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

Kuttichantran Subramaniam, Donald Behringer, Jamie Bojko, Natalya Yutin, Abigail Clark, Kelly Bateman, Ronny van Aerle, David Bass, Rose Kerr, Eugene Koonin, Grant Stentiford, Thomas Waltzek

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Abstract

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 pithoirido-
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).
Original languageEnglish
Article numbere02938-19
JournalmBio
Early online date14 Jan 2020
DOIs
Publication statusE-pub ahead of print - 14 Jan 2020

Fingerprint

DNA Viruses
Virus Diseases
Ecosystem
Viruses
Palinuridae
Brachyura
Iridovirus
Genome
Cytoplasm
Genes
Poxviridae
Metagenomics
Eukaryota
Cell Nucleus
Morphogenesis

Cite this

Subramaniam, K., Behringer, D., Bojko, J., Yutin, N., Clark, A., Bateman, K., ... Waltzek, T. (2020). A New Family of DNA Viruses Causing Disease in Crustaceans from Diverse Aquatic Biomes. mBio, [e02938-19]. https://doi.org/10.1128/mBio.02938-19
Subramaniam, Kuttichantran ; Behringer, Donald ; Bojko, Jamie ; Yutin, Natalya ; Clark, Abigail ; Bateman, Kelly ; van Aerle, Ronny ; Bass, David ; Kerr, Rose ; Koonin, Eugene ; Stentiford, Grant ; Waltzek, Thomas. / A New Family of DNA Viruses Causing Disease in Crustaceans from Diverse Aquatic Biomes. In: mBio. 2020.
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abstract = "ABSTRACT Panulirus argus virus 1 (PaV1) is the only known virus infecting the Caribbeanspiny 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 theUnited Kingdom. The virion morphology of these crustacean viruses is similar to thatof iridoviruses. However, unlike iridoviruses and other nucleocytoplasmic large DNAviruses (NCLDVs), these viruses complete their morphogenesis in the host cell nucleusrather than in the cytoplasm. To date, these crustacean viruses have remainedunclassified due to a lack of genomic data. Using an Illumina MiSeq sequencer, wesequenced the complete genomes of PaV1, CmV1, and DhV1. Comparative genomeanalysis shows that these crustacean virus genomes encode the 10 hallmark proteinspreviously described for the NCLDVs of eukaryotes, strongly suggesting that they aremembers of this group. With a size range of 70 to 74 kb, these are the smallestNCLDV genomes identified to date. Extensive gene loss, divergence of gene sequences,and the accumulation of low-complexity sequences reflect the extremedegradation of the genomes of these “minimal” NCLDVs rather than any direct relationshipwith the NCLDV ancestor. Phylogenomic analysis supports the classificationof these crustacean viruses as a distinct family, “Mininucleoviridae,” within the pithoirido-Marseille branch of the NCLDVs.IMPORTANCE Recent genomic and metagenomic studies have led to a dramatic expansionof the known diversity of nucleocytoplasmic large DNA viruses (NCLDVs) ofeukaryotes, which include giant viruses of protists and important pathogens of vertebrates,such as poxviruses. However, the characterization of viruses from nonmodelhosts still lags behind. We sequenced the complete genomes of three virusesinfecting crustaceans, the Caribbean spiny lobster, demon shrimp, and Europeanshore 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 deteriorationof the transcription apparatus is compatible with microscopic and ultrastructuralobservations indicating that these viruses replicate in the nucleus of infectedcells rather than in the cytoplasm. Phylogenomic analysis indicates that theseviruses are sufficiently distinct from all other NCLDVs to justify the creation of a separatefamily, for which we propose the name “Mininucleoviridae” (i.e., small virusesreproducing in the cell nucleus).",
author = "Kuttichantran Subramaniam and Donald Behringer and Jamie Bojko and Natalya Yutin and Abigail Clark and Kelly Bateman and {van Aerle}, Ronny and David Bass and Rose Kerr and Eugene Koonin and Grant Stentiford and Thomas Waltzek",
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language = "English",
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Subramaniam, K, Behringer, D, Bojko, J, Yutin, N, Clark, A, Bateman, K, van Aerle, R, Bass, D, Kerr, R, Koonin, E, Stentiford, G & Waltzek, T 2020, 'A New Family of DNA Viruses Causing Disease in Crustaceans from Diverse Aquatic Biomes', mBio. https://doi.org/10.1128/mBio.02938-19

A New Family of DNA Viruses Causing Disease in Crustaceans from Diverse Aquatic Biomes. / Subramaniam, Kuttichantran; Behringer, Donald; Bojko, Jamie; Yutin, Natalya; Clark, Abigail; Bateman, Kelly; van Aerle, Ronny; Bass, David ; Kerr, Rose; Koonin, Eugene; Stentiford, Grant; Waltzek, Thomas.

In: mBio, 14.01.2020.

Research output: Contribution to journalArticle

TY - JOUR

T1 - A New Family of DNA Viruses Causing Disease in Crustaceans from Diverse Aquatic Biomes

AU - Subramaniam, Kuttichantran

AU - Behringer, Donald

AU - Bojko, Jamie

AU - Yutin, Natalya

AU - Clark, Abigail

AU - Bateman, Kelly

AU - van Aerle, Ronny

AU - Bass, David

AU - Kerr, Rose

AU - Koonin, Eugene

AU - Stentiford, Grant

AU - Waltzek, Thomas

PY - 2020/1/14

Y1 - 2020/1/14

N2 - ABSTRACT Panulirus argus virus 1 (PaV1) is the only known virus infecting the Caribbeanspiny 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 theUnited Kingdom. The virion morphology of these crustacean viruses is similar to thatof iridoviruses. However, unlike iridoviruses and other nucleocytoplasmic large DNAviruses (NCLDVs), these viruses complete their morphogenesis in the host cell nucleusrather than in the cytoplasm. To date, these crustacean viruses have remainedunclassified due to a lack of genomic data. Using an Illumina MiSeq sequencer, wesequenced the complete genomes of PaV1, CmV1, and DhV1. Comparative genomeanalysis shows that these crustacean virus genomes encode the 10 hallmark proteinspreviously described for the NCLDVs of eukaryotes, strongly suggesting that they aremembers of this group. With a size range of 70 to 74 kb, these are the smallestNCLDV genomes identified to date. Extensive gene loss, divergence of gene sequences,and the accumulation of low-complexity sequences reflect the extremedegradation of the genomes of these “minimal” NCLDVs rather than any direct relationshipwith the NCLDV ancestor. Phylogenomic analysis supports the classificationof these crustacean viruses as a distinct family, “Mininucleoviridae,” within the pithoirido-Marseille branch of the NCLDVs.IMPORTANCE Recent genomic and metagenomic studies have led to a dramatic expansionof the known diversity of nucleocytoplasmic large DNA viruses (NCLDVs) ofeukaryotes, which include giant viruses of protists and important pathogens of vertebrates,such as poxviruses. However, the characterization of viruses from nonmodelhosts still lags behind. We sequenced the complete genomes of three virusesinfecting crustaceans, the Caribbean spiny lobster, demon shrimp, and Europeanshore 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 deteriorationof the transcription apparatus is compatible with microscopic and ultrastructuralobservations indicating that these viruses replicate in the nucleus of infectedcells rather than in the cytoplasm. Phylogenomic analysis indicates that theseviruses are sufficiently distinct from all other NCLDVs to justify the creation of a separatefamily, for which we propose the name “Mininucleoviridae” (i.e., small virusesreproducing in the cell nucleus).

AB - ABSTRACT Panulirus argus virus 1 (PaV1) is the only known virus infecting the Caribbeanspiny 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 theUnited Kingdom. The virion morphology of these crustacean viruses is similar to thatof iridoviruses. However, unlike iridoviruses and other nucleocytoplasmic large DNAviruses (NCLDVs), these viruses complete their morphogenesis in the host cell nucleusrather than in the cytoplasm. To date, these crustacean viruses have remainedunclassified due to a lack of genomic data. Using an Illumina MiSeq sequencer, wesequenced the complete genomes of PaV1, CmV1, and DhV1. Comparative genomeanalysis shows that these crustacean virus genomes encode the 10 hallmark proteinspreviously described for the NCLDVs of eukaryotes, strongly suggesting that they aremembers of this group. With a size range of 70 to 74 kb, these are the smallestNCLDV genomes identified to date. Extensive gene loss, divergence of gene sequences,and the accumulation of low-complexity sequences reflect the extremedegradation of the genomes of these “minimal” NCLDVs rather than any direct relationshipwith the NCLDV ancestor. Phylogenomic analysis supports the classificationof these crustacean viruses as a distinct family, “Mininucleoviridae,” within the pithoirido-Marseille branch of the NCLDVs.IMPORTANCE Recent genomic and metagenomic studies have led to a dramatic expansionof the known diversity of nucleocytoplasmic large DNA viruses (NCLDVs) ofeukaryotes, which include giant viruses of protists and important pathogens of vertebrates,such as poxviruses. However, the characterization of viruses from nonmodelhosts still lags behind. We sequenced the complete genomes of three virusesinfecting crustaceans, the Caribbean spiny lobster, demon shrimp, and Europeanshore 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 deteriorationof the transcription apparatus is compatible with microscopic and ultrastructuralobservations indicating that these viruses replicate in the nucleus of infectedcells rather than in the cytoplasm. Phylogenomic analysis indicates that theseviruses are sufficiently distinct from all other NCLDVs to justify the creation of a separatefamily, for which we propose the name “Mininucleoviridae” (i.e., small virusesreproducing in the cell nucleus).

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DO - 10.1128/mBio.02938-19

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Subramaniam K, Behringer D, Bojko J, Yutin N, Clark A, Bateman K et al. A New Family of DNA Viruses Causing Disease in Crustaceans from Diverse Aquatic Biomes. mBio. 2020 Jan 14. e02938-19. https://doi.org/10.1128/mBio.02938-19