{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,9]],"date-time":"2026-05-09T04:37:17Z","timestamp":1778301437369,"version":"3.51.4"},"reference-count":57,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2022,12,22]],"date-time":"2022-12-22T00:00:00Z","timestamp":1671667200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Microbiol."],"abstract":"<jats:p>Brazil was the epicenter of worldwide pandemics at the peak of its second wave. The genomic\/proteomic perspective of the COVID-19 pandemic in Brazil could provide insights to understand the global pandemics behavior. In this study, we track SARS-CoV-2 molecular information in Brazil using real-time bioinformatics and data science strategies to provide a comparative and evolutive panorama of the lineages in the country. SWeeP vectors represented the Brazilian and worldwide genomic\/proteomic data from Global Initiative on Sharing Avian Influenza Data (GISAID) between February 2020 and August 2021. Clusters were analyzed and compared with PANGO lineages. Hierarchical clustering provided phylogenetic and evolutionary analyses of the lineages, and we tracked the P.1 (Gamma) variant origin. The genomic diversity based on Chao's estimation allowed us to compare richness and coverage among Brazilian states and other representative countries. We found that epidemics in Brazil occurred in two moments with different genetic profiles. The P.1 lineages emerged in the second wave, which was more aggressive. We could not trace the origin of P.1 from the variants present in Brazil. Instead, we found evidence pointing to its external source and a possible recombinant event that may relate P.1 to a B.1.1.28 variant subset. We discussed the potential application of the pipeline for emerging variants detection and the PANGO terminology stability over time. The diversity analysis showed that the low coverage and unbalanced sequencing among states in Brazil could have allowed the silent entry and dissemination of P.1 and other dangerous variants. This study may help to understand the development and consequences of variants of concern (VOC) entry.<\/jats:p>","DOI":"10.3389\/fmicb.2022.1037455","type":"journal-article","created":{"date-parts":[[2022,12,22]],"date-time":"2022-12-22T06:44:26Z","timestamp":1671691466000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":5,"title":["Genomic landscape of the SARS-CoV-2 pandemic in Brazil suggests an external P.1 variant origin"],"prefix":"10.3389","volume":"13","author":[{"given":"Camila P.","family":"Perico","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Camilla R.","family":"De Pierri","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Giuseppe Pasqualato","family":"Neto","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Danrley R.","family":"Fernandes","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Fabio O.","family":"Pedrosa","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Emanuel M.","family":"de Souza","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Roberto T.","family":"Raittz","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1965","published-online":{"date-parts":[[2022,12,22]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"200","DOI":"10.1152\/physiolgenomics.00029.2020","article-title":"Artificial intelligence and machine learning to fight COVID-19","volume":"52","author":"Alimadadi","year":"2020","journal-title":"Physiol. Genomics"},{"key":"B2","doi-asserted-by":"publisher","first-page":"e0141287","DOI":"10.1371\/journal.pone.0141287","article-title":"Continuous distributed representation of biological sequences for deep proteomics and genomics","volume":"10","author":"Asgari","year":"2015","journal-title":"PLoS ONE"},{"key":"B3","year":"2020","journal-title":"Coronav\u00edrus: Na Contram\u00e3o do Mundo, Brasil segue sem restri\u00e7\u00f5es \u00e0 entrada de estrangeiros por aeroportos"},{"key":"B4","doi-asserted-by":"publisher","first-page":"1059","DOI":"10.1038\/s41422-020-00430-4","article-title":"The SARS-CoV-2 spike protein: balancing stability and infectivity","volume":"30","author":"Berger","year":"2020","journal-title":"Cell Res"},{"key":"B5","doi-asserted-by":"publisher","first-page":"1035","DOI":"10.1534\/genetics.106.068874","article-title":"An exact nonparametric method for inferring mosaic structure in sequence triplets","volume":"176","author":"Boni","year":"2007","journal-title":"Genetics"},{"key":"B6","doi-asserted-by":"publisher","first-page":"1255","DOI":"10.1126\/science.abd2161","article-title":"Evolution and epidemic spread of SARS-CoV-2 in Brazil","volume":"369","author":"Candido","year":"2020","journal-title":"Science"},{"key":"B7","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1159\/000515340","article-title":"SARS-CoV-2 lineages and sub-lineages circulating worldwide: a dynamic overview","volume":"66","author":"Cella","year":"2021","journal-title":"Chemotherapy"},{"key":"B8","first-page":"265","article-title":"Nonparametric estimation of the number of classes in a population","volume":"11","author":"Chao","year":"1984","journal-title":"Scand. J. Stat"},{"key":"B9","doi-asserted-by":"publisher","first-page":"1352.e1","DOI":"10.1016\/j.cmi.2021.05.006","article-title":"Spreading of a new SARS-CoV-2 N501Y spike variant in a new lineage","volume":"27","author":"Colson","year":"2021","journal-title":"Clin. Microbiol. Infect"},{"key":"B10","doi-asserted-by":"publisher","first-page":"101","DOI":"10.1098\/rstb.1994.0091","article-title":"Estimating terrestrial biodiversity through extrapolation","volume":"345","author":"Colwell","year":"1994","journal-title":"Philos. Trans. R. Soc. Lond. B Biol. Sci"},{"key":"B11","doi-asserted-by":"publisher","first-page":"eabg3055","DOI":"10.1126\/science.abg3055","article-title":"Estimated transmissibility and impact of SARS-CoV-2 lineage b.1.1.7 in england","volume":"372","author":"Davies","year":"2021","journal-title":"Science"},{"key":"B12","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41598-019-55627-4","article-title":"Sweep: representing large biological sequences datasets in compact vectors","volume":"10","author":"De Pierri","year":"2020","journal-title":"Sci. Rep"},{"key":"B13","doi-asserted-by":"publisher","first-page":"33","DOI":"10.1002\/gch2.1018","article-title":"Data, disease and diplomacy: GISAID's innovative contribution to global health","volume":"1","author":"Elbe","year":"2017","journal-title":"Glob. Challenges"},{"key":"B14","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s12864-015-1647-5","article-title":"An assembly and alignment-free method of phylogeny reconstruction from next-generation sequencing data","volume":"16","author":"Fan","year":"2015","journal-title":"BMC Genomics"},{"key":"B15","doi-asserted-by":"publisher","first-page":"815","DOI":"10.1126\/science.abh2644","article-title":"Genomics and epidemiology of the P. 1 SARS-CoV-2 lineage in Manaus, Brazil","volume":"372","author":"Faria","year":"2021","journal-title":"Science"},{"key":"B16","doi-asserted-by":"publisher","DOI":"10.1101\/2020.09.09.290247","article-title":"rSWeeP: AR\/Bioconductor package deal with SWeeP sequences representation","author":"Fernandes","year":"2020","journal-title":"bioRxiv"},{"key":"B17","doi-asserted-by":"publisher","DOI":"10.1101\/2021.03.08.21253152","article-title":"Mutation hotspots, geographical and temporal distribution of SARS-CoV-2 lineages in Brazil, February 2020 to February 2021: insights and limitations from uneven sequencing efforts","author":"Franceschi","year":"2021","journal-title":"medRxiv"},{"key":"B18","doi-asserted-by":"publisher","first-page":"167051","DOI":"10.1016\/j.jmb.2021.167051","article-title":"Structural modeling of the SARS-CoV-2 Spike\/human ACE2 complex interface can identify high-affinity variants associated with increased transmissibility","volume":"433","author":"Gan","year":"2021","journal-title":"J. Mol. Biol"},{"key":"B19","doi-asserted-by":"publisher","first-page":"573","DOI":"10.1093\/bioinformatics\/16.7.573","article-title":"Sister-scanning: a Monte Carlo procedure for assessing signals in recombinant sequences","volume":"16","author":"Gibbs","year":"2000","journal-title":"Bioinformatics"},{"key":"B20","doi-asserted-by":"publisher","first-page":"104869","DOI":"10.1016\/j.meegid.2021.104869","article-title":"One year into the pandemic: short-term evolution of SARS-CoV-2 and emergence of new lineages","volume":"92","author":"Gonz\u00e1lez-Candelas","year":"2021","journal-title":"Infect. Genet. Evolut"},{"key":"B21","doi-asserted-by":"publisher","first-page":"392","DOI":"10.3390\/v13030392","article-title":"SARS-CoV-2 variant of concern 202012\/01 has about twofold replicative advantage and acquires concerning mutations","volume":"13","author":"Grabowski","year":"2021","journal-title":"Viruses"},{"key":"B22","doi-asserted-by":"publisher","first-page":"4121","DOI":"10.1093\/bioinformatics\/bty407","article-title":"Nextstrain: real-time tracking of pathogen evolution","volume":"34","author":"Hadfield","year":"2018","journal-title":"Bioinformatics"},{"key":"B23","doi-asserted-by":"publisher","first-page":"405","DOI":"10.1093\/oxfordjournals.molbev.a026121","article-title":"Phylogenetic evidence for recombination in dengue virus","volume":"16","author":"Holmes","year":"1999","journal-title":"Mol. Biol. Evol"},{"key":"B24","doi-asserted-by":"publisher","first-page":"21","DOI":"10.1016\/B978-1-4832-3211-9.50009-7","article-title":"Evolution of protein molecules","volume":"3","author":"Jukes","year":"1969","journal-title":"Mammalian Protein Metab"},{"key":"B25","doi-asserted-by":"publisher","first-page":"812","DOI":"10.1016\/j.cell.2020.06.043","article-title":"Tracking changes in SARS-CoV-2 spike: evidence that D614G increases infectivity of the COVID-19 virus","volume":"182","author":"Korber","year":"2020","journal-title":"Cell"},{"key":"B26","doi-asserted-by":"publisher","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":"B27","doi-asserted-by":"publisher","first-page":"giy148","DOI":"10.1093\/gigascience\/giy148","article-title":"Prot-spam: fast alignment-free phylogeny reconstruction based on whole-proteome sequences","volume":"8","author":"Leimeister","year":"2019","journal-title":"GigaScience"},{"key":"B28","doi-asserted-by":"publisher","first-page":"W293","DOI":"10.1093\/nar\/gkab301","article-title":"Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation","volume":"49","author":"Letunic","year":"2021","journal-title":"Nucleic Acids Res"},{"key":"B29","doi-asserted-by":"publisher","first-page":"924","DOI":"10.1016\/j.idm.2021.07.002","article-title":"Estimating the quarantine failure rate for COVID-19","volume":"6","author":"Li","year":"2021","journal-title":"Infect. Dis. Model"},{"key":"B30","doi-asserted-by":"publisher","first-page":"562","DOI":"10.1093\/bioinformatics\/16.6.562","article-title":"RDP: detection of recombination amongst aligned sequences","volume":"16","author":"Martin","year":"2000","journal-title":"Bioinformatics"},{"key":"B31","doi-asserted-by":"publisher","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 Evolut"},{"key":"B32","doi-asserted-by":"publisher","first-page":"1777","DOI":"10.1093\/molbev\/msaa314","article-title":"Phylogenetic analysis of SARS-CoV-2 data is difficult","volume":"38","author":"Morel","year":"2021","journal-title":"Mol. Biol. Evol"},{"key":"B33","doi-asserted-by":"publisher","first-page":"1230","DOI":"10.21203\/rs.3.rs-275494\/v1","article-title":"COVID-19 epidemic in the Brazilian state of Amazonas was driven by long-term persistence of endemic SARS-CoV-2 lineages and the recent emergence of the new Variant of Concern P.1","volume":"27","author":"Naveca","year":"2021","journal-title":"Nat. Med"},{"key":"B34","doi-asserted-by":"publisher","first-page":"218","DOI":"10.1006\/viro.1999.0056","article-title":"Possible emergence of new geminiviruses by frequent recombination","volume":"265","author":"Padidam","year":"1999","journal-title":"Virology"},{"key":"B35","doi-asserted-by":"publisher","first-page":"526","DOI":"10.1093\/bioinformatics\/bty633","article-title":"ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R","volume":"35","author":"Paradis","year":"2019","journal-title":"Bioinformatics"},{"key":"B36","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1016\/j.bbrc.2021.02.080","article-title":"SARS-CoV-2 variants combining spike mutations and the absence of ORF8 may be more transmissible and require close monitoring","volume":"550","author":"Pereira","year":"2021","journal-title":"Biochem. Biophys. Res. Commun"},{"key":"B37","doi-asserted-by":"publisher","first-page":"13757","DOI":"10.1073\/pnas.241370698","article-title":"Evaluation of methods for detecting recombination from DNA sequences: computer simulations","volume":"98","author":"Posada","year":"2001","journal-title":"Proc. Natl. Acad. Sci. U.S.A"},{"key":"B38","doi-asserted-by":"publisher","first-page":"71","DOI":"10.3390\/genes12010071","article-title":"Comparative genomics provides insights into the taxonomy of azoarcus and reveals separate Origins of Nif genes in the proposed azoarcus and aromatoleum genera","volume":"12","author":"Raittz","year":"2021","journal-title":"Genes"},{"key":"B39","doi-asserted-by":"publisher","first-page":"1403","DOI":"10.1038\/s41564-020-0770-5","article-title":"A dynamic nomenclature proposal for SARS-CoV-2 lineages to assist genomic epidemiology","volume":"5","author":"Rambaut","year":"2020","journal-title":"Nat. Microbiol"},{"key":"B40","doi-asserted-by":"publisher","first-page":"e0232391","DOI":"10.1371\/journal.pone.0232391","article-title":"Machine learning using intrinsic genomic signatures for rapid classification of novel pathogens: COVID-19 case study","volume":"15","author":"Randhawa","year":"2020","journal-title":"PLoS ONE"},{"key":"B41","doi-asserted-by":"publisher","DOI":"10.1101\/2020.07.15.176933","article-title":"Alignment-free machine learning approaches for the lethality prediction of potential novel human-adapted coronavirus using genomic nucleotide","author":"Rui","year":"2020","journal-title":"bioRxiv"},{"key":"B42","doi-asserted-by":"publisher","first-page":"1423","DOI":"10.1089\/aid.1995.11.1423","article-title":"Identification of breakpoints in intergenotypic recombinants of HIV type 1 by bootscanning","volume":"11","author":"Salminen","year":"1995","journal-title":"AIDS Res. Hum. Retroviruses"},{"key":"B43","doi-asserted-by":"publisher","first-page":"30494","DOI":"10.2807\/1560-7917.ES.2017.22.13.30494","article-title":"GISAID: global initiative on sharing all influenza data-from vision to reality","volume":"22","author":"Shu","year":"2017","journal-title":"Eurosurveillance"},{"key":"B44","doi-asserted-by":"publisher","first-page":"126","DOI":"10.1007\/BF00182389","article-title":"Analyzing the mosaic structure of genes","volume":"34","author":"Smith","year":"1992","journal-title":"J. Mol. Evol"},{"key":"B45","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41467-018-04217-5","article-title":"Tracking HIV-1 recombination to resolve its contribution to HIV-1 evolution in natural infection","volume":"9","author":"Song","year":"2018","journal-title":"Nat. Commun"},{"key":"B46","doi-asserted-by":"publisher","first-page":"507","DOI":"10.1080\/22221751.2021.1898291","article-title":"Lessons learned 1 year after SARS-CoV-2 emergence leading to covid-19 pandemic","volume":"10","author":"To","year":"2021","journal-title":"Emerg. Microbes Infect"},{"key":"B47","first-page":"2579","article-title":"Visualizing data using t-SNE","volume":"9","author":"Van der Maaten","year":"2008","journal-title":"J. Mach. Learn. Res"},{"key":"B48","doi-asserted-by":"publisher","first-page":"2020","DOI":"10.1101\/2020.08.05.238386","article-title":"Recombinant SARS-CoV-2 genomes are currently circulating at low levels","author":"VanInsberghe","year":"2021","journal-title":"bioRxiv"},{"key":"B49","doi-asserted-by":"publisher","first-page":"iyab074","DOI":"10.1093\/genetics\/iyab074","article-title":"Rapid detection of inter-clade recombination in SARS-CoV-2 with Bolotie","volume":"218","author":"Varabyou","year":"2021","journal-title":"Genetics"},{"key":"B50","doi-asserted-by":"publisher","first-page":"1572","DOI":"10.1093\/bioinformatics\/btq170","article-title":"ConsensusClusterPlus: a class discovery tool with confidence assessments and item tracking","volume":"26","author":"Wilkerson","year":"2010","journal-title":"Bioinformatics"},{"key":"B51","doi-asserted-by":"publisher","first-page":"265","DOI":"10.1038\/s41586-020-2008-3","article-title":"A new coronavirus associated with human respiratory disease in china","volume":"579","author":"Wu","year":"2020","journal-title":"Nature"},{"key":"B52","doi-asserted-by":"publisher","first-page":"12826","DOI":"10.1073\/pnas.0905115106","article-title":"Whole-proteome phylogeny of large dsdna virus families by an alignment-free method","volume":"106","author":"Wu","year":"2009","journal-title":"Proc. Natl. Acad. Sci. U.S.A"},{"key":"B53","doi-asserted-by":"publisher","first-page":"28","DOI":"10.1111\/2041-210X.12628","article-title":"ggtree: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data","volume":"8","author":"Yu","year":"2017","journal-title":"Methods Ecol. Evolut"},{"key":"B54","doi-asserted-by":"publisher","first-page":"739","DOI":"10.1016\/j.cell.2020.09.032","article-title":"Structural and functional analysis of the D614G SARS-CoV-2 spike protein variant","volume":"183","author":"Yurkovetskiy","year":"2020","journal-title":"Cell"},{"key":"B55","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/srep40712","article-title":"Viral phylogenomics using an alignment-free method: a three-step approach to determine optimal length of k-mer","volume":"7","author":"Zhang","year":"2017","journal-title":"Sci. Rep"},{"key":"B56","doi-asserted-by":"publisher","first-page":"2196","DOI":"10.1016\/j.cub.2020.05.023","article-title":"A novel bat coronavirus closely related to SARS-CoV-2 contains natural insertions at the S1\/S2 cleavage site of the spike protein","volume":"30","author":"Zhou","year":"2020","journal-title":"Curr. Biol"},{"key":"B57","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41598-020-78703-6","article-title":"Genomic recombination events may reveal the evolution of coronavirus and the origin of SARS-CoV-2","volume":"10","author":"Zhu","year":"2020","journal-title":"Sci. Rep"}],"container-title":["Frontiers in Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2022.1037455\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,22]],"date-time":"2022-12-22T06:44:32Z","timestamp":1671691472000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2022.1037455\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,12,22]]},"references-count":57,"alternative-id":["10.3389\/fmicb.2022.1037455"],"URL":"https:\/\/doi.org\/10.3389\/fmicb.2022.1037455","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2021.11.10.21266084","asserted-by":"object"}]},"ISSN":["1664-302X"],"issn-type":[{"value":"1664-302X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,12,22]]},"article-number":"1037455"}}