Molecular epidemiology and genetic evolution of the whole genome of G3P[8] human rotavirus in Wuhan, China, from 2000 through 2013

PLoS One. 2014 Mar 27;9(3):e88850. doi: 10.1371/journal.pone.0088850. eCollection 2014.

Abstract

Background: Rotaviruses are a major etiologic agent of gastroenteritis in infants and young children worldwide. Since the latter of the 1990s, G3 human rotaviruses referred to as "new variant G3" have emerged and spread in China, being a dominant genotype until 2010, although their genomic evolution has not yet been well investigated.

Methods: The complete genomes of 33 G3P[8] human rotavirus strains detected in Wuhan, China, from 2000 through 2013 were analyzed. Phylogenetic trees of concatenated sequences of all the RNA segments and individual genes were constructed together with published rotavirus sequences.

Results: Genotypes of 11 gene segments of all the 33 strains were assigned to G3-P[8]-I1-R1-C1-M1-A1-N1-T1-E1-H1, belonging to Wa genogroup. Phylogenetic analysis of the concatenated full genome sequences indicated that all the modern G3P[8] strains were assigned to Cluster 2 containing only one clade of G3P[8] strains in the US detected in the 1970s, which was distinct from Cluster 1 comprising most of old G3P[8] strains. While main lineages of all the 11 gene segments persisted during the study period, different lineages appeared occasionally in RNA segments encoding VP1, VP4, VP6, and NSP1-NSP5, exhibiting various allele constellations. In contrast, only a single lineage was detected for VP7, VP2, and VP3 genes. Remarkable lineage shift was observed for NSP1 gene; lineage A1-2 emerged in 2007 and became dominant in 2008-2009 epidemic season, while lineage A1-1 persisted throughout the study period.

Conclusion: Chinese G3P[8] rotavirus strains have evolved since 2000 by intra-genogroup reassortment with co-circulating strains, accumulating more reassorted genes over the years. This is the first large-scale whole genome-based study to assess the long-term evolution of common human rotaviruses (G3P[8]) in an Asian country.

Publication types

  • Historical Article
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Substitution
  • China / epidemiology
  • Evolution, Molecular*
  • Gene Frequency
  • Genes, Viral
  • Genetic Variation
  • Genome, Viral*
  • Genotype
  • History, 21st Century
  • Humans
  • Phenotype
  • Phylogeny
  • Prevalence
  • RNA, Viral
  • Rotavirus / classification
  • Rotavirus / genetics*
  • Rotavirus Infections / epidemiology*
  • Rotavirus Infections / history
  • Rotavirus Infections / virology*
  • Seasons
  • Sequence Analysis, DNA
  • Spatio-Temporal Analysis

Substances

  • RNA, Viral

Grants and funding

The work was funded by the National Natural Science Foundation of China (Grant no. 81071352), and the fund for experts of Wuhan municipality to Yuan-Hong Wang, and the Grant-in-Aid for Scientific Research (Grant no. 25305022) from the Japan Society for the Promotion of Science, and the Grant-in-Aid for Research on Emerging and Re-emerging Infectious Diseases (grant H25-shinkou-ippan-005) by the Ministry of Health, Labour and Welfare, Japan to NK. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.