Comprehensive investigation of antibiotic resistance gene content in cfiA-harboring Bacteroides fragilis isolates of human and animal origins by whole genome sequencing
Introduction: The emergence of multidrug resistance in Bacteroides fragilis, especially the phylogenetic lineage carrying the carbapenemase gene cfiA, represents an increasing threat to human health. However, knowledge on the diversity of the multidrug-resistant strains and the genetic elements carr...
| Main Authors: | , , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2022-08-01
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| Series: | International Journal of Medical Microbiology |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S1438422122000121 |
| _version_ | 1811183662084915200 |
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| author | Huiluo Cao Melissa Chun-Jiao Liu Man-Ki Tong Shuo Jiang Kin-Hung Chow Kelvin Kai-Wang To Cindy Wing-Sze Tse Pak-Leung Ho |
| author_facet | Huiluo Cao Melissa Chun-Jiao Liu Man-Ki Tong Shuo Jiang Kin-Hung Chow Kelvin Kai-Wang To Cindy Wing-Sze Tse Pak-Leung Ho |
| author_sort | Huiluo Cao |
| collection | DOAJ |
| description | Introduction: The emergence of multidrug resistance in Bacteroides fragilis, especially the phylogenetic lineage carrying the carbapenemase gene cfiA, represents an increasing threat to human health. However, knowledge on the diversity of the multidrug-resistant strains and the genetic elements carrying the antibiotic resistance genes (ARGs) remains limited. Aim: The objective of the study was to describe the resistome in cfiA-positive B. fragilis. Methods: A collection of cfiA-positive B. fragilis from diverse human (8 bacteremias, 15 wound infections) and animal (2 chickens, 2 pigs, 6 dogs, 3 cats) sources in Hong Kong, 2015–2017 was analysed by whole genome sequencing. Results: In the 36 isolates, 13 distinct ARGs (total number 83, median 2, range 0–7 per isolate) other than cfiA were detected. ARGs encoding resistance to aminoglycosides, β-lactams, macrolides, sulphonamides and tetracyclines were carried by CTn341-like, CTnHyb-like, Tn5220-like, Tn4555-like and Tn613-like transposons and were detected in phylogenetically diverse isolates of different host sources. Only few ARGs encoding resistance to metronidazole and tetracyclines were localized on plasmids. In two chicken isolates, a novel transposon (designated as Tn6994) was found to be involved in the dissemination of multiple ARGs mediating resistance to multiple antibiotics, including metronidazole and linezolid that are critically important for treatment of anaerobic infections. In mating experiments, Tn6994 and the associated phenotypic resistance could be transferred to Bacteroides nordii recipient. Conclusion: This study illustrates the importance of transposons in the dissemination of ARGs in the cfiA-positive division of B. fragilis. One Health approach is necessary to track the dissemination of ARGs. |
| first_indexed | 2024-04-11T09:49:32Z |
| format | Article |
| id | doaj.art-4234f1b6d92042559273f416ad32e8db |
| institution | Directory Open Access Journal |
| issn | 1438-4221 |
| language | English |
| last_indexed | 2024-04-11T09:49:32Z |
| publishDate | 2022-08-01 |
| publisher | Elsevier |
| record_format | Article |
| series | International Journal of Medical Microbiology |
| spelling | doaj.art-4234f1b6d92042559273f416ad32e8db2022-12-22T04:30:50ZengElsevierInternational Journal of Medical Microbiology1438-42212022-08-013126151559Comprehensive investigation of antibiotic resistance gene content in cfiA-harboring Bacteroides fragilis isolates of human and animal origins by whole genome sequencingHuiluo Cao0Melissa Chun-Jiao Liu1Man-Ki Tong2Shuo Jiang3Kin-Hung Chow4Kelvin Kai-Wang To5Cindy Wing-Sze Tse6Pak-Leung Ho7Department of Microbiology, Queen Mary Hospital, University of Hong Kong, Hong Kong Special Special Administrative Region of China; Carol Yu Center for Infection, University of Hong Kong, Hong Kong Special Special Administrative Region of ChinaDepartment of Microbiology, Queen Mary Hospital, University of Hong Kong, Hong Kong Special Special Administrative Region of ChinaDepartment of Microbiology, Queen Mary Hospital, University of Hong Kong, Hong Kong Special Special Administrative Region of ChinaDepartment of Microbiology, Queen Mary Hospital, University of Hong Kong, Hong Kong Special Special Administrative Region of ChinaDepartment of Microbiology, Queen Mary Hospital, University of Hong Kong, Hong Kong Special Special Administrative Region of China; Carol Yu Center for Infection, University of Hong Kong, Hong Kong Special Special Administrative Region of ChinaDepartment of Microbiology, Queen Mary Hospital, University of Hong Kong, Hong Kong Special Special Administrative Region of ChinaDepartment of Clinical Pathology, Kwong Wah Hospital, Hospital Authority, Hong Kong Special Special Administrative Region of ChinaDepartment of Microbiology, Queen Mary Hospital, University of Hong Kong, Hong Kong Special Special Administrative Region of China; Carol Yu Center for Infection, University of Hong Kong, Hong Kong Special Special Administrative Region of China; Correspondence to: Department of Microbiology, Queen Mary Hospital, The University of Hong Kong, Pokfulam Road, Hong Kong Special Special Administrative Region of China.Introduction: The emergence of multidrug resistance in Bacteroides fragilis, especially the phylogenetic lineage carrying the carbapenemase gene cfiA, represents an increasing threat to human health. However, knowledge on the diversity of the multidrug-resistant strains and the genetic elements carrying the antibiotic resistance genes (ARGs) remains limited. Aim: The objective of the study was to describe the resistome in cfiA-positive B. fragilis. Methods: A collection of cfiA-positive B. fragilis from diverse human (8 bacteremias, 15 wound infections) and animal (2 chickens, 2 pigs, 6 dogs, 3 cats) sources in Hong Kong, 2015–2017 was analysed by whole genome sequencing. Results: In the 36 isolates, 13 distinct ARGs (total number 83, median 2, range 0–7 per isolate) other than cfiA were detected. ARGs encoding resistance to aminoglycosides, β-lactams, macrolides, sulphonamides and tetracyclines were carried by CTn341-like, CTnHyb-like, Tn5220-like, Tn4555-like and Tn613-like transposons and were detected in phylogenetically diverse isolates of different host sources. Only few ARGs encoding resistance to metronidazole and tetracyclines were localized on plasmids. In two chicken isolates, a novel transposon (designated as Tn6994) was found to be involved in the dissemination of multiple ARGs mediating resistance to multiple antibiotics, including metronidazole and linezolid that are critically important for treatment of anaerobic infections. In mating experiments, Tn6994 and the associated phenotypic resistance could be transferred to Bacteroides nordii recipient. Conclusion: This study illustrates the importance of transposons in the dissemination of ARGs in the cfiA-positive division of B. fragilis. One Health approach is necessary to track the dissemination of ARGs.http://www.sciencedirect.com/science/article/pii/S1438422122000121 |
| spellingShingle | Huiluo Cao Melissa Chun-Jiao Liu Man-Ki Tong Shuo Jiang Kin-Hung Chow Kelvin Kai-Wang To Cindy Wing-Sze Tse Pak-Leung Ho Comprehensive investigation of antibiotic resistance gene content in cfiA-harboring Bacteroides fragilis isolates of human and animal origins by whole genome sequencing International Journal of Medical Microbiology |
| title | Comprehensive investigation of antibiotic resistance gene content in cfiA-harboring Bacteroides fragilis isolates of human and animal origins by whole genome sequencing |
| title_full | Comprehensive investigation of antibiotic resistance gene content in cfiA-harboring Bacteroides fragilis isolates of human and animal origins by whole genome sequencing |
| title_fullStr | Comprehensive investigation of antibiotic resistance gene content in cfiA-harboring Bacteroides fragilis isolates of human and animal origins by whole genome sequencing |
| title_full_unstemmed | Comprehensive investigation of antibiotic resistance gene content in cfiA-harboring Bacteroides fragilis isolates of human and animal origins by whole genome sequencing |
| title_short | Comprehensive investigation of antibiotic resistance gene content in cfiA-harboring Bacteroides fragilis isolates of human and animal origins by whole genome sequencing |
| title_sort | comprehensive investigation of antibiotic resistance gene content in cfia harboring bacteroides fragilis isolates of human and animal origins by whole genome sequencing |
| url | http://www.sciencedirect.com/science/article/pii/S1438422122000121 |
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