Genomics Insight into <i>cfr</i>-Mediated Linezolid-Resistant LA-MRSA in Italian Pig Holdings

The <i>cfr</i> genes encode for a 23S rRNA methyltransferase, conferring a multiresistance phenotype to phenicol, lincosamide, oxazolidinone, pleuromutilin, and streptogramin A antibiotics. These genes have been described in staphylococci, including methicillin-resistant <i>Staphyl...

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Main Authors: Manuela Iurescia, Elena Lavinia Diaconu, Patricia Alba, Fabiola Feltrin, Carmela Buccella, Roberta Onorati, Angelo Giacomi, Andrea Caprioli, Alessia Franco, Antonio Battisti, Virginia Carfora
Format: Article
Language:English
Published: MDPI AG 2023-03-01
Series:Antibiotics
Subjects:
Online Access:https://www.mdpi.com/2079-6382/12/3/530
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author Manuela Iurescia
Elena Lavinia Diaconu
Patricia Alba
Fabiola Feltrin
Carmela Buccella
Roberta Onorati
Angelo Giacomi
Andrea Caprioli
Alessia Franco
Antonio Battisti
Virginia Carfora
author_facet Manuela Iurescia
Elena Lavinia Diaconu
Patricia Alba
Fabiola Feltrin
Carmela Buccella
Roberta Onorati
Angelo Giacomi
Andrea Caprioli
Alessia Franco
Antonio Battisti
Virginia Carfora
author_sort Manuela Iurescia
collection DOAJ
description The <i>cfr</i> genes encode for a 23S rRNA methyltransferase, conferring a multiresistance phenotype to phenicol, lincosamide, oxazolidinone, pleuromutilin, and streptogramin A antibiotics. These genes have been described in staphylococci, including methicillin-resistant <i>Staphylococcus aureus</i> (MRSA). In this study, we retrospectively performed an in-depth genomic characterisation of three <i>cfr</i>-positive, multidrug-resistant (MDR) livestock-associated (LA) MRSA clonal complexes (CCs) 1 and 398 detected in different Italian pig holdings (2008–2011) during population studies on Italian livestock (2008–2014). We used a combined Illumina and Oxford Nanopore Technologies (ONT) whole genome sequencing (WGS) approach on two isolates (the 2008 CC1 and the 2010 CC398 isolates, but not the 2011 CC1 isolate). Interestingly, the three isolates presented different <i>cfr</i> variants, with only one displaying a linezolid-resistant phenotype. In isolate 2008 CC1, the <i>cfr</i> gene was identified within a Tn558 composite transposon-like structure flanked by IS elements located on a novel 44,826 bp plasmid. This represents the first report of CC1 LA-MRSA harbouring the <i>cfr</i> gene in its functional variant. Differently, <i>cfr</i> was chromosomally located in isolate 2010 CC398. Our findings have significant public health implications, confirm the need for the continuous genomic surveillance of <i>cfr</i>-positive zoonotic LA-MRSA, and backdate <i>cfr</i> presence in LA-MRSA from Italian pigs to at least 2008.
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spelling doaj.art-236e78dd96ba4bcfb063195fd47fe17b2023-11-17T09:14:18ZengMDPI AGAntibiotics2079-63822023-03-0112353010.3390/antibiotics12030530Genomics Insight into <i>cfr</i>-Mediated Linezolid-Resistant LA-MRSA in Italian Pig HoldingsManuela Iurescia0Elena Lavinia Diaconu1Patricia Alba2Fabiola Feltrin3Carmela Buccella4Roberta Onorati5Angelo Giacomi6Andrea Caprioli7Alessia Franco8Antonio Battisti9Virginia Carfora10National Reference Laboratory for Antimicrobial Resistance, Department of General Diagnostics, Istituto Zooprofilattico Sperimentale del Lazio e Della Toscana “M. Aleandri”, 00178 Rome, ItalyNational Reference Laboratory for Antimicrobial Resistance, Department of General Diagnostics, Istituto Zooprofilattico Sperimentale del Lazio e Della Toscana “M. Aleandri”, 00178 Rome, ItalyNational Reference Laboratory for Antimicrobial Resistance, Department of General Diagnostics, Istituto Zooprofilattico Sperimentale del Lazio e Della Toscana “M. Aleandri”, 00178 Rome, ItalyNational Reference Laboratory for Antimicrobial Resistance, Department of General Diagnostics, Istituto Zooprofilattico Sperimentale del Lazio e Della Toscana “M. Aleandri”, 00178 Rome, ItalyNational Reference Laboratory for Antimicrobial Resistance, Department of General Diagnostics, Istituto Zooprofilattico Sperimentale del Lazio e Della Toscana “M. Aleandri”, 00178 Rome, ItalyNational Reference Laboratory for Antimicrobial Resistance, Department of General Diagnostics, Istituto Zooprofilattico Sperimentale del Lazio e Della Toscana “M. Aleandri”, 00178 Rome, ItalyNational Reference Laboratory for Antimicrobial Resistance, Department of General Diagnostics, Istituto Zooprofilattico Sperimentale del Lazio e Della Toscana “M. Aleandri”, 00178 Rome, ItalyNational Reference Laboratory for Antimicrobial Resistance, Department of General Diagnostics, Istituto Zooprofilattico Sperimentale del Lazio e Della Toscana “M. Aleandri”, 00178 Rome, ItalyNational Reference Laboratory for Antimicrobial Resistance, Department of General Diagnostics, Istituto Zooprofilattico Sperimentale del Lazio e Della Toscana “M. Aleandri”, 00178 Rome, ItalyNational Reference Laboratory for Antimicrobial Resistance, Department of General Diagnostics, Istituto Zooprofilattico Sperimentale del Lazio e Della Toscana “M. Aleandri”, 00178 Rome, ItalyNational Reference Laboratory for Antimicrobial Resistance, Department of General Diagnostics, Istituto Zooprofilattico Sperimentale del Lazio e Della Toscana “M. Aleandri”, 00178 Rome, ItalyThe <i>cfr</i> genes encode for a 23S rRNA methyltransferase, conferring a multiresistance phenotype to phenicol, lincosamide, oxazolidinone, pleuromutilin, and streptogramin A antibiotics. These genes have been described in staphylococci, including methicillin-resistant <i>Staphylococcus aureus</i> (MRSA). In this study, we retrospectively performed an in-depth genomic characterisation of three <i>cfr</i>-positive, multidrug-resistant (MDR) livestock-associated (LA) MRSA clonal complexes (CCs) 1 and 398 detected in different Italian pig holdings (2008–2011) during population studies on Italian livestock (2008–2014). We used a combined Illumina and Oxford Nanopore Technologies (ONT) whole genome sequencing (WGS) approach on two isolates (the 2008 CC1 and the 2010 CC398 isolates, but not the 2011 CC1 isolate). Interestingly, the three isolates presented different <i>cfr</i> variants, with only one displaying a linezolid-resistant phenotype. In isolate 2008 CC1, the <i>cfr</i> gene was identified within a Tn558 composite transposon-like structure flanked by IS elements located on a novel 44,826 bp plasmid. This represents the first report of CC1 LA-MRSA harbouring the <i>cfr</i> gene in its functional variant. Differently, <i>cfr</i> was chromosomally located in isolate 2010 CC398. Our findings have significant public health implications, confirm the need for the continuous genomic surveillance of <i>cfr</i>-positive zoonotic LA-MRSA, and backdate <i>cfr</i> presence in LA-MRSA from Italian pigs to at least 2008.https://www.mdpi.com/2079-6382/12/3/530<i>Staphylococcus aureus</i>LA-MRSAlinezolid<i>cfr</i>WGSlong reads
spellingShingle Manuela Iurescia
Elena Lavinia Diaconu
Patricia Alba
Fabiola Feltrin
Carmela Buccella
Roberta Onorati
Angelo Giacomi
Andrea Caprioli
Alessia Franco
Antonio Battisti
Virginia Carfora
Genomics Insight into <i>cfr</i>-Mediated Linezolid-Resistant LA-MRSA in Italian Pig Holdings
Antibiotics
<i>Staphylococcus aureus</i>
LA-MRSA
linezolid
<i>cfr</i>
WGS
long reads
title Genomics Insight into <i>cfr</i>-Mediated Linezolid-Resistant LA-MRSA in Italian Pig Holdings
title_full Genomics Insight into <i>cfr</i>-Mediated Linezolid-Resistant LA-MRSA in Italian Pig Holdings
title_fullStr Genomics Insight into <i>cfr</i>-Mediated Linezolid-Resistant LA-MRSA in Italian Pig Holdings
title_full_unstemmed Genomics Insight into <i>cfr</i>-Mediated Linezolid-Resistant LA-MRSA in Italian Pig Holdings
title_short Genomics Insight into <i>cfr</i>-Mediated Linezolid-Resistant LA-MRSA in Italian Pig Holdings
title_sort genomics insight into i cfr i mediated linezolid resistant la mrsa in italian pig holdings
topic <i>Staphylococcus aureus</i>
LA-MRSA
linezolid
<i>cfr</i>
WGS
long reads
url https://www.mdpi.com/2079-6382/12/3/530
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