Diverse Acinetobacter species and Plasmid-Driven spread of carbapenem resistance in pharmaceutical settings in China

Acinetobacter species have emerged as a significant public health concern due to their remarkable capacity to acquire antimicrobial resistance. Environmental reservoirs play a crucial role in spreading antimicrobial resistance genes and potentially pathogenic bacteria to clinical settings. However,...

Full description

Saved in:
Bibliographic Details
Main Authors: Jintao He, Liang Hong, Meijun Song, Yisha Zhang, Wang Zhang, Linghong Zhang, Danyan Zhou, Zhouwei Chen, Yunsong Yu, Huan Chen, Xiaoting Hua
Format: Article
Language:English
Published: Elsevier 2025-04-01
Series:Environment International
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0160412025001242
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849710429534683136
author Jintao He
Liang Hong
Meijun Song
Yisha Zhang
Wang Zhang
Linghong Zhang
Danyan Zhou
Zhouwei Chen
Yunsong Yu
Huan Chen
Xiaoting Hua
author_facet Jintao He
Liang Hong
Meijun Song
Yisha Zhang
Wang Zhang
Linghong Zhang
Danyan Zhou
Zhouwei Chen
Yunsong Yu
Huan Chen
Xiaoting Hua
author_sort Jintao He
collection DOAJ
description Acinetobacter species have emerged as a significant public health concern due to their remarkable capacity to acquire antimicrobial resistance. Environmental reservoirs play a crucial role in spreading antimicrobial resistance genes and potentially pathogenic bacteria to clinical settings. However, most studies on nonhuman isolates have focused on a limited sample size. Comprehensive population sampling on One Health principles is essential to monitor the antibiotic resistome and virulome in Acinetobacter spp. Here, we identified three carbapenems-resistant Acinetobacter spp. isolates harboring blaNDM-1 and discovered two novel Acinetobacter species in pharmaceutical production environments. A total of 94 Acinetobacter spp. strains were isolated from pharmaceutical production environments across 17 cities in China, forming 17 distinct Acinetobacter clusters comprising two novel species and 15 previously known species. Phylogenetic analysis indicated that Acinetobacter spp. isolated from pharmaceutical settings are predominantly confined to these settings. Genomic analysis revealed 10 specific families of blaCHDL genes in 51 isolates and blaNDM-1 in three isolates. The overall rates of phenotypic resistance to antimicrobials were low among Acinetobacter spp. isolates, with less than 10 % resistance observed for all tested drugs, and only three isolates carrying blaNDM-1 were resistant to carbapenems. The blaNDM-1 gene was located in approximately 49 kb PTU-Pse8 conjugative plasmids with conserved backbones, although plasmid pXH1688-NDM displayed enhanced growth and stability. Two novel Acinetobacter species, A. yuyunsongii sp. nov. and A. chenhuanii sp. nov., were characterized using phenotypic and genomic analyses. Particularly, A. yuyunsongii sp. nov. XH1639 harbors a blaOXA-58-carrying conjugative plasmid and exhibits multidrug-resistant phenotype. Our study advances Acinetobacter taxonomy and underscores the urgency of monitoring the dynamics of Acinetobacter species in environmental sources to implement effective measures to mitigate transmission risks to healthcare facilities.
format Article
id doaj-art-d88aa95153be46b29ea0ba634cd20965
institution DOAJ
issn 0160-4120
language English
publishDate 2025-04-01
publisher Elsevier
record_format Article
series Environment International
spelling doaj-art-d88aa95153be46b29ea0ba634cd209652025-08-20T03:14:54ZengElsevierEnvironment International0160-41202025-04-0119810937310.1016/j.envint.2025.109373Diverse Acinetobacter species and Plasmid-Driven spread of carbapenem resistance in pharmaceutical settings in ChinaJintao He0Liang Hong1Meijun Song2Yisha Zhang3Wang Zhang4Linghong Zhang5Danyan Zhou6Zhouwei Chen7Yunsong Yu8Huan Chen9Xiaoting Hua10Department of Infectious Diseases, Sir Run Run Shaw Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, People's Republic of China; Key Laboratory of Microbial Technology and Bioinformatics of Zhejiang Province, Hangzhou, Zhejiang, People's Republic of China; Regional Medical Center for National Institute of Respiratory Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, People's Republic of ChinaTaizhou Institute for Food and Drug Control, Taizhou, Zhejiang, People's Republic of ChinaDepartment of Infectious Diseases, Sir Run Run Shaw Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, People's Republic of China; Key Laboratory of Microbial Technology and Bioinformatics of Zhejiang Province, Hangzhou, Zhejiang, People's Republic of China; Regional Medical Center for National Institute of Respiratory Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, People's Republic of ChinaDepartment of Infectious Diseases, Sir Run Run Shaw Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, People's Republic of China; Key Laboratory of Microbial Technology and Bioinformatics of Zhejiang Province, Hangzhou, Zhejiang, People's Republic of China; Regional Medical Center for National Institute of Respiratory Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, People's Republic of ChinaDepartment of Infectious Diseases, Sir Run Run Shaw Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, People's Republic of China; Key Laboratory of Microbial Technology and Bioinformatics of Zhejiang Province, Hangzhou, Zhejiang, People's Republic of China; Regional Medical Center for National Institute of Respiratory Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, People's Republic of ChinaDepartment of Infectious Diseases, Sir Run Run Shaw Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, People's Republic of China; Key Laboratory of Microbial Technology and Bioinformatics of Zhejiang Province, Hangzhou, Zhejiang, People's Republic of China; Regional Medical Center for National Institute of Respiratory Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, People's Republic of ChinaDepartment of Infectious Diseases, Sir Run Run Shaw Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, People's Republic of China; Key Laboratory of Microbial Technology and Bioinformatics of Zhejiang Province, Hangzhou, Zhejiang, People's Republic of China; Regional Medical Center for National Institute of Respiratory Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, People's Republic of ChinaHangzhou Digital-Micro Biotech Co., Ltd., Hangzhou, Zhejiang, People's Republic of ChinaDepartment of Infectious Diseases, Sir Run Run Shaw Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, People's Republic of China; Key Laboratory of Microbial Technology and Bioinformatics of Zhejiang Province, Hangzhou, Zhejiang, People's Republic of China; Regional Medical Center for National Institute of Respiratory Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, People's Republic of China; Corresponding authors.Department of Infectious Diseases, Sir Run Run Shaw Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, People's Republic of China; Hangzhou Digital-Micro Biotech Co., Ltd., Hangzhou, Zhejiang, People's Republic of China; Zhejiang Chinese Medical University, College of Life Science, Hangzhou, Zhejiang, People's Republic of China; Corresponding authors at: Hangzhou Digital-Micro Biotech Co., Ltd., Hangzhou, Zhejiang, People's Republic of China.Department of Infectious Diseases, Sir Run Run Shaw Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, People's Republic of China; Key Laboratory of Microbial Technology and Bioinformatics of Zhejiang Province, Hangzhou, Zhejiang, People's Republic of China; Regional Medical Center for National Institute of Respiratory Diseases, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, People's Republic of China; Corresponding authors.Acinetobacter species have emerged as a significant public health concern due to their remarkable capacity to acquire antimicrobial resistance. Environmental reservoirs play a crucial role in spreading antimicrobial resistance genes and potentially pathogenic bacteria to clinical settings. However, most studies on nonhuman isolates have focused on a limited sample size. Comprehensive population sampling on One Health principles is essential to monitor the antibiotic resistome and virulome in Acinetobacter spp. Here, we identified three carbapenems-resistant Acinetobacter spp. isolates harboring blaNDM-1 and discovered two novel Acinetobacter species in pharmaceutical production environments. A total of 94 Acinetobacter spp. strains were isolated from pharmaceutical production environments across 17 cities in China, forming 17 distinct Acinetobacter clusters comprising two novel species and 15 previously known species. Phylogenetic analysis indicated that Acinetobacter spp. isolated from pharmaceutical settings are predominantly confined to these settings. Genomic analysis revealed 10 specific families of blaCHDL genes in 51 isolates and blaNDM-1 in three isolates. The overall rates of phenotypic resistance to antimicrobials were low among Acinetobacter spp. isolates, with less than 10 % resistance observed for all tested drugs, and only three isolates carrying blaNDM-1 were resistant to carbapenems. The blaNDM-1 gene was located in approximately 49 kb PTU-Pse8 conjugative plasmids with conserved backbones, although plasmid pXH1688-NDM displayed enhanced growth and stability. Two novel Acinetobacter species, A. yuyunsongii sp. nov. and A. chenhuanii sp. nov., were characterized using phenotypic and genomic analyses. Particularly, A. yuyunsongii sp. nov. XH1639 harbors a blaOXA-58-carrying conjugative plasmid and exhibits multidrug-resistant phenotype. Our study advances Acinetobacter taxonomy and underscores the urgency of monitoring the dynamics of Acinetobacter species in environmental sources to implement effective measures to mitigate transmission risks to healthcare facilities.http://www.sciencedirect.com/science/article/pii/S0160412025001242Acinetobacter speciesPharmaceutical production environmentNovel speciesNDM-1CHDL
spellingShingle Jintao He
Liang Hong
Meijun Song
Yisha Zhang
Wang Zhang
Linghong Zhang
Danyan Zhou
Zhouwei Chen
Yunsong Yu
Huan Chen
Xiaoting Hua
Diverse Acinetobacter species and Plasmid-Driven spread of carbapenem resistance in pharmaceutical settings in China
Environment International
Acinetobacter species
Pharmaceutical production environment
Novel species
NDM-1
CHDL
title Diverse Acinetobacter species and Plasmid-Driven spread of carbapenem resistance in pharmaceutical settings in China
title_full Diverse Acinetobacter species and Plasmid-Driven spread of carbapenem resistance in pharmaceutical settings in China
title_fullStr Diverse Acinetobacter species and Plasmid-Driven spread of carbapenem resistance in pharmaceutical settings in China
title_full_unstemmed Diverse Acinetobacter species and Plasmid-Driven spread of carbapenem resistance in pharmaceutical settings in China
title_short Diverse Acinetobacter species and Plasmid-Driven spread of carbapenem resistance in pharmaceutical settings in China
title_sort diverse acinetobacter species and plasmid driven spread of carbapenem resistance in pharmaceutical settings in china
topic Acinetobacter species
Pharmaceutical production environment
Novel species
NDM-1
CHDL
url http://www.sciencedirect.com/science/article/pii/S0160412025001242
work_keys_str_mv AT jintaohe diverseacinetobacterspeciesandplasmiddrivenspreadofcarbapenemresistanceinpharmaceuticalsettingsinchina
AT lianghong diverseacinetobacterspeciesandplasmiddrivenspreadofcarbapenemresistanceinpharmaceuticalsettingsinchina
AT meijunsong diverseacinetobacterspeciesandplasmiddrivenspreadofcarbapenemresistanceinpharmaceuticalsettingsinchina
AT yishazhang diverseacinetobacterspeciesandplasmiddrivenspreadofcarbapenemresistanceinpharmaceuticalsettingsinchina
AT wangzhang diverseacinetobacterspeciesandplasmiddrivenspreadofcarbapenemresistanceinpharmaceuticalsettingsinchina
AT linghongzhang diverseacinetobacterspeciesandplasmiddrivenspreadofcarbapenemresistanceinpharmaceuticalsettingsinchina
AT danyanzhou diverseacinetobacterspeciesandplasmiddrivenspreadofcarbapenemresistanceinpharmaceuticalsettingsinchina
AT zhouweichen diverseacinetobacterspeciesandplasmiddrivenspreadofcarbapenemresistanceinpharmaceuticalsettingsinchina
AT yunsongyu diverseacinetobacterspeciesandplasmiddrivenspreadofcarbapenemresistanceinpharmaceuticalsettingsinchina
AT huanchen diverseacinetobacterspeciesandplasmiddrivenspreadofcarbapenemresistanceinpharmaceuticalsettingsinchina
AT xiaotinghua diverseacinetobacterspeciesandplasmiddrivenspreadofcarbapenemresistanceinpharmaceuticalsettingsinchina