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Evolutionary explanations for the persistence of cooperative siderophore production in the bacterium Pseudomonas aeruginosa

Applicant Kümmerli Rolf
Number 126337
Funding scheme Ambizione
Research institution Abteilung für Umweltmikrobiologie EAWAG
Institution of higher education Swiss Federal Institute of Aquatic Science and Technology - EAWAG
Main discipline Ecology
Start/End 01.11.2009 - 31.10.2012
Approved amount 540'527.00
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All Disciplines (2)

Discipline
Ecology
Experimental Microbiology

Keywords (7)

Evolution of cooperation; Siderophores; Experimental evolution; inclusive fitness; virulence; evolutionary dynamics; microbes

Lay Summary (English)

Lead
Lay summary
The occurrence of cooperation is one of the greatest challenges for evolutionary biology. The problem is why should individuals carry out cooperative behaviours that are costly to perform but benefit others? Theory has shown that natural selection can favour cooperation if actors receive direct fitness benefits from the cooperative act, or indirect 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 in insects and mammals. Recently, a great variety of cooperative traits have been described in microbes. Intriguingly, it could be shown that the existing theory also successfully explains cooperation in microbes and therefore represents a general theory of social evolution. Consequently, 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; (2) experimental evolution approaches allow observing the evolution of cooperation in real-time; and (3) many cooperative traits are involved with virulence in infections of humans such that the understanding of their evolution has medical relevance.

This work 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 is in an insoluble form. In response to iron deficiency, P. aeruginosa releases siderophores to scavenge iron, making it available for bacterial metabolism. Siderophore production is a cooperative behaviour because neighbouring cells can take up iron bound to siderophore produced by others. Consequently, mutants that do not produce siderophores can avoid the metabolic cost of its production, whilst still gaining the benefit and can therefore be considered as cheats. I will use siderophore production to investigate the ecological and social conditions required for cooperation to be favoured. Specifically, I will study: (i) the cooperative properties of siderophore molecules and the resulting fitness consequences for cooperators and cheats; (ii) conduct experimental evolution studies that investigate the dynamics of cooperators and cheats under different environmental conditions; (iii) study adaptive responses of cooperators to the presence of cheats at the behavioural and genetic level. In addition, I will complement the experimental work with theoretical models to predict the evolutionary stability of siderophore production.
Direct link to Lay Summary Last update: 21.02.2013

Responsible applicant and co-applicants

Employees

Publications

Publication
Cost of cooperation rules selection for cheats in bacterial metapopulations
Dumas Zoé, Kümmerli Rolf (2012), Cost of cooperation rules selection for cheats in bacterial metapopulations, in Journal of Evolutionary Biology, 25, 473.
Inclusive fitness theory and eusociality
Abbot P, Abe J, Alcock J, Alizon S, Alpedrinha JAC, Andersson M, Andre JB, van Baalen M, Balloux F, Balshine S, Barton N, Beukeboom LW, Biernaskie JM, Bilde T, Borgia G, Breed M, Brown S, Bshary R, Buckling A, Burley NT, Burton-Chellew MN, Cant MA, Chapuisat M, Charnov EL, Clutton-Brock T (2011), Inclusive fitness theory and eusociality, in NATURE, 471(7339), E1.
Molecular and regulatory properties of a public good shape the evolution of cooperation
Kummerli R, Brown SP (2010), Molecular and regulatory properties of a public good shape the evolution of cooperation, in PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AME, 107(44), 18921-18926.
Repression of competition favours cooperation: experimental evidence from bacteria
Kummerli R, van den Berg P, Griffin AS, West SA, Gardner A (2010), Repression of competition favours cooperation: experimental evidence from bacteria, in JOURNAL OF EVOLUTIONARY BIOLOGY, 23(4), 699-706.

Collaboration

Group / person Country
Types of collaboration
IST Austria Austria (Europe)
- Publication
ETH Zürich Switzerland (Europe)
- Publication

Scientific events

Active participation

Title Type of contribution Title of article or contribution Date Place Persons involved
14th International Symposium on Microbial Ecology 19.08.2012 Copenhagen
13th Congress of the European Society for Evolutionary Biology 21.08.2011 Tübingen, Germany
4th Congress of European Microbiologists (FEMS) 26.06.2011 Geneva, Switzerland
EPSRC Workshop: evolution of microbial cooperation 20.01.2011 Bath, United Kingdom
13th International Symposium for Microbial Ecology (ISME) 22.08.2010 Seattle, US


Self-organised

Title Date Place
Cooperation and virulence: Symposium at the 13th Congress of the European Society for Evolutionary Biology 24.08.2011 Tübingen, Germany

Associated projects

Number Title Start Funding scheme
114209 L'évolution de la coopération: des testes expérimentaux des explications adaptatives et le développement de la théorie de l'évolution 01.11.2006 Fellowships for prospective researchers

Abstract

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.
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