Aworh Mabel Kamweli, Lawal Opeyemi U, Egyir Beverly, Hendriksen Rene S
Department of Biological and Forensic Sciences, Fayetteville State University, Fayetteville, NC, USA.
ECU Brody School of Medicine, Department of Public Health, East Carolina University, Greenville, NC, USA.
BMC Microbiol. 2025 Apr 8;25(1):200. doi: 10.1186/s12866-025-03913-9.
The emergence of antimicrobial resistance (AMR) in Escherichia coli, particularly extended-spectrum beta-lactamase-producing E. coli (ESBL-EC), is a global public health concern. Bacteriophages (phages) play a significant role in bacterial evolution and the spread of antibiotic resistance genes (ARGs). This study investigates prophages integrated within ESBL-EC genomes to assess their diversity, gene content, and potential contributions to ESBL-EC persistence across human, animal, and environmental reservoirs. Between May and December 2020, a cross-sectional study was conducted in Abuja and Lagos, collecting 448 stool, cecal, and environmental samples from abattoir workers, slaughtered cattle, and the abattoir environment. ESBL-EC genomes from these samples, obtained in an earlier study, were analyzed for phage regions using PHASTER. Intact prophages were analyzed in silico using computational tools to detect ARGs, ESBL genes, virulence factors, and heavy metal resistance. Their genomic relationships were examined with statistical significance of p < 0.05.
Out of 448 samples, ESBL-EC prevalence was 21.7% (97/448). Among 97 ESBL-EC isolates, 646 prophage regions were detected, with 30% (194/646) classified as intact phages. Among the 158 phages with genus assignments, Punavirus was the most prevalent (60.1%). Escherichia was the most frequent predicted host (308/646), particularly in cattle (n = 143) and human (n = 124) sources. Among ESBL-EC genomes, 83.5% (81/97) with intact phages carried phage-associated ARGs, 76.3% (74/97) carried phage-associated ESBL genes, 18.6% (18/97) harbored phage-associated virulence factors, 15.5% (15/97) contained phage-associated plasmids, and 10.3% (10/97) had heavy metal resistance. The most prevalent phage-associated ARGs detected were qnrS1 (73/81) and bla (72/81). Two isolates recovered from abattoir workers carried two phage-like plasmids, each harboring either tet(A) or bla gene. The predominant phage lifestyles were temperate (n = 182), mainly in the Peduoviridae family, and lytic (n = 12) in the Punavirus genus.
This is the first study in Nigeria to characterize phages in ESBL-EC isolates at the One Health interface. The presence of intact phages in humans, animals, and the environment underscores the complex interactions shaping phage ecology. The discovery of ARGs, virulence genes, and heavy metal resistance within prophages suggests a potential role in AMR dissemination. Future research should focus on elucidating mechanisms of ARG transfer mediated by phages in One Health settings.
大肠杆菌中抗菌药物耐药性（AMR）的出现，尤其是产超广谱β-内酰胺酶的大肠杆菌（ESBL-EC），是一个全球公共卫生问题。噬菌体在细菌进化和抗生素耐药基因（ARG）传播中发挥着重要作用。本研究调查整合在ESBL-EC基因组中的前噬菌体，以评估它们的多样性、基因内容以及对ESBL-EC在人类、动物和环境宿主中持续存在的潜在贡献。2020年5月至12月，在阿布贾和拉各斯进行了一项横断面研究，从屠宰场工人、屠宰牛和屠宰场环境中收集了448份粪便、盲肠和环境样本。使用PHASTER对在早期研究中从这些样本获得的ESBL-EC基因组的噬菌体区域进行分析。使用计算工具对完整的前噬菌体进行计算机分析，以检测ARG、ESBL基因、毒力因子和重金属抗性。检验它们的基因组关系，p值<0.05具有统计学意义。
在448份样本中，ESBL-EC的流行率为21.7%（97/448）。在97株ESBL-EC分离株中，检测到646个前噬菌体区域，其中30%（194/646）被归类为完整噬菌体。在158个有属分类的噬菌体中，Punavirus最为常见（60.1%）。埃希氏菌属是最常见的预测宿主（308/646），特别是在牛（n = 143）和人类（n = 124）来源中。在ESBL-EC基因组中，83.5%（81/97）有完整噬菌体的携带噬菌体相关的ARG，76.3%（74/97）携带噬菌体相关的ESBL基因，18.6%（18/97）含有噬菌体相关的毒力因子，15.5%（15/97）含有噬菌体相关的质粒，10.3%（10/97）具有重金属抗性。检测到的最常见的噬菌体相关ARG是qnrS1（73/81）和bla（72/81）。从屠宰场工人中分离出的两株菌株携带两个噬菌体样质粒，每个质粒携带tet(A)或bla基因。主要的噬菌体生活方式是温和型（n = 182），主要在短尾病毒科，溶菌型（n = 12）在Punavirus属。
这是尼日利亚首次在“同一健康”界面表征ESBL-EC分离株中的噬菌体。人类、动物和环境中完整噬菌体的存在突出了塑造噬菌体生态的复杂相互作用。在前噬菌体中发现ARG、毒力基因和重金属抗性表明其在AMR传播中的潜在作用。未来的研究应侧重于阐明“同一健康”环境中噬菌体介导的ARG转移机制。
