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Genetic diversity and evolution of G12P[6] DS-1-like and G12P[9] AU-1-like Rotavirus strains in Brazil

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Abstract

In the early 2000s, the global emergence of rotavirus (RVA) G12P[8] genotype was noted, while G12P[6] and G12P[9] combinations remained rare in humans. This study aimed to characterize and phylogenetically analyze three Brazilian G12P[9] and four G12P[6] RVA strains from 2011 to 2020, through RT-PCR and sequencing, in order to enhance our understanding of the genetic relationship between human and animal-origin RVA strains. G12P[6] strains displayed a DS-1-like backbone, showing a distinct genetic clustering. G12P[6] IAL-R52/2020, IAL-R95/2020 and IAL-R465/2019 strains clustered with 2019 Northeastern G12P[6] Brazilian strains and a 2018 Benin strain, whereas IAL-R86/2011 strain grouped with 2010 Northern G12P[6] Brazilian strains and G2P[4] strains from the United States and Belgium. These findings suggest an African genetic ancestry and reassortments with co-circulating American strains sharing the same DS-1-like constellation. No recent zoonotic reassortment was observed, and the DS-1-like constellation detected in Brazilian G12P[6] strains does not seem to be genetically linked to globally reported intergenogroup G1/G3/G9/G8P[8] DS-1-like human strains. G12P[9] strains exhibited an AU-1-like backbone with two different genotype-lineage constellations: IAL-R566/2011 and IAL-R1151/2012 belonged to a VP3/M3.V Lineage, and IAL-R870/2013 to a VP3/M3.II Lineage, suggesting two co-circulating strains in Brazil. This genetic diversity is not observed elsewhere, and the VP3/M3.II Lineage in G12P[9] strains seems to be exclusive to Brazil, indicating its evolution within the country. All three G12P[9] AU-1-like strains were closely relate to G12P[9] strains from Paraguay (2006–2007) and Brazil (2010). Phylogenetic analysis also highlighted that all South American G12P[9] AU-1-like strains had a common origin and supports the hypothesis of their importation from Asia, with no recent introduction from globally circulating G12P[9] strains or reassortments with local G12 strains P[8] or P[6]. Notably, certain genes in the Brazilian G12P[9] AU-1-like strains share ancestry with feline/canine RVAs (VP3/M3.II, NSP4/E3.IV and NSP2/N3.II), whereas NSP1/A3.VI likely originated from artiodactyls, suggesting a history of zoonotic transmission with human strains. This genomic data adds understanding to the molecular epidemiology of G12P[6] and G12P[9] RVA strains in Brazil, offering insights into their genetic diversity and evolution.

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Acknowledgements

We thank the staff of the Enteric Diseases Laboratory of Adolfo Lutz Institute: Maria do Carmo S. T. Timenetsky, Rita de Cassia C. Carmona, Audrey Cilli, Simone G. Morillo, Antonio Erculiani Junior, Giselle A. Schiavelli and Isabella Guilherme Monteiro. We are grateful to the Center for Surveillance (CVE)—São Paulo State Health Department; Public Health Laboratories (LACENs) and CGLAB/DEVEP/SVS/Ministry of Health—Brasília for assistance in sample collection and epidemiological data. We thank Graduate Program in Science, Coordinator for Disease Control, Ministry of Health-PPG-CCD-SES/SP.

Funding

This study was supported by the Sao Paulo Research Foundation (FAPESP) through the grant numbers #2017/50333–7 to Adolfo Lutz Institute (PDIP), #2015/12944–9 and #2020/14786–0 to Adriana Luchs, #2020/02469–0 and #2021/09064–8 to Yasmin França, #2020/11182–6 to Roberta Salzone Medeiros and #2022/02529–8 to Ellen Viana. Fundo Especial de Saúde para Imunização em Massa e Controle de Doenças (FESIMA) CAF Nº #001/2021, #060/2021 and #012/2023 to Adriana Luchs. Programa de Apoio à Pós-Graduação-Auxílio Financeiro a Projeto Educacional ou de Pesquisa (PROAP-AUXPE) #2022/115. Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-Sistema de Controle de Bolsas e Auxílio (CAPES-SCBA) #2022–0/88881.689557. ACC is supported by a scholarship from Hospital das Clínicas, Faculty of Medicine, University of São Paulo (HCFMUSP) with funds donated by NUBANK under the #HCCOMVIDA scheme.

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Contributions

AL conceived and designed the study; YF, RSM, EV, LSA, RG and ACC participated in the conduct of the study; YF, RSM, RG and AL acquired the data; RG performed the RNA extraction and conducted PAGE screening; YF, RSM, EV, LSA and AL performed the RT-PCR tests; YF, ACC and AL conducted sequencing assays; YF and AL accomplished the phylogenetic analysis; YF and AL analyzed, interpreted the data and drafted the manuscript; RSM, EV, LSA, RG and ACC critically revised the manuscript for intellectual content. All authors read and approved the final version. AL is guarantors of the paper.

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Correspondence to Adriana Luchs.

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The authors declare no competing interests.

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Previous Ethics Committee approval was granted by the Adolfo Lutz Institute, São Paulo, Brazil (CAAE 40718114.5.0000.0059 and CAAE 51963821.3.0000.0059).

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França, Y., Medeiros, R.S., Viana, E. et al. Genetic diversity and evolution of G12P[6] DS-1-like and G12P[9] AU-1-like Rotavirus strains in Brazil. Funct Integr Genomics 24, 92 (2024). https://doi.org/10.1007/s10142-024-01360-9

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