Viscous medium promotes cooperation in the pathogenic bacterium Pseudomonas aeruginosa

There has been extensive theoretical debate over whether population viscosity (limited dispersal) can favour cooperation. While limited dispersal increases the probability of interactions occurring between relatives, which can favour cooperation, it can also lead to an increase in competition between relatives and this can reduce or completely negate selection for cooperation. Despite much theoretical attention, there is a lack of empirical research investigating these issues. We cultured Pseudomonas aeruginosa bacteria in medium with different degrees of viscosity and examined the fitness consequences for a cooperative trait—the production of iron-scavenging siderophore molecules. We found that increasing viscosity of the growth medium (i) significantly limited bacterial dispersal and the diffusion of siderophore molecules and (ii) increased the fitness of individuals that produced siderophores relative to mutants that did not. We propose that viscosity favours siderophore-producing individuals in this system, because the benefits of siderophore production are more likely to accrue to relatives (i.e. greater indirect benefits), and, at the same time, bacteria are more likely to gain direct fitness benefits by taking up siderophore molecules produced by themselves (i.e. the trait becomes less cooperative). Our results suggest that viscosity of the microbial growth environment is a crucial factor determining the dynamics of wild-type bacteria and siderophore-deficient mutants in natural habitats, such as the viscous mucus in cystic fibrosis lung.

[1]  Michael J. Crawley,et al.  The R book , 2022 .

[2]  A. Griffin,et al.  Density Dependence and Cooperation: Theory and a Test with Bacteria , 2009, Evolution; international journal of organic evolution.

[3]  Andy Gardner,et al.  Adaptation and the Evolution of Parasite Virulence in a Connected World , 2009 .

[4]  A. Griffin,et al.  Limited Dispersal, Budding Dispersal, and Cooperation: An Experimental Study , 2009, Evolution; international journal of organic evolution.

[5]  A. Griffin,et al.  Phenotypic plasticity of a cooperative behaviour in bacteria , 2009, Journal of evolutionary biology.

[6]  J. Koo,et al.  Airway mucus: the good, the bad, the sticky. , 2009, Pharmacology & therapeutics.

[7]  Stephen P. Diggle,et al.  Quorum Sensing and the Social Evolution of Bacterial Virulence , 2009, Current Biology.

[8]  A. Gardner,et al.  Nice natives and mean migrants: the evolution of dispersal‐dependent social behaviour in viscous populations , 2008, Journal of evolutionary biology.

[9]  R. Johnstone Kin Selection, Local Competition, and Reproductive Skew , 2008, Evolution; international journal of organic evolution.

[10]  Laurent Lehmann,et al.  Population viscosity can promote the evolution of altruistic sterile helpers and eusociality , 2008, Proceedings of the Royal Society B: Biological Sciences.

[11]  Rufus A. Johnstone,et al.  Sex Differences in Dispersal and the Evolution of Helping and Harming , 2008, The American Naturalist.

[12]  Alan Grafen,et al.  Natural selection of altruism in inelastic viscous homogeneous populations. , 2008, Journal of theoretical biology.

[13]  P. Taylor,et al.  Empty Sites can Promote Altruistic Behavior , 2008, Evolution; international journal of organic evolution.

[14]  M. Baalen,et al.  Self-structuring in spatial evolutionary ecology. , 2008, Ecology letters.

[15]  A. Griffin,et al.  The Social Lives of Microbes , 2007 .

[16]  A. Griffin,et al.  Siderophore-mediated cooperation and virulence in Pseudomonas aeruginosa. , 2007, FEMS Microbiology Ecology.

[17]  D. Sumpter,et al.  The evolution of helping and harming on graphs: the return of the inclusive fitness effect , 2007, Journal of evolutionary biology.

[18]  A Grafen,et al.  An inclusive fitness analysis of altruism on a cyclical network , 2007, Journal of evolutionary biology.

[19]  M. Marahiel,et al.  Siderophore-Based Iron Acquisition and Pathogen Control , 2007, Microbiology and Molecular Biology Reviews.

[20]  A. Griffin,et al.  Evolutionary Explanations for Cooperation , 2007, Current Biology.

[21]  Andy Gardner,et al.  Frequency Dependence and Cooperation: Theory and a Test with Bacteria , 2007, The American Naturalist.

[22]  N. Packer,et al.  Glycosylation of sputum mucins is altered in cystic fibrosis patients. , 2007, Glycobiology.

[23]  Peter D. Taylor,et al.  Evolution of cooperation in a finite homogeneous graph , 2007, Nature.

[24]  Freya Harrison,et al.  Microbial ecology of the cystic fibrosis lung. , 2007, Microbiology.

[25]  Troy Day,et al.  A Biologist's Guide to Mathematical Modeling in Ecology and Evolution , 2007 .

[26]  Alan Grafen,et al.  Detecting kin selection at work using inclusive fitness , 2007, Proceedings of the Royal Society B: Biological Sciences.

[27]  M. Boots,et al.  Local Interactions Select for Lower Pathogen Infectivity , 2007, Science.

[28]  B. Rubin Mucus structure and properties in cystic fibrosis. , 2007, Paediatric respiratory reviews.

[29]  A. Griffin,et al.  Social semantics : altruism , cooperation , mutualism , strong reciprocity and group selection , 2007 .

[30]  M. Nowak Five Rules for the Evolution of Cooperation , 2006, Science.

[31]  T. Murray,et al.  FlhF Is Required for Swimming and Swarming in Pseudomonas aeruginosa , 2006, Journal of bacteriology.

[32]  L. Keller,et al.  The evolution of cooperation and altruism – a general framework and a classification of models , 2006, Journal of evolutionary biology.

[33]  A. Gardner,et al.  Demography, altruism, and the benefits of budding , 2006, Journal of evolutionary biology.

[34]  A. Griffin,et al.  Social evolution theory for microorganisms , 2006, Nature Reviews Microbiology.

[35]  A. Buckling,et al.  Cooperation and virulence in acute Pseudomonas aeruginosa infections , 2006, BMC Biology.

[36]  B. Kerr,et al.  Local migration promotes competitive restraint in a host–pathogen 'tragedy of the commons' , 2006, Nature.

[37]  F. Rousset,et al.  POPULATION DEMOGRAPHY AND THE EVOLUTION OF HELPING BEHAVIORS , 2006, Evolution; international journal of organic evolution.

[38]  H. Ohtsuki,et al.  A simple rule for the evolution of cooperation on graphs and social networks , 2006, Nature.

[39]  M. Knowles,et al.  Mucus clearance and lung function in cystic fibrosis with hypertonic saline. , 2006, The New England journal of medicine.

[40]  S. Allison Cheaters, diffusion and nutrients constrain decomposition by microbial enzymes in spatially structured environments , 2005 .

[41]  Ulf Dieckmann,et al.  Adaptive Evolution of Social Traits: Origin, Trajectories, and Correlations of Altruism and Mobility , 2004, The American Naturalist.

[42]  P. Janmey,et al.  Elastic contributions dominate the viscoelastic properties of sputum from cystic fibrosis patients. , 2004, Biophysical chemistry.

[43]  R. Boucher,et al.  Reevaluating gel-forming mucins' roles in cystic fibrosis lung disease. , 2004, Free radical biology & medicine.

[44]  P. Delepelaire,et al.  Bacterial iron sources: from siderophores to hemophores. , 2004, Annual review of microbiology.

[45]  A. Griffin,et al.  Cooperation and competition in pathogenic bacteria , 2004, Nature.

[46]  Michael Doebeli,et al.  Spatial structure often inhibits the evolution of cooperation in the snowdrift game , 2004, Nature.

[47]  F. Rousset Genetic Structure and Selection in Subdivided Populations (MPB-40) , 2004 .

[48]  G. J. Velicer Social strife in the microbial world. , 2003, Trends in microbiology.

[49]  S. Bonhoeffer,et al.  An evolutionary scenario for the transition to undifferentiated multicellularity , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[50]  S. West,et al.  Cooperation, virulence and siderophore production in bacterial parasites , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[51]  U. Dieckmann,et al.  THE ADAPTIVE DYNAMICS OF ALTRUISM IN SPATIALLY HETEROGENEOUS POPULATIONS , 2003, Evolution; international journal of organic evolution.

[52]  Sam P. Brown,et al.  Does multiple infection select for raised virulence? , 2002, Trends in microbiology.

[53]  M. Vasil,et al.  Siderophore-mediated signaling regulates virulence factor production in Pseudomonas aeruginosa , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[54]  S. West,et al.  Sanctions and mutualism stability: why do rhizobia fix nitrogen? , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[55]  A. Griffin,et al.  Cooperation and Competition Between Relatives , 2002, Science.

[56]  M. Beekman The evolution of social behavior in microorganisms , 2001 .

[57]  H. Budzikiewicz Siderophores of the human pathogenic fluorescent pseudomonads. , 2001, Current topics in medicinal chemistry.

[58]  J. Carlin,et al.  Clinical outcome after early Pseudomonas aeruginosa infection in cystic fibrosis. , 2001, The Journal of pediatrics.

[59]  B. Crespi The evolution of social behavior in microorganisms. , 2001, Trends in ecology & evolution.

[60]  A. Griffin,et al.  Testing Hamilton's rule with competition between relatives , 2001, Nature.

[61]  D. Roze,et al.  Cooperation and conflict in the evolution of multicellularity , 2001, Heredity.

[62]  P D Taylor,et al.  Evolution of dispersal in a stepping-stone population with overlapping generations. , 2000, Theoretical population biology.

[63]  J. Bever,et al.  Evolution of nitrogen fixation in spatially structured populations of Rhizobium , 2000, Heredity.

[64]  P D Taylor,et al.  OVERLAPPING GENERATIONS CAN PROMOTE ALTRUISTIC BEHAVIOR , 2000, Evolution; international journal of organic evolution.

[65]  D. Wilson,et al.  Population viscosity and the evolution of altruism. , 2000, Journal of theoretical biology.

[66]  A. Barbour,et al.  Small worlds , 2000, Random Struct. Algorithms.

[67]  A. Sasaki,et al.  ‘Small worlds’ and the evolution of virulence: infection occurs locally and at a distance , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[68]  S. Siller Foundations of Social Evolution , 1999, Heredity.

[69]  M. Baalen,et al.  The Unit of Selection in Viscous Populations and the Evolution of Altruism. , 1998, Journal of theoretical biology.

[70]  M. Doebeli,et al.  The evolution of interspecific mutualisms. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[71]  M. King,et al.  Sputum rheology changes in cystic fibrosis lung disease following two different types of physiotherapy: flutter vs autogenic drainage. , 1998, Chest.

[72]  Steven A. Frank,et al.  Models of Parasite Virulence , 1996, The Quarterly Review of Biology.

[73]  L. Keller Social evolution in ants , 1996 .

[74]  A. Neely,et al.  Pyoverdin is essential for virulence of Pseudomonas aeruginosa , 1996, Infection and immunity.

[75]  Eörs Szathmáry,et al.  The Major Transitions in Evolution , 1997 .

[76]  S. Shak Aerosolized recombinant human DNase I for the treatment of cystic fibrosis. , 1995, Chest.

[77]  K F Goodnight,et al.  The Effect of Stochastic Variation on Kin Selection in a Budding-Viscous Population , 1992, The American Naturalist.

[78]  John K Kelly,et al.  RESTRICTED MIGRATION AND THE EVOLUTION OF ALTRUISM , 1992, Evolution; international journal of organic evolution.

[79]  D. Queller,et al.  Does population viscosity promote kin selection? , 1992, Trends in ecology & evolution.

[80]  Peter D. Taylor,et al.  Inclusive fitness in a homogeneous environment , 1992, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[81]  G. B. Pollock,et al.  Can altruism evolve in purely viscous populations? , 1992, Evolutionary Ecology.

[82]  P. Taylor Altruism in viscous populations — an inclusive fitness model , 1992, Evolutionary Ecology.

[83]  S. Shak,et al.  Recombinant human DNase I reduces the viscosity of cystic fibrosis sputum. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[84]  D. Haas,et al.  Mapping of mutations affecting pyoverdine production in Pseudomonas aeruginosa , 1986 .

[85]  C. D. Cox,et al.  Effects of siderophores on the growth of Pseudomonas aeruginosa in human serum and transferrin , 1985, Infection and immunity.

[86]  W. Hamilton,et al.  The evolution of cooperation. , 1984, Science.

[87]  M. King Is Cystic Fibrosis Mucus Abnormal? , 1981, Pediatric Research.

[88]  R M May,et al.  Evolutionarily stable dispersal strategies. , 1980, Journal of theoretical biology.

[89]  W. Hamilton,et al.  Altruism and Related Phenomena, Mainly in Social Insects , 1972 .

[90]  L. Reid,et al.  Sputum viscosity in chronic bronchitis, bronchiectasis, asthma and cystic fibrosis. , 1972, Biorheology.

[91]  G. Hardin,et al.  The Tragedy of the Commons , 1968, Green Planet Blues.

[92]  W. Hamilton The genetical evolution of social behaviour. I. , 1964, Journal of theoretical biology.

[93]  A. Buckling,et al.  Cooperative production of siderophores by Pseudomonas aeruginosa. , 2009, Frontiers in bioscience.

[94]  Freya Harrison,et al.  Interspecific competition and siderophore-mediated cooperation in Pseudomonas aeruginosa , 2008, The ISME Journal.

[95]  P. Visca,et al.  Pyoverdine siderophores: from biogenesis to biosignificance. , 2007, Trends in microbiology.

[96]  D. Queller,et al.  Genetic relatedness in viscous populations , 2005, Evolutionary Ecology.

[97]  A. Griffin,et al.  Kin selection: fact and fiction , 2002 .

[98]  C. Ratledge,et al.  Iron metabolism in pathogenic bacteria. , 2000, Annual review of microbiology.

[99]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[100]  M. Guerinot Microbial iron transport. , 1994, Annual review of microbiology.

[101]  J. Neilands,et al.  Universal chemical assay for the detection and determination of siderophores. , 1987, Analytical biochemistry.

[102]  D. Haas,et al.  Transposon insertion mutagenesis of Pseudomonas aeruginosa with a Tn5 derivative: application to physical mapping of the arc gene cluster. , 1985, Gene.

[103]  L Thomas,et al.  On altruism. , 1978, The Journal of the Florida Medical Association.