evolutionary dynamics of competing populations can be strongly affected by frequency-dependent selection and spatial population structure. As co-evolving populations grow into a spatial domain, their initial spatial arrangement and their growth rate differences are important factors that determine the long-term outcome. We here model producer and free-rider co-evolution in the context of a diffusive public good (PG) that is produced by the producers at a cost but evokes local concentration-dependent growth benefits to all. The benefit of the PG can be non-linearly dependent on public good concentration. We consider the spatial growth dynamics of producers and free-riders in one, two and three dimensions by modeling producer cell, free-rider cell and public good densities in space, driven by the processes of birth, death and diffusion (cell movement and public good distribution). Typically, one population goes extinct, but the time-scale of this process varies with initial conditions and the growth rate functions. We establish that spatial variation is transient regardless of dimensionality, and that structured initial conditions lead to increasing times to get close to an extinction state, called ?-extinction time. Further, we find that uncorrelated initial spatial structures do not influence this ?-extinction time in comparison to a corresponding well-mixed (non-spatial) system. In order to estimate the ?-extinction time of either free-riders or producers we derive a slow manifold solution. For invading populations, i.e. for populations that are initially highly segregated, we observe a traveling wave, whose speed can be calculated. Our results provide quantitative predictions for the transient spatial dynamics of cooperative traits under pressure of extinction.
Project description:The human intestine is colonized with trillions of microorganisms important to health and disease. There has been an intensive effort to catalog the species and genetic content of this microbial ecosystem. However, little is known of the ecological interactions between these microbes, a prerequisite to understanding the dynamics and stability of this host-associated microbial community. Here we perform a systematic investigation of public goods-based syntrophic interactions among the abundant human gut bacteria, the Bacteroidales.We find evidence for a rich interaction network based on the breakdown and use of polysaccharides. Species that utilize a particular polysaccharide (producers) liberate polysaccharide breakdown products (PBPs) that are consumed by other species unable to grow on the polysaccharide alone (recipients). Cross-species gene addition experiments demonstrate that recipients can grow on a polysaccharide if the producer-derived glycoside hydrolase, responsible for PBP generation, is provided. These producer-derived glycoside hydrolases are public goods transported extracellularly in outer membrane vesicles allowing for the creation of PBP and concomitant recipient growth spatially distant from the producer. Recipients can exploit these ecological interactions and conditionally outgrow producers. Finally, we show that these public goods-based interactions occur among Bacteroidales species coresident within a natural human intestinal community.This study examines public goods-based syntrophic interactions between bacterial members of the human gut microbial ecosystem. This polysaccharide-based network likely represents foundational relationships creating organized ecological units within the intestinal microbiota, knowledge of which can be applied to impact human health.
Project description:The maintenance of cooperation in populations where public goods are equally accessible to all but inflict a fitness cost on individual producers is a long-standing puzzle of evolutionary biology. An example of such a scenario is the secretion of siderophores by bacteria into their environment to fetch soluble iron. In a planktonic culture, these molecules diffuse rapidly, such that the same concentration is experienced by all bacteria. However, on solid substrates, bacteria form dense and packed colonies that may alter the diffusion dynamics through cell-cell contact interactions. In Pseudomonas aeruginosa microcolonies growing on solid substrate, we found that the concentration of pyoverdine, a secreted iron chelator, is heterogeneous, with a maximum at the center of the colony. We quantitatively explain the formation of this gradient by local exchange between contacting cells rather than by global diffusion of pyoverdine. In addition, we show that this local trafficking modulates the growth rate of individual cells. Taken together, these data provide a physical basis that explains the stability of public goods production in packed colonies.