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Ecology drives the evolution of diverse social strategies in Pseudomonas aeruginosa.

ABSTRACT: Bacteria often cooperate by secreting molecules that can be shared as public goods between cells. Because the production of public goods is subject to cheating by mutants that exploit the good without contributing to it, there has been great interest in elucidating the evolutionary forces that maintain cooperation. However, little is known about how bacterial cooperation evolves under conditions where cheating is unlikely to be of importance. Here we use experimental evolution to follow changes in the production of a model public good, the iron-scavenging siderophore pyoverdine, of the bacterium Pseudomonas aeruginosa. After 1200 generations of evolution in nine different environments, we observed that cheaters only reached high frequency in liquid medium with low iron availability. Conversely, when adding iron to reduce the cost of producing pyoverdine, we observed selection for pyoverdine hyperproducers. Similarly, hyperproducers also spread in populations evolved in highly viscous media, where relatedness between interacting individuals is increased. Whole-genome sequencing of evolved clones revealed that hyperproduction is associated with mutations involving genes encoding quorum-sensing communication systems, while cheater clones had mutations in the iron-starvation sigma factor or in pyoverdine biosynthesis genes. Our findings demonstrate that bacterial social traits can evolve rapidly in divergent directions, with particularly strong selection for increased levels of cooperation occurring in environments where individual dispersal is reduced, as predicted by social evolution theory. Moreover, we establish a regulatory link between pyoverdine production and quorum-sensing, showing that increased cooperation with respect to one trait (pyoverdine) can be associated with the loss (quorum-sensing) of another social trait.

SUBMITTER: Figueiredo ART

PROVIDER: S-EPMC9291133 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:UnlabelledMicrobial population polymorphisms are commonly observed in natural environments, including long-term infected hosts. However, the underlying processes promoting and stabilizing diversity are difficult to unravel and are not well understood. Here, we use chronic infection of cystic fibrosis airways by the opportunistic pathogen Pseudomonas aeruginosa as a system for investigating bacterial diversification processes during the course of infection. We analyze clonal bacterial isolates sampled during a 32-year period and map temporal and spatial variations in population diversity to different infection sites within the infected host. We show that the ancestral infecting strain diverged into distinct sublineages, each with their own functional and genomic signatures and rates of adaptation, immediately after initial colonization. The sublineages coexisted in the host for decades, suggesting rapid evolution of stable population polymorphisms. Critically, the observed generation and maintenance of population diversity was the result of partitioning of the sublineages into physically separated niches in the CF airway. The results reveal a complex within-host population structure not previously realized and provide evidence that the heterogeneity of the highly structured and complex host environment promotes the evolution and long-term stability of pathogen population diversity during infection.ImportanceWithin-host pathogen evolution and diversification during the course of chronic infections is of importance in relation to therapeutic intervention strategies, yet our understanding of these processes is limited. Here, we investigate intraclonal population diversity in P. aeruginosa during chronic airway infections in cystic fibrosis patients. We show the evolution of a diverse population structure immediately after initial colonization, with divergence into multiple distinct sublineages that coexisted for decades and occupied distinct niches. Our results suggest that the spatial heterogeneity in CF airways plays a major role in relation to the generation and maintenance of population diversity and emphasize that a single isolate in sputum may not represent the entire pathogen population in the infected individual. A more complete understanding of the evolution of distinct clonal variants and their distribution in different niches could have positive implications for efficient therapy.

Project description:Vertebrates obtain social information about predation risk by eavesdropping on the alarm calls of sympatric species. In the Holarctic, birds in the family Paridae function as sentinel species; however, factors shaping eavesdroppers' reliance on their alarm calls are unknown. We compared three hypothesized drivers of eavesdropper reliance: (a) foraging ecology, (b) degree of sociality, and (c) call relevance (caller-to-eavesdropper body-size difference). In a rigorous causal-comparative design, we presented Tufted Titmouse (Baeolophus bicolor) alarm calls to 242 individuals of 31 ecologically diverse bird species in Florida forests and recorded presence/absence and type (diving for cover or freezing in place) of response. Playback response was near universal, as individuals responded to 87% of presentations (N = 211). As an exception to this trend, the sit-and-wait flycatcher Eastern Phoebe (Sayornis phoebe) represented 48% of the nonresponses. We tested 12 predictor variables representing measures relevant to the three hypothesized drivers, distance to playback speaker, and vulnerability at time of playback (eavesdropper's microhabitat when alarm call is detected). Using model-averaged generalized linear models, we determined that foraging ecology best predicted playback response, with aerial foragers responding less often. Foraging ecology (distance from trunk) and microhabitat occupied during playback (distance to escape cover) best predicted escape behavior type. We encountered a sparsity of sit-and-wait flycatchers (3 spp.), yet their contrasting responses relative to other foraging behaviors clearly identified foraging ecology as a driver of species-specific antipredator escape behavior. Our findings align well with known links between the exceptional visual acuity and other phenotypic traits of flycatchers that allow them to rely more heavily on personal rather than social information while foraging. Our results suggest that foraging ecology drives species-specific antipredator behavior based on the availability and type of escape cover.

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Ecology drives the evolution of diverse social strategies in Pseudomonas aeruginosa.

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