Genome Sequencing of the Behavior Manipulating Virus LbFV Reveals a Possible New Virus Family

Abstract

Parasites are sometimes able to manipulate the behavior of their hosts. However, the molecular cues underlying this phenomenon are poorly documented. We previously reported that the parasitoid wasp Leptopilina boulardi which develops from Drosophila larvae is often infected by an inherited DNA virus. In addition to being maternally transmitted, the virus benefits from horizontal transmission in superparasitized larvae (Drosophila that have been parasitized several times). Interestingly, the virus forces infected females to lay eggs in already parasitized larvae, thus increasing the chance of being horizontally transmitted. In a first step towards the identification of virus genes responsible for the behavioral manipulation, we present here the genome sequence of the virus, called LbFV. The sequencing revealed that its genome contains an homologous repeat sequence (hrs) found in eight regions in the genome. The presence of this hrs may explain the genomic plasticity that we observed for this genome. The genome of LbFV encodes 108 ORFs, most of them having no homologs in public databases. The virus is however related to Hytrosaviridae, although distantly. LbFV may thus represent a member of a new virus family. Several genes of LbFV were captured from eukaryotes, including two anti-apoptotic genes. More surprisingly, we found that LbFV captured from an ancestral wasp a protein with a Jumonji domain. This gene was afterwards duplicated in the virus genome. We hypothesized that this gene may be involved in manipulating the expression of wasp genes, and possibly in manipulating its behavior.

A behavior-manipulating virus relative as a source of adaptive genes for parasitoid wasps

“…these genes have probably been acquired horizontally by the virus from an ancestral insect before the Leptopilina diversification ( [40], Fig. S1 & 2A).…”

“…Two of them (ORFs 27 and 66) are predicted to encode inhibitors of apoptosis, whereas ORFs 11 and 13 encode a putative demethylase [40]. These two last genes may derive from a single horizontal transfer followed by a subsequent gene duplication [40]. In the following section, we will focus on the second class of genes identified by this blast analysis.…”

“…Second, the previous studies repeatedly identified nudiviruses as the donor family. Here we identify a virus belonging to another, possibly new, virus family [40]. This virus is related to nudiviruses and baculoviruses, but is more closely related to the hytrosaviruses [2], which are known to induce Salivary Gland Hypertrophy in tsetse flies and house flies, although it can also remain symptom-less [1].…”

“…We show that a close relative of the ancestral donor virus is still segregating in the species L. boulardi and its biology has been extensively studied by our group [45][54] [46] [40] [66]. The virus, known as LbFV, belongs to a possibly new dsDNA virus family related to Hytrosaviridae, and more distantly related to Nudiviridae and Baculoviridae [40]. The virus is vertically transmitted and manipulates the wasp behaviour by forcing infected females to lay their eggs into already parasitized larvae.…”

Long-read genome sequencing and assembly ofLeptopilina boulardi: a specialistDrosophilaparasitoid

“…6 causes the females to lay eggs in an already parasitized host (superparasitism). Thereby favoring 116 its transmission, and indirectly helping the parasitoid dodge the immune system of the host 117 (Julien Varaldi et al 2003Varaldi et al , 2009Lepetit et al 2017; J. Varaldi and Lepetit 2018;Martinez et al 118 2012; Patot et al 2012Patot et al , 2009.…”