Adaptation to public goods cheats in Pseudomonas aeruginosa

Abstract

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.

Genetic architecture constrains exploitation of siderophore cooperation in the bacteriumBurkholderia cenocepacia

“…; O'Brien et al. ). However, despite the great advance these insights provide for our understanding of microbial social interactions and community dynamics, most of the work carried out so far stems from one type of siderophore (pyoverdine) produced by one type of bacterium (fluorescent pseudomonads, particularly Pseudomonas aeruginosa ), but also see Cordero et al.…”

“…The key question in this context is how cooperative siderophore secretion can be evolutionarily maintained, given that siderophore-negative cheater mutants can arise and freeride on the public goods produced by others (West et al 2006;Özkaya et al 2017). A large body of work has tackled this question and revealed that cheating and cheater control are major determinants of bacterial population dynamics in host infections, in laboratory experiments, and in environmental communities (Cordero et al 2012;Andersen et al 2015;Kümmerli et al 2015;Bruce et al 2017;Butaitė et al 2017;O'Brien et al 2017). However, despite the great advance these insights provide for our understanding of microbial social interactions and community dynamics, most of the work carried out so far stems from one type of siderophore (pyoverdine) produced by one type of bacterium (fluorescent pseudomonads, particularly Pseudomonas aeruginosa), but also see Cordero et al (2012), Kümmerli et al (2014), and Scholz and Greenberg (2015) for exceptions.…”

Cheaters shape the evolution of phenotypic heterogeneity in Bacillus subtilis biofilms

“…We were further interested if such social cheating could leave a phenotypic or genetic fingerprint in the population of the wild type B. subtilis. Previous studies have shown that cooperators can adapt to presence of cheats for example by decreasing the amount of released public goods and therefore minimizing cheating opportunities [2,14,15]. As B. subtilis exhibits phenotypic heterogeneity in eps matrix gene expression [39,40] ( Supplementary Fig.…”

“…Cooperative interactions are prevalent for all life forms [1], even for simple microbes that often exist in communities of matrix bound surface-attached cells called biofilms [2][3][4][5][6]. However, when costly products such as siderophores [7,8], extracellular polymeric substances [9,10], digestive enzymes [11], and signaling molecules [12,13] are secreted and shared, cooperative behavior 3 becomes susceptible to cheating [2,[14][15][16], where mutants defective in cooperation can still benefit from cooperative community members [4,5,17]. It has been shown that spatially structured biofilms, where interactions with clonemates are common and diffusion of public goods is limited, may serve as natural defense against cheating [18][19][20].…”

“…Recent studies showed that in well-mixed environment, cooperators adapt to cheats by reducing cooperation [14,15,33]. Such reduction could be achieved by various strategies, for instance decrease in motility [15], down regulation or minimal production in public goods [14,15,33], upregulation of other alternative public goods [14], or bi-stable expression in virulence gene [2].…”