Global spread of the linezolid-resistant Enterococcus faecalis ST476 clonal lineage carrying optrA

Author:

Brenciani Andrea1ORCID,Cinthi Marzia2,Coccitto Sonia Nina1,Massacci Francesca Romana3ORCID,Albini Elisa3,Cucco Lucilla3,Paniccià Marta3,Freitas Ana R456ORCID,Schwarz Stefan789ORCID,Giovanetti Eleonora2,Magistrali Chiara Francesca3

Affiliation:

1. Department of Biomedical Sciences and Public Health, Unit of Microbiology, Polytechnic University of Marche Medical School , Ancona , Italy

2. Department of Life and Environmental Sciences, Unit of Microbiology, Polytechnic University of Marche , Ancona , Italy

3. Department of Research and Development, Istituto Zooprofilattico Sperimentale dell'Umbria e delle Marche ‘Togo Rosati’ , Perugia , Italy

4. UCIBIO, Departamento de Ciências Biológicas, Laboratório de Microbiologia, Faculdade de Farmácia, Universidade do Porto , Porto , Portugal

5. Associate Laboratory i4HB, Faculty of Pharmacy, Institute for Health and Bioeconomy, University of Porto , Porto , Portugal

6. 1H-TOXRUN—One Health Toxicology Research Unit, University Institute of Health Sciences, CESPU, CRL , Gandra 4585-116 , Portugal

7. Institute of Microbiology and Epizootics, Centre for Infection Medicine, School of Veterinary Medicine, Freie Universität Berlin , Berlin , Germany

8. Veterinary Centre for Resistance Research (TZR), School of Veterinary Medicine, Freie Universität Berlin , Berlin , Germany

9. Key Laboratory of Animal Antimicrobial Resistance Surveillance, MARA, College of Veterinary Medicine, China Agricultural University , Beijing , People’s Republic of China

Abstract

Abstract Objectives To investigate the global distribution of an optrA-harbouring linezolid-resistant Enterococcus faecalis ST476 clonal lineage. Methods Comprehensive searches of the NCBI database were performed to identify published peer-reviewed articles and genomes of E. faecalis ST476. Each genome was analysed for resistome, virulome, OptrA variant and optrA genetic contexts. A phylogenetic comparison of ST476 genomes with publicly available genomes of other STs was also performed. Results Sixty-six E. faecalis ST476 isolates from 15 countries (China, Japan, South Korea, Austria, Denmark, Spain, Czech Republic, Colombia, Tunisia, Italy, Malaysia, Belgium, Germany, United Arab Emirates and Switzerland) mainly of human and animal origin were identified. Thirty available ST476 genomes compared with genomes of 591 STs indicated a progressive radiation of E. faecalis STs starting from ST21. The closest ancestral node for ST476 was ST1238. Thirty E. faecalis ST476 genomes exhibited 3–916 SNP differences. Several antimicrobial resistance and virulence genes were conserved among the ST476 genomes. The optrA genetic context exhibited a high degree of or complete identity to the chromosomal transposon Tn6674. Only three isolates displayed an optrA-carrying plasmid with complete or partial Tn6674. The WT OptrA protein was most widespread in the ST476 lineage. Conclusions Linezolid-resistant optrA-carrying E. faecalis of the clonal lineage ST476 is globally distributed in human, animal and environmental settings. The presence of such an emerging clone can be of great concern for public health. Thus, a One Health approach is needed to counteract the spread and the evolution of this enterococcal clonal lineage.

Funder

PRIN 2017

MIUR

Publisher

Oxford University Press (OUP)

Reference19 articles.

1. Oxazolidinones: mechanisms of resistance and mobile genetic elements involved;Brenciani;J Antimicrob Chemother,2022

2. Mobile oxazolidinone resistance genes in Gram-positive and Gram-negative bacteria;Schwarz;Clin Microbiol Rev,2021

3. A novel gene, optrA, that confers transferable resistance to oxazolidinones and phenicols and its presence in Enterococcus faecalis and Enterococcus faecium of human and animal origin;Wang;J Antimicrob Chemother,2015

4. Comparative genomics of global optrA-carrying Enterococcus faecalis uncovers a common chromosomal hotspot for optrA acquisition within a diversity of core and accessory genomes;Freitas;Microb Genom,2020

5. LRE-Finder, a Web tool for detection of the 23S rRNA mutations and the optrA, cfr, cfr(B) and poxtA genes encoding linezolid resistance in enterococci from whole-genome sequences;Hasman;J Antimicrob Chemother,2019

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