Antimicrobial resistance, virulence potential and genomic epidemiology of global genomes of the rare Salmonella enterica serovar Orion

IF 2.4 2区农林科学 Q3 INFECTIOUS DISEASES Zoonoses and Public Health Pub Date : 2024-05-03 DOI:10.1111/zph.13140

Leticia Ayumi Hasegawa, Felipe Pinheiro Vilela, Juliana Pfrimer Falcão

{"title":"Antimicrobial resistance, virulence potential and genomic epidemiology of global genomes of the rare Salmonella enterica serovar Orion","authors":"Leticia Ayumi Hasegawa, Felipe Pinheiro Vilela, Juliana Pfrimer Falcão","doi":"10.1111/zph.13140","DOIUrl":null,"url":null,"abstract":"<div>\n \n \n <section>\n \n <h3> Aims</h3>\n \n <p>Our aim is to characterize through whole-genome sequencing (WGS) the antimicrobial resistance (AMR) and heavy metal tolerance (HMT) genes content, plasmid presence, virulence potential and genomic diversity of the rare non-typhoid <i>Salmonella enterica</i> serovar Orion (<i>S</i>. <i>Orion</i>) from 19 countries of the African, American, Eastern Mediterranean, European, Southeastern Asia and Western Pacific regions.</p>\n </section>\n \n <section>\n \n <h3> Methods and Results</h3>\n \n <p>Totally 324 <i>S</i>. <i>Orion</i> genomes were screened for AMR, HMT and virulence genes, plasmids and <i>Salmonella</i> Pathogenicity Islands (SPIs). Genomic diversity was investigated using Multi-Locus Sequence Typing (MLST) and core-genome MLST (cgMLST). Efflux pump encoding genes <i>mdsA</i> and <i>mdsB</i> were present in all genomes analysed, while quinolone chromosomal point mutations and aminoglycoside, beta-lactam, colistin, lincosamide, macrolide, phenicol, sulphonamide, trimethoprim, tetracycline and disinfectant resistance genes were found in 0.3%–5.9%. A total of 17 genomes (5.2%) from Canada, the United Kingdom, the USA and Tanzania showed a potential multi-drug resistance profile. Gold tolerance genes <i>golS</i> and <i>golT</i> were detected in all genomes analysed, while arsenic, copper, mercury, silver and tellurium tolerance genes were found in 0.3%–35.5%. Col(MGD2) was the most frequently detected plasmid, in 15.4% of the genomes. Virulence genes related to adherence, macrophage induction, magnesium uptake, regulation, serum resistance, stress adaptation, type III secretion systems and six SPIs (1, 2, 3, 4, 5, 9, 12, 13, 14 and C63PI) were detected. ST639 was assigned to 89.2% of the <i>S</i>. <i>Orion</i> genomes, while cgMLST showed core-genome STs and clusters of strains specific by countries.</p>\n </section>\n \n <section>\n \n <h3> Conclusion</h3>\n \n <p>The high virulence factor frequencies, the genomic similarity among some non-clinical and clinical strains circulating worldwide and the presence of a strain carrying a resistance gene against a last resource antimicrobial like colistin, highlight the potential risk of <i>S</i>. <i>Orion</i> strains for public health and food safety and reinforce the importance to not underestimate the potential hazard of rare non-typhoid <i>Salmonella</i> serovars.</p>\n </section>\n </div>","PeriodicalId":24025,"journal":{"name":"Zoonoses and Public Health","volume":"71 5","pages":"591-599"},"PeriodicalIF":2.4000,"publicationDate":"2024-05-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Zoonoses and Public Health","FirstCategoryId":"97","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1111/zph.13140","RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q3","JCRName":"INFECTIOUS DISEASES","Score":null,"Total":0}

引用次数: 0

Abstract

Aims

Our aim is to characterize through whole-genome sequencing (WGS) the antimicrobial resistance (AMR) and heavy metal tolerance (HMT) genes content, plasmid presence, virulence potential and genomic diversity of the rare non-typhoid Salmonella enterica serovar Orion (S. Orion) from 19 countries of the African, American, Eastern Mediterranean, European, Southeastern Asia and Western Pacific regions.

Methods and Results

Totally 324 S. Orion genomes were screened for AMR, HMT and virulence genes, plasmids and Salmonella Pathogenicity Islands (SPIs). Genomic diversity was investigated using Multi-Locus Sequence Typing (MLST) and core-genome MLST (cgMLST). Efflux pump encoding genes mdsA and mdsB were present in all genomes analysed, while quinolone chromosomal point mutations and aminoglycoside, beta-lactam, colistin, lincosamide, macrolide, phenicol, sulphonamide, trimethoprim, tetracycline and disinfectant resistance genes were found in 0.3%–5.9%. A total of 17 genomes (5.2%) from Canada, the United Kingdom, the USA and Tanzania showed a potential multi-drug resistance profile. Gold tolerance genes golS and golT were detected in all genomes analysed, while arsenic, copper, mercury, silver and tellurium tolerance genes were found in 0.3%–35.5%. Col(MGD2) was the most frequently detected plasmid, in 15.4% of the genomes. Virulence genes related to adherence, macrophage induction, magnesium uptake, regulation, serum resistance, stress adaptation, type III secretion systems and six SPIs (1, 2, 3, 4, 5, 9, 12, 13, 14 and C63PI) were detected. ST639 was assigned to 89.2% of the S. Orion genomes, while cgMLST showed core-genome STs and clusters of strains specific by countries.

Conclusion

The high virulence factor frequencies, the genomic similarity among some non-clinical and clinical strains circulating worldwide and the presence of a strain carrying a resistance gene against a last resource antimicrobial like colistin, highlight the potential risk of S. Orion strains for public health and food safety and reinforce the importance to not underestimate the potential hazard of rare non-typhoid Salmonella serovars.

查看原文

微信好友朋友圈 QQ好友复制链接

本刊更多论文

全球罕见肠炎沙门氏菌血清 Orion 菌基因组的抗菌性、毒力潜力和基因组流行病学

目的我们的目的是通过全基因组测序（WGS）鉴定非洲、美洲、地中海东部、欧洲、亚洲东南部和西太平洋地区 19 个国家的罕见非伤寒沙门氏菌肠炎血清 Orion（S.方法与结果共筛选了 324 个 S. Orion 基因组，以检测 AMR、HMT 和毒力基因、质粒和沙门氏菌致病岛 (SPI)。利用多焦点序列分型（MLST）和核心基因组多焦点序列分型（cgMLST）研究了基因组多样性。在分析的所有基因组中都发现了外排泵编码基因 mdsA 和 mdsB，而在 0.3%-5.9%的基因组中发现了喹诺酮染色体点突变和氨基糖苷类、β-内酰胺类、可乐定、林可霉素、大环内酯类、苯酚、磺胺类、三甲氧苄啶、四环素和消毒剂耐药基因。加拿大、英国、美国和坦桑尼亚共有 17 个基因组（5.2%）显示出潜在的多重耐药性特征。在分析的所有基因组中都检测到了耐金基因 golS 和 golT，而在 0.3%-35.5%的基因组中发现了耐砷、铜、汞、银和碲基因。在 15.4% 的基因组中，Col(MGD2) 是最常检测到的质粒。检测到了与粘附性、巨噬细胞诱导、镁吸收、调节、血清抗性、应激适应、III型分泌系统和6个SPI（1、2、3、4、5、9、12、13、14和C63PI）有关的病毒性基因。ST639 被分配到 89.2% 的 S. Orion 基因组中，而 cgMLST 则显示了核心基因组 ST 和各国特有的菌株群。Orion 菌株对公共卫生和食品安全的潜在风险，并强化了不要低估罕见非伤寒沙门氏菌血清型潜在危害的重要性。

本文章由计算机程序翻译，如有差异，请以英文原文为准。

求助全文

约1分钟内获得全文去求助

来源期刊

Zoonoses and Public Health 医学-传染病学

CiteScore

5.30

自引率

4.20%

发文量

115

审稿时长

6-12 weeks

期刊介绍： Zoonoses and Public Health brings together veterinary and human health researchers and policy-makers by providing a venue for publishing integrated and global approaches to zoonoses and public health. The Editors will consider papers that focus on timely collaborative and multi-disciplinary research in zoonoses and public health. This journal provides rapid publication of original papers, reviews, and potential discussion papers embracing this collaborative spirit. Papers should advance the scientific knowledge of the sources, transmission, prevention and control of zoonoses and be authored by scientists with expertise in areas such as microbiology, virology, parasitology and epidemiology. Articles that incorporate recent data into new methods, applications, or approaches (e.g. statistical modeling) which enhance public health are strongly encouraged.