Genomic Characteristics and Pathogenicity of Novel Reassortant Mammalian Orthoreoviruses From Sheep, China

IF 3.5 2区农林科学 Q2 INFECTIOUS DISEASES

Transboundary and Emerging Diseases Pub Date : 2025-05-15 DOI:10.1155/tbed/6025244

Xia Li, Xuhang Cai, Yi He, Wenliang Li, Junjun Zhai, Runbo Luo, Sizhu Suolang, Li Mao, Bin Li

{"title":"Genomic Characteristics and Pathogenicity of Novel Reassortant Mammalian Orthoreoviruses From Sheep, China","authors":"Xia Li, Xuhang Cai, Yi He, Wenliang Li, Junjun Zhai, Runbo Luo, Sizhu Suolang, Li Mao, Bin Li","doi":"10.1155/tbed/6025244","DOIUrl":null,"url":null,"abstract":"<div>\n <p>Mammalian orthoreoviruses (MRVs) have a wide geographic distribution worldwide and have been detected from humans and a variety of animal species. This study represents the first isolation of MRV from sheep rectal swabs in China, with analyses of its molecular and pathogenicity characteristics. MRV-positive samples were inoculated into Madin–Darby bovine kidney (MDBK) cells, resulting in stable cytopathic effects (CPEs) after three generations of blind passage. Two isolates were isolated and confirmed as MRV, named MRV-XJ23 and MRV-sheep/SY13, through reverse-transcription polymerase chain reaction (RT-PCR), transmission electron microscopy, and indirect immunofluorescence assay (IFA). The viruses exhibited broad cellular tropism. Whole-genome sequences were obtained and subjected to homology and evolutionary analyses, revealing that MRV-XJ23 and MRV-sheep/SY13 belong to the MRV-1 serotype. Phylogenetic analyses demonstrated that MRV-XJ23 is a reassortant virus containing gene segments from three MRVs that infected humans, bovines, and bats, with nucleotide homology exceeding 94.56%. The gene segments of MRV-sheep/SY13 were derived from five strains—Osaka2005, BatMRV-2/SNU1/Korea/2021, T1/human/Netherlands/1/84, IND/MZ/3013814/reo, and B/03—with nucleotide homology exceeding 95.47%. Animal experiments demonstrated that MRV-sheep/SY13 infection induced significant pathological changes in the respiratory and digestive tracts of mice. In sheep, MRV-sheep/SY13 caused respiratory infections, but no obvious lesion was observed from the digestive tract. This study expands our understanding of the MRV host range, reveals the potential public health risk of MRV transmission across species and zoonotic transmission, and underscores the necessity of further studies on epidemiology, reassortment patterns, and pathogenicity of MRV in sheep and domestic animals.</p>\n </div>","PeriodicalId":234,"journal":{"name":"Transboundary and Emerging Diseases","volume":"2025 1","pages":""},"PeriodicalIF":3.5000,"publicationDate":"2025-05-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1155/tbed/6025244","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Transboundary and Emerging Diseases","FirstCategoryId":"97","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1155/tbed/6025244","RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"INFECTIOUS DISEASES","Score":null,"Total":0}

引用次数: 0

Abstract

Mammalian orthoreoviruses (MRVs) have a wide geographic distribution worldwide and have been detected from humans and a variety of animal species. This study represents the first isolation of MRV from sheep rectal swabs in China, with analyses of its molecular and pathogenicity characteristics. MRV-positive samples were inoculated into Madin–Darby bovine kidney (MDBK) cells, resulting in stable cytopathic effects (CPEs) after three generations of blind passage. Two isolates were isolated and confirmed as MRV, named MRV-XJ23 and MRV-sheep/SY13, through reverse-transcription polymerase chain reaction (RT-PCR), transmission electron microscopy, and indirect immunofluorescence assay (IFA). The viruses exhibited broad cellular tropism. Whole-genome sequences were obtained and subjected to homology and evolutionary analyses, revealing that MRV-XJ23 and MRV-sheep/SY13 belong to the MRV-1 serotype. Phylogenetic analyses demonstrated that MRV-XJ23 is a reassortant virus containing gene segments from three MRVs that infected humans, bovines, and bats, with nucleotide homology exceeding 94.56%. The gene segments of MRV-sheep/SY13 were derived from five strains—Osaka2005, BatMRV-2/SNU1/Korea/2021, T1/human/Netherlands/1/84, IND/MZ/3013814/reo, and B/03—with nucleotide homology exceeding 95.47%. Animal experiments demonstrated that MRV-sheep/SY13 infection induced significant pathological changes in the respiratory and digestive tracts of mice. In sheep, MRV-sheep/SY13 caused respiratory infections, but no obvious lesion was observed from the digestive tract. This study expands our understanding of the MRV host range, reveals the potential public health risk of MRV transmission across species and zoonotic transmission, and underscores the necessity of further studies on epidemiology, reassortment patterns, and pathogenicity of MRV in sheep and domestic animals.

查看原文本刊更多论文

绵羊原肠病毒的基因组特征和致病性

哺乳动物正肠病毒（mrv）在世界范围内具有广泛的地理分布，并已从人类和多种动物物种中检测到。本研究是国内首次从绵羊直肠拭子中分离到MRV，并对其分子和致病性特征进行了分析。mrv阳性样品接种于Madin-Darby牛肾（MDBK）细胞，盲传3代后产生稳定的细胞病变效应（cpe）。经反转录聚合酶链反应（RT-PCR）、透射电镜和间接免疫荧光（IFA）检测，分离得到两株MRV，分别命名为MRV- xj23和MRV-sheep/SY13。病毒表现出广泛的细胞趋向性。获得全基因组序列并进行同源性和进化分析，发现MRV-XJ23和MRV-sheep/SY13属于MRV-1血清型。系统发育分析表明，MRV-XJ23是一种重组病毒，含有感染人类、牛和蝙蝠的三种mrv的基因片段，核苷酸同源性超过94.56%。MRV-sheep/SY13基因片段来源于osaka2005、BatMRV-2/SNU1/Korea/2021、T1/human/Netherlands/1/84、IND/MZ/3013814/reo和B/03，核苷酸同源性均超过95.47%。动物实验表明，MRV-sheep/SY13感染可引起小鼠呼吸道和消化道明显的病理改变。在绵羊中，MRV-sheep/SY13引起呼吸道感染，但消化道未见明显病变。本研究扩大了我们对MRV宿主范围的认识，揭示了MRV跨物种传播和人畜共患传播的潜在公共卫生风险，并强调了进一步研究MRV在绵羊和家畜中的流行病学、重组模式和致病性的必要性。

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分钟内获得全文求助全文

来源期刊

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.