{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,11,30]],"date-time":"2025-11-30T05:31:18Z","timestamp":1764480678503,"version":"3.46.0"},"reference-count":43,"publisher":"MDPI AG","issue":"12","license":[{"start":{"date-parts":[[2025,11,28]],"date-time":"2025-11-28T00:00:00Z","timestamp":1764288000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Health Research Program of Ningxia","award":["2025-NWZC-B020"],"award-info":[{"award-number":["2025-NWZC-B020"]}]},{"name":"National Key Research and Development Program of China","award":["2024YFC2311502","2022YFC2302700"],"award-info":[{"award-number":["2024YFC2311502","2022YFC2302700"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>During the 2023 surveillance of mosquito-borne viruses in Ningxia Hui Autonomous Region, a strain of Umatilla virus (UMAV) was isolated from a pool of Culex pipiens pallens (NX23166) collected in Xiji County and cultured in C6\/36 cells. Electron microscopy revealed that NX23166-infected mosquito cells showed approximately 70-nm virus particles, typical of the genus Orbivirus. Through next-generation sequencing, 10 double-stranded RNA (dsRNA) segments of the virus were obtained. Phylogenetic and homology analyses based on these sequences revealed that this strain was most closely related to the first Chinese isolate from Yunnan in 2013 (DH13M98) and an Australian isolate from 2015 (M4941_15). However, the VP3 protein of this strain showed the closest evolutionary relationship to a German isolate from 2019 (ED-I-205-19), with an amino acid sequence identity of 94.00%. In contrast, the identity of the VP3 protein to that of other strains ranged only from 47.38% to 51.49%, suggesting that these two strains may belong to the same serotype. Nevertheless, this hypothesis needs to be further verified by a serum neutralization test. Furthermore, transcriptome sequencing analysis showed that infection with the Ningxia isolate of UMAV induced significant temporal transcriptomic reprogramming in C6\/36 cells. This reprogramming was characterized by early activation of innate immune responses such as the Toll signaling pathway and autophagy, followed by significant suppression of metabolic pathways, including oxidative phosphorylation in the mid to late stages of infection, demonstrating a molecular phenotype of coordinated immune activation and metabolic suppression. These results provide new insights into the genetic diversity and geographic distribution of the species UMAV.<\/jats:p>","DOI":"10.3390\/microorganisms13122717","type":"journal-article","created":{"date-parts":[[2025,11,28]],"date-time":"2025-11-28T11:19:51Z","timestamp":1764328791000},"page":"2717","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Genomic and Transcriptomic Characterization of Umatilla Virus Isolated and Identified from Mosquitoes in Ningxia, China"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0009-0001-8241-2118","authenticated-orcid":false,"given":"Kun","family":"Han","sequence":"first","affiliation":[{"name":"Ningxia Center for Disease Control and Prevention, Yinchuan 750011, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yuhong","family":"Yang","sequence":"additional","affiliation":[{"name":"National Key Laboratory of Intelligent Tracking and Forecasting for Infectious Diseases, NHC Key Laboratory of Biosafety, National Institute for Viral Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing 102206, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Long","family":"Wang","sequence":"additional","affiliation":[{"name":"Ningxia Center for Disease Control and Prevention, Yinchuan 750011, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Liqin","family":"Yu","sequence":"additional","affiliation":[{"name":"National Key Laboratory of Intelligent Tracking and Forecasting for Infectious Diseases, NHC Key Laboratory of Biosafety, National Institute for Viral Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing 102206, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0009-0007-3068-7578","authenticated-orcid":false,"given":"Ruichen","family":"Wang","sequence":"additional","affiliation":[{"name":"National Key Laboratory of Intelligent Tracking and Forecasting for Infectious Diseases, NHC Key Laboratory of Biosafety, National Institute for Viral Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing 102206, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xiaoyu","family":"Gu","sequence":"additional","affiliation":[{"name":"National Key Laboratory of Intelligent Tracking and Forecasting for Infectious Diseases, NHC Key Laboratory of Biosafety, National Institute for Viral Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing 102206, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Fan","family":"Li","sequence":"additional","affiliation":[{"name":"National Key Laboratory of Intelligent Tracking and Forecasting for Infectious Diseases, NHC Key Laboratory of Biosafety, National Institute for Viral Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing 102206, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8239-0214","authenticated-orcid":false,"given":"Qikai","family":"Yin","sequence":"additional","affiliation":[{"name":"National Key Laboratory of Intelligent Tracking and Forecasting for Infectious Diseases, NHC Key Laboratory of Biosafety, National Institute for Viral Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing 102206, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Shihong","family":"Fu","sequence":"additional","affiliation":[{"name":"National Key Laboratory of Intelligent Tracking and Forecasting for Infectious Diseases, NHC Key Laboratory of Biosafety, National Institute for Viral Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing 102206, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7963-8431","authenticated-orcid":false,"given":"Kai","family":"Nie","sequence":"additional","affiliation":[{"name":"National Key Laboratory of Intelligent Tracking and Forecasting for Infectious Diseases, NHC Key Laboratory of Biosafety, National Institute for Viral Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing 102206, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Qianqian","family":"Cui","sequence":"additional","affiliation":[{"name":"National Key Laboratory of Intelligent Tracking and Forecasting for Infectious Diseases, NHC Key Laboratory of Biosafety, National Institute for Viral Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing 102206, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Songtao","family":"Xu","sequence":"additional","affiliation":[{"name":"National Key Laboratory of Intelligent Tracking and Forecasting for Infectious Diseases, NHC Key Laboratory of Biosafety, National Institute for Viral Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing 102206, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6245-2027","authenticated-orcid":false,"given":"Huanyu","family":"Wang","sequence":"additional","affiliation":[{"name":"National Key Laboratory of Intelligent Tracking and Forecasting for Infectious Diseases, NHC Key Laboratory of Biosafety, National Institute for Viral Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing 102206, China"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2025,11,28]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"372","DOI":"10.4269\/ajtmh.1978.27.372","article-title":"Supplement to International Catalogue of Arboviruses including certain other viruses of vertebrates","volume":"27","author":"Karabatsos","year":"1978","journal-title":"Am. J. Trop. Med. Hyg."},{"doi-asserted-by":"crossref","unstructured":"Belaganahalli, M.N., Maan, S., Maan, N.S., Nomikou, K., Pritchard, I., Lunt, R., Kirkland, P.D., Attoui, H., Brownlie, J., and Mertens, P.P. (2012). Full genome sequencing and genetic characterization of Eubenangee viruses identify Pata virus as a distinct species within the genus Orbivirus. PLoS ONE, 7.","key":"ref_2","DOI":"10.1371\/journal.pone.0031911"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1089\/vbz.2022.0031","article-title":"Genetic Characterization of DH13M98, Umatilla Virus, Isolated from Culex tritaeniorhynchus Giles in Yunnan Province, China","volume":"23","author":"Yang","year":"2023","journal-title":"Vector Borne Zoonotic Dis."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"353","DOI":"10.20506\/rst.34.2.2362","article-title":"Zoonotic and emerging orbivirus infections","volume":"34","author":"Attoui","year":"2015","journal-title":"Rev. Sci. Tech."},{"doi-asserted-by":"crossref","unstructured":"Dennis, S.J., Meyers, A.E., Hitzeroth, I.I., and Rybicki, E.P. (2019). African Horse Sickness: A Review of Current Understanding and Vaccine Development. Viruses, 11.","key":"ref_5","DOI":"10.3390\/v11090844"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1016\/j.coviro.2018.12.005","article-title":"Bluetongue and epizootic hemorrhagic disease viruses: Recent developments with these globally re-emerging arboviral infections of ruminants","volume":"34","author":"Maclachlan","year":"2019","journal-title":"Curr. Opin. Virol."},{"doi-asserted-by":"crossref","unstructured":"Mohd Jaafar, F., Belhouchet, M., Belaganahalli, M., Tesh, R.B., Mertens, P.P., and Attoui, H. (2014). Full-genome characterisation of Orungo, Lebombo and Changuinola viruses provides evidence for co-evolution of orbiviruses with their arthropod vectors. PLoS ONE, 9.","key":"ref_7","DOI":"10.1371\/journal.pone.0086392"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"2185","DOI":"10.3390\/v7052185","article-title":"Genetic characterization of the tick-borne orbiviruses","volume":"7","author":"Belaganahalli","year":"2015","journal-title":"Viruses"},{"doi-asserted-by":"crossref","unstructured":"Barros, L., Silva, S., Cruz, A.C., da Silva, E., Wanzeller, A.L., Carvalho, V., Chiang, J., and Martins, L. (2024). First Isolation and Molecular Characterization of Umatilla Virus (Sedoreoviridae, Orbivirus) in Brazil. Viruses, 16.","key":"ref_9","DOI":"10.3390\/v16071050"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"2985","DOI":"10.1099\/vir.0.024760-0","article-title":"Complete sequence of Great Island virus and comparison with the T2 and outer-capsid proteins of Kemerovo, Lipovnik and Tribec viruses (genus Orbivirus, family Reoviridae)","volume":"91","author":"Belhouchet","year":"2010","journal-title":"J. Gen. Virol."},{"doi-asserted-by":"crossref","unstructured":"Belaganahalli, M.N., Maan, S., Maan, N.S., Tesh, R., Attoui, H., and Mertens, P.P. (2011). Umatilla virus genome sequencing and phylogenetic analysis: Identification of stretch lagoon orbivirus as a new member of the Umatilla virus species. PLoS ONE, 6.","key":"ref_11","DOI":"10.1371\/journal.pone.0023605"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"298","DOI":"10.1016\/j.virol.2009.08.032","article-title":"Peruvian horse sickness virus and Yunnan orbivirus, isolated from vertebrates and mosquitoes in Peru and Australia","volume":"394","author":"Attoui","year":"2009","journal-title":"Virology"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"3409","DOI":"10.1099\/vir.0.81258-0","article-title":"Yunnan orbivirus, a new orbivirus species isolated from Culex tritaeniorhynchus mosquitoes in China","volume":"86","author":"Attoui","year":"2005","journal-title":"J. Gen. Virol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1051\/vetres\/2010007","article-title":"Re-emergence of bluetongue, African horse sickness, and other orbivirus diseases","volume":"41","author":"Maclachlan","year":"2010","journal-title":"Vet. Res."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"2643","DOI":"10.3201\/eid3012.240498","article-title":"Umatilla Virus in Zoo-Dwelling Cape Penguins with Hepatitis, Germany","volume":"30","author":"Mirolo","year":"2024","journal-title":"Emerg. Infect. Dis."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1433","DOI":"10.1099\/vir.0.010074-0","article-title":"Genetic and epidemiological characterization of Stretch Lagoon orbivirus, a novel orbivirus isolated from Culex and Aedes mosquitoes in northern Australia","volume":"90","author":"Cowled","year":"2009","journal-title":"J. Gen. Virol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"2675","DOI":"10.1007\/s00705-014-2117-0","article-title":"First isolation and characterization of a mosquito-borne orbivirus belonging to the species Umatilla virus in East Asia","volume":"159","author":"Ejiri","year":"2014","journal-title":"Arch. Virol."},{"unstructured":"Lu, B.L., and Wu, H.Y. (2003). Classification and Identification of Important Medical Insects of China, Henan Science and Technology Publishing House.","key":"ref_18"},{"key":"ref_19","first-page":"507","article-title":"A Survey of Six Mosquito-Borne Viruses in the Ningxia Hui Autonomous Region in 2023","volume":"41","author":"Yu","year":"2025","journal-title":"Chin. J. Virol."},{"doi-asserted-by":"crossref","unstructured":"Hu, D., Wu, C., Wang, R., Yao, X., Nie, K., Lyu, Q., Fu, S., Yin, Q., Su, W., and Li, F. (2023). Persistence of Tembusu Virus in Culex tritaeniorhynchus in Yunnan Province, China. Pathogens, 12.","key":"ref_20","DOI":"10.3390\/pathogens12030490"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1186\/s12985-018-0966-y","article-title":"Identification and genetic analysis of Kadipiro virus isolated in Shandong province, China","volume":"15","author":"Zhang","year":"2018","journal-title":"Virol. J."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"100179","DOI":"10.1016\/j.imj.2025.100179","article-title":"Isolation and characterization of a novel coltivirus from Haemaphysalis concinna ticks in Northeastern China","volume":"4","author":"Yang","year":"2025","journal-title":"Infect. Med."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"e107","DOI":"10.1002\/imt2.107","article-title":"Ultrafast one-pass FASTQ data preprocessing, quality control, and deduplication using fastp","volume":"2","author":"Chen","year":"2023","journal-title":"Imeta"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1674","DOI":"10.1093\/bioinformatics\/btv033","article-title":"MEGAHIT: An ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph","volume":"31","author":"Li","year":"2015","journal-title":"Bioinformatics"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1038\/nmeth.3176","article-title":"Fast and sensitive protein alignment using DIAMOND","volume":"12","author":"Buchfink","year":"2015","journal-title":"Nat. Methods"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"e29104","DOI":"10.1016\/j.heliyon.2024.e29104","article-title":"Next-generation DNA sequencing of Panax samples revealed new genotypes: Burrows-Wheeler Aligner, Python-based abundance and clustering analysis","volume":"10","author":"Oberc","year":"2024","journal-title":"Heliyon"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"D587","DOI":"10.1093\/nar\/gkac963","article-title":"KEGG for taxonomy-based analysis of pathways and genomes","volume":"51","author":"Kanehisa","year":"2023","journal-title":"Nucleic Acids Res."},{"key":"ref_28","first-page":"436","article-title":"Molecular cloning and expression analysis of cuticular protein gene CpCPR117 in Culex pipiens pallens","volume":"32","author":"Wang","year":"2021","journal-title":"Chin. J. Vector Biol. Control"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"veab085","DOI":"10.1093\/ve\/veab085","article-title":"In action-an early warning system for the detection of unexpected or novel pathogens","volume":"7","author":"Santos","year":"2021","journal-title":"Virus Evol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1099\/jgv.0.001219","article-title":"Skunk River virus, a novel orbivirus isolated from Aedes trivittatus in the United States","volume":"100","author":"Tangudu","year":"2019","journal-title":"J. Gen. Virol."},{"key":"ref_31","first-page":"671","article-title":"The potential role of migratory birds in the transmission of zoonoses","volume":"44","author":"Georgopoulou","year":"2008","journal-title":"Vet. Ital."},{"doi-asserted-by":"crossref","unstructured":"Belaganahalli, M.N., Maan, S., Maan, N.S., Nomikou, K., Guimera, M., Brownlie, J., Tesh, R., Attoui, H., and Mertens, P.P. (2013). Full genome sequencing of Corriparta virus, identifies California mosquito pool virus as a member of the Corriparta virus species. PLoS ONE, 8.","key":"ref_32","DOI":"10.1371\/journal.pone.0070779"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"110","DOI":"10.1099\/vir.0.058800-0","article-title":"Mobuck virus genome sequence and phylogenetic analysis: Identification of a novel Orbivirus isolated from a white-tailed deer in Missouri, USA","volume":"95","author":"Cooper","year":"2014","journal-title":"J. Gen. Virol."},{"doi-asserted-by":"crossref","unstructured":"Li, M., Xing, D., Su, D., Wang, D., Gao, H., Lan, C., Gu, Z., Zhao, T., and Li, C. (2021). Transcriptome Analysis of Responses to Dengue Virus 2 Infection in Aedes albopictus (Skuse) C6\/36 Cells. Viruses, 13.","key":"ref_34","DOI":"10.3390\/v13020343"},{"doi-asserted-by":"crossref","unstructured":"Du, J., Gao, S., Tian, Z., Guo, Y., Kang, D., Xing, S., Zhang, G., Liu, G., Luo, J., and Chang, H. (2019). Transcriptome analysis of responses to bluetongue virus infection in Aedes albopictus cells. BMC Microbiol., 19.","key":"ref_35","DOI":"10.1186\/s12866-019-1498-3"},{"doi-asserted-by":"crossref","unstructured":"Brackney, D.E., Scott, J.C., Sagawa, F., Woodward, J.E., Miller, N.A., Schilkey, F.D., Mudge, J., Wilusz, J., Olson, K.E., and Blair, C.D. (2010). C6\/36 Aedes albopictus cells have a dysfunctional antiviral RNA interference response. PLoS Negl. Trop. Dis., 4.","key":"ref_36","DOI":"10.1371\/journal.pntd.0000856"},{"doi-asserted-by":"crossref","unstructured":"Jiang, H., Kan, X., Ding, C., and Sun, Y. (2022). The Multi-Faceted Role of Autophagy During Animal Virus Infection. Front. Cell Infect. Microbiol., 12.","key":"ref_37","DOI":"10.3389\/fcimb.2022.858953"},{"doi-asserted-by":"crossref","unstructured":"Wang, H., Zheng, Y., Huang, J., and Li, J. (2021). Mitophagy in Antiviral Immunity. Front. Cell Dev. Biol., 9.","key":"ref_38","DOI":"10.3389\/fcell.2021.723108"},{"doi-asserted-by":"crossref","unstructured":"Kawasaki, T., and Kawai, T. (2014). Toll-like receptor signaling pathways. Front. Immunol., 5.","key":"ref_39","DOI":"10.3389\/fimmu.2014.00461"},{"doi-asserted-by":"crossref","unstructured":"Kircheis, R., and Planz, O. (2023). The Role of Toll-like Receptors (TLRs) and Their Related Signaling Pathways in Viral Infection and Inflammation. Int. J. Mol. Sci., 24.","key":"ref_40","DOI":"10.3390\/ijms24076701"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"7023","DOI":"10.1113\/JP273839","article-title":"Oxidative phosphorylation: Regulation and role in cellular and tissue metabolism","volume":"595","author":"Wilson","year":"2017","journal-title":"J. Physiol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"2551","DOI":"10.1007\/s12035-018-1263-x","article-title":"Zika Virus and the Metabolism of Neuronal Cells","volume":"56","author":"Rothan","year":"2019","journal-title":"Mol. Neurobiol."},{"doi-asserted-by":"crossref","unstructured":"Gerresheim, G.K., Roeb, E., Michel, A.M., and Niepmann, M. (2019). Hepatitis C Virus Downregulates Core Subunits of Oxidative Phosphorylation, Reminiscent of the Warburg Effect in Cancer Cells. Cells, 8.","key":"ref_43","DOI":"10.3390\/cells8111410"}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/13\/12\/2717\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,11,30]],"date-time":"2025-11-30T05:27:25Z","timestamp":1764480445000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/13\/12\/2717"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,11,28]]},"references-count":43,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2025,12]]}},"alternative-id":["microorganisms13122717"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms13122717","relation":{},"ISSN":["2076-2607"],"issn-type":[{"type":"electronic","value":"2076-2607"}],"subject":[],"published":{"date-parts":[[2025,11,28]]}}}