Characterization of fossilized relatives of the White Spot Syndrome Virus in genomes of decapod crustaceans

Abstract

BackgroundThe White Spot Syndrome Virus (WSSV) is an important pathogen that infects a variety of decapod species and causes a highly contagious disease in penaeid shrimps. Mass mortalities caused by WSSV have pronounced commercial impact on shrimp aquaculture. Until now WSSV is the only known member of the virus family Nimaviridae, a group with obscure phylogenetic affinities. Its isolated position makes WSSV studies challenging due to large number of genes without homology in other viruses or cellular organisms.ResultsHere we report the discovery of an unusually large amount of sequences with high similarity to WSSV in a genomic library from the Jamaican bromeliad crab Metopaulias depressus. De novo assembly of these sequences allowed for the partial reconstruction of the genome of this endogenized virus with total length of 200 kbp encompassed in three scaffolds. The genome includes at least 68 putative open reading frames with homology in WSSV, most of which are intact. Among these, twelve orthologs of WSSV genes coding for non-structural proteins and nine genes known to code for the major components of the WSSV virion were discovered. Together with reanalysis of two similar cases of WSSV-like sequences in penaeid shrimp genomic libraries, our data allowed comparison of gene composition and gene order between different lineages related to WSSV. Furthermore, screening of published sequence databases revealed sequences with highest similarity to WSSV and the newly described virus in genomic libraries of at least three further decapod species. Analysis of the viral sequences detected in decapods suggests that they are less a result of contemporary WSSV infection, but rather originate from ancestral infection events. Phylogenetic analyses suggest that genes were acquired repeatedly by divergent viruses or viral strains of the Nimaviridae.ConclusionsOur results shed new light on the evolution of the Nimaviridae and point to a long association of this viral group with decapod crustaceans.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0380-7) contains supplementary material, which is available to authorized users.

Crustacean Genome Exploration Reveals the Evolutionary Origin of White Spot Syndrome Virus

“…Meanwhile, we could not find any M. ensis nimavirus-like sequences in the assembly of Metapenaeus joyneri, a penaeid shrimp species closely related to M. ensis. PCR assays also supported the absence of M. ensis nimavirus An endogenous nimavirus was previously reported in the genome of the bromeliad crab Metopaulias depressus, a sesarmid crab endemic to Jamaica (19). We found similar nimavirus genomes from two sesarmid crabs, Chiromantes dehaani and Sesarmops intermedium, as shown in Fig.…”

“…S. intermedium and C. dehaani sequences were an average of 93% identical, but the identity dropped to 83% when they were compared to the M. depressus sequences. Although Rozenberg et al (19) described three viral scaffolds, we could not reproduce them in S. intermedium or C. dehaani sequences. Moreover, some incongruences in gene arrangements were observed.…”

“…Several works have addressed the epidemiology and contemporary evolutionary trends of WSSV (14)(15)(16); however, we know little about the ancient history of WSSV, because we have few nimavirus genomes available for comparative analyses. Interestingly, some decapod crustaceans have been shown to harbor fossilized nimaviruses in their genomes (17)(18)(19). Nimavirus genomes extracted from crustacean genome data would provide unique opportunities for studying the evolutionary genomics of Nimaviridae.…”

The Complete Genome of an Endogenous Nimavirus (Nimav-1_LVa) From the Pacific Whiteleg Shrimp Penaeus (Litopenaeus) Vannamei

“…Although a number of endogenous nimaviruses have been revealed in the genomes of various crustacean species [27,28,80], one compelling question remains, that is whether these endogenous virus sequences are passive relics of some old nimaviruses ("fossilized"), or recent inhabitants in these eukaryotic genomes, from some unidentified free-living viruses, and still possibly possess the capability to proliferate and transmit to different genomes/species under certain circumstances. Currently, at least two cases of endogenous nimaviruses suggest the latter scenario.…”

“…WSSV has long been regarded as the lone virus (type species) of the genus Whispovirus, which is the only genus of the family Nimaviridae [18]. However, this notion is changing with the recent discovery of diverse endogenous WSSV-like nimaviruses [27][28][29][30]. In some crustacean genomes, such as P. monodon (Pm), even two different types of endogenous nimaviruses can be distinguished [28].…”