Co‐evolutionary dynamics between public good producers and cheats in the bacterium Pseudomonas aeruginosa

Abstract

The production of beneficial public goods is common in the microbial world, and so is cheating -the exploitation of public goods by nonproducing mutants. Here, we examine co-evolutionary dynamics between cooperators and cheats and ask whether cooperators can evolve strategies to reduce the burden of exploitation, and whether cheats in turn can improve their exploitation abilities. We evolved cooperators of the bacterium Pseudomonas aeruginosa, producing the shareable iron-scavenging siderophore pyoverdine, together with cheats, defective in pyoverdine production but proficient in uptake. We found that cooperators managed to co-exist with cheats in 56% of all replicates over approximately 150 generations of experimental evolution. Growth and competition assays revealed that co-existence was fostered by a combination of general adaptions to the media and specific adaptions to the co-evolving opponent. Phenotypic screening and whole-genome resequencing of evolved clones confirmed this pattern, and suggest that cooperators became less exploitable by cheats because they significantly reduced their pyoverdine investment. Cheats, meanwhile, improved exploitation efficiency through mutations blocking the costly pyoverdine-signalling pathway. Moreover, cooperators and cheats evolved reduced motility, a pattern that likely represents adaptation to laboratory conditions, but at the same time also affects social interactions by reducing strain mixing and pyoverdine sharing. Overall, we observed parallel evolution, where co-existence of cooperators and cheats was enabled by a combination of adaptations to the abiotic and social environment and their interactions.

A single mutation in rapP induces cheating to prevent cheating in Bacillus subtilis by minimizing public good production

“…However, those strategies, all described in P. aeruginosa and many resulting from experimental evolution rather than naturally occurring mechanisms, are either based on stopping production when it is not needed 16,18 or being willing to reduce the benefit gained from cooperation by down-regulating production when it could be needed 17,19–21 , trading off maximal cooperativity for cheater protection. The B. subtilis system does not make such sacrifices because instead of going below the threshold for maximum cooperative gain, it just avoids overproduction.…”

The path to re-evolve cooperation is constrained inPseudomonas aeruginosa

“…We believe that the insights gained from our study have implications for other public good traits for two reasons. For one thing, it was shown that public goods traits can easily be lost through SNPs in their key regulators [21,22,[34][35][36]. However, regulators are usually highly specialized proteins encoded by a single gene, such that mutational targets allowing reversion or compensation are likely limited [9,37,38].…”

“…Further studies are clearly needed to elucidate these pattern at both across all replicate populations and 20 transfers b assuming a mutation rate of~10 -9 per nucleotide per cell division for P. aeruginosa PAO1 [32] c pvdS gene and upstream promoter region consisting of 666 bp the proximate and ultimate level. The proximate level is of special interest here because the complete loss of pyoverdine production did not involve mutations in pvdS, which has been identified as the main target of selection for the initial reduction in pyoverdine production ( [21,22]; Granato ET, Ziegenhain C, Marvig RL & Kümmerli R, unpublished).…”

“…Finally, we examine whether the genetic background of cheats is an important determinant of whether cooperation can re-evolve. Previous studies ( [21,22]; Granato ET, Ziegenhain C, Marvig RL & Kümmerli R, unpublished) observed the evolution of two types of cheats with greatly decreased pyoverdine production. The first type of cheat has a point mutation in pvdS, the gene encoding the sigma factor regulating pyoverdine production [15], whereas the second type of cheat has a point mutation in the promoter region of pvdS (Fig.…”

“…Pyoverdine is the main siderophore of P. aeruginosa, and is secreted into the environment in response to iron limitation [15]. Pyoverdine acts as a shareable public good that can be exploited by nonproducing cheats that possess the matching receptor for uptake [16,17].…”