Abstract
Group A rotaviruses (RVAs) with distinct G and P genotype combinations have been reported globally. We report the genome composition and possible origin of seven G8P[4] and five G2P[4] human RVA strains based on the genetic evolution of all 11 genome segments at the nucleotide level. Twelve RVA ELISA positive stool samples collected in the representative countries of Eastern, Southern and West Africa during the 2007–2012 surveillance seasons were subjected to sequencing using the Ion Torrent PGM and Illumina MiSeq platforms. A reference-based assembly was performed using CLC Bio’s clc_ref_assemble_long program, and full-genome consensus sequences were obtained. With the exception of the neutralising antigen, VP7, all study strains exhibited the DS-1-like genome constellation (P[4]-I2-R2-C2-M2-A2-N2-T2-E2-H2) and clustered phylogenetically with reference strains having a DS-1-like genetic backbone. Comparison of the nucleotide and amino acid sequences with selected global cognate genome segments revealed nucleotide and amino acid sequence identities of 81.7–100 % and 90.6–100 %, respectively, with NSP4 gene segment showing the most diversity among the strains. Bayesian analyses of all gene sequences to estimate the time of divergence of the lineage indicated that divergence times ranged from 16 to 44 years, except for the NSP4 gene where the lineage seemed to arise in the more distant past at an estimated 203 years ago. However, the long-term effects of changes found within the NSP4 genome segment should be further explored, and thus we recommend continued whole-genome analyses from larger sample sets to determine the evolutionary mechanisms of the DS-1-like strains collected in Africa.
Similar content being viewed by others
References
J.E. Tate, A.H. Burton, C. Boschi-Pinto, A.D. Steele, J. Duque, U.D. Parashar, WHO-coordinated Global Rotavirus Surveillance Network. 2008 estimate of worldwide rotavirus-associated mortality in children younger than 5 years before the introduction of universal rotavirus vaccination programmes: a systematic review and meta-analysis. Lancet Infect. Dis. 2, 136–141 (2012)
M.K. Estes, A.Z. Kapikian, in Fields Virology, ed. by D.M. Knipe (Lippincott Williams and Wilkins, Philadelphia, 2007), pp. 1917–1957
J. Matthijnssens, M. Ciarlet, E. Heiman, I. Arijs, T. Delbeke, S.M. McDonald, E.A. Palombo, M. Iturriza-Gómara, P. Maes, J.T. Patton, M. Rahman, M. Van Ranst, Full genome-based classification of rotaviruses reveals a common origin between human Wa-Like and porcine rotavirus strains and human DS-1-like and bovine rotavirus strains. J. Virol. 82, 3204–3219 (2008)
J. Matthijnssens, M. Ciarlet, M. Rahman, H. Attoui, K. Bányai, M.K. Estes, J.R. Gentsch, M. Iturriza-Gómara, C.D. Kirkwood, V. Martella, P.P. Mertens, O. Nakagomi, J.T. Patton, F.M. Ruggeri, L.J. Saif, N. Santos, A. Steyer, K. Taniguchi, U. Desselberger, M. van Ranst, Recommendations for the classification of group A rotaviruses using all 11 genomic RNA segments. Arch. Virol. 153, 1621–1629 (2008)
J. Matthijnssens, M. Ciarlet, S.M. McDonald, H. Attoui, K. Bányai, J.R. Brister, J. Buesa, M.D. Esona, M.K. Estes, J.R. Gentsch, M. Iturriza-Gómara, R. Johne, C.D. Kirkwood, V. Martella, P.P. Mertens, O. Nakagomi, V. Parreño, M. Rahman, F.M. Ruggeri, L.J. Saif, N. Santos, A. Steyer, K. Taniguchi, J.T. Patton, U. Desselberger, M. van Ranst, Uniformity of rotavirus strain nomenclature proposed by the Rotavirus Classification Working Group (RCWG). Arch. Virol. 156, 1397–1413 (2011)
K.C. Jere, M.D. Esona, Y.H. Ali, I. Peenze, S. Roy, M.D. Bowen, I.K. Saeed, A.I. Khalafalla, M.M. Nyaga, J.M. Mphahlele, D. Steele, M.L. Seheri, Novel NSP1 genotype characterised in an African camel G8P[11] rotavirus strain. Infect. Genet. Evol. 21, 58–66 (2014)
J. Matthijnssens, J. Bilcke, M. Ciarlet, V. Martella, K. Bányai, M. Rahman, M. Zeller, P. Beutels, P. van Damme, M. van Ranst, Rotavirus disease and vaccination: impact on genotype diversity. Future Microbiol. 10, 1303–1316 (2009)
E. Trojnar, J. Sachsenröder, S. Twardziok, J. Reetz, P.H. Otto, R. Johne, Identification of an avian group A rotavirus containing a novel VP4 gene with a close relationship to those of mammalian rotavirus. Curr. Opin. Virol. 4, 426–433 (2013)
J. Matthijnssens, M. van Ranst, Genotype constellation and evolution of group A rotaviruses infecting humans. Curr. Opin. Virol. 2, 426–433 (2012)
K. Bányai, B. László, J. Duque, A.D. Steele, E.A. Nelson, J.R. Gentsch, U.D. Parashar, Systematic review of regional and temporal trends in global rotavirus strain diversity in the pre rotavirus vaccine era: insights for understanding the impact of rotavirus vaccination programs. Vaccine 30, 122–130 (2012)
M.M. Nyaga, K.C. Jere, I. Peenze, L. Mlera, A.A. van Dijk, M.L. Seheri, M.J. Mphahlele, Sequence analysis of the whole genomes of five African human G9 rotavirus strains. Infect. Genet. Evol. 16, 62–77 (2013)
S. Matsuno, A. Hasegawa, A. Mukoyama, S. Inouye, A candidate for a new serotype of human rotavirus. J. Virol. 2, 623–624 (1985)
M.I. Adah, A. Rohwedder, O.D. Olaleye, H. Werchau, Sequence analysis of VP7 gene of two Nigerian rotavirus strains. Acta Virol. 40, 187–193 (1996)
N.A. Cunliffe, B.M. Ngwira, W. Dove, B.D. Thindwa, A.M. Turner, R.L. Broadhead, M.E. Molyneux, C.A. Hart, Epidemiology of rotavirus infection in children in Blantyre, Malawi, 1997-2007. J. Infect. Dis. 202, 168–174 (2010)
N.M. Kiulia, R. Kamenwa, G. Irimu, J.O. Nyangao, Z. Gatheru, A. Nyachieo, A.D. Steele, J.M. Mwenda, The epidemiology of human rotavirus associated with diarrhoea in Kenyan children: a review. J. Trop. Pediatr. 54, 401–405 (2008)
T. Nakagomi, Y.H. Doan, W. Dove, B. Ngwira, M. Iturriza-Gómara, O. Nakagomi, N.A. Cunliffe, G8 rotaviruses with conserved genotype constellations detected in Malawi over 10 years (1997-2007) display frequent gene reassortment among strains co-circulating in humans. J. Gen. Virol. 94, 1273–1295 (2013)
S. Ghosh, N. Kobayashi, Whole-genomic analysis of rotavirus strains: current status and future prospects. Future Microbiol. 9, 1049–1065 (2011)
K.C. Jere, L. Mlera, H.G. O’Neill, A.C. Potgieter, N.A. Page, M.L. Seheri, A.A. van Dijk, Whole genome analyses of African G2, G8, G9, and G12 rotavirus strains using sequence-independent amplification and 454® pyrosequencing. J. Med. Virol. 83, 2018–2042 (2011)
K. Bányai, B. László, J. Duque, A.D. Steele, E.A. Nelson, J.R. Gentsch, U.D. Parashar, Systematic review of regional and temporal trends in global rotavirus strain diversity in the pre rotavirus vaccine era: insights for understanding the impact of rotavirus vaccination programs. Vaccine 30, 22–30 (2012)
A. Djikeng, R. Halpin, R. Kuzmickas, J. Depasse, J. Feldblyum, N. Sengamalay, C. Afonso, X. Zhang, N.G. Anderson, E. Ghedin, D.J. Spiro, Viral genome sequencing by random priming methods. BMC Genomics 9, 5 (2008)
P. Maes, J. Matthijnssens, M. Rahman, M. van Ranst, 238. BMC Microbial 9, 238 (2009)
K. Tamura, D. Peterson, N. Peterson, G. Stecher, M. Nei, S. Kumar, MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731–2739 (2011)
J. Matthijnssens, E. Heylen, M. Zeller, M. Rahman, P. Lemey, M. Van Ranst, Phylodynamic analyses of rotavirus genotypes G9 and G12 underscore their potential for swift global spread. Mol. Biol. Evol. 27, 2431–2436 (2010)
A.J. Drummond, A. Rambaut, BEAST: bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 214 (2007)
J.M. Ball, D.M. Mitchell, T.F. Gibbons, R.D. Parr, Rotavirus NSP4: a multifunctional viral enterotoxin. Viral Immunol. 18, 27–40 (2005)
M.D. Esona, A. Geyer, N. Page, A. Trabelsi, I. Fodha, M. Aminu, V.A. Agbaya, B. Tsion, T.K. Kerin, G.E. Armah, A.D. Steele, R.I. Glass, J.R. Gentsch, Genomic characterization of human rotavirus G8 strains from the African rotavirus network: relationship to animal rotaviruses. J. Med. Virol. 81, 937–951 (2009)
J. Matthijnssens, M. Rahman, X. Yang, T. Delbeke, I. Arijs, J.P. Kabue, J.J. Muyembe, M. van Ranst, G8 rotavirus strains isolated in the Democratic Republic of Congo belong to the DS-1-like genogroup. J. Clin. Microbiol. 44, 1801–1809 (2006)
S. Ghosh, Z. Gatheru, J. Nyangao, N. Adachi, N. Urushibara, N. Kobayashi, Full genomic analysis of a G8P[1] rotavirus strain isolated from an asymptomatic infant in Kenya provides evidence for an artiodactyl-to-human interspecies transmission event. J. Med. Virol. 83, 367–376 (2011)
J. Nyangao, N. Page, M. Esona, I. Peenze, Z. Gatheru, P. Tukei, A.D. Steele, Characterization of human rotavirus strains from children with diarrhea in Nairobi and Kisumu, Kenya, between 2000 and 2002. J. Infect. Dis. 202, 187–192 (2010)
J.M. Mwenda, K.M. Ntoto, A. Abebe, C. Enweronu-Laryea, I. Amina, J. Mchomvu, A. Kisakye, E.M. Mpabalwani, I. Pazvakavambwa, G.E. Armah, L.M. Seheri, N.M. Kiulia, N. Page, M.A. Widdowson, A.D. Steele, Burden and epidemiology of rotavirus diarrhoea in selected African countries: preliminary results from the African Rotavirus Surveillance Network. J. Infect. Dis. 202, 5–11 (2010)
M. Seheri, L. Nemarude, I. Peenze, L. Netshifhefhe, M.M. Nyaga, H.G. Ngobeni, G. Maphalala, L.L. Maake, A.D. Steele, J.M. Mwenda, J.M. Mphahlele, Update of rotavirus strains circulating in Africa from 2007 through 2011. Pediatr. Infect. Dis. J. 1, 76–84 (2014)
S. Ghosh, N. Adachi, Z. Gatheru, J. Nyangao, D. Yamamoto, M. Ishino, N. Urushibara, N. Kobayashi, Whole-genome analysis reveals the complex evolutionary dynamics of Kenyan G2P[4] human rotavirus strains. J. Gen. Virol. 92, 2201–2208 (2011)
T.N. Tran, T. Nakagomi, O. Nakagomi, Evidence for genetic reassortment between human rotaviruses by full genome sequencing of G3P[4] and G2P[4] Strains co-circulating in India. Trop. Med. Health 41, 13–20 (2013)
M.M. Gómez, M.C. de Mendonça, M. Volotão Ede, L.F. Tort, M.F. da Silva, J. Cristina, J.P. Leite, Rotavirus A genotype P[4]G2: genetic diversity and reassortment events among strains circulating in Brazil between 2005 and 2009. J. Med. Virol. 83, 1093–1106 (2011)
M.D. Esona, S. Mijatovic-Rustempasic, K. Foytich, S. Roy, K. Banyai, G.E. Armah, A.D. Steele, E.M. Volotão, M.M. Gomez, M.F. Silva, R. Gautam, O. Quaye, K.I. Tam, J.C. Forbi, M. Seheri, N. Page, J. Nyangao, V.N. Ndze, M. Aminu, M.D. Bowen, J.R. Gentsch, Human G9P[8] rotavirus strains circulating in Cameroon, 1999–2000: genetic relationships with other G9 strains and detection of a new G9 subtype. Infect. Genet. Evol. 18, 315–324 (2013)
M. Zhang, C.Q. Zeng, Y. Dong, J.M. Ball, L.J. Saif, A.P. Morris, M.K. Estes, Mutations in rotavirus nonstructural glycoprotein NSP4 are associated with altered virus virulence. J. virol. 72, 3666–3672 (1998)
Acknowledgments
This project was funded by the South African Medical Research Council, the Poliomyelitis Research Foundation in South Africa, and federal funds from the National Institute of Allergy and Infectious Diseases, National Institutes of Health, Department of Health and Human Services under contract number HHSN272200900007C. We thank Lorens Maake, Kebareng Rakau, Nonkululeko Magagula and Ina Peenze for technical assistance at the MRC/Diarrhoeal Pathogens Research Unit. We also thank the Virology Group at the JCVI, especially Asmik Akopov, Nadia Fedorova and Susmita Shrivastava for their technical assistance in the laboratory and bioinformatics support. In addition, we thank all of the sample collection teams from the different countries that were involved in this study.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Nyaga, M.M., Stucker, K.M., Esona, M.D. et al. Whole-genome analyses of DS-1-like human G2P[4] and G8P[4] rotavirus strains from Eastern, Western and Southern Africa. Virus Genes 49, 196–207 (2014). https://doi.org/10.1007/s11262-014-1091-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11262-014-1091-7