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Rohrmann GF. Baculovirus Molecular Biology [Internet]. Bethesda (MD): National Center for Biotechnology Information (US); 2008.

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Baculovirus Molecular Biology [Internet].

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Chapter 1Introduction to the baculoviruses and their taxonomy

, PhD.

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The discovery of baculoviruses

The history of the discovery of baculoviruses is intimately related to the development of the silk industry that occurred in China as early as 5000 years ago. The culture of silkworms spread throughout Asia and reached Japan via Korea by about 300 A.D. and arrived in Europe by about 550 A.D. By the 12th century it was established in Italy and Spain and eventually spread to France and England and to Mexico by the 1500s. Silk production has been of major cultural significance in both China and Japan. It was a major item of commerce and in Japan is extensively documented in historic prints (1) and although no longer a major industry, silk production is still practiced symbolically by the Japanese royal family. (For a review of the history of silkworm culture, see (2)). As with any agricultural enterprise, problems were encountered caused by a variety of diseases, and these had to be confronted in order for the industry to flourish. Even before the germ theory of disease was introduced, a variety of different types of illnesses afflicting silkworms had been described, and methods to mitigate the effects of these diseases had been developed. With the advent of light microscopy, a prominent feature of one of the types of diseases was characterized by the presence of highly refractile occlusion bodies that were symptomatic of the affected insects. These were commonly polyhedron shaped (Fig. 1.1) and led to the naming of the diseases associated with these structures as 'polyhedroses' by the mid-1800s. Although the presence of infectious particles within occlusion bodies had been suggested earlier, it was not until the late 1940s that the presence of rod-shaped virions was convincingly demonstrated by electron microscopy (3). This and other investigations also established the crystalline nature of the occlusion body structure. Subsequently, two different types of polyhedrosis diseases were distinguished; those in which the polyhedra developed in nuclei and were called nuclear polyhedroses (NPVs), and those with occlusion bodies present in the cytoplasm. These were called cytoplasmic polyhedroses (CPVs) (4). In contrast to the rod-shaped, DNA-containing NPVs, the CPVs were observed to have icosahedral capsids and were placed in the Reoviridae (genus Cypovirus), a family of viruses with segmented double stranded RNA genomes. A second category of baculovirus characterized by the presence of small, granular, ellipsoidal-shaped occlusion bodies was originally reported in the 1920s (5) and was named granulosis viruses (GVs). The division of the baculoviruses into two major groups, the nuclear polyhedrosis viruses [now called nucleopolyhedroviruses (NPV)] and the granulosis viruses [now called granuloviruses (GVs)] based on occlusion body morphology defined the major taxonomical divisions of these viruses until the advent of molecular biology.

Fig

Figure

Fig. 1.1 Baculovirus occlusion bodies. Scanning EM by K. Hughes and R. B. Addison.

The terminology for these viruses went through a series of names, and it was not until 1973 that a nomenclature that included Borrelinavirus, Bergolidavirus, Smithiavirus, Moratorvirus and Vagoiavirus in honor of various historic individuals who had done early research on NPVs and GVs was changed and unified into the Baculoviridae (6). The name baculovirus was proposed by Mauro Martignoni, who because of his Italian-Swiss heritage was a Latin scholar. He suggested that they be named baculoviruses (family = Baculoviridae) because of the rod-shape of their virions, which is derived from Latin baculum = cane, walking stick, staff.

The definition is not in the name: Naming baculoviruses

Baculoviruses are normally named for the initial host from which they were isolated. Consequently, the type NPV species, AcMNPV, was named for its host, the alfalfa looper, Autographa californica (Ac). This naming would be straightforward except that AcMNPV infects a wide variety of lepidopteran insects and its name originated because of its initial association. Consequently, a variety of other virus isolates e.g., Galleria mellonella (GmNPV), Rachiplusia ou (RoNPV), and Plutella xylostella (PlxyNPV), although having unique names, are closely related (~96-98.5% at the amino acid sequence level) variants of AcMNPV. In addition, viruses were originally named by the first letter of the genus and species of their host. However, as more viruses were discovered, some infected different insects that had names with the same first letters. This resulted in different viruses with the same descriptor. Consequently, the first two letters of the genus and species have become the convention, i.e., AcMNPV should really be AucaMNPV. However, since AcMNPV, GmMNPV and RoMNPV have been used so extensively, the original abbreviations have been retained.

What defines a baculovirus?

Genomes and nucleocapsids

Baculoviruses are a very diverse group of viruses with double-stranded, circular, supercoiled genomes, with sizes varying from about 80 to over 180 kb and that encode between 90 and 180 genes. Of these genes, a common set of about 31 homologous genes has been identified, and there are probably others that cannot be recognized because of the extent of changes incorporated over time. The genome is packaged in rod-shaped virions that are over 200 μm in length and 30 μm in diameter. In the most well characterized baculoviruses, the virions are present as two types, occluded virions (ODV) and budded virions (BV). Although these two types of virions are similar in their nucleocapsid structure, they differ in the origin and composition of their envelopes and their roles in the virus life cycle (see below).

Occlusion bodies

Another defining characteristic of baculoviruses is their presence in occlusion bodies called polyhedra for NPVs and granules or capsules for GVs. Occlusion bodies are highly stable and can resist most normal environmental conditions thereby allowing virions to remain infectious indefinitely. Evidence suggests that they can survive passage through the gastrointestinal tract of birds, which can facilitate their dispersal (7). The occlusion body is composed of a crystalline matrix composed of a protein called polyhedrin in NPVs and granulin in GVs. Although they have different names, these two proteins are closely related.

Baculovirus hosts

Over the years, baculoviruses have been reported from a variety of different species of invertebrates. However, the only well-documented hosts are Diptera, Hymenoptera, and Lepidoptera. Convincing documentation has been reported for occluded virions resembling NPVs in a caddis fly (Trichoptera) (8) and a shrimp species (9, 10). An occluded baculovirus-like virus was also reported for a thysanuran, but it did not appear to affect its host and transmission studies failed (11). Baculoviruses have also been reported from Orthoptera (12), but later these were classified as pox viruses, and from Coleoptera, but these are not occluded and were later placed in an unassigned category. Reports of infection of other insects, e.g., a coleopteran (13) could not be confirmed (Rohrmann, unpublished). In addition, there is a report of a baculovirus infecting a neuropteran (14). However, the infection occurred under laboratory conditions, where neuropterans were fed on lepidoptera that had died of an NPV infection. Consequently, the neuropterans were likely heavily contaminated from their food source, and although they appeared to die of an NPV infection, they were probably exposed to an unusually high virus dose. Naturally infected Neuroptera have not been documented. An example of the distribution of baculoviruses in insects that has been reported in the literature (15) is shown in Table 1.1. These numbers should be viewed with caution because many of the reports could be of the same virus infecting different species. However, they do give a good general overview of the likely distribution of baculoviruses. Of particular note is that GVs are confined to the Lepidoptera. In addition, all the hymenopteran hosts belong to a suborder called Symphyta that are comprised of sawflies (named because their ovipositor resembles a saw and in some species is used to cut into plants for egg deposition). Sawflies resemble Lepidoptera; they have herbivorous, caterpillar-like larvae and are distinct from the other hymenopteran suborder, Apocrita, which includes bees, ants, and wasps.

Table 1.1. Distribution1 of baculoviruses in insect orders (15).

Insect ordersNPVsGVs
Diptera27
Hymenoptera30
Lepidoptera456148

1Indicates the number of species that have been reported to be infected

Other defining features of the Baculoviridae: a virus encoded RNA polymerase

In addition to invertebrate hosts, circular, supercoiled double-stranded DNA genomes, rod-shaped enveloped nucleocapsids, and the production of occluded virions, an additional defining feature of baculoviruses is that they encode their own RNA polymerase. The core enzyme is composed of four subunits and functions in the transcription of late promoters that are initiated within a novel sequence element (see Chapter 6). Whereas other DNA viruses of eukaryotes encode their own polymerase, e.g., poxviruses, they replicate in the cytoplasm and therefore do not have access to the host cell transcriptional apparatus located in nuclei. Baculoviruses, in contrast, exploit the host cell transcriptional system for expressing their early genes, but after initiation of DNA replication they are dependent upon their own RNA polymerase for transcription of their late and very late genes.

Baculovirus Diversity

The recent proliferation of baculovirus genome sequences has greatly expanded our understanding of their diversity and evolution. This has yielded distinct patterns of virus relatedness (Fig. 1.2) in which virus lineages are associated by the host that they infect. It has been proposed that members of the Baculoviridae be divided into four major phylogenetic groups (16). The viruses of Lepidoptera would be divided into Alpha- and Beta-baculoviruses encompassing the NPVs and GVs, respectively, and those infecting Hymenoptera and Diptera would be named Gamma- and Deltabaculoviruses, respectively (Table 1.2). Such patterns of host-associated virus diversity were first observed for small DNA viruses (papilloma and polyoma viruses) of primates (17) and suggested for baculoviruses based on N-terminal polyhedrin and granulin sequences (18). In this process, viruses associate with a host and as their host becomes genetically isolated and speciates, so does the virus in a process called host-dependent evolution. As more sequence data has become available, this process has been more convincingly demonstrated for baculoviruses (19) and is clearly reflected in Fig. 1.2 in which the major lineages are clustered into clades based on the host insect that they infect. In GVs, host-dependent evolution has been suggested on the level of insect families (20). A major division has been observed in the lepidopteran NPVs that has resulted in the separation of this lineage into two major Groups, I and II (21). These two groups differ significantly in gene content, most notably Group I NPVs use GP64 as their BV fusion protein, whereas Group II NPVs lack gp64 and utilize a protein called F (22). There are also 11 other genes that appear to be found only in Group I NPVs (Table 1.3), suggesting that the derivation of this group may be more complicated than simply the incorporation of gp64 (23). Although the list of host insects provides information on baculovirus distribution, sequence analysis of common sets of genes from a wide variety of baculoviruses has provided a picture of the actual extent of their diversity (24). From this data, a picture of the lepidopteran viruses has emerged. However, more information on viruses from the other insect orders is needed to complete our understanding of baculovirus evolution.

Fig

Figure

Fig. 1.2. Phylogenetic relatedness of LEF8 from selected baculoviruses. Neighbor joining; bootstrap analysis (1000 reps).

Table 1.2 Genera of the Baculoviridae

GenusMembers
AlphabaculovirusLepidopteran NPVs
BetabaculovirusLepidopteran GVs
GammabaculovirusHymenopteran NPVs
DeltabaculovirusDipteran NPVs

Table 1.3. Genes1 found in and unique to all sequenced Group I NPV genomes

Ac1 (ptp), Ac16 (BV-ODV26), Ac27 (iap-1), Ac30, Ac42 (gta), Ac72, Ac73, Ac114, Ac124, Ac128 (gp64), Ac 132, Ac151 (ie2)

1Genes are designated by their AcMNPV orf number

Multiple versus single nucleocapsids

A prominent feature of the nucleocapsids within polyhedra is their organization into either single or multiple aggregates of nucleocapsids within an envelope. For example, in some NPVs there can be from 1 to 15 nucleocapsids per envelope, with bundles of 5 to 15 predominating. In contrast, strains defined as having a single nucleocapsid per envelope rarely show more than one nucleocapsid per envelope (25). Because this feature is so distinctive and characteristic of specific isolates, it was incorporated into the early nomenclature such that NPVs were categorized as either MNPV or SNPVs (also previously called multiply or singly embedded virions [MEV and SEV]). In addition, whereas MNPVs and SNPVs were both found in lepidopteran viruses, only SNPVs were observed in other insect orders. GVs were also categorized as singly enveloped; however, multiple GVs, although rare, have been described (26). With the accumulation of DNA sequence data that allowed for the determination of definitive phylogenetic relationships, it was found that the MNPV and SNPV division did not conform to the phylogeny of the viruses. For example, at one point BmNPV was considered the type virus for SNPVs because of its production of predominantly single nucleocapsids (27). However, when sequence data became available, BmNPV was found to be closely related to AcMNPV (both belong to Group I), whereas other MNPVs such as LdMNPV and SeMNPV are more distantly related Group II viruses, which also includes SNPV-type viruses. Despite agreement that the MNPV and SNPV designation is not a useful taxonomical trait, it continues to be employed, in part for historical continuity, and also because it can be a convenient method for distinguishing different viruses that are pathogenic for the same host, e.g., OpMNPV and OpSNPV which both infect Orgyia pseudotsugata, but are members of Group I and II, respectively.

Gene content and organization

Although there are major differences in the sizes of baculovirus genomes, a few patterns are evident (Table 1.4). The viruses of members of the Hymenoptera contain the smallest genomes at a little over 80 kb. In contrast, the GV genomes vary from 101 kb (PlxyGV) up to 178 kb (XecnGV). Group I NPVs cluster around 130 kb, whereas Group II show a much higher degree of diversity, varying from about 130 to almost 170 kb. The small size of the hymenopteran NPV genomes might be attributed to a restricted life cycle confined to replication in insect gut cells (28). Consequently, unlike other baculoviruses that cause systemic infections, genes required for spread throughout the insect, where the virus encounters and replicates in a variety of tissues, might not be necessary. In contrast, the large size of a Group II NPV (LdMNPV), which at 161 kb is about 30 kb larger than many other NPV genomes, can be attributed to a combination of repetitive genes (16 bro [baculovirus repeated orf] genes) that add about half of the additional 30 kb, while genes not found in smaller genomes add most of the remainder. These additional genes encode ribonucleotide reductase subunits and two enhancin genes (29). In other viruses with large genomes (e.g., XecnGV), repeated genes including 10 bro and 4 enhancin genes, comprise up to 17% (30 kb) of the genome (30). Despite the large difference in gene content in GV genomes as reflected in their size range, their genomes are surprisingly collinear (31). In contrast, NPVs even from the same order (Lepidoptera) show a high degree of variation (32).

Table 1

Table

Table 1.4. Genome size and predicted ORF content* of selected baculoviruses

Regulatory content: homologous regions (Hrs)

In addition to containing a set of genes encoding proteins required for productive infection, most baculovirus genomes also contain homologous repeated regions. In AcMNPV, hrs are comprised of repeated units of about 70-bp with an imperfect 30-bp palindrome near their center. Hrs are repeated at eight locations in the genome with 2 to 8 repeats at each site. They are highly variable and although they are closely related within a genome, they may show very limited homology between different viruses. For example, in the CpGV genome, tandem repeated sequences are not evident, although a 75-bp imperfect palindrome is present at 13 different locations on the genome (33). In addition, in the TnSNPV (group II) sequence, hrs were not found (34). Hrs have been implicated as both transcriptional enhancers and origins of DNA replication for some baculoviruses (35-40)

Conservation of baculovirus genes

Despite the diversity in gene content present in different baculovirus genomes, a set of about 31 genes that are present in all sequenced baculovirus genomes has been identified (Table 1.5). This set should be viewed with caution; however, as it is likely that many shared genes have diverged to such an extent that their relatedness cannot be readily determined. This is particularly true of the dipteran virus that is most distant from the baculoviruses of Lepidoptera and Hymenoptera. Of the conserved genes, about half are virion-associated proteins that are involved in capsid structure, the occlusion-derived virus envelope, and larval infectivity. Most of the others are related to DNA replication or processing, and late or very late transcription. Despite this limited set of genes that baculoviruses share, they do provide insight into some of the major functions required of all baculoviruses such as a common virion structure, the necessity to infect gut cells, and the use of a novel polymerase for the expression of late genes. Furthermore, there are sets of genes specific to, and conserved in, each clade of viruses such as gp64 in Group I NPVs and a number of GV-specific genes (see below). These genes likely reflect major recombination events that altered the properties of the viruses to such an extent that they subsequently developed along distinctive phylogenetic pathways. The observation that different types of NPVs and GVs and other types of DNA viruses (e.g., entomopox, ascovirus, nudivirus) have the potential to simultaneously infect the same insect indicates how via recombination, genes can be transferred between different viruses and between viruses and the host insect.

Table 1

Table

Table 1.5. Conserved genes in baculoviruses and nudiviruses

Granulovirus-specific genes

In addition to their occlusion body morphology, the pathology of GV infection differs from NPVs. For example, their replication is not confined to nuclei as the nucleus and cytoplasm appear to merge during GV infections. The presence of GV specific genes may be a reflection of these differences. Granuloviruses encode a number of genes that are found in all GV genomes. Of these GV genes, 14 appear to be specific to GVs, whereas others, although found in all GV genomes, are also found in a few other baculoviruses. Examples of the latter are DNA ligase and helicase-2 homologs that, in addition to GV genomes, are also present in one NPV genome (LdMNPV). The helicase-2 homolog is also found in an additional NPV (Maco-B-NPV). There are other GV-specific genes that are found in most, but not all, GV genomes. The only GV specific gene that has been characterized is the XecnGV metalloproteinase. It was found to have proteinase activity and was inhibited by metalloproteinase inhibitors (41).

In addition to baculoviruses, there are a number of viruses pathogenic for invertebrates that have large double-stranded DNA genomes. These include nudiviruses, ascoviruses, irridoviruses and entomopox viruses. However, with the exception of nudiviruses, all these viruses replicate in the cytoplasm or exhibit a combination of both nuclear and cytoplasmic replication (ascoviruses) (reviewed in (42)). In addition, although nudiviruses are an unassigned genus of viruses, they closely resemble baculoviruses and were originally classified as non-occluded baculoviruses, although occlusion bodies have been occasionally reported (e.g., see (43)). Their similarity to baculoviruses includes nuclear replication and rod-shaped, enveloped, nucleocapsids. However, they were removed from the baculoviruses because they are nonoccluded. Hence the etymology of their name (latin nudi = naked, bare, uncovered), because they lack occlusion bodies. As more genome sequence data has become available, homologs of baculovirus genes have been found in many different categories of invertebrate viruses. These appear to be the result of lateral transfer, probably during co-infection of the same host (44). However, the nudiviruses share a significant number of the conserved core genes found in all baculoviruses and therefore their presence does not appear to be a result of lateral gene transfer. As shown in Table 1.5, nudivirus genomes contain homologs of 19 of the 31 core conserved baculovirus genes. These include homologs of genes encoding the novel baculovirus RNA polymerase subunits, virion structural proteins, and a set of genes required for infection of gut tissue. In addition, genes such as DNA helicase are present in many large DNA virus genomes, and LEF-8 has homology to RNA polymerase subunits from many organisms. However, homology searches group these genes from baculoviruses and nudiviruses together. Therefore, based on morphology and molecular phylogeny, these two groups of viruses clearly share membership in a distinct viral lineage.

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1Indicates the number of species that have been reported to be infected

1Genes are designated by their AcMNPV orf number

Copyright © 2008, George Rohrmann.
Bookshelf ID: NBK1764
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