From quorum to cooperation: lessons from bacterial sociality for evolutionary theory.

The study of cooperation and altruism, almost since its inception, has been carried out without reference to the most numerous, diverse and very possibly most cooperative domain of life on the planet: bacteria. This is starting to change, for good reason. Far from being clonal loners, bacteria are highly social creatures capable of astonishingly complex collective behaviour that is mediated, as it is in colonial insects, by chemical communication. The article discusses recent experiments that explore different facets of current theories of the evolution and maintenance of cooperation using bacterial models. Not only do bacteria hold great promise as experimentally tractable, rapidly evolving systems for testing hypotheses, bacterial experiments have already raised interesting questions about the assumptions on which our current understanding of cooperation and altruism rests.

[1]  Cooperation: Integrating Evolutionary and Ecological Perspectives , 2006, Current Biology.

[2]  R. Kolter,et al.  Evolutionary cheating in Escherichia coli stationary phase cultures. , 2001, Genetics.

[3]  James A. Shapiro,et al.  BACTERIA AS MULTICELLULAR ORGANISMS , 1988 .

[4]  J. Michiels,et al.  Quorum sensing and swarming migration in bacteria. , 2004, FEMS microbiology reviews.

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

[6]  Paul B. Rainey,et al.  Evolution of species interactions in a biofilm community , 2007, Nature.

[7]  W. D. Bauer,et al.  Disruption of bacterial quorum sensing by other organisms. , 2002, Current opinion in biotechnology.

[8]  R. Redfield.  Is quorum sensing a side effect of diffusion sensing? , 2002, Trends in microbiology.

[9]  B. Wren,et al.  Biofilm formation in Campylobacter jejuni. , 2006, Microbiology.

[10]  R. Millikan.  On Reading Signs; Some Differences between Us and the Others on Reading Signs on Reading Signs; Some Differences between Us and the Others , 2003 .

[11]  Thomas Bell,et al.  Character Displacement Promotes Cooperation in Bacterial Biofilms , 2006, Current Biology.

[12]  D. Kaiser,et al.  How and why bacteria talk to each other , 1993, Cell.

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

[14]  S. Kjelleberg,et al.  Is there a role for quorum sensing signals in bacterial biofilms? , 2002, Current opinion in microbiology.

[15]  J. Shapiro.  Thinking about bacterial populations as multicellular organisms. , 1998, Annual review of microbiology.

[16]  Bonnie L Bassler,et al.  Chemical communication among bacteria , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[17]  B. Lazazzera,et al.  Quorum sensing and starvation: signals for entry into stationary phase. , 2000, Current opinion in microbiology.

[18]  R. Michod,et al.  Cooperation and conflict during evolutionary transitions in individuality , 2006, Journal of evolutionary biology.

[19]  T. Wenseleers.  Modelling social evolution: the relative merits and limitations of a Hamilton's rule‐based approach , 2006, Journal of evolutionary biology.

[20]  Pamela Lyon,et al.  The biogenic approach to cognition , 2006, Cognitive Processing.

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

[22]  S. Kjelleberg,et al.  Microbial landscapes: new paths to biofilm research. , 2007, Nature reviews. Microbiology.

[23]  V. Jansen,et al.  Kinds of kindness: classifying the causes of altruism and cooperation , 2006, Journal of evolutionary biology.

[24]  E. Greenberg,et al.  Cell-to-cell communication in Escherichia coli and Salmonella typhimurium: they may be talking, but who's listening? , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[25]  P. Watnick,et al.  Biofilm, City of Microbes , 2000 .

[26]  D. Queller.  Social evolution: Kinship is relative , 2004, Nature.

[27]  Hai-Lei Wei,et al.  Quorum-sensing system influences root colonization and biological control ability in Pseudomonas fluorescens 2P24 , 2006, Antonie van Leeuwenhoek.

[28]  O. Leimar,et al.  Facing the facts , 2006, Journal of evolutionary biology.

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

[30]  C. Hauert,et al.  Models of cooperation based on the Prisoner's Dilemma and the Snowdrift game , 2005 .

[31]  J. M. Smith.  Group Selection and Kin Selection , 1964, Nature.

[32]  T. Dayan,et al.  Ecological and community‐wide character displacement: the next generation , 2005 .

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

[34]  A. Grossman,et al.  Purification and characterization of an extracellular peptide factor that affects two different developmental pathways in Bacillus subtilis. , 1996, Genes & development.

[35]  P Stoodley,et al.  Survival strategies of infectious biofilms. , 2005, Trends in microbiology.

[36]  Lian-Hui Zhang,et al.  Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase , 2001, Nature.

[37]  P. Taylor,et al.  The economics of altruism and cooperation in class‐structured populations: what's in a cost? What's in a benefit? , 2006, Journal of evolutionary biology.

[38]  R. Losick,et al.  Cannibalism by Sporulating Bacteria , 2003, Science.

[39]  H Donabedian,et al.  Quorum sensing and its relevance to infectious diseases. , 2003, The Journal of infection.

[40]  D. Wilson.  Structured Demes and the Evolution of Group-Advantageous Traits , 1977, The American Naturalist.

[41]  J. Shapiro.  Bacteria are small but not stupid 1 Bacteria are small but not stupid : Cognition , natural genetic engineering , and sociobacteriology , 2006 .

[42]  J. Strassmann,et al.  Altruism and social cheating in the social amoeba Dictyostelium discoideum , 2000, Nature.

[43]  Christa Lanz,et al.  Comprehensive mutation identification in an evolved bacterial cooperator and its cheating ancestor. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[44]  M. Parsek,et al.  Does Pseudomonas aeruginosa use intercellular signalling to build biofilm communities? , 2006, Cellular microbiology.

[45]  Lian-Hui Zhang.  Quorum quenching and proactive host defense. , 2003, Trends in plant science.

[46]  J. Costerton,et al.  Bacterial biofilms in nature and disease. , 1987, Annual review of microbiology.

[47]  R. Lenski,et al.  Developmental cheating in the social bacterium Myxococcus xanthus , 2000, Nature.

[48]  D. Kimbrough Oller,et al.  Evolution of communication systems : a comparative approach , 2004 .

[49]  M. Merighi,et al.  Chlamydomonas reinhardtii Secretes Compounds That Mimic Bacterial Signals and Interfere with Quorum Sensing Regulation in Bacteria1 , 2004, Plant Physiology.

[50]  M. Dworkin.  Recent advances in the social and developmental biology of the myxobacteria. , 1996, Microbiological reviews.

[51]  S. Rice,et al.  Microcolonies, quorum sensing and cytotoxicity determine the survival of Pseudomonas aeruginosa biofilms exposed to protozoan grazing. , 2004, Environmental microbiology.

[52]  M E Woolhouse,et al.  Population Biology of Multihost Pathogens , 2001, Science.

[53]  John Maynard Smith,et al.  The Concept of Information in Biology , 2000, Philosophy of Science.

[54]  C. Zahn-Waxler,et al.  Unto Others: The Evolution and Psychology of Unselfish Behavior. , 1999 .

[55]  H. Levine,et al.  Bacterial linguistic communication and social intelligence. , 2004, Trends in microbiology.

[56]  R. Palmer,et al.  Genome-genome interactions: bacterial communities in initial dental plaque. , 2005, Trends in microbiology.

[57]  Edward O. Wilson,et al.  Kin Selection as the Key to Altruism: Its Rise and Fall , 2005, Social Research: An International Quarterly.

[58]  T. Wood,et al.  Quorum-sensing antagonist (5Z)-4-bromo-5-(bromomethylene)-3-butyl-2(5H)-furanone influences siderophore biosynthesis in Pseudomonas putida and Pseudomonas aeruginosa , 2005, Applied Microbiology and Biotechnology.

[59]  S. Frank.  A kin selection model for the evolution of virulence , 1992, Proceedings of the Royal Society of London. Series B: Biological Sciences.

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

[61]  S. Frank.  Foundations of Social Evolution , 2019 .

[62]  M. Chicurel.  Bacterial biofilms and infections. Slimebusters. , 2000, Nature.

[63]  K. Nordström,et al.  Quorum-sensing acts at initiation of chromosomal replication in Escherichia coli. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[64]  Vanessa Sperandio,et al.  Bacteria–host communication: The language of hormones , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[65]  Joel L. Sachs.  Cooperation within and among species , 2006, Journal of evolutionary biology.

[66]  Martin Zwick,et al.  Unifying the Theories of Inclusive Fitness and Reciprocal Altruism , 2006, The American Naturalist.

[67]  K. Winzer,et al.  Bacterial cell-to-cell communication: sorry, can't talk now - gone to lunch! , 2002, Current opinion in microbiology.

[68]  Abigail C. Allwood,et al.  Stromatolite reef from the Early Archaean era of Australia , 2006, Nature.

[69]  B. Bassler.  How bacteria talk to each other: regulation of gene expression by quorum sensing. , 1999, Current opinion in microbiology.

[70]  Alfred M. Spormann,et al.  Gliding Motility in Bacteria: Insights from Studies ofMyxococcus xanthus , 1999, Microbiology and Molecular Biology Reviews.

[71]  D. Kaiser,et al.  Cell-to-Cell Transfer of Bacterial Outer Membrane Lipoproteins , 2005, Science.

[72]  P. Lyon.  The agent in the organism : towards a biogenic theory of cognition , 2006 .

[73]  Maureen A. O’Malley,et al.  Size doesn’t matter: towards a more inclusive philosophy of biology , 2007 .

[74]  M. Surette,et al.  Communication in bacteria: an ecological and evolutionary perspective , 2006, Nature Reviews Microbiology.

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

[76]  Marcus W Feldman,et al.  What is altruism? , 2004, Trends in ecology & evolution.

[77]  G. J. Velicer,et al.  Evolution of an obligate social cheater to a superior cooperator , 2006, Nature.

[78]  G L Miklos,et al.  Molecules and cognition: the latterday lessons of levels, language, and lac. Evolutionary overview of brain structure and function in some vertebrates and invertebrates. , 1993, Journal of neurobiology.

[79]  Ronald Noë.  Cooperation experiments: coordination through communication versus acting apart together , 2006, Animal Behaviour.

[80]  D. Coplin,et al.  Quorum sensing in plant-pathogenic bacteria. , 2003, Annual review of phytopathology.

[81]  D. Schluter,et al.  Ecological Character Displacement and Speciation in Sticklebacks , 1992, The American Naturalist.

[82]  Bonnie L. Bassler,et al.  Bacterially Speaking , 2006, Cell.

[83]  J. Losos.  Ecological character displacement and the study of adaptation. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[84]  C. Hauert,et al.  Limits of Hamilton's rule , 2006, Journal of evolutionary biology.

[85]  R. Tompkins,et al.  Analysis of Pseudomonas aeruginosa 4-hydroxy-2-alkylquinolines (HAQs) reveals a role for 4-hydroxy-2-heptylquinoline in cell-to-cell communication. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[86]  J. M. Meyer,et al.  Quorum-sensing and siderophore biosynthesis in Pseudomonas aeruginosa: lasR/lasI mutants exhibit reduced pyoverdine biosynthesis. , 1998, FEMS microbiology letters.

[87]  K. Visick,et al.  An Exclusive Contract: Specificity in the Vibrio fischeri-Euprymna scolopes Partnership , 2000, Journal of bacteriology.

[88]  S. P. Brown,et al.  Cooperation and conflict in host–manipulating parasites , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[89]  E. Greenberg,et al.  Sociomicrobiology: the connections between quorum sensing and biofilms. , 2005, Trends in microbiology.

[90]  R. Kolter.  Surfacing views of biofilm biology. , 2005, Trends in microbiology.

[91]  L. Øvreås,et al.  Use of non‐limiting substrates to increase size; a generic strategy to simultaneously optimize uptake and minimize predation in pelagic osmotrophs? , 2005 .

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

[93]  J. Lengeler,et al.  Genetic Exchange between Microorganisms , 1998 .

[94]  M. Gao,et al.  Production of substances by Medicago truncatula that affect bacterial quorum sensing. , 2003, Molecular plant-microbe interactions : MPMI.

[95]  G. J. Velicer,et al.  Exploitative and Hierarchical Antagonism in a Cooperative Bacterium , 2005, PLoS biology.

[96]  R. Barth,et al.  Quorum sensing: dynamic response of Pseudomonas aeruginosa to external signals. , 2006, Trends in microbiology.

[97]  Dale Kaiser,et al.  Signaling in myxobacteria. , 2004, Annual review of microbiology.

[98]  E. Wilson,et al.  Eusociality: origin and consequences. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[99]  Ned S Wingreen,et al.  Cooperation among Microorganisms , 2006, PLoS biology.

[100]  Bonnie L Bassler,et al.  Small Talk Cell-to-Cell Communication in Bacteria , 2002, Cell.

[101]  R. Lenski,et al.  Rescue of Social Motility Lost during Evolution of Myxococcus xanthus in an Asocial Environment , 2002, Journal of bacteriology.

[102]  S. Kjelleberg,et al.  Eukaryotic interference with homoserine lactone-mediated prokaryotic signalling , 1996, Journal of bacteriology.

[103]  B. Bassler,et al.  Quorum sensing: cell-to-cell communication in bacteria. , 2005, Annual review of cell and developmental biology.

[104]  J. Costerton,et al.  Biofilms, bacterial signaling, and their ties to marine biology , 2003, Journal of Industrial Microbiology and Biotechnology.

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

[106]  N. Moran,et al.  Genes Lost and Genes Found: Evolution of Bacterial Pathogenesis and Symbiosis , 2001, Science.

[107]  R. Trivers.  The Evolution of Reciprocal Altruism , 1971, The Quarterly Review of Biology.

[108]  Martin Dworkin,et al.  Developmental biology of the bacteria , 1985 .

[109]  Tim Tolker-Nielsen,et al.  Gene transfer occurs with enhanced efficiency in biofilms and induces enhanced stabilisation of the biofilm structure. , 2003, Current opinion in biotechnology.

[110]  Hans G. Schlegel,et al.  Biology of the prokaryotes , 1999 .

[111]  B. Bassler,et al.  Quorum sensing in bacteria. , 2001, Annual review of microbiology.

[112]  L. Shimkets.  Intercellular signaling during fruiting-body development of Myxococcus xanthus. , 1999, Annual review of microbiology.

[113]  R. Johnstone,et al.  Cooperation in the dark: signalling and collective action in quorum-sensing bacteria , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[114]  M. Travisano,et al.  Strategies of microbial cheater control. , 2004, Trends in microbiology.

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

[116]  L. Dugatkin.  Cooperation in animals: An evolutionary overview , 2002 .

[117]  R. Kolter,et al.  Biofilm formation as microbial development. , 2000, Annual review of microbiology.

[118]  G. Caetano-Anollés,et al.  Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[119]  J. Bull,et al.  The Evolution of Cooperation , 2004, The Quarterly Review of Biology.

[120]  P. Machamer,et al.  Thinking about Mechanisms , 2000, Philosophy of Science.