A New Family of DNA Viruses Causing Disease in Crustaceans from Diverse Aquatic Biomes

Abstract

Panulirus argus virus 1 (PaV1) is the only known virus infecting the Caribbean spiny lobster (Panulirus argus) from the Caribbean Sea. Recently, related viruses, Dikerogammarus haemobaphes virus 1 (DhV1) and Carcinus maenas virus 1 (CmV1), have been detected in the demon shrimp (Dikerogammarus haemobaphes) and the European shore crab (Carcinus maenas), respectively, from sites in the United Kingdom. The virion morphology of these crustacean viruses is similar to that of iridoviruses. However, unlike iridoviruses and other nucleocytoplasmic large DNA viruses (NCLDVs), these viruses complete their morphogenesis in the host cell nucleus rather than in the cytoplasm. To date, these crustacean viruses have remained unclassified due to a lack of genomic data. Using an Illumina MiSeq sequencer, we sequenced the complete genomes of PaV1, CmV1, and DhV1. Comparative genome analysis shows that these crustacean virus genomes encode the 10 hallmark proteins previously described for the NCLDVs of eukaryotes, strongly suggesting that they are members of this group. With a size range of 70 to 74 kb, these are the smallest NCLDV genomes identified to date. Extensive gene loss, divergence of gene sequences, and the accumulation of low-complexity sequences reflect the extreme degradation of the genomes of these “minimal” NCLDVs rather than any direct relationship with the NCLDV ancestor. Phylogenomic analysis supports the classification of these crustacean viruses as a distinct family, “Mininucleoviridae,” within the pitho-irido-Marseille branch of the NCLDVs. IMPORTANCE Recent genomic and metagenomic studies have led to a dramatic expansion of the known diversity of nucleocytoplasmic large DNA viruses (NCLDVs) of eukaryotes, which include giant viruses of protists and important pathogens of vertebrates, such as poxviruses. However, the characterization of viruses from nonmodel hosts still lags behind. We sequenced the complete genomes of three viruses infecting crustaceans, the Caribbean spiny lobster, demon shrimp, and European shore crab. These viruses have the smallest genomes among the known NCLDVs, with losses of many core genes, some of which are shared with iridoviruses. The deterioration of the transcription apparatus is compatible with microscopic and ultrastructural observations indicating that these viruses replicate in the nucleus of infected cells rather than in the cytoplasm. Phylogenomic analysis indicates that these viruses are sufficiently distinct from all other NCLDVs to justify the creation of a separate family, for which we propose the name “Mininucleoviridae” (i.e., small viruses reproducing in the cell nucleus).

Yes, we can use it: a formal test on the accuracy of low-pass nanopore long-read sequencing for mitophylogenomics and barcoding research using the Caribbean spiny lobster Panulirus argus

“…obs.). Despite its ecological importance, commercial value, and mislabeling in the trade of P. argus, only a few (but increasing) number of genomic resources exist for this species [13,[35][36][37][38]. The development of genomic resources are of utmost importance as they will improve the understanding about the biology of P. argus while also aiding in fishery management and conservation strategies using relative cheap molecular markers.…”

Yaravirus: A novel 80-nm virus infecting Acanthamoeba castellanii

“…Of course, we cannot exclude the possibility that Yaravirus may represent a reduced NCLDV, presenting highly divergent or even absent NCLDV hallmark proteins. Recently, a similar case was described for three small crustacean viruses (44). However, despite their reduced genome when compared to other members of the NCLDV, an important number of hallmark genes were shared with this group, differently as observed for Yaravirus (44).…”

A mysterious 80 nm amoeba virus with a near-complete “ORFan genome” challenges the classification of DNA viruses

“…Recently, a similar case was described for three small crustacean viruses. However, despite their reduced genome when compared to other members of the NCLDV, an important number of hallmark genes were shared with this group, differently as observed for Yaravirus (40). In this scenario, not less exciting, Yaravirus would represent the to-date smallest member of the NCLDVs, both in particle and genome size.…”