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Genetic Lineage and Reassortment of Influenza C Viruses Circulating between 1947 and 2014.

ABSTRACT: Since influenza C virus was first isolated in 1947, the virus has been only occasionally isolated by cell culture; there are only four strains for which complete genome sequences are registered. Here, we analyzed a total of 106 complete genomes, ranging from the first isolate from 1947 to recent isolates from 2014, to determine the genetic lineages of influenza C virus, the reassortment events, and the rates of nucleotide substitution. The results showed that there are six lineages, named C/Taylor, C/Mississippi, C/Aichi, C/Yamagata, C/Kanagawa, and C/Sao Paulo. They contain both antigenic and genetic lineages of the hemagglutinin-esterase (HE) gene, and the internal genes PB2, PB1, P3, NP, M, and NS are divided into two major lineages, a C/Mississippi/80-related lineage and a C/Yamagata/81-related lineage. Reassortment events were found over the entire period of 68 years. Several outbreaks of influenza C virus between 1990 and 2014 in Japan consisted of reassortant viruses, suggesting that the genomic constellation is related to influenza C virus epidemics. The nucleotide sequences were highly homologous to each other. The minimum percent identity between viruses ranged from 91.1% for the HE gene to 96.1% for the M gene, and the rate of nucleotide substitution for the HE gene was the highest, at 5.20 × 10(-4) substitutions/site/year. These results indicate that reassortment is an important factor that increases the genetic diversity of influenza C virus, resulting in its ability to prevail in humans. IMPORTANCE Influenza C virus is a pathogen that causes acute respiratory illness in children and results in hospitalization of infants. We previously demonstrated (Y. Matsuzaki et al., J Clin Virol 61:87-93, 2014, http://dx.doi.org/10.1016/j.jcv.2014.06.017) that periodic epidemics of this virus occurred in Japan between 1996 and 2014 and that replacement of the dominant antigenic group occurred every several years as a result of selection by herd immunity. However, the antigenicity of the HE glycoprotein is highly stable, and antigenic drift has not occurred for at least 30 years. Here, we analyzed a total of 106 complete genomes spanning 68 years for the first time, and we found that influenza C viruses are circulating worldwide while undergoing reassortment as well as selection by herd immunity, resulting in an increased ability to prevail in humans. The results presented in this study contribute to the understanding of the evolution, including reassortment events, underlying influenza C virus epidemics.

SUBMITTER: Matsuzaki Y

PROVIDER: S-EPMC5008092 | biostudies-literature | 2016 Sep

REPOSITORIES: biostudies-literature

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Genetic Lineage and Reassortment of Influenza C Viruses Circulating between 1947 and 2014.

Matsuzaki Yoko Y Sugawara Kanetsu K Furuse Yuki Y Shimotai Yoshitaka Y Hongo Seiji S Oshitani Hitoshi H Mizuta Katsumi K Nishimura Hidekazu H

Journal of virology 20160826 18

Since influenza C virus was first isolated in 1947, the virus has been only occasionally isolated by cell culture; there are only four strains for which complete genome sequences are registered. Here, we analyzed a total of 106 complete genomes, ranging from the first isolate from 1947 to recent isolates from 2014, to determine the genetic lineages of influenza C virus, the reassortment events, and the rates of nucleotide substitution. The results showed that there are six lineages, named C/Tayl ...[more]

PMID: 27384661

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Project description:UNLABELLED:Influenza A(H3N2) viruses became widespread in humans during the 1968 H3N2 virus pandemic and have been a major cause of influenza epidemics ever since. These viruses evolve continuously by reassortment and genomic evolution. Antigenic drift is the cause for the need to update influenza vaccines frequently. Using two data sets that span the entire period of circulation of human influenza A(H3N2) viruses, it was shown that influenza A(H3N2) virus evolution can be mapped to 13 antigenic clusters. Here we analyzed the full genomes of 286 influenza A(H3N2) viruses from these two data sets to investigate the genomic evolution and reassortment patterns. Numerous reassortment events were found, scattered over the entire period of virus circulation, but most prominently in viruses circulating between 1991 and 1998. Some of these reassortment events persisted over time, and one of these coincided with an antigenic cluster transition. Furthermore, selection pressures and nucleotide and amino acid substitution rates of all proteins were studied, including those of the recently discovered PB1-N40, PA-X, PA-N155, and PA-N182 proteins. Rates of nucleotide and amino acid substitutions were most pronounced for the hemagglutinin, neuraminidase, and PB1-F2 proteins. Selection pressures were highest in hemagglutinin, neuraminidase, matrix 1, and nonstructural protein 1. This study of genotype in relation to antigenic phenotype throughout the period of circulation of human influenza A(H3N2) viruses leads to a better understanding of the evolution of these viruses. IMPORTANCE:Each winter, influenza virus infects approximately 5 to 15% of the world's population, resulting in significant morbidity and mortality. Influenza A(H3N2) viruses evolve continuously by reassortment and genomic evolution. This leads to changes in antigenic recognition (antigenic drift) which make it necessary to update vaccines against influenza A(H3N2) viruses frequently. In this study, the relationship of genetic evolution to antigenic change spanning the entire period of A(H3N2) virus circulation was studied for the first time. The results presented in this study contribute to a better understanding of genetic evolution in correlation with antigenic evolution of influenza A(H3N2) viruses.

Project description:Biological diversity has long been used to measure ecological health. While evidence exists from many ecosystems that declines in host biodiversity may lead to greater risk of disease emergence, the role of pathogen diversity in the emergence process remains poorly understood. Particularly, because a more diverse pool of pathogen types provides more ways in which evolutionary innovations may arise, we suggest that host-pathogen systems with high pathogen diversity are more prone to disease emergence than systems with relatively homogeneous pathogen communities. We call this prediction the diversity-emergence hypothesis. To show how this hypothesis could be tested, we studied a system comprised of North American shorebirds and their associated low-pathogenicity avian influenza (LPAI) viruses. These viruses are important as a potential source of genetic innovations in influenza. A theoretical contribution of this study is an expression predicting the rate of viral subtype reassortment to be proportional to both prevalence and Simpson's Index, a formula that has been used traditionally to quantify biodiversity. We then estimated prevalence and subtype diversity in host species at Delaware Bay, a North American AIV hotspot, and used our model to extrapolate from these data. We estimated that 4 to 39 virus subtypes circulated at Delaware Bay each year between 2000 and 2008, and that surveillance coverage (percentage of co-circulating subtypes collected) at Delaware Bay is only about 63.0%. Simpson's Index in the same period varied more than fourfold from 0.22 to 0.93. These measurements together with the model provide an indirect, model-based estimate of the reassortment rate. A proper test of the diversity-emergence hypothesis would require these results to be joined to independent and reliable estimates of reassortment, perhaps obtained through molecular surveillance. These results suggest both that subtype diversity (and therefore reassortment) varies from year to year and that several subtypes contributing to reassortment are going undetected. The similarity between these results and more detailed studies of one host, ruddy turnstone (Arenaria interpres), further suggests that this species may be the primary host for influenza reassortment at Delaware Bay. Biological diversity has long been quantified using Simpson's Index. Our model links this formula to a mechanistic account of reassortment in multipathogen systems in the form of subtype diversity at Delaware Bay, USA. As a theory of how pathogen diversity may influence the evolution of novel pathogens, this work is a contribution to the larger project of understanding the connections between biodiversity and disease.

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Genetic Lineage and Reassortment of Influenza C Viruses Circulating between 1947 and 2014.

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Genetic Lineage and Reassortment of Influenza C Viruses Circulating between 1947 and 2014.

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