Evolution of cooperation; Siderophores; Experimental evolution; inclusive fitness; virulence; evolutionary dynamics; microbes
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The occurrence of cooperation is one of the greatest challenges for evolutionary biology. The problem is why should an individual carry out a cooperative behaviour that is costly to perform, but benefits other individuals? Theory has shown that natural selection can favour cooperation if actors receive direct fitness benefits from the cooperative acts performed, or indirect (kin selected) fitness benefits, whereby cooperators pass their genes to the next generation indirectly by helping relatives to reproduce. This theoretical framework has proofed extremely successful in explaining the evolution of cooperation across a wide number of taxa ranging from insects to birds and mammals. Recently, a great variety of cooperative traits has been discovered in microbes such as the formation of fruiting bodies and the release of extracellular products that benefit the local group. These findings raise the question whether the theory, primarily developed for higher organisms, is of such generality that it could also explain cooperation in microbes. Moreover, investigations of microbial cooperative systems have opened a completely new research area because: (1) microbes offer exciting experimental possibilities to test aspects of theory that has not been possible to test with higher organisms due to experimental constraints; (2) evolutionary approaches are needed to explain why complex cooperative behaviour have been favoured by natural selection and why they persist instead of being exploited by non-cooperative mutants; and (3) many cooperative traits are involved with virulence and resistance to antibiotic treatments in infections of humans, livestock and crops. Thus, the evolutionary understanding of mechanisms maintaining cooperative virulence factors has medical relevance.This proposal focuses on the production of iron-scavenging siderophore molecules in the opportunistic human pathogen Pseudomonas aeruginosa. Iron is a major limiting factor for bacterial growth because most iron in the environment is in the insoluble Fe(III) form and is actively withheld by hosts. In response to iron deficiency, P. aeruginosa releases siderophore molecules into the local environment to scavenge insoluble iron, making it available for bacterial metabolism. Siderophore production is a cooperative behaviour as it can provide a fitness benefit to neighbouring cells, which can take up iron bound to siderophore produced by others. Consequently, individuals that do not produce siderophores can avoid the metabolic cost of its production, whilst still gaining the benefit by exploiting the siderophore produced by others. Such siderophore defective mutants can therefore be considered as cheats and have been observed to emerge under natural conditions.This proposal aims to study the production of pyoverdin, the primary siderophore of P. aeruginosa, a cooperative trait that has been shown to provide both, direct and indirect fitness benefits and is subject to kin selection. I will use this trait to investigate the ecological and social conditions required for cooperation to be favoured and maintained. Specifically, I will study: (i) the properties of pyoverdin molecules as a cooperative good and the resulting fitness consequences for cooperators and cheats in intra- and interspecific competition; (ii) conduct a series of experimental evolution studies that investigate the dynamics of cooperators and cheats under different environmental conditions (varying resource distribution and population structure) as they may occur in nature; and (iii) study adaptive responses of cooperators to the presence of cheats at the behavioural and genetic level in an experimental evolution set up. In addition, the experimental work will be completed with theoretical models to predict the evolutionary stability of microbial cooperative systems under the tested environmental conditions.This research is highly interdisciplinary and relevant for evolutionary biology, microbiology and medicine. It is relevant for evolutionary biology because specific social evolution models will be tested, which have proofed difficult to test with higher organisms. It is relevant for microbiology because important aspects of pyoverdin production and its fitness consequences will be explored at the behavioural and genetic level, which will complement the enormous knowledge on regulatory mechanisms uncovered by microbiologists. It is relevant for medicine because pyoverdin is an important virulence factor damaging host tissue of humans who are immunocompromised or suffer from the genetic respiratory disorder (cystic fibroses). Thus, the understanding of evolutionary dynamics of pyoverdin producers (cooperators) and non-producers (cheats), as they occur in the CF lung, is crucial to understand levels of virulence.