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

• Published in: Journal of virology Vol. 93; no. 3
• Main Authors: Kawato, Satoshi, Shitara, Aiko, Wang, Yuanyuan, Nozaki, Reiko, Kondo, Hidehiro, Hirono, Ikuo
• Format: Journal Article
• Language: English
• Published: United States American Society for Microbiology 01.02.2019
• Subjects: Animals; Evolution, Molecular; Gene Expression Regulation, Viral; Genetic Diversity and Evolution; Genetic Variation; Genome, Viral; Host-Pathogen Interactions; Penaeidae - genetics; Penaeidae - virology; Phylogeny; Spotlight; Viral Proteins - genetics; Virus Diseases - transmission; Virus Diseases - veterinary; White spot syndrome virus 1 - classification; White spot syndrome virus 1 - genetics; White spot syndrome virus 1 - pathogenicity; Nimaviridae; white spot syndrome virus; shrimp; fossilized virus
• ISSN: 0022-538X; 1098-5514
• DOI: 10.1128/jvi.01144-18

White spot syndrome virus (WSSV) is a crustacean-infecting, double-stranded DNA virus and is the most serious viral pathogen in the global shrimp industry. WSSV is the sole recognized member of the family , and the lack of genomic data on other nimaviruses has obscured the evolutionary history of WSSV. Here, we investigated the evolutionary history of WSSV by characterizing WSSV relatives hidden in host genomic data. We surveyed 14 host crustacean genomes and identified five novel nimaviral genomes. Comparative genomic analysis of identified 28 "core genes" that are ubiquitously conserved in ; unexpected conservation of 13 uncharacterized proteins highlighted yet-unknown essential functions underlying the nimavirus replication cycle. The ancestral gene set contained five baculoviral infectivity factor homologs and a sulfhydryl oxidase homolog, suggesting a shared phylogenetic origin of and insect-associated double-stranded DNA viruses. Moreover, we show that novel gene acquisition and subsequent amplification reinforced the unique accessory gene repertoire of WSSV. Expansion of unique envelope protein and nonstructural virulence-associated genes may have been the key genomic event that made WSSV such a deadly pathogen. WSSV is the deadliest viral pathogen threatening global shrimp aquaculture. The evolutionary history of WSSV has remained a mystery, because few WSSV relatives, or nimaviruses, had been reported. Our aim was to trace the history of WSSV using the genomes of novel nimaviruses hidden in host genome data. We demonstrate that WSSV emerged from a diverse family of crustacean-infecting large DNA viruses. By comparing the genomes of WSSV and its relatives, we show that WSSV possesses an expanded set of unique host-virus interaction-related genes. This extensive gene gain may have been the key genomic event that made WSSV such a deadly pathogen. Moreover, conservation of insect-infecting virus protein homologs suggests a common phylogenetic origin of crustacean-infecting and other insect-infecting DNA viruses. Our work redefines the previously poorly characterized crustacean virus family and reveals the ancient genomic events that preordained the emergence of a devastating shrimp pathogen.