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 (Dikerogamma...
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American Society for Microbiology
2020
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oai:doaj.org-article:58f8e400fbf04fe5ae81d468cb9712092021-11-15T15:56:58ZA New Family of DNA Viruses Causing Disease in Crustaceans from Diverse Aquatic Biomes10.1128/mBio.02938-192150-7511https://doaj.org/article/58f8e400fbf04fe5ae81d468cb9712092020-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02938-19https://doaj.org/toc/2150-7511ABSTRACT 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).Kuttichantran SubramaniamDonald C. BehringerJamie BojkoNatalya YutinAbigail S. ClarkKelly S. BatemanRonny van AerleDavid BassRose C. KerrEugene V. KooninGrant D. StentifordThomas B. WaltzekAmerican Society for MicrobiologyarticleCrustaceagenome degradationlarge nucleocytoplasmic DNA viruseslow-complexity sequencesvirus evolutionMicrobiologyQR1-502ENmBio, Vol 11, Iss 1 (2020) |
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DOAJ |
| collection |
DOAJ |
| language |
EN |
| topic |
Crustacea genome degradation large nucleocytoplasmic DNA viruses low-complexity sequences virus evolution Microbiology QR1-502 |
| spellingShingle |
Crustacea genome degradation large nucleocytoplasmic DNA viruses low-complexity sequences virus evolution Microbiology QR1-502 Kuttichantran Subramaniam Donald C. Behringer Jamie Bojko Natalya Yutin Abigail S. Clark Kelly S. Bateman Ronny van Aerle David Bass Rose C. Kerr Eugene V. Koonin Grant D. Stentiford Thomas B. Waltzek A New Family of DNA Viruses Causing Disease in Crustaceans from Diverse Aquatic Biomes |
| description |
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). |
| format |
article |
| author |
Kuttichantran Subramaniam Donald C. Behringer Jamie Bojko Natalya Yutin Abigail S. Clark Kelly S. Bateman Ronny van Aerle David Bass Rose C. Kerr Eugene V. Koonin Grant D. Stentiford Thomas B. Waltzek |
| author_facet |
Kuttichantran Subramaniam Donald C. Behringer Jamie Bojko Natalya Yutin Abigail S. Clark Kelly S. Bateman Ronny van Aerle David Bass Rose C. Kerr Eugene V. Koonin Grant D. Stentiford Thomas B. Waltzek |
| author_sort |
Kuttichantran Subramaniam |
| title |
A New Family of DNA Viruses Causing Disease in Crustaceans from Diverse Aquatic Biomes |
| title_short |
A New Family of DNA Viruses Causing Disease in Crustaceans from Diverse Aquatic Biomes |
| title_full |
A New Family of DNA Viruses Causing Disease in Crustaceans from Diverse Aquatic Biomes |
| title_fullStr |
A New Family of DNA Viruses Causing Disease in Crustaceans from Diverse Aquatic Biomes |
| title_full_unstemmed |
A New Family of DNA Viruses Causing Disease in Crustaceans from Diverse Aquatic Biomes |
| title_sort |
new family of dna viruses causing disease in crustaceans from diverse aquatic biomes |
| publisher |
American Society for Microbiology |
| publishDate |
2020 |
| url |
https://doaj.org/article/58f8e400fbf04fe5ae81d468cb971209 |
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