Sociomicrobiology: the connections between quorum sensing and biofilms.

In the past decade, significant debate has surrounded the relative contributions of genetic determinants versus environmental conditions to certain types of human behavior. While this debate goes on, it is with a certain degree of irony that microbiologists studying aspects of bacterial community behavior face the same questions. Information regarding two social phenomena exhibited by bacteria, quorum sensing and biofilm development, is reviewed here. These two topics have been inextricably linked, possibly because biofilms and quorum sensing represent two areas in which microbiologists focus on social aspects of bacteria. We will examine what is known about this linkage and discuss areas that might be developed. In addition, we believe that these two aspects of bacterial behavior represent a small part of the social repertoire of bacteria. Bacteria exhibit many social activities and they represent a model for dissecting social behavior at the genetic level. Therefore, we introduce the term 'sociomicrobiology'.

[1]  E. Greenberg,et al.  Critical regions of the Vibrio fischeri luxR protein defined by mutational analysis , 1990, Journal of bacteriology.

[2]  E. P. Greenberg,et al.  Metabolism of Acyl-Homoserine Lactone Quorum-Sensing Signals by Variovorax paradoxus , 2000, Journal of bacteriology.

[3]  M. Otto,et al.  Impact of the agr quorum-sensing system on adherence to polystyrene in Staphylococcus aureus. , 2000, The Journal of infectious diseases.

[4]  J. M. Dow,et al.  Biofilm dispersal in Xanthomonas campestris is controlled by cell–cell signaling and is required for full virulence to plants , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[5]  E. Greenberg,et al.  Acyl homoserine-lactone quorum-sensing signal generation. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[6]  E. Greenberg,et al.  Identification, Timing, and Signal Specificity of Pseudomonas aeruginosa Quorum-Controlled Genes: a Transcriptome Analysis , 2003, Journal of bacteriology.

[7]  B. Iglewski,et al.  Quorum-Sensing Genes in Pseudomonas aeruginosa Biofilms: Their Role and Expression Patterns , 2001, Applied and Environmental Microbiology.

[8]  J. M. Dow,et al.  A novel regulatory system required for pathogenicity of Xanthomonas campestris is mediated by a small diffusible signal molecule , 1997, Molecular microbiology.

[9]  Maxwell H. Anderson,et al.  Mutation of luxS Affects Biofilm Formation in Streptococcus mutans , 2003, Infection and Immunity.

[10]  Jared R. Leadbetter,et al.  Utilization of Acyl-Homoserine Lactone Quorum Signals for Growth by a Soil Pseudomonad and Pseudomonas aeruginosa PAO1 , 2003, Applied and Environmental Microbiology.

[11]  Richard F. Lee,et al.  Characterization of Monospecies Biofilm Formation by Helicobacter pylori , 2004, Journal of bacteriology.

[12]  G. Schoolnik,et al.  Molecular analysis of rugosity in a Vibrio cholerae O1 El Tor phase variant , 2004, Molecular microbiology.

[13]  Say Leong Ong,et al.  Acyl‐homoserine lactone acylase from Ralstonia strain XJ12B represents a novel and potent class of quorum‐quenching enzymes , 2003, Molecular microbiology.

[14]  E. Greenberg,et al.  Generation of cell-to-cell signals in quorum sensing: acyl homoserine lactone synthase activity of a purified Vibrio fischeri LuxI protein. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[17]  J. Costerton,et al.  The involvement of cell-to-cell signals in the development of a bacterial biofilm. , 1998, Science.

[18]  S. Molin,et al.  The cep quorum-sensing system of Burkholderia cepacia H111 controls biofilm formation and swarming motility. , 2001, Microbiology.

[19]  G. Dunny,et al.  Cell-cell communication in gram-positive bacteria. , 1997, Annual review of microbiology.

[20]  Leo Eberl,et al.  Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. , 2002, Microbiology.

[21]  J. M. Dow,et al.  Biofilm formation and dispersal in Xanthomonas campestris. , 2004, Microbes and infection.

[22]  S. Kjelleberg,et al.  Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors , 2003, The EMBO journal.

[23]  M. Surette,et al.  Quorum sensing in Escherichia coli and Salmonella typhimurium. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[24]  Paul Stoodley,et al.  Bacterial biofilms: from the Natural environment to infectious diseases , 2004, Nature Reviews Microbiology.

[25]  B. Bassler,et al.  Structural identification of a bacterial quorum-sensing signal containing boron , 2002, Nature.

[26]  S. Molin,et al.  Involvement of N‐acyl‐l‐homoserine lactone autoinducers in controlling the multicellular behaviour of Serratia liquefaciens , 1996, Molecular microbiology.

[27]  E. Greenberg,et al.  A component of innate immunity prevents bacterial biofilm development , 2002, Nature.

[28]  Bonnie L Bassler,et al.  Quorum sensing controls biofilm formation in Vibrio cholerae , 2003, Molecular microbiology.

[29]  W. Schwesinger,et al.  Biofilm Formation and Interaction with the Surfaces of Gallstones by Salmonella spp , 2002, Infection and Immunity.

[30]  R. Burne,et al.  LuxS-Mediated Signaling in Streptococcus mutans Is Involved in Regulation of Acid and Oxidative Stress Tolerance and Biofilm Formation , 2004, Journal of bacteriology.

[31]  P. Schlievert,et al.  Quorum sensing in Staphylococcus infections. , 2003, The Journal of clinical investigation.

[32]  A. Brooks,et al.  Microarray Analysis of Pseudomonas aeruginosa Quorum-Sensing Regulons: Effects of Growth Phase and Environment , 2003, Journal of bacteriology.

[33]  J. Mekalanos,et al.  A Constitutively Active Variant of the Quorum-Sensing Regulator LuxO Affects Protease Production and Biofilm Formation in Vibrio cholerae , 2003, Infection and Immunity.

[34]  E. Greenberg,et al.  A quorum-sensing system in the free-living photosynthetic bacterium Rhodobacter sphaeroides , 1997, Journal of bacteriology.

[35]  E. Greenberg,et al.  Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. , 2001, Annual review of genetics.

[36]  S. Foster,et al.  Staphylococcus aureus accessory regulators: expression within biofilms and effect on adhesion. , 2001, Microbes and infection.

[37]  J. W. Campbell,et al.  Bacterial fatty acid biosynthesis: targets for antibacterial drug discovery. , 2001, Annual review of microbiology.

[38]  J. M. Dow,et al.  A two‐component system involving an HD‐GYP domain protein links cell–cell signalling to pathogenicity gene expression in Xanthomonas campestris , 2000, Molecular microbiology.

[39]  Jun Zhu,et al.  Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae. , 2003, Developmental cell.

[40]  British Biofilm Club. Meeting,et al.  Biofilms : the good, the bad and the ugly : contributions made at the Fourth Meeting of the British Biofilm Club held at Gregynog Hall, Powys 18-20 September, 1999 , 1999 .

[41]  M. Surette,et al.  The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum‐sensing signal molecule , 2001, Molecular microbiology.

[42]  H. C. van der Mei,et al.  Bacterial Strains Isolated from Different Niches Can Exhibit Different Patterns of Adhesion to Substrata , 2004, Applied and Environmental Microbiology.

[43]  C. Fuqua,et al.  Biofilms 2003: Emerging Themes and Challenges in Studies of Surface-Associated Microbial Life , 2004, Journal of bacteriology.

[44]  A. Prince,et al.  Contribution of specific Pseudomonas aeruginosa virulence factors to pathogenesis of pneumonia in a neonatal mouse model of infection , 1996, Infection and immunity.

[45]  E. Greenberg,et al.  Synergistic binding of the Vibrio fischeri LuxR transcriptional activator domain and RNA polymerase to the lux promoter region , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[46]  P. Williams,et al.  The regulation of biofilm development by quorum sensing in Aeromonas hydrophila. , 2002, Environmental microbiology.

[47]  H. Lappin-Scott,et al.  The role of hydrodynamics and AHL signalling moleculesas determinants of the structure of pseudomonas aeruginosabiofilms , 1999 .

[48]  A. Prince,et al.  Pseudomonas aeruginosa Cell-to-Cell Signaling Is Required for Virulence in a Model of Acute Pulmonary Infection , 2000, Infection and Immunity.

[49]  Lian-Hui Zhang,et al.  Species Bacillus Homoserine Lactonases from-Acyl N Identification of Quorum-Quenching , 2002 .

[50]  S. Molin,et al.  Alginate Overproduction Affects Pseudomonas aeruginosa Biofilm Structure and Function , 2001, Journal of bacteriology.

[51]  Søren Molin,et al.  Involvement of bacterial migration in the development of complex multicellular structures in Pseudomonas aeruginosa biofilms , 2003, Molecular microbiology.

[52]  S. Rice,et al.  Quorum Sensing-Controlled Biofilm Development in Serratia liquefaciens MG1 , 2004, Journal of bacteriology.

[53]  M. Smeltzer,et al.  Mutation of sarA in Staphylococcus aureus Limits Biofilm Formation , 2003, Infection and Immunity.

[54]  G. O’Toole,et al.  Rhamnolipid Surfactant Production Affects Biofilm Architecture in Pseudomonas aeruginosa PAO1 , 2003, Journal of bacteriology.

[55]  B. Ersbøll,et al.  Statistical Analysis of Pseudomonas aeruginosa Biofilm Development: Impact of Mutations in Genes Involved in Twitching Motility, Cell-to-Cell Signaling, and Stationary-Phase Sigma Factor Expression , 2002, Applied and Environmental Microbiology.

[56]  C. van Delden,et al.  Swarming of Pseudomonas aeruginosa Is Dependent on Cell-to-Cell Signaling and Requires Flagella and Pili , 2000, Journal of bacteriology.

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

[58]  S. Atkinson,et al.  A hierarchical quorum‐sensing system in Yersinia pseudotuberculosis is involved in the regulation of motility and clumping , 1999, Molecular microbiology.

[59]  M. Kleerebezem,et al.  Cell to cell communication by autoinducing peptides in gram-positive bacteria , 2002, Antonie van Leeuwenhoek.

[60]  E. Greenberg,et al.  Quorum Sensing in Staphylococcus aureus Biofilms , 2004, Journal of bacteriology.

[61]  Margret I. Moré,et al.  Enzymatic Synthesis of a Quorum-Sensing Autoinducer Through Use of Defined Substrates , 1996, Science.

[62]  J. Costerton,et al.  Influence of Hydrodynamics and Cell Signaling on the Structure and Behavior of Pseudomonas aeruginosa Biofilms , 2002, Applied and Environmental Microbiology.