Culicoides -Specific Fitness Increase of Vesicular Stomatitis Virus in Insect-to-Insect Infections.

Simple Summary: Vesicular stomatitis virus (VSV) infects cows, horses, and pigs, economically impacting livestock producers due to animal production losses, quarantines, and animal movement/trade restrictions. Typically, VSV is transmitted from animal to animal by direct contact, but it is also transmitted by insects such as Culicoides biting midges. These tiny flies can ingest virus particles when blood feeding on an infected animal, multiply them inside their bodies, and then transmit them to other animals the next time they feed. In addition, midges are also able to pass the virus from one to another with extremely high efficiency when they mate, even though they carry very little virus in their bodies. Through this mechanism, VSV may be maintained and overwinter in midges and appear again in livestock the next summer once the insects start feeding on blood again. Our research shows that one reason midges can transmit VSV to other midges so efficiently is because viruses that come from insect cells have an increased ability to infect more insect cells. This helps explain the midge-to-midge infection efficiency and highlights the importance of Culicoides midges in VSV maintenance and transmission. Vesicular stomatitis virus (VSV) is an arthropod-borne virus affecting livestock. In the United States, sporadic outbreaks result in significant economic losses. During epizootics, Culicoides biting midges are biological vectors and key to the geographic expansion of outbreaks. Additionally, Culicoides may play a role in VSV overwintering because females and males are capable of highly efficient venereal transmission, despite their relatively low virus titers. We hypothesized that VSV propagated within a midge has increased fitness for subsequent midge infections. To evaluate the potential host-specific fitness increase, we propagated three viral isolates of VSV in porcine skin fibroblasts and Culicoides cell lines. We then evaluated the viral infection dynamics of the different cell-source groups in Culicoides sonorensis. Our results indicate that both mammalian- and insect-derived VSV replicate well in midges inoculated via intrathoracic injection, thereby bypassing the midgut barriers. However, when the virus was required to infect and escape the midgut barrier to disseminate after oral acquisition, the insect-derived viruses had significantly higher titers, infection, and dissemination rates than mammalian-derived viruses. Our research suggests that VSV replication in Culicoides cells increases viral fitness, facilitating midge-to-midge transmission and subsequent replication, and further highlights the significance of Culicoides midges in VSV maintenance and transmission dynamics. [ABSTRACT FROM AUTHOR]