Short Chain N-Acylhomoserine Lactone Production by Clinical Multidrug Resistant Klebsiella pneumoniae Strain CSG20

Klebsiella pneumoniae is one of the most common Gram-negative bacterial pathogens in clinical practice. It is associated with a wide range of disorders, ranging from superficial skin and soft tissue infections to potentially fatal sepsis in the lungs and blood stream. Quorum sensing, or bacterial cell-cell communication, refers to population density-dependent gene expression modulation. Quorum sensing in Proteobacteria relies on the production and sensing of signaling molecules which are mostly N-acylhomoserine lactones. Here, we report the identification of a multidrug resistant clinical isolate, K. pneumoniae strain CSG20, using matrix-assisted laser desorption ionization-time-of-flight (MALDI-TOF) mass spectrometry. We further confirmed quorum sensing activity in this strain with the use of high resolution tandem liquid chromatography quadrupole mass spectrometry and provided evidence K. pneumoniae strain CSG20 produced N-hexanoyl-homoserine lactone (C6-HSL). To the best of our knowledge, this is the first report on the production of N-hexanoylhomoserine lactone (C6-HSL) in clinical isolate K. pneumoniae.

[1]  Wai-Fong Yin,et al.  Inhibition of Quorum Sensing-Controlled Virulence Factor Production in Pseudomonas aeruginosa PAO1 by Ayurveda Spice Clove (Syzygium Aromaticum) Bud Extract , 2012, Sensors.

[2]  J H Lamb,et al.  Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. , 1997, Microbiology.

[3]  Li Ying Tan,et al.  Piper nigrum, Piper betle and Gnetum gnemon- Natural Food Sources with Anti-Quorum Sensing Properties , 2013, Sensors.

[4]  T. Maier,et al.  Fast and reliable MALDI-TOF MS–based microorganism identification , 2006 .

[5]  D. Balestrino,et al.  Quorum sensing affects biofilm formation through lipopolysaccharide synthesis in Klebsiella pneumoniae. , 2010, Research in microbiology.

[6]  Li Ying Tan,et al.  Plant-Derived Natural Products as Sources of Anti-Quorum Sensing Compounds , 2013, Sensors.

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

[8]  H L Houtzager,et al.  Antonie van Leeuwenhoek. , 1983, European journal of obstetrics, gynecology, and reproductive biology.

[9]  Herman Goossens,et al.  Community-Acquired Klebsiella pneumoniae Bacteremia: Global Differences in Clinical Patterns , 2002, Emerging infectious diseases.

[10]  Wai-Fong Yin,et al.  Rapid degradation of N-3-oxo-acylhomoserine lactones by a Bacilluscereus isolate from Malaysian rainforest soil , 2010, Antonie van Leeuwenhoek.

[11]  M K Winson,et al.  Quorum sensing in Aeromonas hydrophila and Aeromonas salmonicida: identification of the LuxRI homologs AhyRI and AsaRI and their cognate N-acylhomoserine lactone signal molecules , 1997, Journal of bacteriology.

[12]  M. Neal Guentzel,et al.  Escherichia, Klebsiella, Enterobacter, Serratia, Citrobacter, and Proteus , 1996 .

[13]  Chin-Yi Chen,et al.  Quorum Sensing and Production of Autoinducer-2 in Campylobacter spp., Escherichia coli O157:H7, and Salmonella enterica Serovar Typhimurium in Foods , 2002, Applied and Environmental Microbiology.

[14]  Wei Zhang,et al.  Evolution of Broad Spectrum β-Lactam Resistance in an Engineered Metallo-β-lactamase* , 2012, The Journal of Biological Chemistry.

[15]  M. Sebaihia,et al.  Carbapenem antibiotic production in Erwinia carotovora is regulated by CarR, a homologue of the LuxR transcriptional activator. , 1995, Microbiology.

[16]  Chang-Wen Chen,et al.  Rapidly fatal outcome of bacteremic Klebsiella pneumoniae pneumonia in alcoholics. , 1995, Chest.

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

[18]  J M McCloud,et al.  Life‐threatening sepsis following treatment for haemorrhoids: a systematic review , 2006, Colorectal disease : the official journal of the Association of Coloproctology of Great Britain and Ireland.

[19]  Kok-Gan Chan,et al.  Characterization of N-acylhomoserine lactone-degrading bacteria associated with the Zingiber officinale (ginger) rhizosphere: Co-existence of quorum quenching and quorum sensing in Acinetobacter and Burkholderia , 2011, BMC Microbiology.

[20]  Wai-Fong Yin,et al.  Coexistence of quorum-quenching and quorum-sensing in tropical marine Pseudomonas aeruginosa strain MW3A , 2011, World Journal of Microbiology and Biotechnology.

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

[22]  Tobin J Dickerson,et al.  Revisiting quorum sensing: Discovery of additional chemical and biological functions for 3-oxo-N-acylhomoserine lactones. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[23]  Lian-Hui Zhang,et al.  Identification of Quorum-Quenching N-Acyl Homoserine Lactonases from Bacillus Species , 2002, Applied and Environmental Microbiology.

[24]  Li Ying Tan,et al.  Silencing Quorum Sensing through Extracts of Melicope lunu-ankenda , 2012, Sensors.

[25]  Kalai Mathee,et al.  Anti-quorum sensing activity of medicinal plants in southern Florida. , 2006, Journal of ethnopharmacology.

[26]  Wai-Fong Yin,et al.  Long Chain N-acyl Homoserine Lactone Production by Enterobacter sp. Isolated from Human Tongue Surfaces , 2012, Sensors.

[27]  Wai-Fong Yin,et al.  Quorum Quenching Revisited—From Signal Decays to Signalling Confusion , 2012, Sensors.

[28]  Chia-Tung Shun,et al.  A Novel Virulence Gene in Klebsiella pneumoniae Strains Causing Primary Liver Abscess and Septic Metastatic Complications , 2004, The Journal of experimental medicine.

[29]  Lian-Hui Zhang,et al.  Quorum-quenching microbial infections: mechanisms and implications , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[30]  S. Molin,et al.  N-Acyl-L-homoserine lactone autoinducers control production of an extracellular lipopeptide biosurfactant required for swarming motility of Serratia liquefaciens MG1. , 1998, Journal of bacteriology.

[31]  B. Bassler,et al.  Interspecies communication in bacteria. , 2003, The Journal of clinical investigation.

[32]  D. Calfee,et al.  Crisis in hospital-acquired, healthcare-associated infections. , 2012, Annual review of medicine.

[33]  B. Bassler,et al.  Quorum sensing in bacteria. , 2001, Annual review of microbiology.

[34]  Maurizio Sanguinetti,et al.  Direct MALDI-TOF Mass Spectrometry Assay of Blood Culture Broths for Rapid Identification of Candida Species Causing Bloodstream Infections: an Observational Study in Two Large Microbiology Laboratories , 2011, Journal of Clinical Microbiology.

[35]  J. Paiva,et al.  Adding risk factors for potentially resistant pathogens, increasing antibiotic pressure and risk creating the “untreatable bacteria”: time to change direction , 2013, Intensive Care Medicine.

[36]  Kok-Gan Chan,et al.  Malabaricone C from Myristica cinnamomea exhibits anti-quorum sensing activity. , 2011, Journal of natural products.

[37]  Vincent H Tam,et al.  Detection and treatment options for Klebsiella pneumoniae carbapenemases (KPCs): an emerging cause of multidrug-resistant infection. , 2010, The Journal of antimicrobial chemotherapy.

[38]  D. Balestrino,et al.  Characterization of Type 2 Quorum Sensing in Klebsiella pneumoniae and Relationship with Biofilm Formation , 2005, Journal of bacteriology.

[39]  P. Nordmann,et al.  Does broad-spectrum beta-lactam resistance due to NDM-1 herald the end of the antibiotic era for treatment of infections caused by Gram-negative bacteria? , 2011, The Journal of antimicrobial chemotherapy.

[40]  Yi-Tsung Lin,et al.  Bacteremic community-acquired pneumonia due to Klebsiella pneumoniae: Clinical and microbiological characteristics in Taiwan, 2001-2008 , 2010, BMC infectious diseases.

[41]  Tom Coenye,et al.  Social interactions in the Burkholderia cepacia complex: biofilms and quorum sensing. , 2010, Future microbiology.

[42]  Fumio Nomura,et al.  Use of the MALDI BioTyper system with MALDI–TOF mass spectrometry for rapid identification of microorganisms , 2011, Analytical and bioanalytical chemistry.

[43]  Myung Hee Kim,et al.  The molecular structure and catalytic mechanism of a quorum-quenching N-acyl-L-homoserine lactone hydrolase. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[44]  Wai-Fong Yin,et al.  Caffeine as a Potential Quorum Sensing Inhibitor , 2013, Sensors.

[45]  W. Johnson.  Time to change direction , 2003 .

[46]  R. Podschun,et al.  Klebsiella spp. as Nosocomial Pathogens: Epidemiology, Taxonomy, Typing Methods, and Pathogenicity Factors , 1998, Clinical Microbiology Reviews.

[47]  Jun Zhu,et al.  Conditional production of acyl-homoserine lactone-type quorum-sensing signals in clinical isolates of enterobacteria. , 2006, Journal of medical microbiology.

[48]  Jeroen S. Dickschat,et al.  Quorum sensing and bacterial biofilms. , 2010, Natural product reports.

[49]  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.

[50]  Wai-Fong Yin,et al.  Short Chain N-acyl Homoserine Lactone Production by Soil Isolate Burkholderia sp. Strain A9 , 2013, Sensors.

[51]  S. Voloshin,et al.  Cell–cell interactions in bacterial populations , 2004, Biochemistry (Moscow).