Extended in vivo transcriptomes of two ascoviruses with different tissue tropisms reveal alternative mechanisms for enhancing virus reproduction in hemolymph

Heba A H Zaghloul,Robert H Hice,Dennis K Bideshi,Peter Arensburger,Brian A Federici

doi:10.1038/s41598-021-95553-y

Abstract

Ascoviruses are large dsDNA viruses characterized by the extraordinary changes they induce in cellular pathogenesis and architecture whereby after nuclear lysis and extensive hypertrophy, each cell is cleaved into numerous vesicles for virion reproduction. However, the level of viral replication and transcription in vesicles compared to other host tissues remains uncertain. Therefore, we applied RNA-Sequencing to compare the temporal transcriptome of Spodoptera frugiperda ascovirus (SfAV) and Trichoplusia ni ascovirus (TnAV) at 7, 14, and 21 days post-infection (dpi). We found most transcription occurred in viral vesicles, not in initial tissues infected, a remarkably novel reproduction mechanism compared to all other viruses and most other intracellular pathogens. Specifically, the highest level of viral gene expression occurred in hemolymph, for TnAV at 7 dpi, and SfAV at 14 dpi. Moreover, we found that host immune genes were partially down-regulated in hemolymph, where most viral replication occurred in highly dense accumulations of vesicles.

Highlights

Ascoviruses are large dsDNA viruses characterized by the extraordinary changes they induce in cellular pathogenesis and architecture whereby after nuclear lysis and extensive hypertrophy, each cell is cleaved into numerous vesicles for virion reproduction
Genomes typically vary from 157 kbp for Spodoptera frugiperda ascovirus 1a, to as much as 190 kbp for Trichoplusia ni ascovirus 2a and Heliothis virescens ascovirus 3 a4
The remarkably unique changes in cell architecture directed by ascoviruses summarized in Fig. 1 lead to nascent vesicles that spill into the hemolymph where progeny virions continue to be produced as the vesicles circulate and grow (Fig. 2)

Summary

Introduction

Ascoviruses are large dsDNA viruses characterized by the extraordinary changes they induce in cellular pathogenesis and architecture whereby after nuclear lysis and extensive hypertrophy, each cell is cleaved into numerous vesicles for virion reproduction. The structure and biochemical composition of their virions, transmission, and pathology at the tissue and cellular level were initially characterized during the 1 980s1–4 Their virions are large (100 × 400 nm), bacilliform to reniform with a highly reticulate outer membrane surrounding an internal particle consisting of a second membrane that envelops the protein/dsDNA genome. Typical insect viruses like baculoviruses and cytoplasmic polyhedrosis viruses, are highly infectious by feeding, but ascoviruses are not Instead, they are transmitted mechanically on the ovipositor of parasitoid wasps during oviposition[14,15,16]. Most RNA viruses of plants and animals replicate exclusively in the cytoplasm[19], whereas replication of DNA viruses such as adenoviruses, baculoviruses, herpesviruses, and parvoviruses occurs in the nucleus[20] without nuclear lysis until cell death

Methods

Results

Conclusion