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Evolutionary timeline of insect dsDNA virus and their associated host species. Nodes 8 and 10 were used to calibrate the insect dsDNA virus phylogeny, and the host tree is drawn from the literature ( SI Text ). Age estimates and their 95% HPD intervals for the corresponding nodes are shown in Table 1. Colors associate each virus to its respective host family.
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To understand how extant viruses interact with their hosts, we need a historical framework of their evolutionary association. Akin to retrovirus or hepadnavirus viral fossils present in eukaryotic genomes, bracoviruses are integrated in braconid wasp genomes and are transmitted by Mendelian inheritance. However, unlike viral genomic fossils, they h...
Contexts in source publication
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... (CiBV) and Cotesia congregata bracovirus (CcBV) was set to 103.38 ± 4.41 Mya, corresponding to C. inanitus (Cheloninae) and C. congregata (Microgastrinae) lineage divergence times. Similarly, the TMRCA of CcBV and Toxoneuron nigriceps bracovirus (TnBV) was set at ∼87 ± 5 Mya, the divergence times between the Micro- gastrinae and Cardiochilinae (Fig. S2). Because bracoviruses are now included in the insect dsDNA virus phylogeny, a Bayesian inference approach, using an autocorrelated lognormal relaxed clock and calibration priors based on the above age estimates, was performed to estimate the divergence times of the nudivirus and baculovirus dsDNA virus ...
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... estimates and 95% highest posterior density (HPD) in- tervals were obtained for each node (virus tree in Fig. 2; Table 1). The TMRCA of nudiviruses and baculoviruses (node 1) is estimated at ∼310 Mya (Carboniferous, late Paleozoic Era). The TMRCA of the nudivirus (node 2) and the baculovirus (node 4) lineages are estimated at ∼222 Mya (Triassic, early Mesozoic Era) and ∼178 Mya (Jurassic, middle Mesozoic Era), respec- tively. Furthermore, the ...
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... relate the evolution of the insect dsDNA viruses to their hosts, the host species tree (Fig. 2) was drawn from the literature (SI Text). This tree shows that the insect and crustacean lineages associated with the dsDNA viruses of this study appeared in the middle Paleozoic Era and the diversification of insect orders occurred during the second half of the Paleozoic Era. Di- versification within insect orders occurred mainly ...
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... the late Carboniferous Period, when the nudivirus and baculovirus families diverged, insects were also diversifying into new orders (Fig. 2). The phylogenies of both the baculovirus and nudivirus lineages are clearly not the mirror images of that of their hosts. This lack of cophylogeny shows that the diversification of both virus families and host orders occurred independently. On the macroevolutionary timescale, this finding suggests that these viruses may have colonized ...
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... at the late Carboniferous Period, the baculovirus lineage appeared shortly after the appearance of holometabo- lous insects, which are insects with larval stages undergoing complete metamorphosis (Fig. 2). These insects form a mono- phyletic clade, including (among others) the orders Diptera, Lepidoptera, Coleoptera, and Hymenoptera (39). Extant bacu- loviruses have only been characterized in holometabolous insect hosts from the orders Diptera, Hymenoptera, and Lepidoptera. Baculovirus phylogenetic studies have shown the ancient co- ...
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... appear to be a more generalist group of viruses. Although the pathological data are sparse, they are known to affect adult as well as larval stages with more varied infection strategies. The lack of environmentally resistant occlusion bodies in nudiviruses has been proposed to Table 1. Age estimates and 95% HPD intervals of the nodes indicated on Fig. 2 Node Time, Mya 95% HPD, Mya 1 312 127-569 2 222 107-392 3 190 101-340 4 178 40-368 5 153 31-321 6 128 11-265 7 116 21-235 8 104 95-112 9 8 lead to the evolution of close association with their hosts, often involving viral persistence or latency (42). Nudiviruses have a broad host spectrum (Fig. 2), encompassing many insect orders but ...
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... and 95% HPD intervals of the nodes indicated on Fig. 2 Node Time, Mya 95% HPD, Mya 1 312 127-569 2 222 107-392 3 190 101-340 4 178 40-368 5 153 31-321 6 128 11-265 7 116 21-235 8 104 95-112 9 8 lead to the evolution of close association with their hosts, often involving viral persistence or latency (42). Nudiviruses have a broad host spectrum (Fig. 2), encompassing many insect orders but also crustaceans like PmNV (17,19). The derived phyloge- netic position of PmNV may imply a large host shift between insects and crustaceans, which could date as far back as 125 ...
Citations
... Insects host a huge diversity of viruses (Bonning 2020;Shi et al. 2016;Yang et al. 2023), some with evolutionary lineages dating back approximately 300 million years (Thézé et al. 2011). Historically, insect virology has focused on economically, socially, or ecologically significant viruses, primarily in silkworms, pollinators, and insect vectors. ...
... We used a Bayesian inference approach implemented in BEAST v1.10.4 [40] to estimate the divergence time of baculoviruses. Twenty core genes that were conserved in all baculoviruses and nudiviruses were identified by Blastp searches [31,41]. In this study, the nucleotide sequences of 20 core genes from 60 baculoviruses and Gryllus bimaculatus nudivirus (GbNV) which was set to an outgroup were aligned separately using the MAFFT programme in Geneious Prime, and then the combined sequences were analysed in BEAST. ...
... The maximum clade credibility tree (Fig. 3) of baculoviruses, which includes the MyseMNPV-Hb related viruses, was constructed based on the nucleotide sequences of 20 core genes shared with nudiviruses to estimate the divergence time of the baculoviruses. We used the age estimated from Thézé et al. [41] to calibrate the baculoviruses phylogeny. With GbNV as an outgroup, the TMRCA of all baculoviruses was set as 178±15 Mya (Fig. 3, node 2), which is the divergence time point between the deltabaculoviruses and other baculoviruses. ...
... Similarly, the TMRCA of alphabaculovirus, betabaculovirus, and gammabaculovirus was set as 153±15 Mya (Fig. 3, node 3). The results showed that the TMRCA of baculovirus and nudivirus was approximately 317 Mya (Fig. 3, node 1; Table 2), which is consistent with the findings of Thézé et al. [41]. ...
Baculoviruses are highly host specific, and their host range is usually restricted to a single or a few closely related insect species, except for few virus species, e.g. Alphabaculovirus aucalifonicae and Alphabaculovirus mabrassicae . In this study, two new alphabaculovirus isolates were isolated from the larvae of Mamestra brassicae and Mythimna separata , which were named as Mamestra brassicae multiple nucleopolyhedrovirus isolate QD (MbMNPV-QD) and Mythimna separata multiple nucleopolyhedrovirus isolate Hb (MyseMNPV-Hb), respectively. The Kimura two-parameter values based on the concatenated 38 core genes of baculovirus revealed that MbMNPV (isolates QD/CHb1/K1/CTa), MyseMNPV-Hb, Helicoverpa armigera multiple nucleopolyhedrovirus (HearMNPV) and Mamestra configurata nucleopolyhedrovirus B (MacoNPV-B) were different isolates of a same virus species. A phylogenetic tree of baculoviruses and nudiviruses constructed from their 20 homologous gene sequences, and that of their isolated hosts constructed from 13 protein-coding genes of the insect mitochondrial genomes, were used to analyse the coevolution of baculoviruses with their isolated hosts. The results showed that M. brassicae was the most likely ancestral host of these virus isolates, included MbMNPV isolates, MyseMNPV-Hb, HearMNPV, and MacoNPV-B. Therefore, we concluded that these virus isolates belong to the existing virus species – Alphabaculovirus mabrassicae with M. brassicae as their ancestral host.
... Viruses do not leave fossil records, but we can trace their evolutionary history by linking it to that of their host (40)(41)(42)(43). As described in a previous section, the evolutionary history of majaniviruses is tightly intertwined with the phylogeography of penaeid shrimps. ...
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.
... Comparative genomics of braconid wasps and bracoviruses, whose genomes are integrated into the genome of braconid wasps, together with baculoviruses and nudiviruses, which are the closest known relatives of bracoviruses, revealed that baculoviruses and nudiviruses evolved from a common ancestor 310 million years ago during the Carboniferous period in the Paleozoic era (Bezier et al., 2009;Theze et al., 2011). Phylogenetic analyses have also extrapolated that Culex nigripalpus NPV (CuniNPV) from dipteran insects is the most ancient lineage of baculoviruses and branched the hymenopteran Neodiprion lecontei NPV (NeleNPV) and Neodiprion sertifer NPV (NeseNPV) before the separation of lepidopteran NPVs and granulo viruses (GVs) (Herniou et al., 2004;Lauzon et al., 2006). ...
Grasserie is a major infectious disease of silkworms caused by the Bombyx mori nuclear polyhedrosis virus. The virus belongs to the family Baculoviridae and is composed of a polyhedron with a single molecule of circular supercoiled double-stranded deoxyribose nucleic acid. The disease causes massive mortality (more than 60% of the total crop loss caused by different diseases), causing significant great crop loss to the sericulturists by reducing the cocoon crop and silk produce. There has been no effective solution for preventing and treating the disease. In the present review, the authors explore the subject in detail and inspire the researchers to search for molecular mechanisms of gene action and promote disease-resistant silkworm breeding.. KEYWORDS :Bombyx mori,,Baculoviridae, Disease resistance, Nuclear polyhedrosis virus, Polyhedron, Silkworm
... Through evolutionary convergence, wasps in each DEV-hosting lineage have coopted these virions or VLPs for a new essential function: transfer of virulence factors to hosts that enable wasp offspring to develop (5). The largest DEV-associated lineage evolved ~100 million years ago from a virus in the family Nudiviridae that integrated into the germline of a parasitoid in the family Braconidae (7)(8)(9)(10). Speciation events have since given rise to a hyperdiverse, monophyletic assemblage (~50,000 spp.) of braconids named the microgastroid complex with DEVs named bracoviruses (BVs) (11). ...
Bracoviruses (BVs) are endogenized nudiviruses in parasitoid wasps of the microgastroid complex (order Hymenoptera: Family Braconidae). BVs produce replication-defective virions that adult female wasps use to transfer DNAs encoding virulence genes to parasitized hosts. Some BV genes are shared with nudiviruses and baculoviruses with studies of the latter providing insights on function, whereas other genes are only known from nudiviruses or other BVs which provide no functional insights. A proteomic analysis of Microplitis demolitor bracovirus (MdBV) virions recently identified 16 genes encoding nucleocapsid components. In this study, we further characterized most of these genes. Some nucleocapsid genes exhibited early or intermediate expression profiles, while others exhibited late expression profiles. RNA interference (RNAi) assays together with transmission electron microscopy indicated vp39 , HzNVorf9-like2 , HzNVorf93-like , HzNVorf106-like , HzNVorf118-like , and 27b are required to produce capsids with a normal barrel-shaped morphology. RNAi knockdown of vlf-1a , vlf-1b-1 , vlf-1b-2 , int-1, and p6.9-1 did not alter the formation of barrel-shaped capsids but each reduced processing of amplified proviral segments and DNA packaging as evidenced by the formation of electron translucent capsids. All of the genes required for normal capsid assembly were also required for proviral segment processing and DNA packaging. Collectively, our results deorphanize several BV genes with previously unknown roles in virion morphogenesis.
IMPORTANCE
Understanding how bracoviruses (BVs) function in wasps is of broad interest in the study of virus evolution. This study characterizes most of the Microplitis demolitor bracovirus (MdBV) genes whose products are nucleocapsid components. Results indicate several genes unknown outside of nudiviruses and BVs are essential for normal capsid assembly. Results also indicate most MdBV tyrosine recombinase family members and the DNA binding protein p6.9-1 are required for DNA processing and packaging into nucleocapsids.
... The tree shown in Fig. 6 displays two well-defined viral and eukaryal branches. Due to the distribution in eukaryotes and the absence of bacterial homologs, it appears that viral Erv1/Alr was acquired once by the NCLDV ancestor prior to the emergence of the last eukaryotic common ancestor and, later, in evolutionary-related insect-infecting Nudiviridae and Baculoviridae (Thézé et al. 2011). Proteins belonging to the same group of enzymes in these viral families had previously been reported and characterized. ...
The Nucleo-Cytoplasmic Large DNA Viruses (NCLDVs) infect a wide range of eukaryotic species, including amoeba, algae, fish, amphibia, arthropods, birds, and mammals. This group of viruses has linear or circular double-stranded DNA genomes whose size spans approximately one order of magnitude, from 100 to 2500 kbp. The ultimate origin of this peculiar group of viruses remains an open issue. Some have argued that NCLDVs’ origin may lie in a bacteriophage ancestor that increased its genome size by subsequent recruitment of eukaryotic and bacterial genes. Others have suggested that NCLDVs families originated from cells that underwent an irreversible process of genome reduction. However, the hypothesis that a number of NCLDVs sequences have been recruited from the host genomes has been largely ignored. In the present work, we have performed pangenomic analyses of each of the seven known NCLDVs families. We show that these families' core- and shell genes have cellular homologs, supporting possible escaping-gene events as part of its evolution. Furthermore, the detection of sequences that belong to two protein families (small chain ribonucleotide reductase and Erv1/Air) and to one superfamily [2OG-Fe(II) oxygenases] that are for distribution in all NCLDVs core and shell clusters encoding for oxygen-dependent enzymes suggests that the highly conserved core these viruses originated after the Proterozoic Great Oxidation Event that transformed the terrestrial atmosphere 2.4–2.3 Ga ago.
... Furthermore, PIF proteins are also found in the viriform particles formed in the calyx of female braconid wasps, which are classified in the genus Bracoviriform in the recently renamed family Polydnaviriformidae [5,6,23]. These expressed bracoviriform PIF proteins originate from the endogenization of an ancient nudivirus [5,12,27]. ...
Viruses of four families of arthropod-specific, large dsDNA viruses (the nuclear arthropod large DNA viruses, or NALDVs) possess homologs of genes encoding conserved components involved in the baculovirus primary infection mechanism. The presence of such homologs encoding per os infectivity factors (pif genes), along with their absence from other viruses and the occurrence of other shared characteristics, suggests a common origin for the viruses of these families. Therefore, the class Naldaviricetes was recently established, accommodating these four families. In addition, within this class, the ICTV approved the creation of the order Lefavirales for three of these families, whose members carry homologs of the baculovirus genes that code for components of the viral RNA polymerase, which is responsible for late gene expression. We further established a system for the binomial naming of all virus species in the order Lefavirales, in accordance with a decision by the ICTV in 2019 to move towards a standardized nomenclature for all virus species. The binomial species names for members of the order Lefavirales consist of the name of the genus to which the species belongs (e.g., Alphabaculovirus), followed by a single epithet that refers to the host species from which the virus was originally isolated. The common names of viruses and the abbreviations thereof will not change, as the format of virus names lies outside the remit of the ICTV.
Supplementary Information
The online version contains supplementary material available at 10.1007/s00705-023-05793-8.
... However, these analyses also demonstrated the polyphyly of family Polydnaviridae. Bracoviriforms are highly likely derivatives of an ancient member of the betanudiviral clade of family Nudiviridae [11,12,[16][17][18] which, together with families Baculoviridae, Hytrosaviridae, and Nimaviridae, constitute the doublestranded DNA virus class Naldaviricetes [19] that is currently unassigned but likely belongs in the realm Varidnaviria [20][21][22]. By contrast, there is no evidence of ichnoviriforms being related to bracoviriforms and/or deriving from nudivirids, and their possible virus ancestor remains elusive [11,12,[16][17][18]23]. ...
... Bracoviriforms are highly likely derivatives of an ancient member of the betanudiviral clade of family Nudiviridae [11,12,[16][17][18] which, together with families Baculoviridae, Hytrosaviridae, and Nimaviridae, constitute the doublestranded DNA virus class Naldaviricetes [19] that is currently unassigned but likely belongs in the realm Varidnaviria [20][21][22]. By contrast, there is no evidence of ichnoviriforms being related to bracoviriforms and/or deriving from nudivirids, and their possible virus ancestor remains elusive [11,12,[16][17][18]23]. ...
The International Committee on Taxonomy of Viruses (ICTV) recently accepted viriforms as a new polyphyletic category of classifiable virus-derived genetic elements, juxtaposed to the polyphyletic virus, viroid, and satellite nucleic acid categories. Viriforms are endogenized former viruses that have been exapted by their cellular hosts to fulfill functions important for the host's life cycle. While morphologically resembling virions, particles made by viriforms do not package the viriform genomes but instead transport host genetic material. Known viriforms are highly diverse: members of family Polydnaviriformidae (former Polydnaviridae) have thus far been found exclusively in the genomes of braconid and ichneumonid parasitoid wasps, whereas the completely unrelated gene transfer agents (GTAs) are widely distributed among prokaryotes. In addition, recent discoveries likely extend viriforms to mammalian genomes. Here, we briefly outline the properties of these viriform groups and the first accepted and proposed ICTV frameworks for viriform classification.
... As both AC81 and P33 are conserved among the members of the Lefavirales, we speculate that the pathway of viral disulfide bond oxidation and isomerization is an ancient mechanism as these viruses evolved more than 300 million years ago (40). The functions of the 13 core genes shared by these viruses are now all identified, and these genes are involved in DNA replication/transcription, oral infection/entry, and disulfide bond formation. ...
The correct formation of native disulfide bonds is critical for the proper structure and function of many proteins. Cellular disulfide bond formation pathways commonly consist of two parts: sulfhydryl oxidase-mediated oxidation and disulfide isomerase-mediated isomerization. Some large DNA viruses, such as baculoviruses, encode sulfhydryl oxidases, but viral disulfide isomerases have not yet been identified, although G4L in poxvirus has been suggested to serve such a function. Here, we report that the baculovirus core gene ac81 encodes a putative disulfide isomerase. ac81 is conserved in baculoviruses, nudiviruses, and hytrosaviruses. We found that AC81 homologs contain a typical thioredoxin fold conserved in disulfide isomerases. To determine the role of AC81, a series of Autographa californica nucleopolyhedrovirus (AcMNPV) bacmids containing ac81 knockout or point mutations was generated, and the results showed that AC81 is essential for budded virus production, multinucleocapsid occlusion-derived virus (ODV) formation, and ODV embedding in occlusion bodies. Nonreducing Western blot analysis indicated that disulfide bond formation in per os infectivity factor 5 (PIF5), a substrate of the baculoviral sulfhydryl oxidase P33, was abnormal when ac81 was knocked out or mutated. Pulldown assays showed that AC81 interacted with PIF5 and P33 in infected cells. In addition, two critical regions that harbor key amino acids for function were identified in AC81. Taken together, our results suggest that AC81 is a key component involved in the baculovirus disulfide bond formation pathway and likely functions as a disulfide isomerase. IMPORTANCE Many large DNA viruses, such as poxvirus, asfarvirus, and baculovirus, encode their own sulfhydryl oxidase to facilitate the disulfide bond formation of viral proteins. Here, we show that AC81 functions as a putative disulfide isomerase and is involved in multiple functions of the baculovirus life cycle. Interestingly, AC81 and P33 (sulfhydryl oxidase) are conserved in baculoviruses, nudiviruses, and hytrosaviruses, which are all insect-specific large DNA viruses replicating in the nucleus, suggesting that viral disulfide bond formation is an ancient mechanism shared by these viruses.
... PIF-mediated entry is a commonly used and ancient entry mechanism since PIFs are highly conserved in a diverse range of viruses with large, circular, double-stranded DNA genomes that co-evolved with their hosts for millions of years [8,[52][53][54]. BmNPV ODV entry is a complicated process that includes at least 9 PIF proteins. ...
Baculoviruses are virulent pathogens that infect a wide range of insects. They initiate infections via specific interactions between the structural proteins on the envelopes of occlusion-derived virions (ODVs) and the midgut cell surface receptors in hosts. However, host factors that are hijacked by baculoviruses for efficient infection remain largely unknown. In this study, we identified a membrane-associated protein sucrose hydrolase (BmSUH) as an ODV binding factor during Bombyx mori nucleopolyhedrovirus (BmNPV) primary infection. BmSUH was specifically expressed in the midgut microvilli where the ODV-midgut fusion happened. Knockout of BmSUH by CRISPR/Cas9 resulted in a significantly higher survival rate after BmNPV orally infection. Liquid chromatography-tandem mass spectrometry analysis and co-immunoprecipitation analysis demonstrated that PIF protein complex required for ODV binding could interact with BmSUH. Furthermore, fluorescence dequenching assay showed that the amount of ODV binding and fusion to the midgut decreased in BmSUH mutants compared to wild-type silkworm, suggesting the role of BmSUH as an ODV binding factor that mediates the ODV entry process. Based on a multilevel survey, the data showed that BmSUH acted as a host factor that facilitates BmNPV oral infection. More generally, this study indicated that disrupting essential protein-protein interactions required for baculovirus efficient entry may be broadly applicable to against viral infection.
