Genomic Characterization of Extended-Spectrum β-Lactamase (ESBL) Producing E. coli Harboring blaOXA−1-catB3-arr-3 Genes Isolated From Dairy Farm Environment in China

IF 3.5 2区 农林科学 Q2 INFECTIOUS DISEASES
Muhammad Shoaib, Minjia Tang, Furqan Awan, Amjad Islam Aqib, Ruochen Hao, Saad Ahmad, Shengyi Wang, Ruofeng Shang, Wanxia Pu
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Abstract

Anthropogenic activities in the environment affect the ecosystem and can play an important role in selecting and spreading antibiotic-resistant bacteria (ARB) and genes (ARGs). The dairy farm environment may serve as a hotspot and reservoir for exchanging and spreading ARGs, but studies are scarce. Here, we investigated and characterized the extended-spectrum β-lactamase producing Escherichia coli strains recovered from the dairy farm environment co-harboring blaOXA−1, catB3, and arr-3 genes. The isolates were identified and characterized by PCR, antimicrobial susceptibility testing, conjugation assay, whole genome sequencing (WGS), and multiple bioinformatics tools. Seven E. coli strains co-harboring blaOXA−1, catB3, and arr-3 genes were identified which belonged to distinct sequence types (STs) and carried diverse plasmid replicon types. The conjugation assay revealed a successful transfer of blaOXA−1, catB3, and arr-3 genes into the recipient E. coli J53 with a co-conjugation frequency ranging from (2.25 ± 0.3) × 10−4 to (3.85 ± 0.3) × 10−3. Bioinformatics analysis of WGS revealed the diversity of acquired ARGs, conferring resistance to aminoglycosides, beta-lactams, quinolones, tetracyclines, macrolides, trimethoprim–sulfamethoxazole, phosphonic, phenicol, and rifamycin. The genetic environment analysis showed that aac(6)-Ib-cr-blaOXA−1-catB3-arr-3-qacE1-sul1 was the common genetic backbone among the seven E. coli strains. Among the mobile genetic elements, insertion sequences were the predominant elements as compared to transposons. The phylogenetic analysis demonstrated a close relationship between the E. coli of this study and other strains of human–animal-environment origin retrieved from the NCBI database. This study presented the whole genome-based characterization of E. coli strains carrying the blaOXA−1-catB3-arr-3 genes. It provided evidence that the dairy environment may harbor a variety of ARGs and act as a potential reservoir for their spread in the ecosystem. The results recommend the routine surveillance of ARGs carrying bacteria in dairy environments and the need for additional studies to understand the dissemination mechanism within One Health perspective to prevent their further spread.

Abstract Image

中国奶牛场环境中分离出的携带 blaOXA-1-catB3-arr-3 基因的产广谱 β-内酰胺酶 (ESBL) 大肠杆菌的基因组学特征
环境中的人为活动会影响生态系统,并在选择和传播耐抗生素细菌(ARB)和基因(ARGs)方面发挥重要作用。奶牛场环境可能是交换和传播 ARGs 的热点和蓄水池,但这方面的研究却很少。在此,我们调查并鉴定了从奶牛场环境中回收的产生广谱β-内酰胺酶的大肠埃希菌菌株,这些菌株同时携带 blaOXA-1、catB3 和 arr-3 基因。通过聚合酶链式反应(PCR)、抗菌药物敏感性试验、连接试验、全基因组测序(WGS)和多种生物信息学工具对分离菌株进行了鉴定和特征描述。鉴定出了七株共同携带 blaOXA-1、catB3 和 arr-3 基因的大肠杆菌,它们属于不同的序列类型(ST),携带不同的质粒复制子类型。共轭试验显示,blaOXA-1、catB3 和 arr-3 基因成功转移到了受体大肠杆菌 J53 中,共轭频率从 (2.25 ± 0.3) × 10-4 到 (3.85 ± 0.3) × 10-3。对 WGS 的生物信息学分析表明,获得性 ARGs 具有多样性,可产生对氨基糖苷类、β-内酰胺类、喹诺酮类、四环素类、大环内酯类、三甲双胍-磺胺甲噁唑、膦酸、苯酚和利福霉素的耐药性。遗传环境分析表明,aac(6′)-Ib-cr-blaOXA-1-catB3-arr-3-qacE1-sul1 是 7 株大肠杆菌共同的遗传骨架。与转座子相比,插入序列是流动遗传因子中最主要的遗传因子。系统进化分析表明,本研究中的大肠杆菌与从 NCBI 数据库中检索到的其他来源于人类-动物-环境的菌株之间存在密切关系。本研究对携带 blaOXA-1-catB3-arr-3 基因的大肠杆菌菌株进行了全基因组鉴定。它提供了证据表明,乳制品环境可能蕴藏着多种 ARGs,并成为其在生态系统中传播的潜在贮藏库。研究结果建议对乳制品环境中携带 ARGs 的细菌进行常规监测,并需要开展更多研究,从 "一个健康 "的角度了解其传播机制,以防止其进一步扩散。
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来源期刊
Transboundary and Emerging Diseases
Transboundary and Emerging Diseases 农林科学-传染病学
CiteScore
8.90
自引率
9.30%
发文量
350
审稿时长
1 months
期刊介绍: Transboundary and Emerging Diseases brings together in one place the latest research on infectious diseases considered to hold the greatest economic threat to animals and humans worldwide. The journal provides a venue for global research on their diagnosis, prevention and management, and for papers on public health, pathogenesis, epidemiology, statistical modeling, diagnostics, biosecurity issues, genomics, vaccine development and rapid communication of new outbreaks. Papers should include timely research approaches using state-of-the-art technologies. The editors encourage papers adopting a science-based approach on socio-economic and environmental factors influencing the management of the bio-security threat posed by these diseases, including risk analysis and disease spread modeling. Preference will be given to communications focusing on novel science-based approaches to controlling transboundary and emerging diseases. The following topics are generally considered out-of-scope, but decisions are made on a case-by-case basis (for example, studies on cryptic wildlife populations, and those on potential species extinctions): Pathogen discovery: a common pathogen newly recognised in a specific country, or a new pathogen or genetic sequence for which there is little context about — or insights regarding — its emergence or spread. Prevalence estimation surveys and risk factor studies based on survey (rather than longitudinal) methodology, except when such studies are unique. Surveys of knowledge, attitudes and practices are within scope. Diagnostic test development if not accompanied by robust sensitivity and specificity estimation from field studies. Studies focused only on laboratory methods in which relevance to disease emergence and spread is not obvious or can not be inferred (“pure research” type studies). Narrative literature reviews which do not generate new knowledge. Systematic and scoping reviews, and meta-analyses are within scope.
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