{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,9]],"date-time":"2026-01-09T17:45:45Z","timestamp":1767980745559,"version":"3.49.0"},"reference-count":39,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2020,5,4]],"date-time":"2020-05-04T00:00:00Z","timestamp":1588550400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>Human Adenovirus species C (HAdV-C) is the most common etiologic agent of respiratory disease. In the present study, we characterized the nearly full-length genome of one potential new HAdV-C recombinant strain constituted by Penton and Fiber proteins belonging to type 89 and a chimeric Hexon protein of types 1 and 89. By using viral metagenomics techniques, we screened out, in the states of Tocantins and Par\u00e1, Northern and North regions of Brazil, from 2010 to 2016, 251 fecal samples of children between 0.5 to 2.5 years old. These children were presenting acute diarrhea not associated with common pathogens (i.e., rotavirus, norovirus). We identified two HAdV-C strains in two distinct patients. Phylogenetic analysis performed using all complete genomes available at GenBank database indicated that one strain (HAdV-C BR-245) belonged to type 1. The phylogenetic analysis also indicated that the second strain (HAdV-C BR-211) was located at the base of the clade formed by the newly HAdV-C strains type 89. Recombination analysis revealed that strain HAdV-C BR-211 is a chimera in which the variable regions of Hexon gene combined HAdV-C1 and HAdV-C89 sequences. Therefore, HAdV-C BR-211 strain possesses a genomic backbone of type HAdV-C89 and a unique insertion of HAdV-C1 in the Hexon sequence. Recombination may play an important driving force in HAdV-C diversity and evolution. Studies employing complete genomic sequencing on circulating HAdV-C strains in Brazil are needed to understand the clinical significance of the presented data.<\/jats:p>","DOI":"10.3390\/v12050508","type":"journal-article","created":{"date-parts":[[2020,5,4]],"date-time":"2020-05-04T14:00:43Z","timestamp":1588600843000},"page":"508","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":11,"title":["Genomic Analyses of Potential Novel Recombinant Human Adenovirus C in Brazil"],"prefix":"10.3390","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-9631-5530","authenticated-orcid":false,"given":"Roozbeh","family":"Tahmasebi","sequence":"first","affiliation":[{"name":"Polytechnic School of University of Sao Paulo, Sao Paulo 01246-903, Brazil"},{"name":"Institute of Tropical Medicine, University of Sao Paulo, Sao Paulo 01246-903, Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5516-5177","authenticated-orcid":false,"given":"Antonio Charlys","family":"da Costa","sequence":"additional","affiliation":[{"name":"Institute of Tropical Medicine, University of Sao Paulo, Sao Paulo 01246-903, Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kaelan","family":"Tardy","sequence":"additional","affiliation":[{"name":"Institute of Tropical Medicine, University of Sao Paulo, Sao Paulo 01246-903, Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7093-8844","authenticated-orcid":false,"given":"Rory","family":"J. Tinker","sequence":"additional","affiliation":[{"name":"Faculty of Biology, Medicine and Health, University of Manchester, Manchester M13 9PL, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6889-8772","authenticated-orcid":false,"given":"Flavio Augusto","family":"de Padua Milagres","sequence":"additional","affiliation":[{"name":"LIM\/46, Faculty of Medicine, University of Sao Paulo, Sao Paulo 01246-903, Brazil"},{"name":"Secretary of Health of Tocantins, Tocantins 77453-000, Brazil"},{"name":"Institute of Biological Sciences, Federal University of Tocantins, Tocantins 77001-090, Brazil"},{"name":"Public Health Laboratory of Tocantins State (LACEN\/TO), Tocantins 77016-330, Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Rafael","family":"Brustulin","sequence":"additional","affiliation":[{"name":"LIM\/46, Faculty of Medicine, University of Sao Paulo, Sao Paulo 01246-903, Brazil"},{"name":"Secretary of Health of Tocantins, Tocantins 77453-000, Brazil"},{"name":"Institute of Biological Sciences, Federal University of Tocantins, Tocantins 77001-090, Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Maria da Aparecida","family":"Rodrigues Teles","sequence":"additional","affiliation":[{"name":"Secretary of Health of Tocantins, Tocantins 77453-000, Brazil"},{"name":"Public Health Laboratory of Tocantins State (LACEN\/TO), Tocantins 77016-330, Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Rog\u00e9rio","family":"Togisaki das Chagas","sequence":"additional","affiliation":[{"name":"Secretary of Health of Tocantins, Tocantins 77453-000, Brazil"},{"name":"Public Health Laboratory of Tocantins State (LACEN\/TO), Tocantins 77016-330, Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Cassia Vit\u00f3ria","family":"de Deus Alves Soares","sequence":"additional","affiliation":[{"name":"Secretary of Health of Tocantins, Tocantins 77453-000, Brazil"},{"name":"Public Health Laboratory of Tocantins State (LACEN\/TO), Tocantins 77016-330, Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Aripuana","family":"Sakurada Aranha Watanabe","sequence":"additional","affiliation":[{"name":"Department of Parasitology, Microbiology and Immunology, Federal University of Juiz de Fora, Juiz de Fora, MG 34092829, Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3583-2275","authenticated-orcid":false,"given":"Cecilia","family":"Salete Alencar","sequence":"additional","affiliation":[{"name":"Central Laboratory Division-DLC-HCSP, Clinical Laboratory and LIM 03-Department of Pathology, Clinical Hospital, University of Sao Paulo Medical School, Sao Paulo 01246-000, Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Fabiola","family":"Villanova","sequence":"additional","affiliation":[{"name":"Institute of Biological Sciences, Federal University of Para, Para 66075-000, Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xutao","family":"Deng","sequence":"additional","affiliation":[{"name":"Vitalant Research Institute, 270 Masonic Avenue, San Francisco, CA 94118-4417, USA"},{"name":"Department Laboratory Medicine, University of California San Francisco, San Francisco, CA 94143, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6296-4484","authenticated-orcid":false,"given":"Eric","family":"Delwart","sequence":"additional","affiliation":[{"name":"Vitalant Research Institute, 270 Masonic Avenue, San Francisco, CA 94118-4417, USA"},{"name":"Department Laboratory Medicine, University of California San Francisco, San Francisco, CA 94143, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Adriana","family":"Luchs","sequence":"additional","affiliation":[{"name":"Enteric Disease Laboratory, Virology Center, Adolfo Lutz Institute, Sao Paulo 01246-000, Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3463-0492","authenticated-orcid":false,"given":"\u00c9lcio","family":"Leal","sequence":"additional","affiliation":[{"name":"Institute of Biological Sciences, Federal University of Para, Para 66075-000, Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ester","family":"Cerdeira Sabino","sequence":"additional","affiliation":[{"name":"Polytechnic School of University of Sao Paulo, Sao Paulo 01246-903, Brazil"},{"name":"Institute of Tropical Medicine, University of Sao Paulo, Sao Paulo 01246-903, Brazil"},{"name":"LIM\/46, Faculty of Medicine, University of Sao Paulo, Sao Paulo 01246-903, Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2020,5,4]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"2182","DOI":"10.1038\/s41598-019-38719-z","article-title":"Recombination analysis of human mastadenovirus c whole genomes","volume":"9","author":"Rivailler","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1812","DOI":"10.1038\/srep01812","article-title":"Molecular evolution of human adenoviruses","volume":"3","author":"Robinson","year":"2013","journal-title":"Sci. Rep."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"441","DOI":"10.1128\/CMR.00116-13","article-title":"Adenovirus infections in immunocompetent and immunocompromised patients","volume":"27","author":"Lion","year":"2014","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"744","DOI":"10.1002\/jmv.25392","article-title":"High prevalence of enteric viruses associated with acute gastroenteritis in pediatric patients in a low-income area in vitoria, southeastern brazil","volume":"91","author":"Miagostovich","year":"2019","journal-title":"J. Med. Virol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1099\/jmm.0.46685-0","article-title":"Adenoviruses associated with acute gastroenteritis in hospitalized and community children up to 5 years old in rio de janeiro and salvador, brazil","volume":"56","author":"Filho","year":"2007","journal-title":"J. Med. Microbiol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"e3577","DOI":"10.1097\/MD.0000000000003577","article-title":"Molecular epidemiology and clinical manifestations of adenovirus respiratory infections in taiwanese children","volume":"95","author":"Wang","year":"2016","journal-title":"Medicine (Baltimore)"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1039","DOI":"10.1038\/s41598-018-37249-4","article-title":"Molecular evolution of human adenovirus (hadv) species c","volume":"9","author":"Dhingra","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"9781","DOI":"10.1038\/s41598-019-46228-2","article-title":"Human adenovirus species c recombinant virus continuously circulated in china","volume":"9","author":"Yang","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1038\/mt.2015.194","article-title":"Development of novel adenoviral vectors to overcome challenges observed with hadv-5-based constructs","volume":"24","author":"Papp","year":"2016","journal-title":"Mol. Ther."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"3482","DOI":"10.1128\/JCM.00156-11","article-title":"Computational analysis of two species c human adenoviruses provides evidence of a novel virus","volume":"49","author":"Walsh","year":"2011","journal-title":"J. Clin. Microbiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1261","DOI":"10.1093\/infdis\/jiy323","article-title":"Use of whole-genome sequencing of adenovirus in immunocompromised pediatric patients to identify nosocomial transmission and mixed-genotype infection","volume":"218","author":"Houldcroft","year":"2018","journal-title":"J. Infect. Dis."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"15380","DOI":"10.1038\/s41598-017-15336-2","article-title":"Whole genomic analysis of two potential recombinant strains within human mastadenovirus species c previously found in beijing, china","volume":"7","author":"Mao","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1742","DOI":"10.3201\/eid2310.170307","article-title":"Spread of chikungunya virus east\/central\/south african genotype in northeast brazil","volume":"23","author":"Theze","year":"2017","journal-title":"Emerg. Infect. Dis."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"e180574","DOI":"10.1590\/0074-02760180574","article-title":"Human sapovirus gi.2 and gi.3 from children with acute gastroenteritis in northern brazil","volume":"114","author":"Cilli","year":"2019","journal-title":"Mem\u00f3rias Inst. Oswaldo Cruz"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"332","DOI":"10.1007\/s11262-019-01648-0","article-title":"Discovery of cucumis melo endornavirus by deep sequencing of human stool samples in brazil","volume":"55","author":"Leal","year":"2019","journal-title":"Virus Genes"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"e46","DOI":"10.1093\/nar\/gkv002","article-title":"An ensemble strategy that significantly improves de novo assembly of microbial genomes from metagenomic next-generation sequencing data","volume":"43","author":"Deng","year":"2015","journal-title":"Nucleic Acids Res."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"2947","DOI":"10.1093\/bioinformatics\/btm404","article-title":"Clustal w and clustal x version 2.0","volume":"23","author":"Larkin","year":"2007","journal-title":"Bioinformatics"},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Price, M.N., Dehal, P.S., and Arkin, A.P. (2010). Fasttree 2\u2014Approximately maximum-likelihood trees for large alignments. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0009490"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1253","DOI":"10.1093\/molbev\/msn083","article-title":"Jmodeltest: Phylogenetic model averaging","volume":"25","author":"Posada","year":"2008","journal-title":"Mol. Biol. Evol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1547","DOI":"10.1093\/molbev\/msy096","article-title":"Mega x: Molecular evolutionary genetics analysis across computing platforms","volume":"35","author":"Kumar","year":"2018","journal-title":"Mol. Biol. Evol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"vev003","DOI":"10.1093\/ve\/vev003","article-title":"Rdp4: Detection and analysis of recombination patterns in virus genomes","volume":"1","author":"Martin","year":"2015","journal-title":"Virus Evol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1093\/bioinformatics\/bti770","article-title":"The swiss-model workspace: A web-based environment for protein structure homology modelling","volume":"22","author":"Arnold","year":"2006","journal-title":"Bioinformatics"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1038\/nmeth.1818","article-title":"Hhblits: Lightning-fast iterative protein sequence searching by hmm-hmm alignment","volume":"9","author":"Remmert","year":"2011","journal-title":"Nat. Methods"},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"da Costa, A.C., Luchs, A., Milagres, F.A.P., Komninakis, S.V., Gill, D.E., Lobato, M., Brustulin, R., das Chagas, R.T., Abrao, M., and Soares, C. (2018). Recombination located over 2a-2b junction ribosome frameshifting region of saffold cardiovirus. Viruses, 10.","DOI":"10.3390\/v10100520"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"4336","DOI":"10.1111\/j.1742-4658.2006.05430.x","article-title":"Structural and biochemical characterization of a human adenovirus 2\/12 penton base chimera","volume":"273","author":"Zubieta","year":"2006","journal-title":"FEBS J."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"12304","DOI":"10.1038\/s41598-018-30214-1","article-title":"Near full length genome of a recombinant (e\/d) cosavirus strain from a rural area in the central region of brazil","volume":"8","author":"Luchs","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Leal, E., Luchs, A., Milagres, F.A.P., Komninakis, S.V., Gill, D.E., Lobato, M., Brustulin, R., Chagas, R.T.D., Abrao, M., and Soares, C. (2019). Recombinant strains of human parechovirus in rural areas in the north of brazil. Viruses, 11.","DOI":"10.3390\/v11060488"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"470","DOI":"10.1007\/s11262-018-1557-0","article-title":"Wuhan large pig roundworm virus identified in human feces in brazil","volume":"54","author":"Luchs","year":"2018","journal-title":"Virus Genes"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"e190160","DOI":"10.1590\/0074-02760190160","article-title":"The rare enterovirus c99 and echovirus 29 strains in brazil: Potential risks associated to silent circulation","volume":"114","author":"Luchs","year":"2019","journal-title":"Mem\u00f3rias Inst. Oswaldo Cruz"},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Ribeiro, G.O., Luchs, A., Milagres, F.A.P., Komninakis, S.V., Gill, D.E., Lobato, M., Brustulin, R., Chagas, R.T.D., Abrao, M., and Soares, C. (2018). Detection and characterization of enterovirus b73 from a child in brazil. Viruses, 11.","DOI":"10.3390\/v11010016"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"18599","DOI":"10.1038\/s41598-019-55216-5","article-title":"First identification of mammalian orthoreovirus type 3 by gut virome analysis in diarrheic child in brazil","volume":"9","author":"Rosa","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"e00235-18","DOI":"10.1128\/genomeA.00235-18","article-title":"Complete genome sequences of six human bocavirus strains from patients with acute gastroenteritis in the north region of brazil","volume":"6","author":"Watanabe","year":"2018","journal-title":"Genome Announc."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"677","DOI":"10.1002\/jmv.25008","article-title":"Detection of enteric- and non-enteric adenoviruses in gastroenteritis patients, bangladesh, 2012\u20132015","volume":"90","author":"Afrad","year":"2018","journal-title":"J. Med. Virol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1556\/EuJMI.4.2014.1.2","article-title":"Human adenovirus: Viral pathogen with increasing importance","volume":"4","author":"Ghebremedhin","year":"2014","journal-title":"Eur. J. Microbiol. Immunol. (Bp.)"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1016\/j.jcv.2018.10.010","article-title":"Surveillance and molecular characterization of human adenovirus in patients with acute gastroenteritis in the era of rotavirus vaccine, brazil, 2012\u20132017","volume":"109","author":"Primo","year":"2018","journal-title":"J. Clin. Virol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"3583","DOI":"10.1002\/1873-3468.13693","article-title":"Genomic foundations of evolution and ocular pathogenesis in human adenovirus species d","volume":"593","author":"Ismail","year":"2019","journal-title":"FEBS Lett."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"272","DOI":"10.1016\/j.virol.2018.03.002","article-title":"Hexon and fiber of adenovirus type 14 and 55 are major targets of neutralizing antibody but only fiber-specific antibody contributes to cross-neutralizing activity","volume":"518","author":"Feng","year":"2018","journal-title":"Virology"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"100","DOI":"10.1016\/j.virusres.2018.08.007","article-title":"Identification of adenovirus neutralizing antigens using capsid chimeric viruses","volume":"256","author":"Liu","year":"2018","journal-title":"Virus Res."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"e01643-17","DOI":"10.1128\/JVI.01643-17","article-title":"Identification of a critical and conformational neutralizing epitope in human adenovirus type 4 hexon","volume":"92","author":"Tian","year":"2018","journal-title":"J. Virol."}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/12\/5\/508\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,13]],"date-time":"2025-10-13T14:09:56Z","timestamp":1760364596000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/12\/5\/508"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,5,4]]},"references-count":39,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2020,5]]}},"alternative-id":["v12050508"],"URL":"https:\/\/doi.org\/10.3390\/v12050508","relation":{},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,5,4]]}}}