Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators

It has long been appreciated that certain groups of bacteria exhibit cooperative behavioral patterns. For example, feeding and sporulation of both myxobacteria and actinomycetes seem optimized for large populations of cells behaving almost as a single multicellular organism. The swarming motility of microorganisms such as Vibrio parahaemolyticus and Proteus mirabilis provides another excellent example of multicellular behavior among bacteria (2). Intercellular communication likewise has been appreciated for several years in Vibrio fischeri, Myxococcus xanthus, Bacillus subtilis, Streptomyces spp., the eukaryotic slime mold Dictyostelium discoideum, and other species (44). Here we first review how the marine luminescent bacterium V. fischeri uses the LuxR and LuxI proteins for intercellular communication and then describe a newly discovered family of LuxR and LuxI homologs in diverse bacterial species.

[1]  K. Nealson,et al.  Cellular Control of the Synthesis and Activity of the Bacterial Luminescent System , 1970, Journal of bacteriology.

[2]  A. Eberhard Inhibition and Activation of Bacterial Luciferase Synthesis , 1972, Journal of bacteriology.

[3]  E. Ruby,et al.  Symbiotic association of Photobacterium fischeri with the marine luminous fish Monocentris japonica; a model of symbiosis based on bacterial studies. , 1976, The Biological bulletin.

[4]  M. Montagu,et al.  Substrate induction of conjugative activity of Agrobacterium tumefaciens Ti plasmids , 1978, Nature.

[5]  E. Ruby,et al.  Seasonal changes in the species composition of luminous bacteria in nearshore seawater , 1978 .

[6]  R. Schilperoort,et al.  Negative control of octopine degradation and transfer genes of octopine Ti plasmids in Agrobacterium tumefaciens , 1979, Journal of bacteriology.

[7]  K. Nealson,et al.  Bacterial bioluminescence: its control and ecological significance , 1979, Microbiological reviews.

[8]  E. Greenberg,et al.  Planktonic Marine Luminous Bacteria: Species Distribution in the Water Column , 1980, Applied and Environmental Microbiology.

[9]  G L Kenyon,et al.  Structural identification of autoinducer of Photobacterium fischeri luciferase. , 1981, Biochemistry.

[10]  K. Nealson,et al.  Bacterial bioluminescence: Isolation and genetic analysis of functions from Vibrio fischeri , 1983, Cell.

[11]  J. Devereux,et al.  A comprehensive set of sequence analysis programs for the VAX , 1984, Nucleic Acids Res..

[12]  M. Silverman,et al.  Identification of genes and gene products necessary for bacterial bioluminescence. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[13]  E. Greenberg,et al.  Diffusion of autoinducer is involved in regulation of the Vibrio fischeri luminescence system , 1985, Journal of bacteriology.

[14]  P. Dunlap,et al.  Control of Vibrio fischeri luminescence gene expression in Escherichia coli by cyclic AMP and cyclic AMP receptor protein , 1985, Journal of bacteriology.

[15]  J. Mekalanos,et al.  Cholera toxin transcriptional activator ToxR is a transmembrane DNA binding protein , 1987, Cell.

[16]  M. Silverman,et al.  Nucleotide sequence of the regulatory locus controlling expression of bacterial genes for bioluminescence. , 1987, Nucleic acids research.

[17]  P. Dunlap,et al.  Control of Vibrio fischeri lux gene transcription by a cyclic AMP receptor protein-luxR protein regulatory circuit , 1988, Journal of bacteriology.

[18]  B. Iglewski,et al.  Molecular characterization and nucleotide sequence of the Pseudomonas aeruginosa elastase structural gene , 1988, Journal of bacteriology.

[19]  A. Driessen,et al.  University of Groningen Accumulation of a nod Gene Inducer, the Flavonoid Naringenin, in the Cytoplasmic Membrane of Rhizobium leguminosarum biovar viciae Is Caused by the pH-Dependent Hydrophobicity of Naringenin Recourt, , 2017 .

[20]  V. Stewart,et al.  Structure of genes narL and narX of the nar (nitrate reductase) locus in Escherichia coli K-12 , 1989, Journal of bacteriology.

[21]  M. Nishiyama,et al.  Nucleotide sequence and transcriptional analysis of the Streptomyces griseus gene (afsA) responsible for A-factor biosynthesis , 1989, Journal of bacteriology.

[22]  E. Meighen,et al.  Purification and structural identification of an autoinducer for the luminescence system of Vibrio harveyi. , 1989, The Journal of biological chemistry.

[23]  T. Baldwin,et al.  Identification of the operator of the lux regulon from the Vibrio fischeri strain ATCC7744. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[24]  H. Spaink,et al.  Subcellular localization of the nodD gene product in Rhizobium leguminosarum , 1989, Journal of bacteriology.

[25]  P. Dunlap,et al.  Regulation of luminescence by cyclic AMP in cya-like and crp-like mutants of Vibrio fischeri , 1989, Journal of bacteriology.

[26]  S. Henikoff,et al.  Finding protein similarities with nucleotide sequence databases. , 1990, Methods in enzymology.

[27]  V. Braun,et al.  Novel two-component transmembrane transcription control: regulation of iron dicitrate transport in Escherichia coli K-12 , 1990, Journal of bacteriology.

[28]  M. Silverman,et al.  Cloning and nucleotide sequence of luxR, a regulatory gene controlling bioluminescence in Vibrio harveyi , 1990, Journal of bacteriology.

[29]  A. Hamood,et al.  Expression of the Pseudomonas aeruginosa toxA positive regulatory gene (regA) in Escherichia coli , 1990, Journal of bacteriology.

[30]  E. Ruby,et al.  Depressed light emission by symbiotic Vibrio fischeri of the sepiolid squid Euprymna scolopes , 1990, Journal of bacteriology.

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

[32]  T. Baldwin,et al.  Use of regulated cell lysis in a lethal genetic selection in Escherichia coli: identification of the autoinducer-binding region of the LuxR protein from Vibrio fischeri ATCC 7744 , 1990, Journal of bacteriology.

[33]  T. Baldwin,et al.  The Vibrio fischeri LuxR protein is capable of bidirectional stimulation of transcription and both positive and negative regulation of the luxR gene , 1991, Journal of bacteriology.

[34]  C. Hughes,et al.  Bacterial swarming: an example of prokaryotic differentiation and multicellular behaviour. , 1991, Science progress.

[35]  E. Ruby,et al.  Symbiont recognition and subsequent morphogenesis as early events in an animal-bacterial mutualism. , 1991, Science.

[36]  M. Gambello,et al.  Pseudomonas aeruginosa LasA: a second elastase under the transcriptional control of lasR , 1991, Molecular microbiology.

[37]  D. Kahn,et al.  Modular structure of FixJ: homology of the transcriptional activator domain with the -35 binding domain of sigma factors. , 1991, Molecular microbiology.

[38]  L. Rothfield,et al.  A factor that positively regulates cell division by activating transcription of the major cluster of essential cell division genes of Escherichia coli. , 1991, The EMBO journal.

[39]  E. Meighen,et al.  Molecular biology of bacterial bioluminescence. , 1991, Microbiological reviews.

[40]  E. Greenberg,et al.  The C-terminal region of the Vibrio fischeri LuxR protein contains an inducer-independent lux gene activating domain. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[41]  M. Gambello,et al.  Cloning and characterization of the Pseudomonas aeruginosa lasR gene, a transcriptional activator of elastase expression , 1991, Journal of bacteriology.

[42]  A. Grossman,et al.  The spo0K locus of Bacillus subtilis is homologous to the oligopeptide permease locus and is required for sporulation and competence , 1991, Journal of bacteriology.

[43]  S. Ulitzur,et al.  Formation of the LuxR protein in the Vibrio fischeri lux system is controlled by HtpR through the GroESL proteins , 1992, Journal of bacteriology.

[44]  H. Cuypers,et al.  NosR, a membrane-bound regulatory component necessary for expression of nitrous oxide reductase in denitrifying Pseudomonas stutzeri , 1992, Journal of bacteriology.

[45]  P. Dunlap,et al.  Cell density-dependent modulation of the Vibrio fischeri luminescence system in the absence of autoinducer and LuxR protein , 1992, Journal of bacteriology.

[46]  M K Winson,et al.  Small molecule-mediated density-dependent control of gene expression in prokaryotes: bioluminescence and the biosynthesis of carbapenem antibiotics. , 1992, FEMS microbiology letters.

[47]  E. Ruby,et al.  A squid that glows in the night: development of an animal-bacterial mutualism , 1992, Journal of bacteriology.

[48]  E. Greenberg,et al.  Evidence that GroEL, not sigma 32, is involved in transcriptional regulation of the Vibrio fischeri luminescence genes in Escherichia coli , 1992, Journal of bacteriology.

[49]  G. Salmond,et al.  A general role for the lux autoinducer in bacterial cell signalling: control of antibiotic biosynthesis in Erwinia. , 1992, Gene.

[50]  M. Silverman,et al.  The luxR gene product of Vibrio harveyi is a transcriptional activator of the lux promoter , 1992, Journal of bacteriology.

[51]  Purification and molecular cloning of a butyrolactone autoregulator receptor from Streptomyces virginiae. , 1992, The Journal of biological chemistry.

[52]  J. S. Parkinson,et al.  Communication modules in bacterial signaling proteins. , 1992, Annual review of genetics.

[53]  G. Hayman,et al.  Opine catabolism and conjugal transfer of the nopaline Ti plasmid pTiC58 are coordinately regulated by a single repressor. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[54]  S. C. Winans Two-way chemical signaling in Agrobacterium-plant interactions. , 1992, Microbiological reviews.

[55]  J. Downie,et al.  Molecular characterization and regulation of the rhizosphere-expressed genes rhiABCR that can influence nodulation by Rhizobium leguminosarum biovar viciae , 1992, Journal of bacteriology.

[56]  S. C. Winans,et al.  The A. tumefaciens transcriptional activator OccR causes a bend at a target promoter, which is partially relaxed by a plant tumor metabolite , 1992, Cell.

[57]  T. Baldwin,et al.  Identification of a distantly located regulatory element in the luxD gene required for negative autoregulation of the Vibrio fischeri luxR gene. , 1992, The Journal of biological chemistry.

[58]  E. Greenberg,et al.  Genetic dissection of DNA binding and luminescence gene activation by the Vibrio fischeri LuxR protein , 1992, Journal of bacteriology.

[59]  J. Findlay,et al.  The haemoglobin‐like protein (HMP) of Escherichia coli has ferrisiderophore reductase activity and its C‐terminal domain shares homology with ferredoxin NADP+ reductases , 1992, FEBS letters.

[60]  S. Horinouchi,et al.  Autoregulatory factors and communication in actinomycetes. , 1992, Annual review of microbiology.

[61]  Don B. Clewell,et al.  Bacterial sex pheromone-induced plasmid transfer , 1993, Cell.

[62]  P. Murphy,et al.  Agrobacterium conjugation and gene regulation by N-acyl-L-homoserine lactones , 1993, Nature.

[63]  P. Reeves,et al.  The lux autoinducer regulates the production of exoenzyme virulence determinants in Erwinia carotovora and Pseudomonas aeruginosa. , 1993, The EMBO journal.

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

[65]  M. Gambello,et al.  LasR of Pseudomonas aeruginosa is a transcriptional activator of the alkaline protease gene (apr) and an enhancer of exotoxin A expression , 1993, Infection and immunity.

[66]  M. Pirhonen,et al.  A small diffusible signal molecule is responsible for the global control of virulence and exoenzyme production in the plant pathogen Erwinia carotovora. , 1993, The EMBO journal.

[67]  M. Suzuki Common features in DNA recognition helices of eukaryotic transcription factors. , 1993, The EMBO journal.

[68]  M. Gambello,et al.  Expression of Pseudomonas aeruginosa virulence genes requires cell-to-cell communication. , 1993, Science.

[69]  E. Meighen,et al.  Biosynthesis and stereochemistry of the autoinducer controlling luminescence in Vibrio harveyi , 1993, Journal of bacteriology.

[70]  Stephen K. Farrand,et al.  Conjugation factor of Agrobacterium tumefaciens regulates Ti plasmid transfer by autoinduction , 1993, Nature.

[71]  P. Dunlap,et al.  Physiological, biochemical and genetic control of bacterial bioluminescence. , 1993, Advances in microbial physiology.

[72]  E. Greenberg,et al.  The Vibrio fischeri luminescence gene activator LuxR is a membrane-associated protein , 1993, Journal of bacteriology.

[73]  B. Bassler,et al.  Intercellular signalling in Vibrio harveyi: sequence and function of genes regulating expression of luminescence , 1993, Molecular microbiology.

[74]  V. Stewart,et al.  Autogenous regulation of gene expression , 1993, Journal of bacteriology.

[75]  E. Greenberg,et al.  Structure of the autoinducer required for expression of Pseudomonas aeruginosa virulence genes. , 1994, Proceedings of the National Academy of Sciences of the United States of America.