{"title":"Decoding the enigma: unveiling the transmission characteristics of waterfowl-associated <i>bla</i> <sub>NDM-5</sub>-positive <i>Escherichia coli</i> in select regions of China.","authors":"Shaqiu Zhang, Yanxi Shu, Zhechen Yang, Zhijun Zhong, Mingshu Wang, Renyong Jia, Shun Chen, Mafeng Liu, Dekang Zhu, Xinxin Zhao, Ying Wu, Qiao Yang, Juan Huang, Xumin Ou, Di Sun, Bin Tian, Zhen Wu, Yu He, Anchun Cheng","doi":"10.3389/fmicb.2024.1501594","DOIUrl":null,"url":null,"abstract":"<p><p><i>Escherichia coli</i> (<i>E. coli</i>) serves as a critical indicator microorganism for assessing the prevalence and dissemination of antibiotic resistance, notably harboring various antibiotic-resistant genes (ARGs). Among these, the emergence of the <i>bla</i> <sub>NDM</sub> gene represents a significant threat to public health, especially since carbapenem antibiotics are vital for treating severe infections caused by Gram-negative bacteria. This study aimed to characterize the antibiotic resistance features of <i>bla</i> <sub>NDM-5</sub>-positive <i>E. coli</i> strains isolated from waterfowl in several regions of China and elucidate the dissemination patterns of the <i>bla</i> <sub>NDM-5</sub> gene. We successfully isolated 103 <i>bla</i> <sub>NDM-5</sub>-positive <i>E. coli</i> strains from 431 intestinal fecal samples obtained from waterfowl across five provincial-level units in China, with all strains exhibiting multidrug resistance (MDR). Notably, the <i>bla</i> <sub>NDM-5</sub> gene was identified on plasmids, which facilitate efficient and stable horizontal gene transfer (HGT). Our adaptability assays indicated that while the <i>bla</i> <sub>NDM-5</sub>-positive plasmid imposed a fitness cost on the host bacteria, the NDM-5 protein was successfully induced and purified, exhibiting significant enzymatic activity. One strain, designated DY51, exhibited a minimum inhibitory concentration (MIC) for imipenem of 4 mg/L, which escalated to 512 mg/L following exposure to increasing imipenem doses. This altered strain demonstrated stable resistance to imipenem alongside improved adaptability, correlating with elevated relative expression levels of the <i>bla</i> <sub>NDM-5</sub> and overexpression of efflux pumps. Collectively, this study highlights the horizontal dissemination of the <i>bla</i> <sub>NDM-5</sub> plasmid among <i>E. coli</i> strains, confirms the associated fitness costs, and provides insights into the mechanisms underlying the stable increase in antibiotic resistance to imipenem. These findings offer a theoretical framework for understanding the dissemination dynamics of <i>bla</i> <sub>NDM-5</sub> in <i>E. coli</i>, which is essential for developing effective strategies to combat carbapenem antibiotic resistance.</p>","PeriodicalId":12466,"journal":{"name":"Frontiers in Microbiology","volume":"15 ","pages":"1501594"},"PeriodicalIF":4.0000,"publicationDate":"2024-12-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11663885/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Frontiers in Microbiology","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.3389/fmicb.2024.1501594","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/1/1 0:00:00","PubModel":"eCollection","JCR":"Q2","JCRName":"MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Escherichia coli (E. coli) serves as a critical indicator microorganism for assessing the prevalence and dissemination of antibiotic resistance, notably harboring various antibiotic-resistant genes (ARGs). Among these, the emergence of the blaNDM gene represents a significant threat to public health, especially since carbapenem antibiotics are vital for treating severe infections caused by Gram-negative bacteria. This study aimed to characterize the antibiotic resistance features of blaNDM-5-positive E. coli strains isolated from waterfowl in several regions of China and elucidate the dissemination patterns of the blaNDM-5 gene. We successfully isolated 103 blaNDM-5-positive E. coli strains from 431 intestinal fecal samples obtained from waterfowl across five provincial-level units in China, with all strains exhibiting multidrug resistance (MDR). Notably, the blaNDM-5 gene was identified on plasmids, which facilitate efficient and stable horizontal gene transfer (HGT). Our adaptability assays indicated that while the blaNDM-5-positive plasmid imposed a fitness cost on the host bacteria, the NDM-5 protein was successfully induced and purified, exhibiting significant enzymatic activity. One strain, designated DY51, exhibited a minimum inhibitory concentration (MIC) for imipenem of 4 mg/L, which escalated to 512 mg/L following exposure to increasing imipenem doses. This altered strain demonstrated stable resistance to imipenem alongside improved adaptability, correlating with elevated relative expression levels of the blaNDM-5 and overexpression of efflux pumps. Collectively, this study highlights the horizontal dissemination of the blaNDM-5 plasmid among E. coli strains, confirms the associated fitness costs, and provides insights into the mechanisms underlying the stable increase in antibiotic resistance to imipenem. These findings offer a theoretical framework for understanding the dissemination dynamics of blaNDM-5 in E. coli, which is essential for developing effective strategies to combat carbapenem antibiotic resistance.
期刊介绍:
Frontiers in Microbiology is a leading journal in its field, publishing rigorously peer-reviewed research across the entire spectrum of microbiology. Field Chief Editor Martin G. Klotz at Washington State University is supported by an outstanding Editorial Board of international researchers. This multidisciplinary open-access journal is at the forefront of disseminating and communicating scientific knowledge and impactful discoveries to researchers, academics, clinicians and the public worldwide.