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J Virol. Dec 2001; 75(23): 11811–11820.
PMCID: PMC114767

Complete Genome Sequence of the Shrimp White Spot Bacilliform Virus

Abstract

We report the first complete genome sequence of a marine invertebrate virus. White spot bacilliform virus (WSBV; or white spot syndrome virus) is a major shrimp pathogen with a high mortality rate and a wide host range. Its double-stranded circular DNA genome of 305,107 bp contains 181 open reading frames (ORFs). Nine homologous regions containing 47 repeated minifragments that include direct repeats, atypical inverted repeat sequences, and imperfect palindromes were identified. This is the largest animal virus that has been completely sequenced. Although WSBV is morphologically similar to insect baculovirus, the two viruses are not detectably related at the amino acid level. Rather, some WSBV genes are more homologous to eukaryotic genes than viral genes. In fact, sequence analysis indicates that WSBV differs from all known viruses, although a few genes display a weak homology to herpesvirus genes. Most of the ORFs encode proteins that bear no homology to any known proteins, either suggesting that WSBV represents a novel class of viruses or perhaps implying a significant evolutionary distance between marine and terrestrial viruses. The most unique feature of WSBV is the presence of an intact collagen gene, a gene encoding an extracellular matrix protein of animal cells that has never been found in any viruses. Determination of the genome of WSBV will facilitate a better understanding of the molecular mechanism underlying the pathogenesis of the WSBV virus and will also provide useful information concerning the evolution and divergence of marine and terrestrial animal viruses at the molecular level.

White spot bacilliform virus (WSBV) or white spot syndrome virus (WSSV) is a major shrimp pathogen that is highly virulent in penaeid shrimp, the most important species used in aquaculture, and can also infect most species of crustacean (15, 32). Infection of penaeid shrimp by WSBV can result in mortality of up to 90 to 100% within 3 to 7 days (57). A major outbreak of WSBV infection in 1993 resulted in a 70% reduction in shrimp production in China (14, 57) and has raised major concerns in aquaculture around the world. Prevention and inhibition of infection by this virus can be difficult due largely to the ability of WSBV to survive for a long time in the environment (2 years in a shrimp pond) and also due to a poor understanding of this virus at the molecular level.

WSBV was originally classified as an unassigned member of the Baculoviridae because of its rod-shaped, enveloped morphology (20). However, it was recently excluded from the baculovirus family and is temporarily unclassified due to the lack of molecular information (53). The virus is known generally as white spot syndrome virus (WSSV) (31), and a new genus name, Whispovirus, was proposed by Vlak et al. (48). Sequence analysis of individual genes and proteins later showed that most WSBV proteins bear poor sequence homology to baculovirus proteins but have repeated regions similar to those of some baculoviruses. To understand the molecular basis of viral replication and infection, we decided to sequence the whole genome of WSBV.

MATERIALS AND METHODS

Isolation and sequencing of WSBV genomic DNA.

Intact WSBV genomic DNA was isolated from dead and moribund WSBV-infected Penaeus japonicus shrimp which were collected from shrimp ponds in Tongan, Xiamen, east China, in October 1996 as previously described (56). A whole-genome random sequencing method (19) was used to obtain the complete genome sequence for WSBV. Genomic DNA was cloned by the shotgun method into SmalI-linearized pUC18 vector, amplified, and sequenced using ABI BigDye Terminator chemistry on ABI 377 and ABI 3700 capillary sequencers. Large DNA fragments of 5 to 10 kb were also obtained by partial digestion with Sau3A1 and cloned into the pBluescript vectors (41). This was used to form a genome scaffold and to verify the orientation and integrity of the contigs formed from the shotgun library. A total of 5,770 sequences for sevenfold coverage were assembled using the InnerPeace software by Charles Lawrence based on the Phred, Phrap, and Consed program originally developed at the University of Washington.

The WSBV genome sequence was confirmed by comparison of the observed restriction fragments from seven restriction enzymes (BamHI, EcoRI, HindIII, KpnI, PstI, SalI, and XbaI) to those predicted from the sequence data and was also confirmed by the genome scaffold produced by sequence pairs from 1,495 large-insert clones, which covered 90% of the main genome.

Gaps were closed by a combination of sequence-walking of shotgun and PCR large-fragment libraries.

DNA sequence analysis.

Genome DNA composition, structure, repeats, restriction enzyme patterns, and translation were analyzed with the DNAMAN software (Lynnon BioSoft, Vaudreuil, Canada). Open reading frames (ORFs) consisted of more than 60 codons that are initiated with a methionine codon. For detection of potential protein-coding regions, the codon usage bias and positional base preference were evaluated by determining the codon frequency of known WSBV genes or cDNA cloned from the WSBV cDNA library. Homology searches were performed with the FASTA (38) and BLAST programs (3). Protein motifs were analyzed by using the PROSITE database, release 16 (25). Transmembrane domains and signal peptides were predicted with ANTHEPROT (23).

Preparation and screening of a WSBV cDNA library.

Poly(A) mRNA was isolated from WSBV-infected shrimp tissue using the PolyATtract System 1000 kit (Promega). Double-stranded cDNAs were synthesized using the SUPERSCRIPT plasmid system for cDNA synthesis and plasmid cloning (GIBCO BRL). WSBV cDNA clones were selected by hybridization with the digoxigenin (DIG)-labeled WSBV genomic DNA probe (DIG labeling kit; Boehringer Mannheim) and sequenced. The transcription of some ORFs was also verified by PCR on a cDNA cocktail using ORF-specific primers.

Nucleotide sequence accession number.

The complete WSBV sequence can be obtained from the GenBank database (accession no. AF332093).

RESULTS AND DISCUSSION

General features of the WSBV genome.

We have previously developed a unique method that enables us to highly purify the WSBV virus from infected shrimp tissue (56). A random shotgun method was employed to sequence the entire genome of WSBV; the sequence was subsequently confirmed by the genome scaffold formed by sequencing a large-fragment DNA library. The complete WSBV genome is a double-stranded circular DNA of 305,107 bp, similar to a previous estimate of 290 kb (56). Since the origin of replication was unknown, the start of the largest BamHI fragment was chosen to be base 1 (Fig. (Fig.1).1). Three percent of the WSBV genome is made up of nine homologous regions (hrs), while the remaining 97% of the sequences are unique (see description below). The genome has a total G+C content of 41%.

FIG. 1
Circular representation of the WSBV genome. Arrows, positions (outer ring) of the 181 ORFs (red and blue indicate the different directions of transcription); green rectangles, 9 hrs. B, sites of BamHI restriction enzymes (inner ring; their positions are ...

A total of 531 putative ORFs were identified by sequence analysis, among which 181 ORFs are likely to encode functional proteins (Table (Table1).1). This corresponds to an average gene density of one gene per 1.7 kb. Thirty-six of the 181 ORFs annotated here either have been identified by screening and sequencing a WSBV cDNA library (Table (Table1)1) or have been reported previously to encode functional proteins (45, 46, 48, 49, 50). Transcription of another 52 ORFs was confirmed by reverse transcription-PCR (RT-PCR; see Material and Methods) (Table (Table1).1). The relative positions of the ORFs and hrs in the genome are shown in Fig. Fig.1.1. For 80% of the putative 181 ORFs there is a potential polyadenylation site (AATAAA) downstream of the ORF (Table (Table1).1).

TABLE 1
Listing of potentially expressed ORFs in WSBV

WSBV ORFs encode gene products homologous to known proteins.

Table Table11 contains a list of the 181 predicted WSBV ORFs. Among 181 ORFs, the proteins encoded by 18 ORFs show 40 to 68% identity to known proteins from other viruses or organisms or contain an identifiable functional domain. These proteins include enzymes involved in nucleic acid metabolism and DNA replication, a collagen-like protein, and three viral structure proteins (for details, see below). Thirty ORFs predicted proteins that show a partial homology (20 to 39% identity) to known proteins or contain one or two sequence motifs (versus a real functional domain). The remaining 133 ORFs encode proteins with no homology to any known proteins or motifs.

Enzymes involved in nucleotide metabolism.

Among the 18 ORFs encoding proteins that show extensive homologies with previously identified proteins, WSV067, WSV112, WSV172, WSV188, and WSV395 may encode the WSBV homologues of enzymes involved in nucleic acid metabolism (Table (Table1).1). The highest degree of homology (67% identity over 287 amino acids) was detected between the product of WSV067 and the human thymidylate synthase. The 29-amino-acid thymidylate synthase prosite motif (PS00091), which contains the catalytic cysteine residue, is 100% conserved in the product of WSV067. In addition, WSV112 may encode a WSBV homologue of dUTPase (37% identity over 161 amino acids) since the five conserved regions of dUTPase, especially the highly conserved substrate-binding residues, were identified in the product of WSV112 (13, 35). dUTPase has been shown to be essential for the replication of DNA viruses (5). Consistent with the previous reports by van Hulten et al. (48) and Tsai et al. (45, 46), WSBV contains ribonucleotide reductases (products of WSV172 and WSV188) and also thymidylate/thymidine kinase (product of WSV395). Among these enzymes, thymidylate synthase catalyzes the methylation of dUTP to yield the nucleotide precursor dTMP. This is an important step in the de novo pathway of biosynthesis of pyrimidine (12). Despite its ubiquitous distribution in nature, a viral thymidylate synthase was found only in a few herpesviruses (2, 10, 26, 39), Melanoplus sanguinipes entomopoxvirus (MsEPV) (1), Chilo iridescent virus (CIV) (36), and bacteriophages (9). Most viruses do not contain thymidylate synthase, as they depend mostly on the host enzymatic machinery for the replication of their genomes so as to keep the viral genome small (36). WSBV and other thymidylate synthase-containing viruses may therefore exhibit a considerable independence from the host deoxyribonucleotide synthesis. This may represent a significant advantage for viral genome replication that may ultimately lead to persistence of infection and a broad host range for viral infection (36). It is possible that WSBV acquires these replication-related genes from its host and/or from a coinfecting virus that might occur at an earlier period in evolution. However, since the shrimp homologues of these genes have not been cloned, we are not able to test this hypothesis.

Proteins involved in DNA replication and transcription.

WSBV contains genes encoding proteins involved in DNA replication such as DNA polymerase (product of WSV514). The WSBV DNA polymerase was putatively identified by the presence of three highly conserved motifs, YGDTDSVFC (DNA polymerase family B signature PS00116), KLGMNSMYG, and DMTSLYP (conserved amino acid residues are underlined), that are found in most eukaryotic DNA polymerases (4) as well as in some viral polymerases (18, 29, 43). However, since the degree of amino acid similarity between the product of WSV514 and known DNA polymerases is low (24% identity over 201 amino acids), its putative activity as a DNA polymerase still awaits future experimental verification. Interestingly, the size of this putative WSBV polymerase (2,195 amino acids) is much larger than those of the regular polymerases found in other organisms.

Products of ORFs that show weak similarity (BlastP score, <100; identity, <20 to 39%) to known proteins include putative TATA-box binding protein (TBP) (product of WSV303, containing partial conservation with transcription initiation factor IID repeat signature PS00351) (Fig. (Fig.2A),2A), the putative CREB-binding protein (CBP) (product of WSV100) (Fig. (Fig.2B),2B), nuclease (product of WSV191, containing most residues of DNA/RNA nonspecific endonuclease active site PS01070), the putative helicase (product of WSV447), and protein kinases (products of WSV083, WSV289, and WSV423). Most of them play important roles in the regulation of gene transcription. TBP and CBP, which have never been reported in a virus genome, deserve special attention since they are critical basal transcription regulators in eukaryotic cells (21, 51). However, their functions in virus are yet to be determined.

FIG. 2
Multiple amino acid sequence alignment of products of WSV303 and WSV100. The homology regions are shaded (black, 100%; pink, >75%; blue, >50%). The positions of the amino acid sequence are indicated on both ends. ...

Structure proteins.

A unique feature of WSBV is that it contains a collagen-like gene, WSV001, which encodes a predicted 1,684-amino-acid protein and whose transcription has been confirmed by RT-PCR. The product of this ORF displays the highest degree of homology to human collagen type VII (42% identity over 1,336 amino acids) (Fig. (Fig.3).3). This is the first time that an intact collagen gene has been reported in a virus genome. The collagen-like protein of WSBV contains a typical repeat of Gly-X-Y (X is mostly proline, and Y can be any amino acid) that can form the triple-helical structure characteristics of animal collagen fiber. The presence of this collagen-like protein may help to protect the WSBV from environmental factors and may contribute to its ability to survive for a long time in a shrimp pond.

FIG. 3
Multiple amino acid sequence alignment of the product of WSV001 with human (Homo sapiens) type VII collagen, accession no. L23982; fruit fly (Drosophila melanogaster ...

Previously only a short segment of collagen-homologous sequence was found in the structural proteins of ectocarpus siliculosus virus 1 (EsV-1) (16), hepersvirus saimiri (HVS) (2, 22), and bacteriophage PRD1 (6, 7) (Fig. (Fig.3).3). In EsV-1, the collagen-like sequence was found in the N-terminal half of both vp55 and vp74 (16), which were encoded by the EsV-1 genome and which are likely to be the components of the viral core structure. In HVS, the Gly-X-Y motif is repeated 18 times and is located in the central region of saimiri transformation-associated protein (STP). These collagen-like repeats may serve as a hinge to extend the active domain of STP to its site of action (2). Finally, in bacteriophage PRD1, a minor capsid protein was found to contain a short collagen-like region (Gly-X-Y)6 (7). All of the collagen-like segments present in these proteins are short. These segments may play only a supplementary role in protein functions.

In addition, WSV002 and WSV311 encode a nucleocapsid protein, and the product of WSV421 shows characteristics of an envelope protein. These proteins have recently been purified from the nucleocapsid and envelope of WSBV (49, 50).

WSV214 encodes a polypeptide with 44.2% basic amino acid residues (Arg/Lys) and 24.6% Ser residues. This amino acid composition is similar to that of the DNA-binding protein of insect baculoviruses (34, 40, 55). Homologs of these DNA-binding proteins have also been found in granulosis virus (47). The basic residues of these DNA-binding proteins have a high affinity for the phosphate backbone of DNA, enabling the generation of a highly compact form of viral genomic DNA. Upon entry into a host cell, the DNA-binding protein may become phosphorylated by a protein kinase, resulting in the unpacking of the viral DNA (54).

Protein motifs.

ORFs containing zinc finger and leucine zipper motifs have been found in WSBV (Table (Table1).1). These motifs have been shown to be involved in DNA-protein interaction and in regulation of transcriptional activation. Ring-H2 finger motifs, a variation of the Ring finger motif (30, 44) found in proteins critical for virus survival and replication (11, 42), are also detected. Products of WSV079 and WSV427 contain an EF-hand calcium-binding motif (PS00018). Proteins with these motifs are found in some prokaryotic and all eukaryotic organisms and play important roles in the regulation and control of normal cellular functions. The detection of these motifs in proteins of a marine virus suggests that some of these basic regulatory activities are well conserved throughout evolution.

The remaining 133 ORFs encode novel proteins of unknown function. These novel genes obviously will provide ample opportunities for future research and for exploration of molecular mechanisms by which a virus and its host interact to survive in the marine environment.

Among the 181 ORFs examined, the products of 96 have potential transmembrane domains and 32 proteins contain both signal peptide sequences and substantial hydrophobic domains, suggesting that they may be membrane-associated proteins and that they may play an important role in the WSBV-host cell interaction and host range determination. Other than the putative signal sequences and hydrophobic domains, these proteins are not obviously related to other known proteins.

Repetitive regions.

Three percent of the WSBV genome is composed of highly repetitive sequences, and the repeats are distributed throughout the genome. We found nine hrs with a total of 47 repeated minifragments encompassing direct repeats, atypical inverted repeat sequences, and imperfect palindromic sequences. The nine hrs vary in size from 0.76 to 3.62 kb, and hr1 to hr9 are separated in the WSBV genome by about 49, 13, 15, 28, 20, 28, 46, 36, and 55 kb of DNA, respectively. Each hr contains several repeated minifragments, each with a size around 300 bp. These minifragments are referred here as a, b, c, d, e, f, etc. (Table (Table2).2). The percentage of homology among the consensus sequences within the same homologous region is over 73%, while the identity among the hrs is 61.6% (Table (Table2).2). A few sequence motifs were found to be present at very high copy numbers. For example, sequences CCAGAAA or TTTCTGG, AGNGGTCCACC, and AACTTGACAT are repeated 219, 88, and 47 times, respectively.

TABLE 2
Positions and identities of hrs in WSBV genome

As an example of such repetitive region, the homology among the b minifragments of the nine hrs is shown in Fig. Fig.4.4. Both GC-rich sequences and AT-rich sequences are found in the repeats. In the imperfect palindromic sequences, there are 2- or 3-bp mismatches that always exist in the same location within every palindrome (Fig. (Fig.4),4), suggesting a functional significance for the mismatch. Atypical inverted repeat sequences that can form one or two hairpin loops are also found within the repeat segments. The AT-rich elements, inverted repeat sequences, and loop structures are reminiscent of the origin of replication in eukaryotic cells and also in some of the viruses (17, 37). The presence of hrs is a feature of many baculovirus genomes. The hrs may serve as transcription enhancers and origins of DNA replication and play a fundamental role in the viral life cycle (24, 27, 28, 33). The presence of nine hrs suggests that WSBV may contain multiple replication origins. This may account for the fast replication and the growth rate of WSBV. Furthermore, although the organization of WSBV hrs is similar to that of baculovirus, no homology among most of their ORFs is detected. Thus, future investigations are needed to determine whether WSBV is a seawater baculovirus and whether the ancestors of WSBV and insect baculoviruses evolved by separate routes, acquiring genes independently in different environments.

FIG. 4
Alignment of partial consensus sequences within each hr. The consensus minifragments b are shown in order: hr1 to hr9. The hrs are shaded (black, 100%; pink, >75%; blue, >50%), and the numbers on both ends refer ...

In summary, we have obtained the complete genome sequence of WSBV. This is the first complete genome sequence from a marine invertebrate virus. It is also the largest animal virus genome sequenced (8, 52). As the genomic data demonstrated, more than 80% of WSBV proteins bear no homology to previously identified proteins. This leads us to consider a separate evolutionary origin for this virus. Among the proteins that show homology with known proteins, most seem to be related to eukaryotic proteins and relatively few seem to be related to viral proteins (Table (Table1).1). Although a few genes show weak similarities to genes of herpesvirus (data not shown), the morphology and the double-stranded circular WSBV genome differ significantly from those of herpesvirus, which contains an icosahedral capsid and a linear double-stranded DNA molecule. On the other hand, WSBV shares some complex morphological traits with the insect baculovirus, and a pattern of interspersed repetitive regions in WSBV is similar to that found in some of the insect baculoviruses, but sequence comparison indicates that they are not detectably related at the amino acid level. Unfortunately, until now there were no genome sequence data available for the nonoccluded baculovirus. Based on genetic analysis, WSBV clearly should not be included in any of the currently recognizable baculovirus subfamilies and perhaps should be classified in a new virus family. It is possible that other WSBV-like viruses that can infect other organisms may exist. As the sequence of a representative of a marine DNA virus, the complete WSBV genome sequence should provide valuable information to serve as the genetic basis for future studies. Future work may shed more light on the evolution of these viruses.

ACKNOWLEDGMENTS

We thank Mei He and Yun Ye for their assistance, and we acknowledge the support of Mingwei Wang, Lin Zao, and Yan Shen. We thank Mark Yandell, Jennifer R. Wortman, Chinnappa Kodira, P. W. Li, and Z. Deng of Celera Genomics for coordinating the project at Celera. We thank Kunxin Luo of Lawrence Berkeley National Laboratory and UC Berkeley for data analysis and critical reading of the manuscript.

This work is funded by the Chinese High Tech “863” Program (Z19-02-05-01), Fujian Science Fund (C97053), and Science Foundation of the State Oceanic Administration.

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