Fungal DNA virus infects a mycophagous insect and utilizes it as a transmission vector

Abstract

Mycoviruses are usually transmitted horizontally via hyphal anastomosis and vertically via sexual/asexual spores. Previously, we reported that a gemycircularvirus, Sclerotinia sclerotiorum hypovirulence-associated DNA virus 1 (SsHADV-1), could infect its fungal host extracellularly. Here, we discovered that SsHADV-1 could infect a mycophagous insect, Lycoriella ingenua, and use it as a transmission vector. Virus acquired by larvae feeding on colonies of a virus-infected strain of S. sclerotiorum was replicated and retained in larvae, pupae, adults, and eggs. Virus could be transmitted to insect offspring when larvae were injected with virus particles and allowed to feed on a nonhost fungus. Virus replication in insect cells was further confirmed by inoculating Spodoptera frugiperda cells with virus particles and analyzing with RT-PCR, Northern blot, immunofluorescence, and flow cytometry assays. Larvae could transmit virus once they acquired virus by feeding on virus-infected fungal colony. Offspring larvae hatched from viruliferous eggs were virus carriers and could also successfully transmit virus. Virus transmission between insect and fungus also occurred on rapeseed plants. Virus-infected isolates produced less repellent volatile substances to attract adults of L. ingenua. Furthermore, L. ingenua was easily observed on Sclerotinia lesions in rapeseed fields, and viruliferous adults were captured from fields either sprayed with a virus-infected fungal strain or nonsprayed. Our findings may facilitate the exploration of mycoviruses for control of fungal diseases and enhance our understanding of the ecology of SsHADV-1 and other newly emerging SsHADV-1–like viruses, which were recently found to be widespread in various niches including human HIV-infected blood, human and animal feces, insects, plants, and even sewage. Significance Sclerotinia sclerotiorum hypovirulence-associated DNA virus 1 (SsHADV-1) was originally isolated from a fungal pathogen; recent research revealed that SsHADV-1–like viruses are widespread in various niches including human tissues. Here, we discovered that SsHADV-1 could infect a mycophagous insect, Lycoriella ingenua, when larvae fed on virus-infected fungus; and viruliferous adults could transmit SsHADV-1 transovarially. We further found that SsHADV-1–infected fungus could suppress the production of repellent volatile substances to attract adults to lay eggs on its colony and that virus infection could stimulate female adults to produce more eggs. Our findings may facilitate the exploration of mycoviruses to control fungal diseases and suggest that insects may play an important role in the transmission and distribution of these newly emerging viruses.