Tn5253 Family Integrative and Conjugative Elements Carrying mef(I) and catQ Determinants in Streptococcus pneumoniae and Streptococcus pyogenes

ABSTRACT The linkage between the macrolide efflux gene mef(I) and the chloramphenicol inactivation gene catQ was first described in Streptococcus pneumoniae (strain Spn529), where the two genes are located in a module designated IQ element. Subsequently, two different defective IQ elements were detected in Streptococcus pyogenes (strains Spy029 and Spy005). The genetic elements carrying the three IQ elements were characterized, and all were found to be Tn5253 family integrative and conjugative elements (ICEs). The ICE from S. pneumoniae (ICESpn529IQ) was sequenced, whereas the ICEs from S. pyogenes (ICESpy029IQ and ICESpy005IQ, the first Tn5253-like ICEs reported in this species) were characterized by PCR mapping, partial sequencing, and restriction analysis. ICESpn529IQ and ICESpy029IQ were found to share the intSp23FST81 integrase gene and an identical Tn916 fragment, whereas ICESpy005IQ has int5252 and lacks Tn916. All three ICEs were found to lack the linearized pC194 plasmid that is usually associated with Tn5253-like ICEs, and all displayed a single copy of a toxin-antitoxin operon that is typically contained in the direct repeats flanking the excisable pC194 region when this region is present. Two different insertion sites of the IQ elements were detected, one in ICESpn529IQ and ICESpy029IQ, and another in ICESpy005IQ. The chromosomal integration of the three ICEs was site specific, depending on the integrase (intSp23FST81 or int5252). Only ICESpy005IQ was excised in circular form and transferred by conjugation. By transformation, mef(I) and catQ were cotransferred at a high frequency from S. pyogenes Spy005 and at very low frequencies from S. pneumoniae Spn529 and S. pyogenes Spy029.

[1]  M. Mingoia,et al.  Genetic determinants and elements associated with antibiotic resistance in viridans group streptococci. , 2014, The Journal of antimicrobial chemotherapy.

[2]  M. Mingoia,et al.  ICESp1116, the Genetic Element Responsible for erm(B)-Mediated, Inducible Erythromycin Resistance in Streptococcus pyogenes, Belongs to the TnGBS Family of Integrative and Conjugative Elements , 2014, Antimicrobial Agents and Chemotherapy.

[3]  G. Gherardi,et al.  Genetic diversity and virulence properties of Streptococcus dysgalactiae subsp. equisimilis from different sources. , 2014, Journal of medical microbiology.

[4]  G. Pozzi,et al.  Nucleotide Sequence Analysis of Integrative Conjugative Element Tn5253 of Streptococcus pneumoniae , 2013, Antimicrobial Agents and Chemotherapy.

[5]  Andries J. van Tonder,et al.  Evidence of antimicrobial resistance-conferring genetic elements among pneumococci isolated prior to 1974 , 2013, BMC Genomics.

[6]  P. Christie,et al.  The expanding bacterial type IV secretion lexicon. , 2013, Research in microbiology.

[7]  M. Mingoia,et al.  Unconventional Circularizable Bacterial Genetic Structures Carrying Antibiotic Resistance Determinants , 2013, Antimicrobial Agents and Chemotherapy.

[8]  C. Yeo,et al.  Toxin-Antitoxin Genes of the Gram-Positive Pathogen Streptococcus pneumoniae: So Few and Yet So Many , 2012, Microbiology and Molecular Reviews.

[9]  Eleonora Morici,et al.  ICESp1116, the Genetic Element Responsible for erm(B)-Mediated, Inducible Resistance to Erythromycin in Streptococcus pyogenes , 2012, Antimicrobial Agents and Chemotherapy.

[10]  P. Bagnarelli,et al.  Characterization of a Streptococcus suis tet(O/W/32/O)-Carrying Element Transferable to Major Streptococcal Pathogens , 2012, Antimicrobial Agents and Chemotherapy.

[11]  Songnian Hu,et al.  Complete Genome and Transcriptomes of Streptococcus parasanguinis FW213: Phylogenic Relations and Potential Virulence Mechanisms , 2012, PloS one.

[12]  A. Pantosti,et al.  Genetic Resistance Elements Carrying mef Subclasses Other than mef(A) in Streptococcus pyogenes , 2011, Antimicrobial Agents and Chemotherapy.

[13]  J. Burton,et al.  Rapid Pneumococcal Evolution in Response to Clinical Interventions , 2011, Science.

[14]  M. P. Montanari,et al.  Heterogeneity of Tn5253-Like Composite Elements in Clinical Streptococcus pneumoniae Isolates , 2011, Antimicrobial Agents and Chemotherapy.

[15]  Matthew K. Waldor,et al.  Integrative and conjugative elements: mosaic mobile genetic elements enabling dynamic lateral gene flow , 2010, Nature Reviews Microbiology.

[16]  T. Tolker-Nielsen,et al.  Characterization and transfer studies of macrolide resistance genes in Streptococcus pneumoniae from Denmark , 2010, Scandinavian journal of infectious diseases.

[17]  G. Pozzi,et al.  Nucleotide sequence and functional analysis of the tet (M)-carrying conjugative transposon Tn5251 of Streptococcus pneumoniae. , 2010, FEMS microbiology letters.

[18]  Y. Rikihisa Anaplasma phagocytophilum and Ehrlichia chaffeensis: subversive manipulators of host cells , 2010, Nature Reviews Microbiology.

[19]  Armanda Pugnaloni,et al.  Φm46.1, the Main Streptococcus pyogenes Element Carrying mef(A) and tet(O) Genes , 2009, Antimicrobial Agents and Chemotherapy.

[20]  N. Croucher,et al.  Genome Watch: Breaking the ICE , 2009, Nature Reviews Microbiology.

[21]  A. Roberts,et al.  Diversity of putative Tn5253-like elements in Streptococcus pneumoniae. , 2009, International journal of antimicrobial agents.

[22]  M. Quail,et al.  Role of Conjugative Elements in the Evolution of the Multidrug-Resistant Pandemic Clone Streptococcus pneumoniaeSpain23F ST81 , 2008, Journal of bacteriology.

[23]  Songnian Hu,et al.  Genome evolution driven by host adaptations results in a more virulent and antimicrobial-resistant Streptococcus pneumoniae serotype 14 , 2009, BMC Genomics.

[24]  E. Ilina,et al.  Mechanisms of Macrolide Resistance among Streptococcus pneumoniae Isolates from Russia , 2008, Antimicrobial Agents and Chemotherapy.

[25]  James M. Musser,et al.  Contribution of Exogenous Genetic Elements to the Group A Streptococcus Metagenome , 2007, PloS one.

[26]  M. Vecchi,et al.  Composite Structure of Streptococcus pneumoniae Containing the Erythromycin Efflux Resistance Gene mef(I) and the Chloramphenicol Resistance Gene catQ , 2007, Antimicrobial Agents and Chemotherapy.

[27]  Anton Meinhart,et al.  Molecular and Structural Characterization of the PezAT Chromosomal Toxin-Antitoxin System of the Human Pathogen Streptococcus pneumoniae* , 2007, Journal of Biological Chemistry.

[28]  M. Vecchi,et al.  Molecular Characterization of Pneumococci with Efflux-Mediated Erythromycin Resistance and Identification of a Novel mef Gene Subclass, mef(I) , 2005, Antimicrobial Agents and Chemotherapy.

[29]  S. Schwarz,et al.  Molecular basis of bacterial resistance to chloramphenicol and florfenicol. , 2004, FEMS microbiology reviews.

[30]  Vincent Burrus,et al.  Shaping bacterial genomes with integrative and conjugative elements. , 2004, Research in microbiology.

[31]  E. Giovanetti,et al.  Conjugative transfer of the erm(A) gene from erythromycin-resistant Streptococcus pyogenes to macrolide-susceptible S. pyogenes, Enterococcus faecalis and Listeria innocua. , 2002, The Journal of antimicrobial chemotherapy.

[32]  W. Saenger,et al.  In vitro and in vivo Stability of the 2ζ2 Protein Complex of the Broad Host-Range Streptococcus pyogenes pSM19035 Addiction System , 2002, Biological chemistry.

[33]  A. Pantosti,et al.  Macrolide Efflux Genes mef(A) and mef(E) Are Carried by Different Genetic Elements in Streptococcus pneumoniae , 2002, Journal of Clinical Microbiology.

[34]  D. Stephens,et al.  Structure and dissemination of a chromosomal insertion element encoding macrolide efflux in Streptococcus pneumoniae. , 2001, The Journal of infectious diseases.

[35]  M. N. Vijayakumar,et al.  Genetic and transcriptional analysis of a regulatory region in streptococcal conjugative transposon Tn5252. , 2000, Plasmid.

[36]  G. Pozzi,et al.  Characterization of a Genetic Element Carrying the Macrolide Efflux Gene mef(A) in Streptococcus pneumoniae , 2000, Antimicrobial Agents and Chemotherapy.

[37]  T. Grebe,et al.  Detection of erythromycin-resistant determinants by PCR , 1996, Antimicrobial agents and chemotherapy.

[38]  G. Pozzi,et al.  Competence for genetic transformation in encapsulated strains of Streptococcus pneumoniae: two allelic variants of the peptide pheromone , 1996, Journal of bacteriology.

[39]  S. Al-Khaldi,et al.  Identification and nucleotide sequence analysis of a transfer-related region in the streptococcal conjugative transposon Tn5252 , 1994, Journal of bacteriology.

[40]  P. Trieu-Cuot,et al.  Study of heterogeneity of chloramphenicol acetyltransferase (CAT) genes in streptococci and enterococci by polymerase chain reaction: characterization of a new CAT determinant , 1993, Antimicrobial Agents and Chemotherapy.

[41]  S. Ayalew,et al.  Nucleotide sequence analysis of the termini and chromosomal locus involved in site-specific integration of the streptococcal conjugative transposon Tn5252 , 1993, Journal of bacteriology.

[42]  P. Ayoubi,et al.  Tn5253, the pneumococcal omega (cat tet) BM6001 element, is a composite structure of two conjugative transposons, Tn5251 and Tn5252 , 1991, Journal of bacteriology.

[43]  B. Wren,et al.  Hybridization analysis of three chloramphenicol resistance determinants from Clostridium perfringens and Clostridium difficile , 1989, Antimicrobial Agents and Chemotherapy.