Evolution and Spread of a Multidrug-resistant Proteus Mirabilis Clone with Chromosomal AmpC-type Cephalosporinases in Europe

Overview

Journal Antimicrob Agents Chemother

Publisher American Society for Microbiology

Specialty Pharmacology

Date 2011 Mar 16

PMID 21402851

Citations 30

Authors

M M DAndrea

E Literacka

A Zioga

T Giani

A Baraniak

J Fiett

E Sadowy

P T Tassios

G M Rossolini

M Gniadkowski

V Miriagou

Affiliations

Soon will be listed here.

Abstract

Proteus mirabilis isolates obtained in 1999 to 2008 from three European countries were analyzed; all carried chromosomal AmpC-type cephalosporinase bla(CMY) genes from a Citrobacter freundii origin (bla(CMY-2)-like genes). Isolates from Poland harbored several bla(CMY) genes (bla(CMY-4), bla(CMY-12), bla(CMY-14), bla(CMY-15), and bla(CMY-38) and the new gene bla(CMY-45)), while isolates from Italy and Greece harbored bla(CMY-16) only. Earlier isolates with bla(CMY-4) or bla(CMY-12), recovered in France from Greek and Algerian patients, were also studied. All isolates showed striking similarities. Their bla(CMY) genes resided within ISEcp1 transposition modules, named Tn6093, characterized by a 110-bp distance between ISEcp1 and bla(CMY), and identical fragments of both C. freundii DNA and a ColE1-type plasmid backbone. Moreover, these modules were inserted into the same chromosomal site, within the pepQ gene. Since ColE1 plasmids carrying ISEcp1 with similar C. freundii DNA fragments (Tn6114) had been identified earlier, it is likely that a similar molecule had mediated at some stage this DNA transfer between C. freundii and P. mirabilis. In addition, isolates with bla(CMY-12), bla(CMY-15), and bla(CMY-38) genes harbored a second bla(CMY) copy within a shorter ISEcp1 module (Tn6113), always inserted downstream of the ppiD gene. Sequence analysis of all mobile bla(CMY-2)-like genes indicated that those integrated in the P. mirabilis chromosome form a distinct cluster that may have evolved by the stepwise accumulation of mutations. All of these observations, coupled to strain typing data, suggest that the bla(CMY) genes studied here may have originated from a single ISEcp1-mediated mobilization-transfer-integration process, followed by the spread and evolution of a P. mirabilis clone over time and a large geographic area.

Citing Articles

The Impact of Urban Pollution on Plasmid-Mediated Resistance Acquisition in Enterobacteria from a Tropical River.

Mendoza-Guido B, Barrantes K, Rodriguez C, Rojas-Jimenez K, Arias-Andres M Antibiotics (Basel). 2024; 13(11).

PMID: 39596782 PMC: 11591392. DOI: 10.3390/antibiotics13111089.

Multidrug-Resistant Bacteria in Surgical Intensive Care Units: Antibiotic Susceptibility and β-Lactamase Characterization.

Bandic Pavlovic D, Pospisil M, Nad M, Vrbanovic Mijatovic V, Luxner J, Zarfel G Pathogens. 2024; 13(5).

PMID: 38787264 PMC: 11124292. DOI: 10.3390/pathogens13050411.

Multidrug-Resistant Infections and Clinical Outcome at Tertiary Hospital in Riyadh, Saudi Arabia.

Hafiz T, Alghamdi G, Alkudmani Z, Alyami A, Almazyed A, Alhumaidan O Infect Drug Resist. 2024; 17:571-581.

PMID: 38375102 PMC: 10875173. DOI: 10.2147/IDR.S448335.

Antimicrobial Properties of Capsaicin: Available Data and Future Research Perspectives.

Periferakis A, Periferakis A, Periferakis K, Caruntu A, Badarau I, Savulescu-Fiedler I Nutrients. 2023; 15(19).

PMID: 37836381 PMC: 10574431. DOI: 10.3390/nu15194097.

Green synthesis of silver nanoparticles derived from lemon and pomegranate peel extracts to combat multidrug-resistant bacterial isolates.

Abdelrazik M, Elkotaby H, Yousef A, El-Sayed A, Khedr M J Genet Eng Biotechnol. 2023; 21(1):97.

PMID: 37815647 PMC: 10564695. DOI: 10.1186/s43141-023-00547-0.

References

Hopkins K, Liebana E, Villa L, Batchelor M, Threlfall E, Carattoli A . Replicon typing of plasmids carrying CTX-M or CMY beta-lactamases circulating among Salmonella and Escherichia coli isolates. Antimicrob Agents Chemother. 2006; 50(9):3203-6. PMC: 1563510. DOI: 10.1128/AAC.00149-06. View

Pearson M, Sebaihia M, Churcher C, Quail M, Seshasayee A, Luscombe N . Complete genome sequence of uropathogenic Proteus mirabilis, a master of both adherence and motility. J Bacteriol. 2008; 190(11):4027-37. PMC: 2395036. DOI: 10.1128/JB.01981-07. View

Hopkins K, Batchelor M, Liebana E, Deheer-Graham A, Threlfall E . Characterisation of CTX-M and AmpC genes in human isolates of Escherichia coli identified between 1995 and 2003 in England and Wales. Int J Antimicrob Agents. 2006; 28(3):180-92. DOI: 10.1016/j.ijantimicag.2006.03.027. View

Luzzaro F, Brigante G, DAndrea M, Pini B, Giani T, Mantengoli E . Spread of multidrug-resistant Proteus mirabilis isolates producing an AmpC-type beta-lactamase: epidemiology and clinical management. Int J Antimicrob Agents. 2008; 33(4):328-33. DOI: 10.1016/j.ijantimicag.2008.09.007. View

Pignato S, Giammanco G, Grimont F, Grimont P, Giammanco G . Molecular characterization of the genera Proteus, Morganella, and Providencia by ribotyping. J Clin Microbiol. 1999; 37(9):2840-7. PMC: 85391. DOI: 10.1128/JCM.37.9.2840-2847.1999. View

DAndrea M, Nucleo E, Luzzaro F, Giani T, Migliavacca R, Vailati F . CMY-16, a novel acquired AmpC-type beta-lactamase of the CMY/LAT lineage in multifocal monophyletic isolates of Proteus mirabilis from northern Italy. Antimicrob Agents Chemother. 2006; 50(2):618-24. PMC: 1366893. DOI: 10.1128/AAC.50.2.618-624.2006. View

Struelens M, Schwam V, Deplano A, Baran D . Genome macrorestriction analysis of diversity and variability of Pseudomonas aeruginosa strains infecting cystic fibrosis patients. J Clin Microbiol. 1993; 31(9):2320-6. PMC: 265754. DOI: 10.1128/jcm.31.9.2320-2326.1993. View

Literacka E, Empel J, Baraniak A, Sadowy E, Hryniewicz W, Gniadkowski M . Four variants of the Citrobacter freundii AmpC-Type cephalosporinases, including novel enzymes CMY-14 and CMY-15, in a Proteus mirabilis clone widespread in Poland. Antimicrob Agents Chemother. 2004; 48(11):4136-43. PMC: 525428. DOI: 10.1128/AAC.48.11.4136-4143.2004. View

Zioga A, Whichard J, Kotsakis S, Tzouvelekis L, Tzelepi E, Miriagou V . CMY-31 and CMY-36 cephalosporinases encoded by ColE1-like plasmids. Antimicrob Agents Chemother. 2008; 53(3):1256-9. PMC: 2650574. DOI: 10.1128/AAC.01284-08. View

10.

Whichard J, Gay K, Stevenson J, Joyce K, Cooper K, Omondi M . Human Salmonella and concurrent decreased susceptibility to quinolones and extended-spectrum cephalosporins. Emerg Infect Dis. 2008; 13(11):1681-8. PMC: 3375806. DOI: 10.3201/eid1311.061438. View

11.

Woodford N, Reddy S, Fagan E, Hill R, Hopkins K, Kaufmann M . Wide geographic spread of diverse acquired AmpC beta-lactamases among Escherichia coli and Klebsiella spp. in the UK and Ireland. J Antimicrob Chemother. 2006; 59(1):102-5. DOI: 10.1093/jac/dkl456. View

12.

Giles W, Benson A, Olson M, Hutkins R, Whichard J, Winokur P . DNA sequence analysis of regions surrounding blaCMY-2 from multiple Salmonella plasmid backbones. Antimicrob Agents Chemother. 2004; 48(8):2845-52. PMC: 478531. DOI: 10.1128/AAC.48.8.2845-2852.2004. View

13.

Nakano R, Okamoto R, Nakano Y, Kaneko K, Okitsu N, Hosaka Y . CFE-1, a novel plasmid-encoded AmpC beta-lactamase with an ampR gene originating from Citrobacter freundii. Antimicrob Agents Chemother. 2004; 48(4):1151-8. PMC: 375250. DOI: 10.1128/AAC.48.4.1151-1158.2004. View

14.

Vourli S, Tsorlini H, Katsifa H, Polemis M, Tzouvelekis L, Kontodimou A . Emergence of Proteus mirabilis carrying the bla metallo-beta-lactamase gene. Clin Microbiol Infect. 2006; 12(7):691-4. DOI: 10.1111/j.1469-0691.2006.01489.x. View

15.

Bauernfeind A, Stemplinger I, Jungwirth R, Giamarellou H . Characterization of the plasmidic beta-lactamase CMY-2, which is responsible for cephamycin resistance. Antimicrob Agents Chemother. 1996; 40(1):221-4. PMC: 163087. DOI: 10.1128/AAC.40.1.221. View

16.

Wu S, Dornbusch K, Kronvall G, Norgren M . Characterization and nucleotide sequence of a Klebsiella oxytoca cryptic plasmid encoding a CMY-type beta-lactamase: confirmation that the plasmid-mediated cephamycinase originated from the Citrobacter freundii AmpC beta-lactamase. Antimicrob Agents Chemother. 1999; 43(6):1350-7. PMC: 89277. DOI: 10.1128/AAC.43.6.1350. View

17.

Didelot X, Falush D . Inference of bacterial microevolution using multilocus sequence data. Genetics. 2006; 175(3):1251-66. PMC: 1840087. DOI: 10.1534/genetics.106.063305. View

18.

Lartigue M, Poirel L, Aubert D, Nordmann P . In vitro analysis of ISEcp1B-mediated mobilization of naturally occurring beta-lactamase gene blaCTX-M of Kluyvera ascorbata. Antimicrob Agents Chemother. 2006; 50(4):1282-6. PMC: 1426957. DOI: 10.1128/AAC.50.4.1282-1286.2006. View

19.

Huson D, Bryant D . Application of phylogenetic networks in evolutionary studies. Mol Biol Evol. 2005; 23(2):254-67. DOI: 10.1093/molbev/msj030. View

20.

Decre D, Verdet C, Raskine L, Blanchard H, Burghoffer B, Philippon A . Characterization of CMY-type beta-lactamases in clinical strains of Proteus mirabilis and Klebsiella pneumoniae isolated in four hospitals in the Paris area. J Antimicrob Chemother. 2002; 50(5):681-8. DOI: 10.1093/jac/dkf193. View