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Characterization of a Venom Gland-Associated Rhabdovirus in the Parasitoid Wasp Diachasmimorpha Longicaudata ⇑ Tyler J

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Characterization of a Venom Gland-Associated Rhabdovirus in the Parasitoid Wasp Diachasmimorpha Longicaudata ⇑ Tyler J Journal of Insect Physiology 91-92 (2016) 48–55 Contents lists available at ScienceDirect Journal of Insect Physiology journal homepage: www.elsevier.com/locate/jinsphys Characterization of a venom gland-associated rhabdovirus in the parasitoid wasp Diachasmimorpha longicaudata ⇑ Tyler J. Simmonds a, Daniel Carrillo b, Gaelen R. Burke a, a Department of Entomology, University of Georgia, Athens, GA 30602, USA b Tropical Research and Education Center, University of Florida-IFAS, Homestead, FL 33031, USA article info abstract Article history: Parasitoid wasps reproduce by laying their eggs on or inside of a host insect, which triggers a defense Received 17 May 2016 response in the host insect that kills the developing wasp. To counteract the host’s lethal response, some Received in revised form 28 June 2016 parasitoid wasps are associated with symbiotic viruses that alter host metabolism and development to Accepted 29 June 2016 promote successful development of the wasp embryo. These symbiotic viruses display a number of char- Available online 29 June 2016 acteristics that differ from those of pathogenic viruses, but are poorly understood with the exception of one group, the polydnaviruses. Here, we characterize the genome of a non-polydnavirus associated with Keywords: parasitoid wasps, Diachasmimorpha longicaudata rhabdovirus (DlRhV), and assess its role as a potential Parasitoid wasp mutualistic virus. Our results show that the DlRhV genome contains six open reading frames (ORFs). Symbiont Tephritid Three ORFs show sequence homology to known viral genes and one ORF encodes a previously identified Braconid protein, called parasitism-specific protein 24 (PSP24), that has been hypothesized to play a role in Rhabdovirus promoting successful parasitism by D. longicaudata. We constructed a phylogeny that shows that DlRhV is most closely related to other insect-infecting rhabdoviruses. Finally, we report that DlRhV infec- tion does not occur in all populations of D. longicaudata, and is not required for successful parasitism. Ó 2016 Elsevier Ltd. All rights reserved. 1. Introduction interfering with the host’s immune system and/or altering host metabolism or development to favor growth of the wasp (Strand Beneficial microbial symbionts play an important role in the life and Burke, 2014). This type of counter-defense strategy is best history of many species of insects. Symbionts can provide novel studied in parasitoid wasps that carry polydnaviruses (PDVs), abilities to their hosts, which allow hosts to occupy previously which have developed an obligate, mutualistic relationship with unavailable niches and promotes diversification of host lineages some parasitoid wasp species over the course of millions of years (Moran, 2006). The majority of research on microbial symbiosis of co-evolution (Strand and Burke, 2014). For PDV-associated has focused on bacteria, but viruses have also been shown to form wasps, reproductive success is dependent on the injection of PDV symbiotic relationships with eukaryotes (Roossinck, 2011). Some virions during parasitism. If PDV virions are not co-injected with of the most evolutionarily successful examples of viral- the egg during oviposition, the wasp larva is killed by the host’s eukaryotic beneficial symbioses are found in the parasitoid wasps. immune response before it can complete development In order to reproduce, parasitoid wasps must lay their eggs on or (Edson et al., 1981). PDVs are vertically transmitted as an inte- inside the body of a host insect, which provides the developing grated provirus that is found in the genome of all individuals of a wasps with protection and nutrition. Parasitism by the wasp trig- given species, but virions are only observed in a specialized region gers defense responses in the host insect that are often lethal for of the ovaries of female wasps. In addition to the well-studied and the developing wasp, and in turn, parasitoid wasps have evolved clearly mutualistic PDV-associated wasps, there are many species a number of strategies for circumventing the host’s defense of wasps that carry a non-PDV virus localized to their reproductive response (Pennacchio and Strand, 2006; Strand and Pech, 1995). organs. These non-PDV wasp-associated viruses are understudied, One successful strategy for disrupting host defenses is the injec- and little is known about their potential roles in the successful tion of a beneficial, symbiotic virus into the host during oviposi- parasitism of wasp hosts (Dheilly et al., 2015; Lawrence, 2005). tion. These viruses allow wasps to complete development by D. longicaudata is a parasitoid wasp native to South East Asia, which has been introduced across North and South America as part ⇑ Corresponding author. of a biological pest control program against tephritid fruit flies, E-mail address: [email protected] (G.R. Burke). including the Caribbean Fruit Fly, Anastrepha suspensa, in Florida http://dx.doi.org/10.1016/j.jinsphys.2016.06.009 0022-1910/Ó 2016 Elsevier Ltd. All rights reserved. T.J. Simmonds et al. / Journal of Insect Physiology 91-92 (2016) 48–55 49 (Baranowski et al., 1993; Bess et al., 1961). D. longicaudata has been they reached the third instar (seven days) (Burditt et al., 1974). used for biological control because it is a species that is amenable Water was provided for D. longicaudata and A. suspensa using to mass rearing, specifically parasitizes tephritids, and is able to 1 oz. 0.6% agar cubes. establish in a variety of environments (Baranowski et al., 1993). For parasitism, third instar A. suspensa larvae were placed inside Their role in biological control programs has prompted research of a plastic embroidery ring, between two pieces of organza fabric, into D. longicaudata life history and physiology to improve their and placed on a mesh opening at the top of the wasp cages. Wasps use in pest control. These studies revealed that female D. longicau- were allowed to parasitize the larvae for one to two hours. After data are associated with two vertically transmitted viruses that are parasitism, the larvae were removed from the disk and placed into present in the wasp’s venom glands. One of these viral symbionts is vermiculite that was mixed 1:1 by weight with water to allow the a poxvirus, known as D. longicaudata entomopoxvirus (DlEPV), and larvae to pupate. Seven days after parasitism, the pupae were the other is a rhabdovirus, called D. longicaudata rhabdovirus transferred from the vermiculite into an adult wasp cage, where (DlRhV). The virions of both viruses were observed in all D. longi- the insects were allowed to emerge. The D. longicaudata that caudata individuals collected from locations in Florida and Hawaii. emerged from pupae were removed from the cage and placed into These data suggested that like PDVs, DlEPV and DlRhV were a new cage containing other adult wasps that emerged that same co-symbionts: obligate, mutualistic, wasp-associated viruses day, while the A. suspensa that emerged were discarded. (Lawrence, 2005; Lawrence and Akin, 1990; Lawrence and Matos, 2005). This study focuses on the genetic characterization and 2.2. Sequencing and annotation of the DlRhV genome prevalence of DlRhV in D. longicaudata. Rhabdoviruses are single-stranded negative-sense RNA viruses, and have a broad host Total RNA was extracted from dissected adult D. longicaudata range, which includes mammals, fish, plants, and insects. Insects venom glands using the QIAGEN RNeasy mini kit with on-column are the primary vector for most rhabdoviruses, but some described DNAse treatment to give 1 lg of template for library construction. rhabdoviruses are direct pathogens of insects (Gallione et al., 1981; The RNA for sequencing the DlRhV genome was total RNA Hogenhout et al., 2003). The effect of DlRhV infection on extracted in June 2014 from individuals from the March 2014 col- D. longicaudata parasitism success is currently unknown, but it ony. Standard Illumina-compatible library construction methods has been hypothesized that, like PDVs, non-PDV viruses of with oligo-dT priming were used at the Georgia Genomics Facility parasitoid wasps are co-evolving with their wasp host towards a to make a stranded library for sequencing reverse transcribed RNA mutualistic relationship (Lawrence, 2005). transcripts, with median library size of 509 bp. Illumina miSeq In this study, we sequenced and annotated the DlRhV genome PE150 sequencing generated 7,539,511 read pairs, of which to further characterize this virus and its potential roles in para- 6,495,404 pairs met quality filtering standards of >90% of bases sitism. Our annotation of the DlRhV genome identified a gene at PHRED score 30 or higher for both reads in a pair. Paired reads encoding a previously identified ‘‘parasitism-specific protein” that were mapped against the DlEPV genome (unpublished data) with was suggested to be important for successful D. longicaudata para- tophat v2.0.11 and cufflinks v2.2.1 (Kim et al., 2013; Trapnell sitism, but had unclear genetic origin (Rolle and Lawrence, 1994a, et al., 2012), and reads that did not map to the DlEPV sequences b; Shi et al., 1999). We determined that DlRhV is related to other (non-DlEPV transcripts) were extracted using samtools v0.2.0-rc6 insect-infecting rhabdoviruses and is not necessary for successful (Li et al., 2009). parasitism in D. longicaudata populations. In contrast to previous Non-DlEPV reads were assembled to reconstruct wasp tran- reports, our analysis revealed that DlRhV is not present in all D. scripts and the DlRhV RNA genome. 4,740,777 paired reads were longicaudata individuals, and we therefore concluded that DlRhV assembled de novo using Vicuna v1.0 with default parameters, is not an obligate mutualistic virus. Further investigation is needed allowing 5% maximum divergence between individual reads and to characterize any facultative contributions that DlRhV may make consensus contigs (Yang et al., 2012). The resulting contigs were to parasitism success. cut into non-overlapping 3 kb pieces, and all sequences were ana- lyzed by BLASTX against the non-redundant protein database from NCBI in September 2014.
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