Bracoviruses Contain a Large Multigene Family Coding for Protein Tyrosine Phosphatases

Abstract

The relationship between parasitic wasps and bracoviruses constitutes one of the few known mutualisms between viruses and eukaryotes. The virions produced in the wasp ovaries are injected into host lepidopteran larvae, where virus genes are expressed, allowing successful development of the parasite by inducing host immune suppression and developmental arrest. Bracovirus-bearing wasps have a common phylogenetic origin, and contemporary bracoviruses are hypothesized to have been inherited by chromosomal transmission from a virus that originally integrated into the genome of the common ancestor wasp living 73.7 ؎ 10 million years ago. However, so far no conserved genes have been described among different braconid wasp subfamilies. Here we show that a gene family is present in bracoviruses of different braconid wasp subfamilies (Cotesia congregata, Microgastrinae, and Toxoneuron nigriceps, Cardiochilinae) which likely corresponds to an ancient component of the bracovirus genome that might have been present in the ancestral virus. The genes encode proteins belonging to the protein tyrosine phosphatase family, known to play a key role in the control of signal transduction pathways. Bracovirus protein tyrosine phosphatase genes were shown to be expressed in different tissues of parasitized hosts, and two protein tyrosine phosphatases were produced with recombinant baculoviruses and tested for their biochemical activity. One protein tyrosine phosphatase is a functional phosphatase. These results strengthen the hypothesis that protein tyrosine phosphatases are involved in virally induced alterations of host physiology during parasitism.

PTP-H2 and PTP-H3 from Microplitis demolitor Bracovirus Localize to Focal Adhesions and Are Antiphagocytic in Insect Immune Cells

“…In contrast, no experimental data prior to the present study indicate whether PTP-like genes encoded by PDVs function as virulence factors (12,13,44,60,62). Our previous studies indicate that MdBV immunosuppresses insects by inhibiting several effector functions, including adhesion and phagocytosis by immune cells.…”

“…These subtypes also divide themselves into nontransmembrane (NT) (i.e., cytosolic) and transmembrane forms. All predicted MdBV PTPs were of the NT form, with the highest similarity matches (1 e Ϫ81 ) being to PTPs encoded by BVs from the wasps Cotesia congregata (CcBV) and Cotesia plutellae (13,44). Conserved-domain searches also identified high similarity matches to PTPs encoded by other organisms.…”

When parasitic wasps hijacked viruses: genomic and functional evolution of polydnaviruses

“…According to the 'birth and death' model, genes arise continuously by duplication and are lost by deletion or by mutational events. An ongoing process of pseudogenization was also observed for copies corresponding to different ptp genes in different species [60]. As shown in primates, Drosophila or large DNA viruses such as poxviruses, gene expansion and contraction could explain important adaptive traits allowing physiological adaptations of their host species [91][92][93].…”

“…Among the genes transferred into BVs, two families of virulence genes are particularly remarkable, the ankyrin and the ptp genes [59][60][61][62]. Apart from CiBV (Cheloninae), these genes are found in all BVs studied, including Toxoneuron nigriceps BV (Cardiochilinae) and MdBV, Glyptapanteles BV and Cotesia BV (Microgastrinae).…”

“…High PDV gene divergence compared with insect homologues generally leads to loss of phylogenetic signal [63]. This divergence could be explained by the time (100 Myr) elapsed since integration in BV genomes but could also reflect high selection pressures imposed by the interaction with the lepidopteran host [60,63,64] (see §4). However, phylogenetic analyses of the sugar transporter gene family recently acquired by Glyptapanteles BVs showed the BV genes were more closely related to hymenopteran than lepidopteran genes [37].…”