Enzyme-Mediated Quenching of the Pseudomonas Quinolone Signal (PQS) Promotes Biofilm Formation of Pseudomonas aeruginosa by Increasing Iron Availability

Beatrix Tettmann1, Christine Niewerth2, Frank Kirschhöfer1, Anke Neidig1, Andreas Dötsch1, Gerald Brenner‐Weiß1, Susanne Fetzner2, Joerg Overhage1
1Karlsruhe Institute of Technology, Institute of Functional Interfaces, Karlsruhe, Germany
2Institute for Molecular Microbiology and Biotechnology, University of Münster, Münster, Germany

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Anders, 2015, HTSeq - a Python framework to work with high-throughput sequencing data, Bioinformatics, 31, 166, 10.1093/bioinformatics/btu638

Banin, 2005, Iron and Pseudomonas aeruginosa biofilm formation, Proc. Natl. Acad. Sci. U.S.A., 102, 11076, 10.1073/pnas.0504266102

Beermann, 2007, Stability, unfolding, and structural changes of cofactor-free 1H-3-hydroxy-4-oxoquinaldine 2,4-dioxygenase, Biochemistry, 46, 4241, 10.1021/bi0622423

Bredenbruch, 2006, The Pseudomonas aeruginosa quinolone signal (PQS) has an iron-chelating activity, Environ. Microbiol., 8, 1318, 10.1111/j.1462-2920.2006.01025.x

Breidenstein, 2012, The Lon protease is essential for full virulence in Pseudomonas aeruginosa, PLoS ONE, 7, e49123, 10.1371/journal.pone.0049123

Caballero, 2001, Pseudomonas aeruginosa protease IV enzyme assays and comparison to other Pseudomonas proteases, Anal. Biochem., 290, 330, 10.1006/abio.2001.4999

Déziel, 2005, The contribution of MvfR to Pseudomonas aeruginosa pathogenesis and quorum sensing circuitry regulation: multiple quorum sensing-regulated genes are modulated without affecting lasRI, rhlRI or the production of N-acyl-L-homoserine lactones, Mol. Microbiol., 55, 998, 10.1111/j.1365-2958.2004.04448.x

Diggle, 2007, The Pseudomonas aeruginosa 4-quinolone signal molecules HHQ and PQS play multifunctional roles in quorum sensing and iron entrapment, Chem. Biol., 14, 87, 10.1016/j.chembiol.2006.11.014

Diggle, 2003, The Pseudomonas aeruginosa quinolone signal molecule overcomes the cell density-dependency of the quorum sensing hierarchy, regulates rhl-dependent genes at the onset of stationary phase and can be produced in the absence of LasR, Mol. Microbiol., 50, 29, 10.1046/j.1365-2958.2003.03672.x

Elias, 2011, FvbA is required for vibriobactin utilization in Pseudomonas aeruginosa, Microbiology, 157, 2172, 10.1099/mic.0.044768-0

Fetzner, 2015, Quorum quenching enzymes, J. Biotechnol., 201, 2, 10.1016/j.jbiotec.2014.09.001

Frangipani, 2014, The Gac/Rsm and cyclic-di-GMP signalling networks coordinately regulate iron uptake in Pseudomonas aeruginosa, Environ. Microbiol., 16, 676, 10.1111/1462-2920.12164

Frerichs-Deeken, 2004, Dioxygenases without requirement for cofactors and their chemical model reaction: compulsory order ternary complex mechanism of 1H-3-hydroxy-4-oxoquinaldine 2,4-dioxygenase involving general base catalysis by histidine 251 and single-electron oxidation of the substrate dianion, Biochemistry, 43, 14485, 10.1021/bi048735u

Friedman, 2004, Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms, Mol. Microbiol., 51, 675, 10.1046/j.1365-2958.2003.03877.x

García-Contreras, 2013, Resistance to quorum-quenching compounds, Appl. Environ. Microbiol., 79, 6840, 10.1128/aem.02378-13

Gellatly, 2013, Pseudomonas aeruginosa: new insights into pathogenesis and host defenses, Path. Dis., 67, 159, 10.1111/2049-632x.12033

Guo, 2014, PqsR-dependent and PqsR-independent regulation of motility and biofilm formation by PQS in Pseudomonas aeruginosa PAO1, J. Basic Microbiol., 54, 633, 10.1002/jobm.201300091

Hänsch, 2014, The Pseudomonas quinolone signal (PQS) stimulates chemotaxis of polymorphonuclear neutrophils, J. Appl. Biomater. Funct. Mater., 12, 21, 10.5301/jabfm.5000204

Hassett, 1997, An operon containing fumC and sodA encoding fumarase C and manganese superoxide dismutase is controlled by the ferric uptake regulator in Pseudomonas aeruginosa: fur mutants produce elevated alginate levels, J. Bacteriol., 179, 1452, 10.1128/jb.179.5.1452-1459.1997

Häussler, 2008, The Pseudomonas quinolone signal (PQS) balances life and death in Pseudomonas aeruginosa populations, PLoS Pathog., 4, e1000166, 10.1371/journal.ppat.1000166

Herigstad, 2001, How to optimize the drop plate method for enumerating bacteria, J. Microbiol. Methods, 44, 121, 10.1016/s0167-7012(00)00241-4

Hooi, 2004, Differential immune modulatory activity of Pseudomonas aeruginosa quorum-sensing signal molecules, Infect. Immun., 72, 6463, 10.1128/iai.72.11.6463-6470.2004

Hutchison, 1999, Pathogenicity of microbes associated with cystic fibrosis, Microbes Infect., 1, 1005, 10.1016/S1286-4579(99)80518-8

Langmead, 2012, Fast gapped-read alignment with Bowtie 2, Nat. Methods, 9, 357, 10.1038/nmeth.1923

Leduc, 2007, The Pseudomonas aeruginosa LasB metalloproteinase regulates the human urokinase-type plasminogen activator receptor through domain-specific endoproteolysis, Infect. Immun., 75, 3848, 10.1128/iai.00015-07

Lépine, 2003, A stable isotope dilution assay for the quantification of the Pseudomonas quinolone signal in Pseudomonas aeruginosa cultures, Biochim. Biophys. Acta, 1622, 36, 10.1016/s0304-4165(03)00103-x

Lesic, 2007, Inhibitors of pathogen intercellular signals as selective anti-infective compounds, PLoS Pathog., 3, e126, 10.1371/journal.ppat.0030126

Li, 2013, Hydrophobic liquid-infused porous polymer surfaces for antibacterial applications, ACS Appl. Mater. Interfaces, 5, 6704, 10.1021/am401532z

Liberati, 2006, An ordered, nonredundant library of Pseudomonas aeruginosa strain PA14 transposon insertion mutants, Proc. Natl. Acad. Sci. U.S.A., 103, 2833, 10.1073/pnas.0511100103

Love, 2014, Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2, Genome Biol., 15, 550, 10.1186/s13059-014-0550-8

Lu, 2014, Overcoming the unexpected functional inversion of a PqsR antagonist in Pseudomonas aeruginosa: an in vivo potent antivirulence agent targeting pqs quorum sensing, Angew. Chem. Int. Ed. Engl., 53, 1109, 10.1002/anie.201307547

Mashburn, 2005, Membrane vesicles traffic signals and facilitate group activities in a prokaryote, Nature, 437, 422, 10.1038/nature03925

Murray, 2012, The carbon monoxide releasing molecule CORM-2 attenuates Pseudomonas aeruginosa biofilm formation, PLoS ONE, 7, e35499, 10.1371/journal.pone.0035499

Musk, 2005, Iron salts perturb biofilm formation and disrupt existing biofilms of Pseudomonas aeruginosa, Chem. Biol., 12, 789, 10.1016/j.chembiol.2005.05.007

Müsken, 2010, Genetic determinants of Pseudomonas aeruginosa biofilm establishment, Microbiology, 156, 431, 10.1099/mic.0.033290-0

Ochsner, 2002, GeneChip® expression analysis of the iron starvation response in Pseudomonas aeruginosa: identification of novel pyoverdine biosynthesis genes, Mol. Microbiol., 45, 1277, 10.1046/j.1365-2958.2002.03084.x

Overhage, 2008, Swarming of Pseudomonas aeruginosa is a complex adaptation leading to increased production of virulence factors and antibiotic resistance, J. Bacteriol., 190, 2671, 10.1128/jb.01659-07

Patriquin, 2008, Influence of quorum sensing and iron on twitching motility and biofilm formation in Pseudomonas aeruginosa, J. Bacteriol., 190, 662, 10.1128/jb.01473-07

Pesci, 1999, Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa, Proc. Natl. Acad. Sci. U.S.A., 11229

Pustelny, 2009, Dioxygenase-mediated quenching of quinolone-dependent quorum sensing in Pseudomonas aeruginosa, Chem. Biol., 16, 1259, 10.1016/j.chembiol.2009.11.013

Rahme, 1995, Common virulence factors for bacterial pathogenicity in plants and animals, Science, 268, 1899, 10.1126/science.7604262

Rajan, 2002, Pulmonary infections in patients with cystic fibrosis, Semin. Respir. Infect., 17, 47, 10.1053/srin.2002.31690

Schweizer, 1996, Regulation of glycerol metabolism in Pseudomonas aeruginosa: characterization of the glpR repressor gene, J. Bacteriol., 178, 5215, 10.1128/jb.178.17.5215-5221.1996

Singh, 2004, Iron sequestration by human lactoferrin stimulates P. aeruginosa surface motility and blocks biofilm formation, Biometals, 17, 267, 10.1023/B:BIOM.0000027703.77456.27

Singh, 2002, A component of innate immunity prevents bacterial biofilm development, Nature, 417, 552, 10.1038/417552a

Skindersoe, 2009, Pseudomonas aeruginosa quorum-sensing signal molecules interfere with dendritic cell-induced T-cell proliferation, FEMS Immunol. Med. Microbiol., 55, 335, 10.1111/j.1574-695X.2008.00533.x

Sonnleitner, 2011, Small RNAs as regulators of primary and secondary metabolism in Pseudomonas species, Appl. Microbiol. Biotechnol., 91, 63, 10.1007/s00253-011-3332-1

Storz, 2012, Validation of PqsD as an anti-biofilm target in Pseudomonas aeruginosa by development of small-molecule inhibitors, J. Am. Chem. Soc., 134, 16143, 10.1021/ja3072397

Tettmann, 2014, Knockout of extracytoplasmic function sigma factor ECF-10 affects stress resistance and biofilm formation in Pseudomonas putida KT2440, Appl. Environ. Microbiol., 80, 4911, 10.1128/aem.01291-14

Thaden, 2010, Quorum-sensing regulation of a copper toxicity system in Pseudomonas aeruginosa, J. Bacteriol., 192, 2557, 10.1128/jb.01528-09

Wade, 2005, Regulation of Pseudomonas quinolone signal synthesis in Pseudomonas aeruginosa, J. Bacteriol., 187, 4372, 10.1128/JB.187.13.4372-4380.2005

Wells, 1952, Ozonization of some antibiotic substances produced by Pseudomonas aeruginosa, J. Biol. Chem., 196, 321, 10.1016/S0021-9258(18)55736-7

Wilderman, 2004, Identification of tandem duplicate regulatory small RNAs in Pseudomonas aeruginosa involved in iron homeostasis, Proc. Natl. Acad. Sci. U.S.A., 101, 9792, 10.1073/pnas.0403423101

Williams, 2007, Look who's talking: communication and quorum sensing in the bacterial world, Philos. Trans. R. Soc. London Ser B, 362, 1119, 10.1098/rstb.2007.2039

Winsor, 2009, Pseudomonas Genome Database: facilitating user-friendly, comprehensive comparisons of microbial genomes, Nucl. Acids Res., 37, D483, 10.1093/nar/gkn861

Xiao, 2006, MvfR, a key Pseudomonas aeruginosa pathogenicity LTTR-class regulatory protein, has dual ligands, Mol. Microbiol., 62, 1689, 10.1111/j.1365-2958.2006.05462.x

Yang, 2007, Effects of iron on DNA release and biofilm development by Pseudomonas aeruginosa, Microbiology, 153, 1318, 10.1099/mic.0.2006/004911-0

Yeung, 2011, The sensor kinase CbrA is a global regulator that modulates metabolism, virulence, and antibiotic resistance in Pseudomonas aeruginosa, J. Bacteriol., 193, 918, 10.1128/jb.00911-10