Structural and molecular biology of Acheta domesticus segmented densovirus, the first parvovirus to harbor a bipartite genome

Parvoviruses (family Parvoviridae) are defined by their linear monopartite ssDNA genome, T=1 icosahedral capsid, and distinct structural (VP) and non-structural (NS) protein expression cassettes within their genome. Here, we report the first parvovirus with a segmented genome, Acheta domesticus segmented densovirus (AdSDV), a house cricket (Acheta domesticus) pathogen. The AdSDV harbors its NS and VP cassettes on two separate segmented genomes. Its VP segment acquired a phospholipase A2-encoding gene via inter-subfamily recombination, which is absent from its capsid. The AdSDV evolved a transcription profile in response to its multipartite replication strategy that has diverged from its Brevihamaparvovirus ancestors. Furthermore, AdSDV assembles three capsid populations, which package one genome segment per particle. The cryoEM structures of these three capsids (2.3 to 3.3 [A] resolution) reveal a genome packaging mechanism, which differs from other parvoviruses. This study provides a new perspective on ssDNA genome segmentation and on the plasticity of parvovirus biology.