Genomic characterization of arboviruses discovered between the 1950s and 1980s

Arthropod-borne viruses (arboviruses) pose a major threat to global public health, impacting both human and animal health. Genomic characterization is important for arboviruses because it allows for an understanding of their evolution and improves timely outbreak and epidemic response. In this study, we used high-throughput sequencing and computational analyses to characterize the genomes and evolution of 46 previously unsequenced or partially sequenced arbovirus isolates collected across 23 countries between 1954 and 1984. Our analyses revealed that these viruses belong to 11 genera in eight viral families, including Sedoreoviridae (n = 26), Peribunyaviridae (n = 12), Rhabdoviridae (n = 3), Spinareoviridae (n = 1), Phenuiviridae (n=1), Togaviridae (n=1), Flaviviridae (n=1), and Nairoviridae (n = 1). Based on our genomic and evolutionary characterization, we propose 15 novel arbovirus species, including six that are likely mosquito-borne, six likely tick-borne, and three isolated from birds, lizards, and humans. Furthermore, we found that the Ossa virus (genus Orthobunyavirus) is a reassortant, possessing a unique M segment and S and L segments derived from the Madrid virus (Orthobunyavirus madridense), while the Brus Laguna virus (Orthobunyavirus gamboaense) exhibits an M segment derived from the Alajuela virus (Orthobunyavirus gamboaense). Additionally, our viral genome composition-based analysis indicates that Lanjan, Zingilamo, Tindholmur (Orbivirus magninsulae), and Bauline viruses (Orbivirus magninsulae) have a high likelihood of producing human infection, suggesting the risk of emergence and indicating the need for further experimental investigation. Collectively, our findings contribute to the understanding of arbovirus diversity, evolution, and taxonomy, providing a valuable genomic resource for future research on arbovirus biology and emergence potential.IMPORTANCEGenomic data can reveal critical insights into virus ecology and evolution and become critical to viral surveillance systems. In the last decades, advancements in genomic technology have significantly expanded the discovery of new viruses. However, many arthropod-borne viruses (arboviruses) isolated before the genomic era lack sequencing information, which limits our understanding of their impact on human and animal health. In this study, we sequenced 46 previously unsequenced or partially sequenced arbovirus isolates collected from 23 countries between the 1950s and 1980s. Next, we conducted a comprehensive genomic and evolutionary characterization, which revealed that these viruses belong to 11 genera across eight viral families. Our findings expand the genomic data of arboviruses, which can be used for the development of detection methods and contribute to a better understanding of their diversity, evolution, taxonomy, and pathogenic potential.