Abstract
Genetic reassortments occurred continuously among multiple subtypes or genotypes of influenza viruses prevalent in pigs. Of note, some reassortant viruses bearing the internal genes of the 2009 pandemic H1N1 (2009/H1N1) virus sporadically caused human infection, which highlights their potential threats to human public health. In this study, we performed phylogenetic analysis on swine influenza viruses (SIVs) circulating in Liaoning Province, China. A total of 22 viruses, including 18 H1N1 and 4 H1N2 viruses, were isolated from 5,750 nasal swabs collected from pigs in slaughterhouses from 2014 to 2016. H1N1 viruses formed four genotypes, which included Eurasian avian-like H1N1 (EA H1N1) and double/triple reassortant H1N1 derived from EA H1N1, 2009/H1N1, and triple reassortant H1N2 (TR H1N2) viruses. H1N1 SIVs with different genotypes and even those within the same genotypes represented different pathogenicities in mice. We further characterized two naturally isolated H1N1 SIVs that had similar viral genomes but differed substantially in their virulence in mice and found that a single amino acid at position 431 in the basic polymerase 2 (PB2) protein significantly affected the viral replication capacity and virulence of these two viruses. Taken together, our findings revealed the diverse genomic origins and virulence of the SIVs prevalent in Liaoning Province during 2014 to 2016, which highlights that continuous surveillance is essential to monitor the evolution of SIVs. We identified a naturally occurring amino acid mutation in the PB2 protein of H1N1 SIVs that impacts the viral replication and virulence in mice by altering the viral polymerase activity.IMPORTANCE The frequent reassortment among different influenza viruses in pigs adds complexity to the epidemiology of swine influenza. The diverse viral virulence phenotypes underline the need to investigate the possible genetic determinants for evaluating the pandemic potential to human public health. Here, we found that multiple genotypes of influenza viruses cocirculate in the swine population in Liaoning Province, China. Furthermore, we pinpointed a single amino acid at position 431 in the PB2 protein which plays a critical role in the virulence of H1N1 viruses in mice and found that the alteration of viral polymerase activities is the cause of the different virulence. Our study further indicated that the virulence of influenza virus is a polygenic trait, and the newly identified virulence-related residue in the PB2 provides important information for broadening knowledge on the genetic basis of viral virulence of influenza viruses.
Highlights
Genetic reassortments occurred continuously among multiple subtypes or genotypes of influenza viruses prevalent in pigs
To characterize the gene segments of these viruses, we constructed unrooted phylogenetic trees using the gene sequences of 247 H1N1 reference strains previously isolated in mainland China, which were downloaded from the global initiative on sharing all influenza data (GISAID) until July 2019
The genetic trees constructed for the basic polymerase 1 (PB1) and acidic polymerase (PA) genes were similar to that for the PB2 gene, which showed that 11 H1N1 and 4 H1N2 viruses clustered into the 2009/H1N1 lineage and 7 H1N1 viruses clustered into the Eurasian avian-like H1N1 (EA H1N1) lineage (Fig. 2C and D)
Summary
Genetic reassortments occurred continuously among multiple subtypes or genotypes of influenza viruses prevalent in pigs. Our findings revealed the diverse genomic origins and virulence of the SIVs prevalent in Liaoning Province during 2014 to 2016, which highlights that continuous surveillance is essential to monitor the evolution of SIVs. We identified a naturally occurring amino acid mutation in the PB2 protein of H1N1 SIVs that impacts the viral replication and virulence in mice by altering the viral polymerase activity. Sporadic human infections of endemic and novel reassortant SIVs [21,22,23,24,25,26,27] and the seropositivity of at-risk populations, such as swine workers [28,29,30], underscore the importance of influenza surveillance in pigs. We investigated the molecular determinants of two genetically similar viruses showing different virulence in mice and explored the possible underlying mechanism
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