OXA-372, a novel carbapenem-hydrolysing class D β-lactamase from a Citrobacter freundii isolated from a hospital wastewater plant

Antonelli, A.; D'Andrea, M. M.; Vaggelli, G.; Docquier, Jean-Denis; Rossolini, G. M.

doi:10.1093/jac/dkv181

Article (Scientific journals)

OXA-372, a novel carbapenem-hydrolysing class D β-lactamase from a Citrobacter freundii isolated from a hospital wastewater plant

Antonelli, A.; D'Andrea, M. M.; Vaggelli, G. et al.

2015 • In Journal of Antimicrobial Chemotherapy, 70 (10), p. 2749-2756

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/252806

DOI
10.1093/jac/dkv181

PubMed
26126492

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

63.pdf

Publisher postprint (723.97 kB)

Request a copy

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

Article; Citrobacter freundii; Escherichia coli; Italy; DNA sequence; Amino Acid Sequence; Anti-Bacterial Agents; Bacterial Proteins; Carbapenems; Cloning, Molecular; Humans; Microbial Sensitivity Tests; Molecular Sequence Data; Phylogeny; Sequence Alignment; Sequence Analysis, DNA; Waste Water

Abstract :

[en] Objectives: The objective of this study was to characterize a novel class D carbapenemase, named OXA-372, identified in a carbapenem-resistant Citrobacter freundii strain (Cfr-FI-07) isolated from a hospital wastewater plant in central Italy. Methods: Cfr-FI-07 was isolated using a selective chromogenic medium for carbapenem-resistant Enterobacteriaceae. Carbapenemase production was confirmed by spectrophotometric assay. WGS was carried out using an Illumina MiSeq platform. The functional profile of OXA-372 was investigated by expression of the cloned gene in Escherichia coli and by analysis of kinetic parameters of the purified enzyme. Results: C. freundii Cfr-FI-07 produced carbapenemase activity, but tested negative for common carbapenemase genes. WGS confirmed the absence of known carbapenemase genes and revealed the presence of a novel class D b-lactamase (DBL) determinant, named blaOXA-372, encoding a protein distantly related to other DBLs. In E. coli, production of OXA-372 conferred resistance to penicillins, including temocillin, and reduced susceptibility to carbapenems, while susceptibility to expanded-spectrum cephalosporins was virtually unaffected. This substrate specificity was confirmed by kinetic characterization of the purified enzyme, which exhibited high catalytic efficiencies for carbapenems (kcat/KM values ≥0.22 s2-1.μM-1). The blaOXA-372 genewas associated with a genetic platform of original structure consisting of a Tn402/Tn5053 hybrid transposon derivative, named Tn6255, inserted into a TnPa38-like transposon, named Tn6256, located on an IncA/C-IncN plasmid of approximately 140 kb. Conclusions: OXA-372 is a novel class D carbapenemase, belonging to a new lineage of DBLs, encoded by a gene associated with mobile elements. Functional properties revealed similarities, but also some differences, compared with other class D carbapenemases. © The Author 2015. Published by Oxford University Press on behalf of the British Society for Antimicrobial Chemotherapy. All rights reserved.

Disciplines :

Biochemistry, biophysics & molecular biology
Microbiology

Author, co-author :

Antonelli, A.; Department of Medical Biotechnology, University of Siena, Siena, Italy, Department of Experimental and Clinical Medicine, University of Florence, Florence, Italy

D'Andrea, M. M.; Department of Medical Biotechnology, University of Siena, Siena, Italy

Vaggelli, G.; Clinical Microbiology and Virology Unit, Florence Careggi University Hospital, Florence, Italy

Docquier, Jean-Denis ; Université de Liège - ULiège > Département des sciences de la vie > Centre d'ingénierie des protéines

Rossolini, G. M.; Department of Medical Biotechnology, University of Siena, Siena, Italy, Clinical Microbiology and Virology Unit, Florence Careggi University Hospital, Florence, Italy

Language :

English

Title :

OXA-372, a novel carbapenem-hydrolysing class D β-lactamase from a Citrobacter freundii isolated from a hospital wastewater plant

Publication date :

2015

Journal title :

Journal of Antimicrobial Chemotherapy

ISSN :

0305-7453

eISSN :

1460-2091

Publisher :

Oxford University Press

Volume :

Issue :

Pages :

2749-2756

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 19 November 2020

Statistics

Number of views

28 (1 by ULiège)

Number of downloads

1 (1 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Rossolini GM, Arena F, Pecile P et al. Update on the antibiotic resistance crisis. Curr Opin Pharmacol 2014; 18: 56-60.
Temkin E, Adler A, Lerner A et al. Carbapenem-resistant Enterobacteriaceae: biology, epidemiology, and management. Ann NY Acad Sci 2014; 1323: 22-42.
Canton R, Akova M, Carmeli Y et al. Rapid evolution and spread of carbapenemases among Enterobacteriaceae in Europe. Clin Microbiol Infect 2012; 18: 413-31.
Glasner C, Albiger B, Buist G et al. Carbapenemase-producing Enterobacteriaceae in Europe: a survey among national experts from 39 countries, February 2013. Euro Surveill 2013; 18: pii=20525.
Munoz-Price LS, Poirel L, Bonomo RA et al. Clinical epidemiology of the global expansion of Klebsiella pneumoniae carbapenemases. Lancet Infect Dis 2013; 13: 785-96.
Nordmann P, Poirel L. The difficult-to-control spread of carbapenemase producers among Enterobacteriaceae worldwide. Clin Microbiol Infect 2014; 20: 821-30.
Rossolini GM. Extensively drug-resistant carbapenemase-producing Enterobacteriaceae: an emerging challenge for clinicians and healthcare systems. J Intern Med 2015; 277: 528-31.
Tzouvelekis LS, Markogiannakis A, Psichogiou M et al. Carbapenemases in Klebsiella pneumoniae and other Enterobacteriaceae: an evolving crisis of global dimensions. Clin Microbiol Rev 2012; 25: 682-707.
Huang TD, Berhin C, Bogaerts P et al. Prevalence and mechanisms of resistance to carbapenems in Enterobacteriaceae isolates from 24 hospitals in Belgium. J Antimicrob Chemother 2013; 68: 1832-7.
Carrer A, Poirel L, Yilmaz M et al. Spread of OXA-48-encoding plasmid in Turkey and beyond. Antimicrob Agents Chemother 2010; 54: 1369-73.
Poirel L, Potron A, Nordmann P. OXA-48-like carbapenemases: the phantom menace. J Antimicrob Chemother 2012; 67: 1597-606.
Djahmi N, Dunyach-Remy C, Pantel A et al. Epidemiology of carbapenemase-producing Enterobacteriaceae and Acinetobacter baumannii in Mediterranean countries. Biomed Res Int 2014; 2014: 305784.
Potron A, Poirel L, Rondinaud E et al. Intercontinental spread of OXA-48 β-lactamase-producing Enterobacteriaceae over a 11-year period, 2001 to 2011. Euro Surveill 2013; 18: pii=20549.
Sambrook J, Russell DW. Molecular Cloning: A Laboratory Manual. 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 2001.
Grant SG, Jessee J, Bloom FR et al. Differential plasmid rescue from transgenic mouse DNAs into Escherichia coli methylation-restriction mutants. Proc Natl Acad Sci USA 1990; 87: 4645-9.
Jacoby GA, Han P. Detection of extended-spectrum b-lactamases in clinical isolates of Klebsiella pneumoniae and Escherichia coli. J Clin Microbiol 1996; 34: 908-11.
Clinical and Laboratory Standards Institute. Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically- Tenth Edition: Approved Standard M07-A10. CLSI, Wayne, PA, USA, 2015.
EUCAST. Breakpoint Tables for Interpretation of MICs and Zone Diameters, Version 5.0, 2015. http://www.eucast.org/clinical_breakpoints/.
Poirel L, Walsh TR, Cuvillier V et al. Multiplex PCR for detection of acquired carbapenemase genes. Diagn Microbiol Infect Dis 2011; 70: 119-23.
Lauretti L, Riccio ML, Mazzariol A et al. Cloning and characterization of blaVIM, a new integron-borne metallo-b-lactamase gene from a Pseudomonas aeruginosa clinical isolate. Antimicrob Agents Chemother 1999; 43: 1584-90.
Tsakris A, Poulou A, Pournaras S et al. A simple phenotypic method for the differentiation of metallo-b-lactamases and class A KPC carbapenemases in Enterobacteriaceae clinical isolates. J Antimicrob Chemother 2010; 65: 1664-71.
Simpson JT, Wong K, Jackman SD et al. ABySS: a parallel assembler for short read sequence data. Genome Res 2009; 19: 1117-23.
Aziz RK, Bartels D, Best AA et al. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 2008; 9: 75.
Sullivan MJ, Petty NK, Beatson SA. Easyfig: a genome comparison visualizer. Bioinformatics 2011; 27: 1009-10.
Page RD. TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 1996; 12: 357-8.
Docquier JD, Riccio ML, Mugnaioli C et al. IMP-12, a new plasmidencoded metallo-b-lactamase from a Pseudomonas putida clinical isolate. Antimicrob Agents Chemother 2003; 47: 1522-8.
Johnson TJ, Bielak EM, Fortini D et al. Expansion of the IncX plasmid family for improved identification and typing of novel plasmids in drug-resistant Enterobacteriaceae. Plasmid 2012; 68: 43-50.
Garcia-Fernandez A, Fortini D, Veldman K et al. Characterization of plasmids harbouring qnrS1, qnrB2 and qnrB19 genes in Salmonella. J Antimicrob Chemother 2009; 63: 274-81.
Carattoli A, Bertini A, Villa L et al. Identification of plasmids by PCR-based replicon typing. J Microbiol Meth 2005; 63: 219-28.
Barton BM, Harding GP, Zuccarelli AJ. A general method for detecting and sizing large plasmids. Anal Biochem 1995; 226: 235-40.
Borgianni L, Vandenameele J, Matagne A et al. Mutational analysis of VIM-2 reveals an essential determinant for metallo-b-lactamase stability and folding. Antimicrob Agents Chemother 2010; 54: 3197-204.
Smith DB, Johnson KS. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene 1988; 67: 31-40.
Studier FW. Protein production by auto-induction in high density shaking cultures. Protein Expr Purif 2005; 41: 207-34.
Docquier JD, Lamotte-Brasseur J, Galleni M et al. On functional and structural heterogeneity of VIM-type metallo-b-lactamases. J Antimicrob Chemother 2003; 51: 257-66.
Giani T, Pini B, Arena F et al. Epidemic diffusion of KPC carbapenemaseproducing Klebsiella pneumoniae in Italy: results of the first countrywide survey, 15 May to 30 June 2011. Euro Surveill 2013; 18: pii=20489.
El Garch F, Bogaerts P, Bebrone C et al. OXA-198, an acquired carbapenem-hydrolyzing class D b-lactamase from Pseudomonas aeruginosa. Antimicrob Agents Chemother 2011; 55: 4828-33.
Couture F, Lachapelle J, Levesque RC. Phylogeny of LCR-1 and OXA-5 with class A and class D b-lactamases. Mol Microbiol 1992; 6: 1693-705.
De LF, Benvenuti M, Carboni F et al. Evolution to carbapenemhydrolyzing activity in noncarbapenemase class D b-lactamase OXA-10 by rational protein design. Proc Natl Acad Sci USA 2011; 108: 18424-9.
Radstrom P, Skold O, Swedberg G et al. Transposon Tn5090 of plasmid R751, which carries an integron, is related to Tn7, Mu, and the retroelements. J Bacteriol 1994; 176: 3257-68.
Kholodii GY, Yurieva OV, Lomovskaya OL et al. Tn5053, a mercury resistance transposon with integron's ends. J Mol Biol 1993; 230: 1103-7.
Hawkey PM, Xiong J, Ye H et al. Occurrence of a new metallob- lactamase IMP-4 carried on a conjugative plasmid in Citrobacter youngae from the People's Republic of China. FEMS Microbiol Lett 2001; 194: 53-7.
Juan C, Zamorano L, Mena A et al. Metallo-β-lactamase-producing Pseudomonas putida as a reservoir of multidrug resistance elements that can be transferred to successful Pseudomonas aeruginosa clones. J Antimicrob Chemother 2010; 65: 474-8.
Labbate M, Roy CP, Stokes HW. A class 1 integron present in a human commensal has a hybrid transposition module compared to Tn402: evidence of interaction with mobile DNA from natural environments. J Bacteriol 2008; 190: 5318-27.
Rau MH, Marvig RL, Ehrlich GD et al. Deletion and acquisition of genomic content during early stage adaptation of Pseudomonas aeruginosa to a human host environment. Environ Microbiol 2012; 14: 2200-11.
Molina L, Bernal P, Udaondo Z et al. Complete genome sequence of a Pseudomonas putida clinical isolate, strain H8234. Genome Announc 2013; 1: e00496-13.
Rhodes G, Parkhill J, Bird C et al. Complete nucleotide sequence of the conjugative tetracycline resistance plasmid pFBAOT6, a member of a group of IncU plasmids with global ubiquity. Appl Environ Microbiol 2004; 70: 7497-510.
Dolejska M, Villa L, Dobiasova H et al. Plasmid content of a clinically relevant Klebsiella pneumoniae clone from the Czech Republic producing CTX-M-15 and QnrB1. Antimicrob Agents Chemother 2013; 57: 1073-6.
Docquier JD, Calderone V, De LF et al. Crystal structure of the OXA-48 b-lactamase reveals mechanistic diversity among class D carbapenemases. Chem Biol 2009; 16: 540-7.
Poirel L, Hé ritier C, Tolün C et al. Emergence of oxacillinase-mediated resistance to imipenem in Klebsiella pneumoniae. Antimicrob Agents Chemother 2004; 48: 15-22.
Poirel L, Marque S, Heritier C et al. OXA-58, a novel class D b-lactamase involved in resistance to carbapenems in Acinetobacter baumannii. Antimicrob Agents Chemother 2005; 49: 202-8.
Kaitany KC, Klinger NV, June CM et al. Structures of the class D Carbapenemases OXA-23 and OXA-146: mechanistic basis of activity against carbapenems, extended-spectrum cephalosporins, and aztreonam. Antimicrob Agents Chemother 2013; 57: 4848-55.
Poirel L, Ros A, Carricajo A et al. Extremely drug-resistant Citrobacter freundii isolate producing NDM-1 and other carbapenemases identified in a patient returning from India. Antimicrob Agents Chemother 2011; 55: 447-8.
Peter S, Wolz C, Kaase M et al. Emergence of Citrobacter freundii carrying IMP-8 metallo-b-lactamase in Germany. New Microbes New Infect 2014; 2: 42-5.
Gaibani P, Ambretti S, Farruggia P et al. Outbreak of Citrobacter freundii carrying VIM-1 in an Italian Hospital, identified during the carbapenemases screening actions, June 2012. Int J Infect Dis 2013; 17: e714-7.
Li G, Wei Q, Wang Y et al. Novel genetic environment of the plasmidmediated KPC-3 gene detected in Escherichia coli and Citrobacter freundii isolates from China. Eur J Clin Microbiol Infect Dis 2011; 30: 575-80.
Gomez-Gil MR, Pano-Pardo JR, Romero-Gomez MP et al. Detection of KPC-2-producing Citrobacter freundii isolates in Spain. J Antimicrob Chemother 2010; 65: 2695-7.