Accumulated metagenomic studies reveal recent migration, whole genome evolution, and taxonomic incompleteness of orthomyxoviruses

Abstract

AbstractMetagenomic studies have uncovered an abundance of novel viruses by looking beyond hosts of obvious public health or economic interest. The discovery of conserved genes in viruses infecting geographically and phylogenetically diverse hosts has provided important evolutionary context for human and animal pathogens. However, the resulting viral genomes are often incomplete, and analyses largely characterize the distribution of viruses over their dynamics. Here, we show how the accumulated data of metagenomic studies can be integrated to reveal geographic and evolutionary dynamics in a case study ofOrthomyxoviridae, the family of RNA viruses containing influenza virus. First, we use sequences of the orthomyxovirid Wǔhàn mosquito virus 6 to track the global migrations of its host. We then look at overall orthomyxovirus genome evolution, finding significant gene gain and loss across members of the family, especially in the surface proteins responsible for cell and host tropism. We find that the surface protein of Wǔhàn mosquito virus 6 exhibits accelerated non-synonymous evolution suggestive of antigenic evolution, and an entire quaranjavirid group bearing highly diverged surface proteins. Finally we quantify the progress of orthomyxovirus discovery and forecast that many highly divergedOrthomyxoviridaemembers remain to be found. We argue that continued metagenomic studies will be fruitful for understanding the dynamics, evolution, ecology of viruses and their hosts, regardless of whether novel viruses are actually identified or not, as long as study designs allowing for the resolution of complete viral genomes are employed.