The social evolution of siderophore production in Pseudomonas aeruginosa is environmentally determined

Bacteria secrete various exoproducts whose benefits can be shared by all cells in the vicinity. The potential importance of these “public goods” in bacterial evolutionary ecology has been extensively studied. Cheating by siderophore-null mutants of the opportunistic pathogen Pseudomonas aeruginosa has received particular attention. The potential of siderophore mutants to attenuate virulence, and the possibility of exploiting this for clinical ends, have generated a wealth of publications. However, the possibility that genotype · environment interactions govern the evolutionary consequences of siderophore loss has been almost entirely ignored. A review of the available literature revealed (i) widespread use of an undefined mutant as a siderophore cheat; and (ii) a reliance on experiments conducted in iron-limited minimal medium. Whole genome sequencing of the undefined mutant revealed a range of mutations affecting phenotypes other than siderophore production. We then conducted cheating assays using defined deletion mutants, grown in conditions designed to model infected fluids and tissue in CF lung infection and non-healing wounds. Depending on the environment, we found that siderophore loss could lead to cheating, simple fitness defects, or no fitness effect at all. It is therefore crucial to develop appropriate in vitro growth conditions in order to better predict the social evolution of traits in vivo.

[1]  S. Diggle,et al.  The Fitness of Pseudomonas aeruginosa Quorum Sensing Signal Cheats Is Influenced by the Diffusivity of the Environment , 2016, mBio.

[2]  S. Diggle,et al.  An ex vivo lung model to study bronchioles infected with Pseudomonas aeruginosa biofilms. , 2016, Microbiology.

[3]  A. Griffin,et al.  Pyoverdin cheats fail to invade bacterial populations in stationary phase , 2016, Journal of evolutionary biology.

[4]  R. Kümmerli,et al.  When is a bacterial “virulence factor” really virulent? , 2016, bioRxiv.

[5]  R. Hunter,et al.  Evidence and Role for Bacterial Mucin Degradation in Cystic Fibrosis Airway Disease , 2016, bioRxiv.

[6]  M. Callaghan,et al.  Iron acquisition in the cystic fibrosis lung and potential for novel therapeutic strategies. , 2016, Microbiology.

[7]  S. Diggle,et al.  The limitations of in vitro experimentation in understanding biofilms and chronic infection , 2015, bioRxiv.

[8]  A. Griffin,et al.  Co‐evolutionary dynamics between public good producers and cheats in the bacterium Pseudomonas aeruginosa , 2015, Journal of evolutionary biology.

[9]  A. Griffin,et al.  Long-term social dynamics drive loss of function in pathogenic bacteria , 2015, Proceedings of the National Academy of Sciences.

[10]  D. Newman,et al.  Pediatric Cystic Fibrosis Sputum Can Be Chemically Dynamic, Anoxic, and Extremely Reduced Due to Hydrogen Sulfide Formation , 2015, mBio.

[11]  K. Hornischer,et al.  The Pseudomonas aeruginosa Transcriptional Landscape Is Shaped by Environmental Heterogeneity and Genetic Variation , 2015, mBio.

[12]  D. Newman,et al.  Sputum Iron Levels During Cystic Fibrosis Pulmonary Exacerbation: A Longitudinal Study , 2015 .

[13]  M. Whiteley,et al.  Essential genome of Pseudomonas aeruginosa in cystic fibrosis sputum , 2015, Proceedings of the National Academy of Sciences.

[14]  R. Kümmerli,et al.  Evolutionary dynamics of interlinked public goods traits: an experimental study of siderophore production in Pseudomonas aeruginosa , 2015, Journal of evolutionary biology.

[15]  R. Kümmerli,et al.  EXPLAINING THE SOCIOBIOLOGY OF PYOVERDIN PRODUCING PSEUDOMONAS: A COMMENT ON ZHANG AND RAINEY (2013) , 2014, Evolution; international journal of organic evolution.

[16]  S. Diggle,et al.  Development of an Ex Vivo Porcine Lung Model for Studying Growth, Virulence, and Signaling of Pseudomonas aeruginosa , 2014, Infection and Immunity.

[17]  Forest Rohwer,et al.  Biogeochemical Forces Shape the Composition and Physiology of Polymicrobial Communities in the Cystic Fibrosis Lung , 2014, mBio.

[18]  A. Griffin,et al.  An experimental test of whether cheating is context dependent , 2014, Journal of evolutionary biology.

[19]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[20]  P. Rainey,et al.  EXPLORING THE SOCIOBIOLOGY OF PYOVERDIN‐PRODUCING PSEUDOMONAS , 2013, Evolution; international journal of organic evolution.

[21]  Thomas Bjarnsholt,et al.  The in vivo biofilm. , 2013, Trends in microbiology.

[22]  D. Newman,et al.  Ferrous Iron Is a Significant Component of Bioavailable Iron in Cystic Fibrosis Airways , 2013, mBio.

[23]  R. Kümmerli,et al.  Switching between apparently redundant iron-uptake mechanisms benefits bacteria in changeable environments , 2013, Proceedings of the Royal Society B: Biological Sciences.

[24]  Mohammad Wahid Ansari,et al.  The legal status of in vitro embryos , 2014 .

[25]  A. Charkowski,et al.  Salmonella enterica Suppresses Pectobacterium carotovorum subsp. carotovorum Population and Soft Rot Progression by Acidifying the Microaerophilic Environment , 2013, mBio.

[26]  Anders Folkesson,et al.  Adaptation of Pseudomonas aeruginosa to the cystic fibrosis airway: an evolutionary perspective , 2012, Nature Reviews Microbiology.

[27]  A. Griffin,et al.  The Dynamics of Cooperative Bacterial Virulence in the Field , 2012, Science.

[28]  S. West,et al.  Density-dependent fitness benefits in quorum-sensing bacterial populations , 2012, Proceedings of the National Academy of Sciences.

[29]  R. Kümmerli,et al.  Cost of cooperation rules selection for cheats in bacterial metapopulations , 2012, Journal of evolutionary biology.

[30]  Anders Folkesson,et al.  Evolutionary dynamics of bacteria in a human host environment , 2011, Proceedings of the National Academy of Sciences.

[31]  S. Diggle,et al.  Cooperation and cheating in Pseudomonas aeruginosa: the roles of the las, rhl and pqs quorum-sensing systems , 2011, The ISME Journal.

[32]  A. Buckling,et al.  Wider Access to Genotypic Space Facilitates Loss of Cooperation in a Bacterial Mutator , 2011, PloS one.

[33]  Sanford Weisberg,et al.  An R Companion to Applied Regression , 2010 .

[34]  Sam P. Brown,et al.  Molecular and regulatory properties of a public good shape the evolution of cooperation , 2010, Proceedings of the National Academy of Sciences.

[35]  N. Thomson,et al.  Studying bacterial transcriptomes using RNA-seq , 2010, Current opinion in microbiology.

[36]  V. Tam,et al.  Impact of multidrug-resistant Pseudomonas aeruginosa infection on patient outcomes , 2010, Expert review of pharmacoeconomics & outcomes research.

[37]  A. Griffin,et al.  Fitness correlates with the extent of cheating in a bacterium , 2010, Journal of evolutionary biology.

[38]  A. Griffin,et al.  Repression of competition favours cooperation: experimental evidence from bacteria , 2010, Journal of evolutionary biology.

[39]  C. Sternberg,et al.  An in vitro model of bacterial infections in wounds and other soft tissues , 2010, APMIS : acta pathologica, microbiologica, et immunologica Scandinavica.

[40]  Stephen P. Diggle,et al.  Social evolution in micro-organisms and a Trojan horse approach to medical intervention strategies , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[41]  Freya Harrison,et al.  Viscous medium promotes cooperation in the pathogenic bacterium Pseudomonas aeruginosa , 2009, Proceedings of the Royal Society B: Biological Sciences.

[42]  A. Camilli,et al.  Tn-seq; high-throughput parallel sequencing for fitness and genetic interaction studies in microorganisms , 2009, Nature Methods.

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

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

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

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

[47]  A. Buckling,et al.  Siderophore production and biofilm formation as linked social traits , 2009, The ISME Journal.

[48]  T. Hothorn,et al.  Simultaneous Inference in General Parametric Models , 2008, Biometrical journal. Biometrische Zeitschrift.

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

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

[51]  P. Visca,et al.  Regulation of the Pseudomonas aeruginosa toxA, regA and ptxR genes by the iron-starvation sigma factor PvdS under reduced levels of oxygen. , 2007, Microbiology.

[52]  A. Griffin,et al.  Cooperation and conflict in quorum-sensing bacterial populations , 2007, Nature.

[53]  M. Whiteley,et al.  Nutritional Cues Control Pseudomonas aeruginosa Multicellular Behavior in Cystic Fibrosis Sputum , 2007, Journal of bacteriology.

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

[55]  R. Boucher Airway surface dehydration in cystic fibrosis: pathogenesis and therapy. , 2007, Annual review of medicine.

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

[57]  M. Tsuda,et al.  A positive regulatory gene,pvdS, for expression of pyoverdin biosynthetic genes inPseudomonas aeruginosa PAO , 1995, Molecular and General Genetics MGG.

[58]  E. Greenberg,et al.  Iron and Pseudomonas aeruginosa biofilm formation. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[59]  Pradeep K. Singh,et al.  Cystic Fibrosis Sputum Supports Growth and Cues Key Aspects of Pseudomonas aeruginosa Physiology , 2005, Journal of bacteriology.

[60]  Kevin R Foster,et al.  Hamiltonian Medicine: Why the Social Lives of Pathogens Matter , 2005, Science.

[61]  S. Lory,et al.  A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa. , 2004, Developmental cell.

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

[63]  S. Beatson,et al.  FpvB, an alternative type I ferripyoverdine receptor of Pseudomonas aeruginosa. , 2004, Microbiology.

[64]  R. Axelrod,et al.  Evolutionary Dynamics , 2004 .

[65]  W. Peng,et al.  The Pseudomonas aeruginosa alternative sigma factor PvdS controls exotoxin A expression and is expressed in lung infections associated with cystic fibrosis. , 2002, Microbiology.

[66]  Roger E. Bumgarner,et al.  Gene expression in Pseudomonas aeruginosa biofilms , 2001, Nature.

[67]  I. Lamont,et al.  Analysis of Promoters Recognized by PvdS, an Extracytoplasmic-Function Sigma Factor Protein fromPseudomonas aeruginosa , 2001, Journal of bacteriology.

[68]  S. Lory,et al.  Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen , 2000, Nature.

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

[70]  M. Drumm in vivo. , 1999 .

[71]  H. Cunliffe,et al.  Exotoxin A production in Pseudomonas aeruginosa requires the iron‐regulated pvdS gene encoding an alternative sigma factor , 1996, Molecular microbiology.

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

[73]  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.

[74]  L. Young,et al.  Pseudomonas aeruginosa infections. , 2008, CRC critical reviews in clinical laboratory sciences.

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

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