Global distribution and genomic characteristics analysis of avian-derived mcr-1-positive Escherichia coli

Qianlong Li; Jing Yang; Mingshu Wang; Renyong Jia; Shun Chen; Mafeng Liu; Dekang Zhu; Xinxin Zhao; Ying Wu; Qiao Yang; Juan Huang; Xumin Ou; Di Sun; Bin Tian; Yu He; Zhen Wu; Anchun Cheng; Shaqiu Zhang

Ecotoxicology and Environmental Safety (Oct 2024)

Global distribution and genomic characteristics analysis of avian-derived mcr-1-positive Escherichia coli

Qianlong Li,
Jing Yang,
Mingshu Wang,
Renyong Jia,
Shun Chen,
Mafeng Liu,
Dekang Zhu,
Xinxin Zhao,
Ying Wu,
Qiao Yang,
Juan Huang,
Xumin Ou,
Di Sun,
Bin Tian,
Yu He,
Zhen Wu,
Anchun Cheng,
Shaqiu Zhang

Affiliations

Qianlong Li: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China
Jing Yang: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China
Mingshu Wang: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, PR China; Engineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the P.R.China, PR China
Renyong Jia: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, PR China; Engineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the P.R.China, PR China
Shun Chen: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, PR China; Engineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the P.R.China, PR China
Mafeng Liu: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, PR China; Engineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the P.R.China, PR China
Dekang Zhu: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Engineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the P.R.China, PR China
Xinxin Zhao: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, PR China; Engineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the P.R.China, PR China
Ying Wu: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, PR China; Engineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the P.R.China, PR China
Qiao Yang: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, PR China; Engineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the P.R.China, PR China
Juan Huang: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, PR China; Engineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the P.R.China, PR China
Xumin Ou: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, PR China; Engineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the P.R.China, PR China
Di Sun: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, PR China; Engineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the P.R.China, PR China
Bin Tian: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, PR China; Engineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the P.R.China, PR China
Yu He: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, PR China; Engineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the P.R.China, PR China
Zhen Wu: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, PR China; Engineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the P.R.China, PR China
Anchun Cheng: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, PR China; Engineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the P.R.China, PR China; Corresponding authors at: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China.
Shaqiu Zhang: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China; Key Laboratory of Animal Disease and Human Health of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, PR China; Engineering Research Center of Southwest Animal Disease Prevention and Control Technology, Ministry of Education of the P.R.China, PR China; Corresponding authors at: Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, PR China.

Journal volume & issue: Vol. 285
p. 117109

Abstract

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The prevalence of avian-derived Escherichia coli (E. coli) carrying mcr-1 poses a significant threat to the development of the poultry industry and public health safety. Despite ongoing in-depth epidemiological research worldwide, a comprehensive macroscopic study based on genomics is still lacking. In response, this study collected 1104 genomic sequences of avian-derived mcr-1-positive E. coli (MCRPEC) from the NCBI public database, covering 31 countries. The majority of sequences originated from China (48.82 %), followed by the Netherlands (10.41 %). In terms of avian hosts, chicken accounted for the largest proportion (44.11 %), followed by gallus (24.09 %). Avian-derived MCRPEC also serves as a reservoir for other antibiotic resistance genes (ARGs), with 179 ARGs coexisting with mcr-1 identified. A total of 206 virulence-associated genes were also identified, revealing the pathogenic risks of MCRPEC. Pan-genome analysis revealed that avian-derived MCRPEC from different hosts, countries of origin, and serotypes exhibit minor SNP differences, indicating a high risk of cross-regional and cross-host transmission. The ST types of MCRPRC are diverse, with ST10 being the most prevalent (n=70). Spearman analysis showed a significant correlation between the number of ARGs and the insertion sequences (ISs) as well as plasmid replicon in ST10 strains. Furthermore, ST10 strains share a similar genetic basis with human-derived MCRPEC, suggesting the possibility of clonal dissemination. Pan-genome-wide association studies (pan-GWAS) indicated that the differential genes of MCRPEC from different countries and host sources are significantly different, mainly related to genes encoding type IV secretion systems and mobile genetic elements (MGEs). Plasmid mapping of showed that the prevalent plasmid types vary by country and host, with IncI2 and IncX4 being the main mcr-1-positive plasmids. Among the 12 identified mcr-1 genetic contexts with ISs, the Tn6330 transposon was the predominant carrier of mcr-1. In summary, the potential threat of avian-derived MCRPEC cannot be ignored, and long-term and comprehensive monitoring are essential.

Published in Ecotoxicology and Environmental Safety

ISSN: 0147-6513 (Print); 1090-2414 (Online)
Publisher: Elsevier
Country of publisher: United States
LCC subjects: Technology: Environmental technology. Sanitary engineering: Environmental pollution; Geography. Anthropology. Recreation: Environmental sciences
Website: https://www.journals.elsevier.com/ecotoxicology-and-environmental-safety

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