Dynamic regulation of N-acyl-homoserine lactone production and degradation in Pseudomonas putida IsoF.

The biocontrol strain Pseudomonas putida IsoF, which was isolated from a tomato rhizosphere, is a known N-acyl-homoserine lactone (AHL) producer with only one LuxI/LuxR-like quorum-sensing (QS) system. The production and degradation of AHLs were analysed in different growth phases of the bacterium. Using the analytical tools of ultra performance liquid chromatography and high resolution MS, it was possible to determine not only the various AHLs synthesized over time but also their degradation products. 3-oxo-decanoyl-homoserine lactone was found to be the dominant AHL, which reached its maximum in the early logarithmic growth phase. Although the pH of the medium was neutral, the AHLs were degraded thereafter rapidly to the corresponding homoserines and other metabolites. The proposed lactonase gene of P. putida IsoF could not be identified, because it is apparently quite different from hitherto described lactonases. The analytical data were used to calculate the rates and thresholds of AHL production by mathematical modelling, allowing quantitative predictions and a further understanding of the QS-based regulations in this bacterium. This study, combining microbiological, chemical and mathematical approaches, suggests that AHL degradation is an integral part of the whole autoinducer circuit of P. putida IsoF.

[1]  I. Joint,et al.  Turnover of quorum sensing signal molecules modulates cross-kingdom signalling. , 2009, Environmental microbiology.

[2]  G. Manco,et al.  Evolution in the amidohydrolase superfamily: substrate-assisted gain of function in the E183K mutant of a phosphotriesterase-like metal-carboxylesterase. , 2009, Biochemistry.

[3]  M. Schloter,et al.  Endophytic Root Colonization of Gramineous Plants by Herbaspirillum Frisingense , 2008 .

[4]  J. Caballero-Mellado,et al.  The new group of non-pathogenic plant-associated nitrogen-fixing Burkholderia spp. shares a conserved quorum-sensing system, which is tightly regulated by the RsaL repressor. , 2008, Microbiology.

[5]  Burkhard A. Hense,et al.  Sensitivity of the quorum sensing system is achieved by low pass filtering , 2008, Biosyst..

[6]  P. Oger,et al.  Quorum-quenching Lactonases Defines a Novel Class of Large-spectrum -encoded Enzyme Rhodococcus Qsda a Supplemental Material , 2007 .

[7]  T. Cataldi,et al.  Profiling of N-acyl-homoserine lactones by liquid chromatography coupled with electrospray ionization and a hybrid quadrupole linear ion-trap and Fourier-transform ion-cyclotron-resonance mass spectrometry (LC-ESI-LTQ-FTICR-MS). , 2007, Journal of mass spectrometry : JMS.

[8]  P. Schröder,et al.  Uptake, degradation and chiral discrimination of N-acyl-D/L-homoserine lactones by barley (Hordeum vulgare) and yam bean (Pachyrhizus erosus) plants , 2007, Analytical and bioanalytical chemistry.

[9]  C. Kuttler,et al.  The hydrolysis of unsubstituted N-acylhomoserine lactones to their homoserine metabolites. Analytical approaches using ultra performance liquid chromatography. , 2007, Journal of chromatography. A.

[10]  K. Winzer,et al.  Look who's talking: communication and quorum sensing in the bacterial world , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[11]  A. Griffin,et al.  Evolutionary theory of bacterial quorum sensing: when is a signal not a signal? , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[12]  L. Eberl,et al.  A Marine Mesorhizobium sp. Produces Structurally Novel Long-Chain N-Acyl-l-Homoserine Lactones , 2007, Applied and Environmental Microbiology.

[13]  Burkhard A. Hense,et al.  Does efficiency sensing unify diffusion and quorum sensing? , 2007, Nature Reviews Microbiology.

[14]  K. Timmis,et al.  Shift from Acetoclastic to H2-Dependent Methanogenesis in a West Siberian Peat Bog at Low pH Values and Isolation of an Acidophilic Methanobacterium Strain , 2007, Applied and Environmental Microbiology.

[15]  Paul Stoodley,et al.  The effect of the chemical, biological, and physical environment on quorum sensing in structured microbial communities , 2006, Analytical and bioanalytical chemistry.

[16]  P. Williams,et al.  Comprehensive profiling of N-acylhomoserine lactones produced by Yersinia pseudotuberculosis using liquid chromatography coupled to hybrid quadrupole–linear ion trap mass spectrometry , 2007, Analytical and bioanalytical chemistry.

[17]  J. Leadbetter,et al.  Acyl-HSL signal decay: intrinsic to bacterial cell-cell communications. , 2007, Advances in applied microbiology.

[18]  J. Fekete,et al.  Identification of bacterial N-acylhomoserine lactones (AHLs) with a combination of ultra-performance liquid chromatography (UPLC), ultra-high-resolution mass spectrometry, and in-situ biosensors , 2007, Analytical and bioanalytical chemistry.

[19]  Juan E. González,et al.  Messing with Bacterial Quorum Sensing , 2006, Microbiology and Molecular Biology Reviews.

[20]  Guonan Chen,et al.  Development and application of a method for the analysis of N-acylhomoserine lactones by solid-phase extraction and ultra high pressure liquid chromatography. , 2006, Journal of chromatography. A.

[21]  Giuseppe Manco,et al.  The latent promiscuity of newly identified microbial lactonases is linked to a recently diverged phosphotriesterase. , 2006, Biochemistry.

[22]  C. Kuttler,et al.  Cell–cell communication by quorum sensing and dimension-reduction , 2006, Journal of mathematical biology.

[23]  L. Eberl,et al.  Induction of systemic resistance in tomato by N-acyl-L-homoserine lactone-producing rhizosphere bacteria. , 2006, Plant, cell & environment.

[24]  J. Dubern,et al.  The ppuI-rsaL-ppuR Quorum-Sensing System Regulates Biofilm Formation of Pseudomonas putida PCL1445 by Controlling Biosynthesis of the Cyclic Lipopeptides Putisolvins I and II , 2006, Journal of bacteriology.

[25]  E. Greenberg,et al.  A network of networks: quorum-sensing gene regulation in Pseudomonas aeruginosa. , 2006, International journal of medical microbiology : IJMM.

[26]  Oscar P. Kuipers,et al.  Phenotypic variation in bacteria: the role of feedback regulation , 2006, Nature Reviews Microbiology.

[27]  A. Goryachev,et al.  Systems analysis of a quorum sensing network: design constraints imposed by the functional requirements, network topology and kinetic constants. , 2006, Bio Systems.

[28]  F. Polticelli,et al.  The Quorum-Sensing Negative Regulator RsaL of Pseudomonas aeruginosa Binds to the lasI Promoter , 2006, Journal of bacteriology.

[29]  Joon-Hee Lee,et al.  Activity of purified QscR, a Pseudomonas aeruginosa orphan quorum‐sensing transcription factor , 2006, Molecular microbiology.

[30]  R. Lamont,et al.  Bacterial cell-to-cell communication : role in virulence and pathogenesis , 2006 .

[31]  R. Pukall,et al.  Discovery of Complex Mixtures of Novel Long‐Chain Quorum Sensing Signals in Free‐Living and Host‐Associated Marine Alphaproteobacteria , 2005, Chembiochem : a European journal of chemical biology.

[32]  L. Gram,et al.  Ecology, Inhibitory Activity, and Morphogenesis of a Marine Antagonistic Bacterium Belonging to the Roseobacter Clade , 2005, Applied and Environmental Microbiology.

[33]  S. Farrand,et al.  Activation of the phz Operon of Pseudomonas fluorescens 2-79 Requires the LuxR Homolog PhzR, N-(3-OH-Hexanoyl)-l-Homoserine Lactone Produced by the LuxI Homolog PhzI, and a cis-Acting phz Box , 2005, Journal of bacteriology.

[34]  J. Leadbetter,et al.  Rapid Acyl-Homoserine Lactone Quorum Signal Biodegradation in Diverse Soils , 2005, Applied and Environmental Microbiology.

[35]  R. Kolter,et al.  A Pseudomonas aeruginosa quorum‐sensing molecule influences Candida albicans morphology , 2004, Molecular microbiology.

[36]  Vittorio Venturi,et al.  Regulation of the N-Acyl Homoserine Lactone-Dependent Quorum-Sensing System in Rhizosphere Pseudomonas putida WCS358 and Cross-Talk with the Stationary-Phase RpoS Sigma Factor and the Global Regulator GacA , 2004, Applied and Environmental Microbiology.

[37]  M. Elowitz,et al.  Modeling a synthetic multicellular clock: repressilators coupled by quorum sensing. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[38]  R. Fray,et al.  Integration of environmental and host‐derived signals with quorum sensing during plant–microbe interactions , 2004, Cellular microbiology.

[39]  K. Nealson.  Autoinduction of bacterial luciferase , 1977, Archives of Microbiology.

[40]  E. Greenberg,et al.  The Vibrio fischeri quorum‐sensing systems ain and lux sequentially induce luminescence gene expression and are important for persistence in the squid host , 2003, Molecular microbiology.

[41]  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.

[42]  S. Molin,et al.  Identification and Characterization of an N-Acylhomoserine Lactone-Dependent Quorum-Sensing System in Pseudomonas putida Strain IsoF , 2002, Applied and Environmental Microbiology.

[43]  Steve Atkinson,et al.  N-Acylhomoserine Lactones Undergo Lactonolysis in a pH-, Temperature-, and Acyl Chain Length-Dependent Manner during Growth of Yersinia pseudotuberculosis and Pseudomonas aeruginosa , 2002, Infection and Immunity.

[44]  E. Greenberg,et al.  Signalling: Listening in on bacteria: acyl-homoserine lactone signalling , 2002, Nature Reviews Molecular Cell Biology.

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

[46]  Lian-Hui Zhang,et al.  Genetic control of quorum-sensing signal turnover in Agrobacterium tumefaciens , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[47]  L. Eberl,et al.  Visualization of N-Acylhomoserine Lactone-Mediated Cell-Cell Communication between Bacteria Colonizing the Tomato Rhizosphere , 2001, Applied and Environmental Microbiology.

[48]  J. Keener,et al.  A mathematical model for quorum sensing in Pseudomonas aeruginosa , 2001, Bulletin of mathematical biology.

[49]  S. Kjelleberg,et al.  A novel and sensitive method for the quantification of N-3-oxoacyl homoserine lactones using gas chromatography-mass spectrometry: application to a model bacterial biofilm. , 2000, Environmental microbiology.

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

[51]  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.

[52]  S. Farrand,et al.  Production of acyl-homoserine lactone quorum-sensing signals by gram-negative plant-associated bacteria. , 1998, Molecular plant-microbe interactions : MPMI.

[53]  John W. Beaber,et al.  Analogs of the Autoinducer 3-Oxooctanoyl-Homoserine Lactone Strongly Inhibit Activity of the TraR Protein ofAgrobacterium tumefaciens , 1998, Journal of bacteriology.

[54]  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.

[55]  K. Rinehart,et al.  Detecting and characterizing N-acyl-homoserine lactone signal molecules by thin-layer chromatography. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[56]  E. Greenberg,et al.  A second N-acylhomoserine lactone signal produced by Pseudomonas aeruginosa. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[57]  E. Greenberg,et al.  Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators , 1994, Journal of bacteriology.

[58]  E. Greenberg,et al.  Physical and functional maps of the luminescence gene cluster in an autoinducer-deficient Vibrio fischeri strain isolated from a squid light organ , 1992, Journal of bacteriology.

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

[60]  L. Lewandowski,et al.  A mutation suppressing streptomycin dependence. I. An effect on ribosome function. , 1967, Journal of molecular biology.

[61]  O. Maaløe,et al.  DNA replication and the division cycle in Escherichia coli , 1967 .