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Cited by 9Aquaculture disease management and microbiotaBacteriophages and microbial interactionsChromosomal and Genetic Variations

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Integrase-associated niche differentiation of endogenous large DNA viruses in crustaceans

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Kawato, Satoshi, Nozaki, Reiko, Kondo, Hidehiro, Hirono, Ikuo·2024·Microbiology Spectrum
DOI 10.1128/spectrum.00559-23PMC PMC10871703

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Abstract

Crustacean genomes harbor sequences originating from nimaviruses, a family of large double-stranded DNA viruses infecting crustaceans. In this study, we recovered metagenome-assembled genomes of 27 endogenous nimaviruses from crustacean genome data. Phylogenetic analysis revealed four major lineages within Nimaviridae , and for three of these lineages, we propose novel genera of endogenous nimaviruses: “Majanivirus” and “Pemonivirus” identified from penaeid shrimp genomes, and “Clopovirus” identified from terrestrial isopods. Majanivirus genomes contain multiple eukaryotic-like genes such as baculoviral inhibitor of apoptosis repeat-containing genes, innexins, and heat shock protein 70-like genes, some of which contain introns. An alignment of long reads revealed that each endogenous nimavirus species specifically inserts into host microsatellites or within 28S rDNA. This insertion preference was associated with the type of virus-encoded DNA recombination enzymes, the integrases. Majaniviruses, pemoniviruses, some whispoviruses, and possibly clopoviruses specifically insert into the arthropod telomere repeat motif (TAACC/GGTTA)n and all possessed a specific tyrosine recombinase family. Pasiphaea japonica whispovirus and Portunus trituberculatus whispovirus, the closest relatives of white spot syndrome virus, integrate into the host 28S rDNA and are equipped with members of another family of tyrosine recombinases that are distantly related to telomere-specific tyrosine recombinases. Endogenous nimavirus genomes identified from sesarmid crabs, which lack tyrosine recombinases and are flanked by a 46-bp inverted terminal repeat, integrate into (AT/TA)n microsatellites through the acquisition of a Ginger2-like cut-and-paste DDE transposase. These results suggest that endogenous nimaviruses are giant transposable elements that occupy different sequence niches through the acquisition of different integrase families. IMPORTANCE: Crustacean genomes harbor sequences originating from a family of large DNA viruses called nimaviruses, but it is unclear why they are present. We show that endogenous nimaviruses selectively insert into repetitive sequences within the host genome, and this insertion specificity was correlated with different types of integrases, which are DNA recombination enzymes encoded by the nimaviruses themselves. This suggests that endogenous nimaviruses have colonized various genomic niches through the acquisition of integrases with different insertion specificities. Our results point to a novel survival strategy of endogenous large DNA viruses colonizing the host genomes. These findings may clarify the evolution and spread of nimaviruses in crustaceans and lead to measures to control and prevent the spread of pathogenic nimaviruses in aquaculture settings.

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Figures

Fig 1 Phylogenomic tree of Nimaviridae. Amino acid sequences of nine nimaviral core genes (wsv026, wsv282, wsv289, wsv303, wsv343, wsv360, wsv433, wsv447, and wsv514; 12,905 amino acids; substitution model: JTT + F + I + I + R5) were used for the analysis. Virus names are colored according to insertion motif specificity as indicated on the lower left. The bar in the middle of the figure denotes substitution per site. Ultrafast bootstrap value (1,000 trials) was 100% unless indicated beside the node. Proposed genus names are quoted and unitalicized. WSSV, white spot syndrome virus; CoBV, Chionoecetes opilio bacilliform virus; MdWSSV-like, Metopaulias depressus WSSV-like virus; see Table 2 for the abbreviations for the other viruses.
Fig 1 Phylogenomic tree of Nimaviridae. Amino acid sequences of nine nimaviral core genes (wsv026, wsv282, wsv289, wsv303, wsv343, wsv360, wsv433, wsv447, and wsv514; 12,905 amino acids; substitution model: JTT + F + I + I + R5) were used for the analysis. Virus names are colored according to insertion motif specificity as indicated on the lower left. The bar in the middle of the figure denotes substitution per site. Ultrafast bootstrap value (1,000 trials) was 100% unless indicated beside the node. Proposed genus names are quoted and unitalicized. WSSV, white spot syndrome virus; CoBV, Chionoecetes opilio bacilliform virus; MdWSSV-like, Metopaulias depressus WSSV-like virus; see Table 2 for the abbreviations for the other viruses.CC BY · PubMed Central
Fig 2 Genome diagram of majaniviruses. (A) Genome diagrams of majaniviruses. Arrows indicate predicted genes and their transcriptional orientations; blue, WSSV homologs; yellow, baculoviral inhibitor of apoptosis repeat-containing proteins; gray, hypothetical and other eukaryotic-like proteins; red, tyrosine recombinases. Blue ribbons indicate pairwise TBLASTX hits (e-value :1−e3, bitscore: 50). (B) ONT read alignments flanking the 5′- and 3′-ends of majanivirus genomes.
Fig 2 Genome diagram of majaniviruses. (A) Genome diagrams of majaniviruses. Arrows indicate predicted genes and their transcriptional orientations; blue, WSSV homologs; yellow, baculoviral inhibitor of apoptosis repeat-containing proteins; gray, hypothetical and other eukaryotic-like proteins; red, tyrosine recombinases. Blue ribbons indicate pairwise TBLASTX hits (e-value :1−e3, bitscore: 50). (B) ONT read alignments flanking the 5′- and 3′-ends of majanivirus genomes.CC BY · PubMed Central
Fig 3 Phylogenetic analysis of eukaryotic-like genes in majaniviruses. (A) Maximum-likelihood phylogenetic tree of 80 baculoviral inhihbitor of apoptosis repeat-containing proteins (266 sites; model: LG + I + G4). (B) Maximum-likelihood phylogenetic tree of 162 HSP70-like proteins (579 sites; model: LG + R7). (C) Maximum-likelihood phylogenetic tree of 158 innexin proteins (251 sites; model: LG + R6).
Fig 3 Phylogenetic analysis of eukaryotic-like genes in majaniviruses. (A) Maximum-likelihood phylogenetic tree of 80 baculoviral inhihbitor of apoptosis repeat-containing proteins (266 sites; model: LG + I + G4). (B) Maximum-likelihood phylogenetic tree of 162 HSP70-like proteins (579 sites; model: LG + R7). (C) Maximum-likelihood phylogenetic tree of 158 innexin proteins (251 sites; model: LG + R6).CC BY · PubMed Central
Fig 4 Genome diagrams of pemoniviruses. (A) Genome diagrams of pemoniviruses. Arrows indicate predicted genes and their transcriptional orientations; blue, WSSV homologs; yellow, baculoviral inhibitor of apoptosis repeat-containing proteins; gray, hypothetical and other eukaryotic-like proteins; red, tyrosine recombinases. Blue ribbons indicate pairwise TBLASTX hits (e-value: 1−e3, bitscore: 50). (B) ONT read alignments flanking the 5′- and 3′-ends of pemonivirus genomes.
Fig 4 Genome diagrams of pemoniviruses. (A) Genome diagrams of pemoniviruses. Arrows indicate predicted genes and their transcriptional orientations; blue, WSSV homologs; yellow, baculoviral inhibitor of apoptosis repeat-containing proteins; gray, hypothetical and other eukaryotic-like proteins; red, tyrosine recombinases. Blue ribbons indicate pairwise TBLASTX hits (e-value: 1−e3, bitscore: 50). (B) ONT read alignments flanking the 5′- and 3′-ends of pemonivirus genomes.CC BY · PubMed Central
Fig 5 The clopoviruses. (A) Genome diagrams of clopoviruses. Arrows indicate predicted genes and their transcriptional orientations; blue, WSSV homologs; yellow, baculoviral inhibitor of apoptosis repeat-containing proteins; gray, hypothetical and other eukaryotic-like proteins; red, tyrosine recombinases. Blue ribbons indicate pairwise TBLASTX hits (e-value: 1−e3, bitscore: 50). (B) ONT read alignments flanking the 5′- and 3′-ends of clopovirus genomes.
Fig 5 The clopoviruses. (A) Genome diagrams of clopoviruses. Arrows indicate predicted genes and their transcriptional orientations; blue, WSSV homologs; yellow, baculoviral inhibitor of apoptosis repeat-containing proteins; gray, hypothetical and other eukaryotic-like proteins; red, tyrosine recombinases. Blue ribbons indicate pairwise TBLASTX hits (e-value: 1−e3, bitscore: 50). (B) ONT read alignments flanking the 5′- and 3′-ends of clopovirus genomes.CC BY · PubMed Central
Fig 6 Telomere-inserting whispoviruses. (A) Genome diagrams of whispoviruses. Arrows indicate predicted genes and their transcriptional orientations; blue, WSSV homologs; yellow, baculoviral inhibitor of apoptosis repeat-containing proteins; gray, hypothetical and other eukaryotic-like proteins; red, tyrosine recombinases. Blue ribbons indicate pairwise TBLASTX hits (e-value: 1−e3, bitscore: 50). (B) ONT read alignments flanking the 5′- and 3′-ends of whispovirus genomes.
Fig 6 Telomere-inserting whispoviruses. (A) Genome diagrams of whispoviruses. Arrows indicate predicted genes and their transcriptional orientations; blue, WSSV homologs; yellow, baculoviral inhibitor of apoptosis repeat-containing proteins; gray, hypothetical and other eukaryotic-like proteins; red, tyrosine recombinases. Blue ribbons indicate pairwise TBLASTX hits (e-value: 1−e3, bitscore: 50). (B) ONT read alignments flanking the 5′- and 3′-ends of whispovirus genomes.CC BY · PubMed Central
Fig 7 Nimaviral tyrosine recombinases. (A) Gene diagram of nimaviral tyrosine recombinases. (B) Maximum-likelihood phylogenetic tree of 342 tyrosine recombinases (555 sites; model: LG + R7). (C) Subtree of (B) showing the phylogenetic relationships of the nimaviral tyrosine recombinases.
Fig 7 Nimaviral tyrosine recombinases. (A) Gene diagram of nimaviral tyrosine recombinases. (B) Maximum-likelihood phylogenetic tree of 342 tyrosine recombinases (555 sites; model: LG + R7). (C) Subtree of (B) showing the phylogenetic relationships of the nimaviral tyrosine recombinases.CC BY · PubMed Central
Fig 8 Genome diagrams of 28S rDNA-specific whispoviruses. (A) Genome diagram of sesarmid nimavirus genomes. Arrows indicate predicted genes and their transcriptional orientations; blue, WSSV homologs; yellow, baculoviral inhibitor of apoptosis repeat-containing proteins; gray, hypothetical and other eukaryotic-like proteins; red, tyrosine recombinases. Blue ribbons indicate pairwise TBLASTX hits (e-value: 1−e3, bitscore: 50). (B) ONT read alignments flanking the 5′- and 3′-ends of 28S rDNA-specific whispoviruses. (C) 28S rDNA-specific whispovirus target site duplication.
Fig 8 Genome diagrams of 28S rDNA-specific whispoviruses. (A) Genome diagram of sesarmid nimavirus genomes. Arrows indicate predicted genes and their transcriptional orientations; blue, WSSV homologs; yellow, baculoviral inhibitor of apoptosis repeat-containing proteins; gray, hypothetical and other eukaryotic-like proteins; red, tyrosine recombinases. Blue ribbons indicate pairwise TBLASTX hits (e-value: 1−e3, bitscore: 50). (B) ONT read alignments flanking the 5′- and 3′-ends of 28S rDNA-specific whispoviruses. (C) 28S rDNA-specific whispovirus target site duplication.CC BY · PubMed Central
Fig 9 Ginger2 exaptation in sesarmid nimaviruses. (A) Genome diagram of sesarmid nimavirus genomes. Arrows indicate predicted genes and their transcriptional orientations; blue, WSSV homologs; gray, hypothetical and eukaryotic-like proteins; red, integrases. Blue ribbons indicate pairwise TBLASTX hits (e-value: 1−e3, bitscore: 50). (B) 5′- and 3′-end flanking sequences of the SiNMV genome. (C) Gene diagram of the integrase-like gene in the SiNMV genome. (D) Maximum-likelihood phylogenetic tree of 57 DDE transposases (422 sites; model: Q.insect + I + G4). (E) Subtree of (D) showing the phylogenetic relationships of Ginger2-like elements.
Fig 9 Ginger2 exaptation in sesarmid nimaviruses. (A) Genome diagram of sesarmid nimavirus genomes. Arrows indicate predicted genes and their transcriptional orientations; blue, WSSV homologs; gray, hypothetical and eukaryotic-like proteins; red, integrases. Blue ribbons indicate pairwise TBLASTX hits (e-value: 1−e3, bitscore: 50). (B) 5′- and 3′-end flanking sequences of the SiNMV genome. (C) Gene diagram of the integrase-like gene in the SiNMV genome. (D) Maximum-likelihood phylogenetic tree of 57 DDE transposases (422 sites; model: Q.insect + I + G4). (E) Subtree of (D) showing the phylogenetic relationships of Ginger2-like elements.CC BY · PubMed Central
Fig 10 Divergence time estimation of Nimaviridae. A total of nine nimaviral core protein sequences (12,905 sites) were used in the analysis. Blue bars indicate 95% confidence intervals of estimated divergence dates. Numbers on nodes correspond to two calibration points described in Table S5. All nodes were supported by a posterior probability of 1. Proposed viral genus names are quoted and unitalicized. WSSV, white spot syndrome virus; CoBV, Chionoecetes opilio bacilliform virus; MdWSSV-like, Metopaulias depressus WSSV-like virus; see Table 2 for the abbreviations for the other viruses.
Fig 10 Divergence time estimation of Nimaviridae. A total of nine nimaviral core protein sequences (12,905 sites) were used in the analysis. Blue bars indicate 95% confidence intervals of estimated divergence dates. Numbers on nodes correspond to two calibration points described in Table S5. All nodes were supported by a posterior probability of 1. Proposed viral genus names are quoted and unitalicized. WSSV, white spot syndrome virus; CoBV, Chionoecetes opilio bacilliform virus; MdWSSV-like, Metopaulias depressus WSSV-like virus; see Table 2 for the abbreviations for the other viruses.CC BY · PubMed Central

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Metadata

Authors
Kawato, S., Nozaki, R., Kondo, H., & Hirono, I.
Affiliations
  • Tokyo University of Marine Science and Technology (JP)
  • Laboratory of Genome Science, Tokyo University of Marine Science and Technology , Tokyo, Japan
ORCID
Venue
Microbiology Spectrum
Publisher
American Society for Microbiology
Published
2024-01-11
Volume
12
Issue
1
Pages
e0055923-e0055923
ISSN
2165-0497 (ISSN-L)
DOI
10.1128/spectrum.00559-23
PMC
PMC10871703
OpenAlex
W4389488615
Cited by
9
References
124
Citations by year
2026: 3 · 2025: 3 · 2024: 3
FWCI
0.98
Type
journal article
Language
en
Open access
Licence
Locations
  • Microbiology Spectrum (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • MEXT | Japan Science and Technology Agency (JPMJSA1806)
  • MEXT | Japan Society for the Promotion of Science (19J21518, JP22H00379)
Topics
  • Life Sciences › Immunology and Microbiology › Immunology › Aquaculture disease management and microbiota
  • Life Sciences › Immunology and Microbiology › Virology › Bacteriophages and microbial interactions
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Chromosomal and Genetic Variations
Keywords
usage, crustacean viruses, integrase, tyrosine recombinases, metagenome-assembled genomes, white spot syndrome virus, transposable elements, host-virus coevolution, terrestrial isopods, swimming crab, inverted terminal repeats
MeSH terms
DNA Viruses, Repetitive Sequences, Nucleic Acid, Genome, Integrases

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Kawato, S., Nozaki, R., Kondo, H., & Hirono, I. (2024). Integrase-associated niche differentiation of endogenous large DNA viruses in crustaceans. Microbiology Spectrum. https://doi.org/10.1128/spectrum.00559-23

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