Quorum sensing as an integral component of gene regulatory networks in Gram-negative bacteria.

Bacterial cell-to-cell communication (quorum sensing) relies upon the interaction of a small diffusible signal molecule with a sensor or transcriptional activator to couple gene expression with cell population density. In Gram-negative bacteria, it is now clear that N-acylhomoserine lactones bind directly to LuxR homologues and can be synthesized via one of three unrelated bacterial protein families and by transgenic plants. New chemical classes of signal molecules have been identified, some of which exhibit crosstalk with N-acylhomoserine-lactone-mediated quorum sensing. As the determinant of cell population density, quorum sensing is emerging as an integral component of bacterial global gene regulatory networks responsible for facilitating bacterial adaptation to environmental stress. N-acylhomoserine lactones are produced during experimental animal and human infections, and a function beyond quorum sensing has been suggested by their intrinsic immunomodulatory and pharmacological activities.

[1]  G. Salmond,et al.  In vitro biosynthesis of the Pseudomonas aeruginosa quorum‐sensing signal molecule N‐butanoyl‐L‐homoserine lactone , 1998, Molecular microbiology.

[2]  C. Reimmann,et al.  The global activator GacA of Pseudomonas aeruginosa PAO positively controls the production of the autoinducer N‐butyryl‐homoserine lactone and the formation of the virulence factors pyocyanin, cyanide, and lipase , 1997, Molecular microbiology.

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

[4]  P. Williams,et al.  Plants genetically modified to produce N-acylhomoserine lactones communicate with bacteria , 1999, Nature Biotechnology.

[5]  P. Revell,et al.  A chromosomally encoded regulator is required for expression of the Yersinia enterocolitica inv gene and for virulence , 2000, Molecular microbiology.

[6]  T. Cover,et al.  Intercellular Communication in Helicobacter pylori: luxS Is Essential for the Production of an Extracellular Signaling Molecule , 2000, Infection and Immunity.

[7]  R. England Microbial Signalling and Communication , 1999 .

[8]  K. Tanaka,et al.  A hierarchical quorum‐sensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhIR (VsmR) to expression of the stationary‐phase sigma factor RpoS , 1996, Molecular microbiology.

[9]  J. García‐Lara,et al.  An extracellular factor regulates expression of sdiA, a transcriptional activator of cell division genes in Escherichia coli , 1996, Journal of bacteriology.

[10]  Yinping Qin,et al.  Quorum‐sensing signal binding results in dimerization of TraR and its release from membranes into the cytoplasm , 2000, The EMBO journal.

[11]  P. Dunlap,et al.  LuxR- and Acyl-Homoserine-Lactone-Controlled Non-luxGenes Define a Quorum-Sensing Regulon in Vibrio fischeri , 2000, Journal of bacteriology.

[12]  E. Greenberg,et al.  Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

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

[14]  Lian-Hui Zhang,et al.  AiiA, an enzyme that inactivates the acylhomoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora , 2000 .

[15]  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.

[16]  Gary M. Dunny,et al.  Cell-cell signaling in bacteria , 1999 .

[17]  M Welch,et al.  N‐acyl homoserine lactone binding to the CarR receptor determines quorum‐sensing specificity in Erwinia , 2000, The EMBO journal.

[18]  P. Williams,et al.  Stimulation of bacterial growth by heat-stable, norepinephrine-induced autoinducers. , 1999, FEMS microbiology letters.

[19]  D. Wheeler,et al.  The Pseudomonas aeruginosaQuorum-Sensing Signal MoleculeN-(3-Oxododecanoyl)-l-Homoserine Lactone Has Immunomodulatory Activity , 1998, Infection and Immunity.

[20]  M. Surette,et al.  Quorum sensing in Escherichia coli, Salmonella typhimurium, and Vibrio harveyi: a new family of genes responsible for autoinducer production. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[21]  D. Pritchard,et al.  Quorum sensing and the population-dependent control of virulence. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[22]  P. Seed,et al.  Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa , 1997, Journal of bacteriology.

[23]  Kun-Soo Kim,et al.  Octopine‐type Ti plasmids code for a mannopine‐inducible dominant‐negative allele of traR, the quorum‐sensing activator that regulates Ti plasmid conjugal transfer , 1998, Molecular microbiology.

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

[25]  S. Diggle,et al.  The Pseudomonas aeruginosa Lectins PA-IL and PA-IIL Are Controlled by Quorum Sensing and by RpoS , 2000, Journal of bacteriology.

[26]  S. Rice,et al.  Quorum‐sensing cross talk: isolation and chemical characterization of cyclic dipeptides from Pseudomonas aeruginosa and other Gram‐negative bacteria , 1999, Molecular microbiology.

[27]  M. Schell,et al.  Joint Transcriptional Control of xpsR, the Unusual Signal Integrator of the Ralstonia solanacearum Virulence Gene Regulatory Network, by a Response Regulator and a LysR-Type Transcriptional Activator , 1998, Journal of bacteriology.

[28]  B. Iglewski,et al.  Active Efflux and Diffusion Are Involved in Transport of Pseudomonas aeruginosa Cell-to-Cell Signals , 1999, Journal of bacteriology.

[29]  P. Dunlap,et al.  Acylhomoserine Lactone Synthase Activity of the Vibrio fischeri AinS Protein , 1999, Journal of bacteriology.

[30]  F. O'Gara,et al.  The biocontrol strain Pseudomonas fluorescens F113 produces the Rhizobium small bacteriocin, N-(3-hydroxy-7-cis-tetradecenoyl)homoserine lactone, via HdtS, a putative novel N-acylhomoserine lactone synthase. , 2000, Microbiology.

[31]  Shouguang Jin,et al.  migA, a quorum-responsive gene of Pseudomonas aeruginosa, is highly expressed in the cystic fibrosis lung environment and modifies low-molecular-mass lipopolysaccharide. , 2000, Microbiology.

[32]  G. Pessi,et al.  Transcriptional Control of the Hydrogen Cyanide Biosynthetic Genes hcnABC by the Anaerobic Regulator ANR and the Quorum-Sensing Regulators LasR and RhlR inPseudomonas aeruginosa , 2000, Journal of bacteriology.

[33]  Matthew R. Parsek,et al.  Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms , 2000, Nature.

[34]  M. Schell,et al.  Hierarchical autoinduction in Ralstonia solanacearum: control of acyl-homoserine lactone production by a novel autoregulatory system responsive to 3-hydroxypalmitic acid methyl ester , 1997, Journal of bacteriology.

[35]  F. Wisniewski-Dyé,et al.  The regulatory locus cinRI in Rhizobium leguminosarum controls a network of quorum‐sensing loci , 2000, Molecular microbiology.

[36]  B. Bassler,et al.  Regulation of quorum sensing in Vibrio harveyi by LuxO and Sigma‐54 , 2000, Molecular microbiology.

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

[38]  Y. Liu,et al.  Identification of a global repressor gene, rsmA, of Erwinia carotovora subsp. carotovora that controls extracellular enzymes, N-(3-oxohexanoyl)-L-homoserine lactone, and pathogenicity in soft-rotting Erwinia spp , 1995, Journal of bacteriology.

[39]  D. Coplin,et al.  A negative regulator mediates quorum-sensing control of exopolysaccharide production in Pantoea stewartii subsp. stewartii. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[40]  S. Molin,et al.  Detection of N-acylhomoserine lactones in lung tissues of mice infected with Pseudomonas aeruginosa. , 2000, Microbiology.

[41]  A. Maurelli,et al.  Shigella flexneri LuxS Quorum-Sensing System Modulates virB Expression but Is Not Essential for Virulence , 2001, Infection and Immunity.

[42]  M. Vasil,et al.  The pvc Gene Cluster ofPseudomonas aeruginosa: Role in Synthesis of the Pyoverdine Chromophore and Regulation by PtxR and PvdS , 1999, Journal of bacteriology.

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

[44]  S. C. Winans,et al.  Autoinducer binding by the quorum-sensing regulator TraR increases affinity for target promoters in vitro and decreases TraR turnover rates in whole cells. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[45]  M. Schell,et al.  An RpoS (σS) homologue regulates acylhomoserine lactone‐dependent autoinduction in Ralstonia solanacearum , 1998, Molecular microbiology.

[46]  B. Iglewski,et al.  The Pseudomonas Quinolone Signal Regulates rhl Quorum Sensing in Pseudomonas aeruginosa , 2000, Journal of bacteriology.

[47]  D. Wood,et al.  Two-Component Transcriptional Regulation of N -Acyl-Homoserine Lactone Production inPseudomonas aureofaciens , 1999, Applied and Environmental Microbiology.

[48]  P. Rather,et al.  Escherichia coli genes regulated by cell-to-cell signaling. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[49]  B. Bassler,et al.  Sequence and Function of LuxU: a Two-Component Phosphorelay Protein That Regulates Quorum Sensing inVibrio harveyi , 1999, Journal of bacteriology.

[50]  M. Cámara,et al.  The Pseudomonas aeruginosa quorum‐sensing signal molecule, N‐(3‐oxododecanoyl)‐L‐homoserine lactone, inhibits porcine arterial smooth muscle contraction , 1999, British journal of pharmacology.

[51]  Yang Liu,et al.  rsmC of the Soft-Rotting Bacterium Erwinia carotovora subsp. carotovora Negatively Controls Extracellular Enzyme and HarpinEcc Production and Virulence by Modulating Levels of Regulatory RNA (rsmB) and RNA-Binding Protein (RsmA) , 1999, Journal of bacteriology.

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

[53]  N. Thomson,et al.  The Rap and Hor proteins of Erwinia, Serratia and Yersinia: a novel subgroup in a growing superfamily of proteins regulating diverse physiological processes in bacterial pathogens , 1997, Molecular microbiology.

[54]  E. Greenberg,et al.  Regulation of Quorum Sensing by RpoS inPseudomonas aeruginosa , 2000, Journal of bacteriology.

[55]  V. Sperandio,et al.  Quorum sensing controls expression of the type III secretion gene transcription and protein secretion in enterohemorrhagic and enteropathogenic Escherichia coli. , 1999, Proceedings of the National Academy of Sciences of the United States of America.