Culicoides-specific fitness increase of vesicular stomatitis virus in insect-to-insect infections

Authors: ROZO-LOPEZ, PAULA - University Of Tennessee; Drolet, Barbara

Submitted to: Insects
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/3/2023
Publication Date: 1/5/2023
Citation: Rozo-Lopez, P., Drolet, B.S. 2023. Culicoides-specific fitness increase of vesicular stomatitis virus in insect-to-insect infections. Insects. 15(1):34-47. https://doi.org/10.3390/insects15010034.
DOI: https://doi.org/10.3390/insects15010034

Interpretive 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 on a premises by direct contact, but it is also transmitted by insects such as Culicoides biting midges. These tiny flies can take a few viruses when feeding on blood, multiply them inside of 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 when they mate with extremely high efficiency, 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 again. Our research shows that one reason midges can transmit VSV to other midges so efficiently is that 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 also highlights the importance of Culicoides midges in VSV maintenance and transmission.

Technical Abstract: Vesicular stomatitis virus (VSV) is an arthropod-borne virus affecting livestock. In the United States, sporadic outbreaks result in significant economic losses. During outbreaks, Culicoides biting midges are biological vectors and key to 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 vectors have increased fitness for subsequent midge infections. To evaluate the potential host-specific fitness increase, we propagated three viral isolates of VSV in porcine epidermal and Culicoides cell lines. We then evaluated the infection dynamics of the different cell-sourced groups in Culicoides sonorensis. Our results indicate that both mammalian- and in-sect-derived VSV replicate well in midges inoculated via intrathoracic injection, thereby bypassing the midgut barriers. However, when 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 for efficient midge-to-midge transmission and subsequent replication. Additionally, our study emphasizes the significance of Culicoides in VSV maintenance and transmission dynamics.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.