Discovery of a Novel Double-Stranded DNA Virus Reveals its Long-term Co-evolution with Ants

Large double-stranded DNA (dsDNA) viruses have been shown to have a wide host range in insects. However, their infection in ants has not yet been described. In this study, a novel filamentous virus, Camponotus japonicus labial gland disease virus (CjLGDV), was identified in the enlarged labial gland of Camponotus japonicus. By transmission electron microscopy, the nucleus of infected labial gland cell was shown to be full of non-enveloped nucleocapsids, and enveloped virus particles were observed in the cytoplasm. Genome sequencing analysis shows that CjLGDV possesses a circular dsDNA genome of 142 kb. By sequence alignment, a CjLGDV-like viral genome was found in Anoplolepis gracilipes, and conservation of gene synteny was observed between CjLGDV and the CjLGDV-like virus. Phylogenetic analysis suggests that CjLGDV and CjLGDV-like virus represent two members of a novel virus family, distantly related to unclassified Apis mellifera filamentous virus and Apis mellifera filamentous-like virus. These viruses have common genomic characteristics and key conserved genes with the viral members in the order Lefavirales, class Naldaviricetes. By mining public databases, CjLGDV-related endogenous viral elements (EVEs) were detected in the genome of multiple ant species, and phylogenetic analysis indicated a long-term coevolutionary relationship between the EVEs and its host. These findings expand the known lineage of nuclear arthropod large DNA viruses (NALDVs), broaden our understanding of their host range, and reveal a long and frequent interaction history between CjLGDV and its ant hosts.