Emergence of plasmid-mediated tigecycline resistance tet(X4) gene in Enterobacterales isolated from wild animals in captivity

Background: Over the past few decades, antimicrobial resistance (AMR) has emerged as a global health challenge in human and veterinary medicine. Research on AMR genes in captive wild animals has increased. However, the presence and molecular characteristics of tet(X)-carrying bacteria in these anima...

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Main Authors: Lei Lei, Panfeng Xiong, Zelin Yan, Yanyan Zhang, Yuchen Wu, Gongxiang Chen, Houhui Song, Rong Zhang
Format: Article
Language:English
Published: Elsevier 2024-01-01
Series:Science in One Health
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Online Access:http://www.sciencedirect.com/science/article/pii/S2949704324000088
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author Lei Lei
Panfeng Xiong
Zelin Yan
Yanyan Zhang
Yuchen Wu
Gongxiang Chen
Houhui Song
Rong Zhang
author_facet Lei Lei
Panfeng Xiong
Zelin Yan
Yanyan Zhang
Yuchen Wu
Gongxiang Chen
Houhui Song
Rong Zhang
author_sort Lei Lei
collection DOAJ
description Background: Over the past few decades, antimicrobial resistance (AMR) has emerged as a global health challenge in human and veterinary medicine. Research on AMR genes in captive wild animals has increased. However, the presence and molecular characteristics of tet(X)-carrying bacteria in these animals remain unknown. Methods: Eighty-four samples were collected from captive wild animals. tet(X) variants were detected using polymerase chain reaction and the isolates were identified using matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. All isolated strains were subjected to antimicrobial susceptibility testing and whole-genome sequencing. The virulence of an Escherichia coli strain carrying enterotoxin genes was assessed using a Galleria mellonella larval model. Results: We isolated two tet(X4)-positive E. coli strains and one tet(X4)-positive Raoultella ornithinolytica strain. Antimicrobial susceptibility tests revealed that all three tet(X4)-carrying bacteria were sensitive to the 13 tested antimicrobial agents, but exhibited resistance to tigecycline. Notably, one tet(X4)-carrying E. coli strain producing an enterotoxin had a toxic effect on G. mellonella larvae. Whole-genome sequencing analysis showed that the two tet(X4)-carrying E. coli strains had more than 95% similarity to tet(X4)-containing E. coli strains isolated from pigs and humans in China. Conclusion: The genetic environment of tet(X4) closely resembled that of the plasmid described in previous studies. Our study identified tet(X4)-positive strains in wildlife and provided valuable epidemiological data for monitoring drug resistance. The identification of enterotoxin-producing E. coli strains also highlights the potential risks posed by virulence genes.
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spelling doaj-art-4bf1918f7a55425f88f09b3fbd9b22bc2024-12-12T05:24:52ZengElsevierScience in One Health2949-70432024-01-013100069Emergence of plasmid-mediated tigecycline resistance tet(X4) gene in Enterobacterales isolated from wild animals in captivityLei Lei0Panfeng Xiong1Zelin Yan2Yanyan Zhang3Yuchen Wu4Gongxiang Chen5Houhui Song6Rong Zhang7Key Laboratory of Applied Technology on Green-Eco-Healthy Animal Husbandry of Zhejiang Province, Zhejiang Provincial Engineering Laboratory for Animal Health Inspection & Internet Technology, Zhejiang International Science and Technology Cooperation Base for Veterinary Medicine and Health Management, China-Australia Joint Laboratory for Animal Health Big Data Analytics, College of Animal Science and Technology & College of Veterinary Medicine, Zhejiang Agriculture and Forestry University, Hangzhou, Zhejiang 311300, ChinaKey Laboratory of Applied Technology on Green-Eco-Healthy Animal Husbandry of Zhejiang Province, Zhejiang Provincial Engineering Laboratory for Animal Health Inspection & Internet Technology, Zhejiang International Science and Technology Cooperation Base for Veterinary Medicine and Health Management, China-Australia Joint Laboratory for Animal Health Big Data Analytics, College of Animal Science and Technology & College of Veterinary Medicine, Zhejiang Agriculture and Forestry University, Hangzhou, Zhejiang 311300, China; Department of Clinical Laboratory, The Second Affiliated Hospital of Zhejiang University School of Medicine, Hangzhou, Zhejiang 310009, ChinaDepartment of Clinical Laboratory, The Second Affiliated Hospital of Zhejiang University School of Medicine, Hangzhou, Zhejiang 310009, ChinaDepartment of Clinical Laboratory, The Second Affiliated Hospital of Zhejiang University School of Medicine, Hangzhou, Zhejiang 310009, ChinaDepartment of Clinical Laboratory, The Second Affiliated Hospital of Zhejiang University School of Medicine, Hangzhou, Zhejiang 310009, ChinaDepartment of Clinical Laboratory, The Second Affiliated Hospital of Zhejiang University School of Medicine, Hangzhou, Zhejiang 310009, ChinaKey Laboratory of Applied Technology on Green-Eco-Healthy Animal Husbandry of Zhejiang Province, Zhejiang Provincial Engineering Laboratory for Animal Health Inspection & Internet Technology, Zhejiang International Science and Technology Cooperation Base for Veterinary Medicine and Health Management, China-Australia Joint Laboratory for Animal Health Big Data Analytics, College of Animal Science and Technology & College of Veterinary Medicine, Zhejiang Agriculture and Forestry University, Hangzhou, Zhejiang 311300, China; Corresponding author.Department of Clinical Laboratory, The Second Affiliated Hospital of Zhejiang University School of Medicine, Hangzhou, Zhejiang 310009, China; Corresponding author.Background: Over the past few decades, antimicrobial resistance (AMR) has emerged as a global health challenge in human and veterinary medicine. Research on AMR genes in captive wild animals has increased. However, the presence and molecular characteristics of tet(X)-carrying bacteria in these animals remain unknown. Methods: Eighty-four samples were collected from captive wild animals. tet(X) variants were detected using polymerase chain reaction and the isolates were identified using matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. All isolated strains were subjected to antimicrobial susceptibility testing and whole-genome sequencing. The virulence of an Escherichia coli strain carrying enterotoxin genes was assessed using a Galleria mellonella larval model. Results: We isolated two tet(X4)-positive E. coli strains and one tet(X4)-positive Raoultella ornithinolytica strain. Antimicrobial susceptibility tests revealed that all three tet(X4)-carrying bacteria were sensitive to the 13 tested antimicrobial agents, but exhibited resistance to tigecycline. Notably, one tet(X4)-carrying E. coli strain producing an enterotoxin had a toxic effect on G. mellonella larvae. Whole-genome sequencing analysis showed that the two tet(X4)-carrying E. coli strains had more than 95% similarity to tet(X4)-containing E. coli strains isolated from pigs and humans in China. Conclusion: The genetic environment of tet(X4) closely resembled that of the plasmid described in previous studies. Our study identified tet(X4)-positive strains in wildlife and provided valuable epidemiological data for monitoring drug resistance. The identification of enterotoxin-producing E. coli strains also highlights the potential risks posed by virulence genes.http://www.sciencedirect.com/science/article/pii/S2949704324000088Wild animaltet(X4)EnterobacteralesEnterotoxinTigecycline resistanceEpidemiology
spellingShingle Lei Lei
Panfeng Xiong
Zelin Yan
Yanyan Zhang
Yuchen Wu
Gongxiang Chen
Houhui Song
Rong Zhang
Emergence of plasmid-mediated tigecycline resistance tet(X4) gene in Enterobacterales isolated from wild animals in captivity
Science in One Health
Wild animal
tet(X4)
Enterobacterales
Enterotoxin
Tigecycline resistance
Epidemiology
title Emergence of plasmid-mediated tigecycline resistance tet(X4) gene in Enterobacterales isolated from wild animals in captivity
title_full Emergence of plasmid-mediated tigecycline resistance tet(X4) gene in Enterobacterales isolated from wild animals in captivity
title_fullStr Emergence of plasmid-mediated tigecycline resistance tet(X4) gene in Enterobacterales isolated from wild animals in captivity
title_full_unstemmed Emergence of plasmid-mediated tigecycline resistance tet(X4) gene in Enterobacterales isolated from wild animals in captivity
title_short Emergence of plasmid-mediated tigecycline resistance tet(X4) gene in Enterobacterales isolated from wild animals in captivity
title_sort emergence of plasmid mediated tigecycline resistance tet x4 gene in enterobacterales isolated from wild animals in captivity
topic Wild animal
tet(X4)
Enterobacterales
Enterotoxin
Tigecycline resistance
Epidemiology
url http://www.sciencedirect.com/science/article/pii/S2949704324000088
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