Mapping the widespread distribution and transmission dynamics of linezolid resistance in humans, animals, and the environment.

optrA Animal Environment Human Linezolid resistance One health

Journal

Microbiome
ISSN: 2049-2618
Titre abrégé: Microbiome
Pays: England
ID NLM: 101615147

Informations de publication

Date de publication:
13 Mar 2024
Historique:
received: 10 10 2023
accepted: 19 12 2023
medline: 14 3 2024
pubmed: 14 3 2024
entrez: 14 3 2024
Statut: epublish

Résumé

The rise of linezolid resistance has been widely observed both in clinical and non-clinical settings. However, there were still data gaps regarding the comprehensive prevalence and interconnections of linezolid resistance genes across various niches. We screened for potential linezolid resistance gene reservoirs in the intestines of both humans and animals, in meat samples, as well as in water sources. A total of 796 bacteria strains out of 1538 non-duplicated samples were identified to be positive for at least one linezolid resistance gene, optrA, poxtA, cfr, and cfr(D). The prevalence of optrA reached 100% (95% CI 96.3-100%) in the intestines of pigs, followed by fish, ducks, and chicken at 77.5% (95% CI 67.2-85.3%), 62.0% (95% CI 52.2-70.9%), and 61.0% (95% CI 51.2-70.0%), respectively. The meat and water samples presented prevalences of 80.0% (95% CI 70.6-87.0%) and 38.0% (95% CI 25.9-51.9%), respectively. The unreported prevalence of the cfr(D) gene was also relatively higher at 13.0% (95% CI 7.8-21.0%) and 19.0% (95% CI 10.9-25.6%) for the feces samples of ducks and pigs, respectively. Enterococci were the predominant hosts for all genes, while several non-enterococcal species were also identified. Phylogenetic analysis revealed a significant genetic distance among linezolid resistance gene reservoirs, with polyclonal structures observed in strains within the same niche. Similar genetic arrays harboring assorted insertion sequences or transposons were shared by reservoirs displaying heterogeneous backgrounds, though large diversity in the genetic environment of linezolid resistance genes was also observed. The linezolid resistance genes were widespread among various niches. The horizontal transfer played a crucial role in driving the circulation of linezolid resistance reservoirs at the human-animal-environment interfaces. Video Abstract.

Sections du résumé

BACKGROUND BACKGROUND
The rise of linezolid resistance has been widely observed both in clinical and non-clinical settings. However, there were still data gaps regarding the comprehensive prevalence and interconnections of linezolid resistance genes across various niches.
RESULTS RESULTS
We screened for potential linezolid resistance gene reservoirs in the intestines of both humans and animals, in meat samples, as well as in water sources. A total of 796 bacteria strains out of 1538 non-duplicated samples were identified to be positive for at least one linezolid resistance gene, optrA, poxtA, cfr, and cfr(D). The prevalence of optrA reached 100% (95% CI 96.3-100%) in the intestines of pigs, followed by fish, ducks, and chicken at 77.5% (95% CI 67.2-85.3%), 62.0% (95% CI 52.2-70.9%), and 61.0% (95% CI 51.2-70.0%), respectively. The meat and water samples presented prevalences of 80.0% (95% CI 70.6-87.0%) and 38.0% (95% CI 25.9-51.9%), respectively. The unreported prevalence of the cfr(D) gene was also relatively higher at 13.0% (95% CI 7.8-21.0%) and 19.0% (95% CI 10.9-25.6%) for the feces samples of ducks and pigs, respectively. Enterococci were the predominant hosts for all genes, while several non-enterococcal species were also identified. Phylogenetic analysis revealed a significant genetic distance among linezolid resistance gene reservoirs, with polyclonal structures observed in strains within the same niche. Similar genetic arrays harboring assorted insertion sequences or transposons were shared by reservoirs displaying heterogeneous backgrounds, though large diversity in the genetic environment of linezolid resistance genes was also observed.
CONCLUSIONS CONCLUSIONS
The linezolid resistance genes were widespread among various niches. The horizontal transfer played a crucial role in driving the circulation of linezolid resistance reservoirs at the human-animal-environment interfaces. Video Abstract.

Identifiants

DOI: 10.1186/s40168-023-01744-2 PMID: 38481333
pubmed: 38481333
doi: 10.1186/s40168-023-01744-2
pii: 10.1186/s40168-023-01744-2
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

52

Subventions

Organisme : National Key Research and Development Program of China
ID : 2022YFD1800403
Organisme : National Natural Science Foundation of China
ID : 81971988

Informations de copyright

© 2024. The Author(s).

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Auteurs

Weiyi Shen (W)

Clinical Microbiology Laboratory, The Second Affiliated Hospital of Zhejiang University School of Medicine, Zhejiang University, Hangzhou, China.

Chang Cai (C)

China Australia Joint Laboratory for Animal Health Big Data Analytics, College of Animal Science and Technology, Zhejiang Agricultural and Forestry University, Hangzhou, China.

Ning Dong (N)

Department of Medical Microbiology, School of Biology and Basic Medical Science, Medical College of Soochow University, Suzhou, China.
Suzhou Key Laboratory of Pathogen Bioscience and Anti-Infective Medicine, Soochow University, Suzhou, China.

Jiawei Chen (J)

Clinical Microbiology Laboratory, The Second Affiliated Hospital of Zhejiang University School of Medicine, Zhejiang University, Hangzhou, China.

Rong Zhang (R)

Clinical Microbiology Laboratory, The Second Affiliated Hospital of Zhejiang University School of Medicine, Zhejiang University, Hangzhou, China. zhang-rong@zju.edu.cn.

Jiachang Cai (J)

Clinical Microbiology Laboratory, The Second Affiliated Hospital of Zhejiang University School of Medicine, Zhejiang University, Hangzhou, China. caijiachang@zju.edu.cn.

Classifications MeSH