{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,16]],"date-time":"2026-10-16T18:07:09Z","timestamp":1792174029857,"version":"4.4.0"},"reference-count":46,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2025,10,25]],"date-time":"2025-10-25T00:00:00Z","timestamp":1761350400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"National Key Research and Development Plan","award":["2023YFD1800605"],"award-info":[{"award-number":["2023YFD1800605"]}]},{"DOI":"10.13039\/100007219","name":"Shanghai Municipal Natural Science Foundation","doi-asserted-by":"crossref","award":["2023-02-08-00-12-F04617"],"award-info":[{"award-number":["2023-02-08-00-12-F04617"]}],"id":[{"id":"10.13039\/100007219","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100007219","name":"Shanghai Municipal Natural Science Foundation","doi-asserted-by":"crossref","award":["K2024003"],"award-info":[{"award-number":["K2024003"]}],"id":[{"id":"10.13039\/100007219","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"crossref","award":["32573348"],"award-info":[{"award-number":["32573348"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"crossref","award":["32172835"],"award-info":[{"award-number":["32172835"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"crossref","award":["32273001"],"award-info":[{"award-number":["32273001"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"crossref"}]},{"name":"Innovation Program of Chinese Academy of Agricultural Sciences","award":["CAAS-CSLPDCP-202402"],"award-info":[{"award-number":["CAAS-CSLPDCP-202402"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>Avian viral arthritis (AVA), caused by avian reovirus (ARV), is a viral disease in chickens that has led to significant economic losses in the poultry industry. Recent studies have shown that traditional ARV vaccines based on the S1133 strain fail to protect against emerging ARV variants. In this study, we isolated and characterized three ARV strains (G4, YV, WF) from immunized chicken flocks with respiratory and arthritic symptoms. Genomic analysis revealed that the \u03c3C genes of G4, YV, and WF shared only 55.5%, 55.7%, and 58.7% sequence homology, respectively, with the S1133 strain. Phylogenetic analysis placed them in different branches, indicating they are variant strains. YV and WF belong to genotype III, and G4 falls into genotype VI. Whole genome analysis revealed gene segment reassortment among the variants. Pathogenicity testing in three-week-old SPF chickens showed that G4 (genotype VI) caused swelling of footpads, whereas WF (genotype III) did not. G4-infected chickens exhibited significantly higher viral loads in the thymus, lungs, spleen, and bursa of Fabricius than those in the WF-infected chickens, indicating viruses from different genotypes showed various pathogenesis. These results suggested an urgent need for new updates of vaccines against the variant ARVs, especially the genotype VI virus.<\/jats:p>","DOI":"10.3390\/microorganisms13112450","type":"journal-article","created":{"date-parts":[[2025,10,27]],"date-time":"2025-10-27T02:50:48Z","timestamp":1761533448000},"page":"2450","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Genetic and Pathogenic Characteristics of Variant Avian Reovirus Strains Isolated from Diseased Chickens in China"],"prefix":"10.3390","volume":"13","author":[{"given":"Shiqi","family":"Niu","sequence":"first","affiliation":[{"name":"Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Shanghai 200241, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zihua","family":"Wu","sequence":"additional","affiliation":[{"name":"Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Shanghai 200241, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shenghui","family":"Pan","sequence":"additional","affiliation":[{"name":"Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Shanghai 200241, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0007-3549-1072","authenticated-orcid":false,"given":"Tianxin","family":"Ma","sequence":"additional","affiliation":[{"name":"Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Shanghai 200241, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yunxiang","family":"Zhang","sequence":"additional","affiliation":[{"name":"Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Shanghai 200241, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bangfeng","family":"Xu","sequence":"additional","affiliation":[{"name":"Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Shanghai 200241, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8039-4668","authenticated-orcid":false,"given":"Dawei","family":"Yan","sequence":"additional","affiliation":[{"name":"Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Shanghai 200241, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qiaoyang","family":"Teng","sequence":"additional","affiliation":[{"name":"Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Shanghai 200241, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chunxiu","family":"Yuan","sequence":"additional","affiliation":[{"name":"Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Shanghai 200241, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xue","family":"Pan","sequence":"additional","affiliation":[{"name":"Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Shanghai 200241, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhifei","family":"Zhang","sequence":"additional","affiliation":[{"name":"Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Shanghai 200241, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0005-9037-5328","authenticated-orcid":false,"given":"Minghao","family":"Yan","sequence":"additional","affiliation":[{"name":"Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Shanghai 200241, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaona","family":"Shi","sequence":"additional","affiliation":[{"name":"Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Shanghai 200241, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zejun","family":"Li","sequence":"additional","affiliation":[{"name":"Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Shanghai 200241, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9516-2130","authenticated-orcid":false,"given":"Qinfang","family":"Liu","sequence":"additional","affiliation":[{"name":"Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Shanghai 200241, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,10,25]]},"reference":[{"key":"ref_1","first-page":"13","article-title":"Studies on Chronic Respiratory Disease of Chickens II. Isolation of a Virus","volume":"18","author":"Fahey","year":"1954","journal-title":"Can. J. Comp. Med. Vet. Sci."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1507","DOI":"10.1099\/0022-1317-81-6-1507","article-title":"Complete sequence determination and genetic analysis of Banna virus and Kadipiro virus: Proposal for assignment to a new genus (Seadornavirus) within the family Reoviridae","volume":"81","author":"Attoui","year":"2000","journal-title":"J. Gen. Virol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1016\/S0022-5320(72)90039-1","article-title":"Electron microscopic study of an avian reovirus that causes arthritis","volume":"41","author":"Walker","year":"1972","journal-title":"J. Ultrastruct. Res."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"460","DOI":"10.2307\/1590407","article-title":"Role of route of exposure, age, sex, and type of chicken on the pathogenicity of avian reovirus strain 81-176","volume":"30","author":"Montgomery","year":"1986","journal-title":"Avian Dis."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1080\/03079457708418237","article-title":"Viral arthritis\/tenosynovitis: A review","volume":"6","year":"1977","journal-title":"Avian Pathol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"9","DOI":"10.2307\/1588321","article-title":"Isolation and characterization of an enterovirus from baby chicks having an enteric infection II. Physical and chemical characteristics and ultrastructure","volume":"11","author":"Dutta","year":"1967","journal-title":"Avian Dis."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1080\/01652176.2001.9695099","article-title":"Isolation of a new serotype of avian reovirus associated with malabsorption syndrome in chickens","volume":"23","author":"Koopman","year":"2001","journal-title":"Vet. Q."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"451","DOI":"10.2307\/1591672","article-title":"Enteritis (so-called runting stunting syndrome) in Georgia broiler chicks","volume":"37","author":"Goodwin","year":"1993","journal-title":"Avian Dis."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Zhou, L., and Zheng, S.J. (2019). The Roles of MicroRNAs (miRNAs) in Avian Response to Viral Infection and Pathogenesis of Avian Immunosuppressive Diseases. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20215454"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"968","DOI":"10.1128\/jvi.19.3.968-976.1976","article-title":"Physical and chemical characterization of an avian reovirus","volume":"19","author":"Spandidos","year":"1976","journal-title":"J. Virol."},{"key":"ref_11","first-page":"67","article-title":"Early steps in avian reovirus morphogenesis","volume":"309","author":"Benavente","year":"2006","journal-title":"Curr. Top. Microbiol. Immunol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1128\/jvi.71.1.59-64.1997","article-title":"Protein architecture of avian reovirus S1133 and identification of the cell attachment protein","volume":"71","author":"Grande","year":"1997","journal-title":"J. Virol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"336","DOI":"10.1016\/S0042-6822(03)00415-X","article-title":"Molecular evolution of avian reovirus: Evidence for genetic diversity and reassortment of the S-class genome segments and multiple cocirculating lineages","volume":"314","author":"Liu","year":"2003","journal-title":"Virology"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"413","DOI":"10.1007\/BF01241740","article-title":"The Crawley agent: An avian reovirus","volume":"21","author":"Petek","year":"1967","journal-title":"Arch. Gesamte Virusforsch."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Farkas, S.L., Marton, S., Dand\u00e1r, E., Kugler, R., G\u00e1l, B., Jakab, F., B\u00e1lint, \u00c1., Kecskem\u00e9ti, S., and B\u00e1nyai, K. (2016). Lineage diversification, homo- and heterologous reassortment and recombination shape the evolution of chicken orthoreoviruses. Sci. Rep., 6.","DOI":"10.1038\/srep36960"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1186\/1743-422X-10-12","article-title":"Molecular characterization of avian reovirus isolates in Tunisia","volume":"10","author":"Gribaa","year":"2013","journal-title":"Virol. J."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"611","DOI":"10.1080\/03079457.2020.1804528","article-title":"Genotypic characterization and molecular evolution of avian reovirus in poultry flocks from Brazil","volume":"49","author":"Wolf","year":"2020","journal-title":"Avian Pathol."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Lu, H., Tang, Y., Dunn, P.A., Wallner-Pendleton, E.A., Lin, L., and Knoll, E.A. (2015). Isolation and molecular characterization of newly emerging avian reovirus variants and novel strains in Pennsylvania, USA, 2011\u20132014. Sci. Rep., 5.","DOI":"10.1038\/srep14727"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1777","DOI":"10.1099\/vir.0.000110","article-title":"Isolation and genomic characterization of a novel orthoreovirus from a brown-eared bulbul (Hypsipetes amaurotis) in Japan","volume":"96","author":"Ogasawara","year":"2015","journal-title":"J. Gen. Virol."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Vibin, J., Chamings, A., Klaassen, M., and Alexandersen, S. (2020). Metagenomic characterisation of additional and novel avian viruses from Australian wild ducks. Sci. Rep., 10.","DOI":"10.1038\/s41598-020-79413-9"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1016\/j.meegid.2015.03.029","article-title":"Genomic characterization of a turkey reovirus field strain by Next-Generation Sequencing","volume":"32","author":"Tang","year":"2015","journal-title":"Infect. Genet. Evol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1016\/j.meegid.2015.01.029","article-title":"Genomic characterization of a broiler reovirus field strain detected in Pennsylvania","volume":"31","author":"Tang","year":"2015","journal-title":"Infect. Genet. Evol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"2629","DOI":"10.1007\/s00705-015-2547-3","article-title":"Genomic characterization of a novel avian arthritis orthoreovirus variant by next-generation sequencing","volume":"160","author":"Tang","year":"2015","journal-title":"Arch. Virol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"435","DOI":"10.1637\/aviandiseases-D-22-99994","article-title":"Evaluation of Pathogenicity and Antigenicity of Avian Reoviruses and Disease Control Through Vaccination","volume":"66","author":"Markis","year":"2022","journal-title":"Avian Dis."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Narvaez, S.A., Harrell, T.L., Oluwayinka, O., Sellers, H.S., Khalid, Z., Hauck, R., Chowdhury, E.U., and Conrad, S.J. (2023). Optimizing the Conditions for Whole-Genome Sequencing of Avian Reoviruses. Viruses, 15.","DOI":"10.3390\/v15091938"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"5321","DOI":"10.3382\/ps\/pez319","article-title":"Genetic and pathogenic characteristics of newly emerging avian reovirus from infected chickens with clinical arthritis in China","volume":"98","author":"Zhang","year":"2019","journal-title":"Poult. Sci."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Ayalew, L.E., Gupta, A., Fricke, J., Ahmed, K.A., Popowich, S., Lockerbie, B., Tikoo, S.K., Ojkic, D., and Gomis, S. (2017). Phenotypic, genotypic and antigenic characterization of emerging avian reoviruses isolated from clinical cases of arthritis in broilers in Saskatchewan, Canada. Sci. Rep., 7.","DOI":"10.1038\/s41598-017-02743-8"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1080\/03079457.2015.1125443","article-title":"Clinicopathological characterization and genomic sequence differences observed in a highly virulent fowl Aviadenovirus serotype 4","volume":"45","year":"2016","journal-title":"Avian Pathol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"441","DOI":"10.1016\/0022-2836(75)90213-2","article-title":"A rapid method for determining sequences in DNA by primed synthesis with DNA polymerase","volume":"94","author":"Sanger","year":"1975","journal-title":"J. Mol. Biol."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Jiang, X., Yao, Z., He, D., Wu, B., Wei, F., Li, G., Wu, Q., Tang, Y., and Diao, Y. (2022). Genetic and pathogenic characteristics of two novel\/recombinant avian orthoreovirus. Vet. Microbiol., 275.","DOI":"10.1016\/j.vetmic.2022.109601"},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Liang, Z., Guo, J., Yuan, S., Cheng, Q., Zhang, X., Liu, Z., Wang, C., Li, Z., Hou, B., and Huang, S. (2022). Pathological and Molecular Characterization of a Duck Plague Outbreak in Southern China in 2021. Animals, 12.","DOI":"10.3390\/ani12243523"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1016\/j.virusres.2015.11.018","article-title":"Phylogenetic analysis of a novel reassortant orthoreovirus strain detected in partridge (Perdix perdix)","volume":"215","author":"Kugler","year":"2016","journal-title":"Virus Res."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1080\/03079457.2019.1654086","article-title":"Molecular characterization of avian reovirus causing tenosynovitis outbreaks in broiler flocks, Iran","volume":"49","author":"Mirbagheri","year":"2020","journal-title":"Avian Pathol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"346","DOI":"10.1637\/0005-2086-65.3.346","article-title":"Genetic Analysis of Avian Reovirus Isolated from Chickens in Japan","volume":"65","author":"Mase","year":"2021","journal-title":"Avian Dis."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Kim, S.W., Choi, Y.R., Park, J.Y., Wei, B., Shang, K., Zhang, J.F., Jang, H.K., Cha, S.Y., and Kang, M. (2022). Isolation and Genomic Characterization of Avian Reovirus From Wild Birds in South Korea. Front. Vet. Sci., 9.","DOI":"10.3389\/fvets.2022.794934"},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Liu, L., Lu, X., Guo, X., Gong, X., Hu, F., Jiang, Y., Gao, Y., Ma, X., Li, Y., and Huang, B. (2025). Phylogenetic Analysis and Pathogenicity of Avian Reoviruses Isolated from Viral Arthritis Cases in China 2010\u20132024. Vet. Sci., 12.","DOI":"10.3390\/vetsci12040307"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1203","DOI":"10.1099\/0022-1317-77-6-1203","article-title":"Evidence for the multimeric nature and cell binding ability of avian reovirus sigma 3 protein","volume":"77","author":"Shapouri","year":"1996","journal-title":"J. Gen. Virol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"688","DOI":"10.1006\/viro.1993.1309","article-title":"Avian reovirus proteins associated with neutralization of virus infectivity","volume":"194","author":"Wickramasinghe","year":"1993","journal-title":"Virology"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"400","DOI":"10.1080\/03079457.2024.2342889","article-title":"Diagnostic investigation of avian reovirus field variants circulating in broiler chickens in Pennsylvania of United States between 2017 and 2022","volume":"53","author":"Shabbir","year":"2024","journal-title":"Avian Pathol."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Franzo, G., Tucciarone, C.M., Faustini, G., Poletto, F., Baston, R., Cecchinato, M., and Legnardi, M. (2024). Reconstruction of Avian Reovirus History and Dispersal Patterns: A Phylodynamic Study. Viruses, 16.","DOI":"10.3389\/fmicb.2025.1527335"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"veaa025","DOI":"10.1093\/ve\/veaa025","article-title":"The dynamics of molecular evolution of emerging avian reoviruses through accumulation of point mutations and genetic re-assortment","volume":"6","author":"Ayalew","year":"2020","journal-title":"Virus Evol."},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Yan, T., Guo, L., Jiang, X., Wang, H., Yao, Z., Zhu, S., Diao, Y., and Tang, Y. (2021). Discovery of a novel recombinant avian orthoreovirus in China. Vet. Microbiol., 260.","DOI":"10.1016\/j.vetmic.2021.109094"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"3552","DOI":"10.1111\/tbed.13961","article-title":"Genetic characterization and pathogenicity of a divergent broiler-origin orthoreovirus causing arthritis in China","volume":"68","author":"Jiang","year":"2021","journal-title":"Transbound. Emerg. Dis."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Liu, R., Luo, D., Gao, J., Li, K., Liu, C., Qi, X., Cui, H., Zhang, Y., Wang, S., and Wang, X. (2023). A Novel Variant of Avian Reovirus Is Pathogenic to Vaccinated Chickens. Viruses, 15.","DOI":"10.3390\/v15091800"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"334","DOI":"10.1080\/03079457.2019.1600656","article-title":"Pathogenicity and genomic characterization of a novel avian orthoreovius variant isolated from a vaccinated broiler flock in China","volume":"48","author":"Chen","year":"2019","journal-title":"Avian Pathol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"199538","DOI":"10.1016\/j.virusres.2025.199538","article-title":"Pathogenicity of avian reovirus variant in the immune organs of broiler chicks","volume":"353","author":"Yu","year":"2025","journal-title":"Virus Res."}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/13\/11\/2450\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,28]],"date-time":"2025-10-28T05:17:35Z","timestamp":1761628655000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/13\/11\/2450"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,10,25]]},"references-count":46,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2025,11]]}},"alternative-id":["microorganisms13112450"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms13112450","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,10,25]]}}}