Open Access

A neurotropic herpesvirus infecting the gastropod, abalone, shares ancestry with oyster herpesvirus and a herpesvirus associated with the amphioxus genome

  • Keith W Savin1Email author,
  • Benjamin G Cocks1, 5,
  • Frank Wong2, 3,
  • Tim Sawbridge1, 5,
  • Noel Cogan1,
  • David Savage1, 4 and
  • Simone Warner2
Virology Journal20107:308

https://doi.org/10.1186/1743-422X-7-308

Received: 4 August 2010

Accepted: 10 November 2010

Published: 10 November 2010

Abstract

Background

With the exception of the oyster herpesvirus OsHV-1, all herpesviruses characterized thus far infect only vertebrates. Some cause neurological disease in their hosts, while others replicate or become latent in neurological tissues. Recently a new herpesvirus causing ganglioneuritis in abalone, a gastropod, was discovered. Molecular analysis of new herpesviruses, such as this one and others, still to be discovered in invertebrates, will provide insight into the evolution of herpesviruses.

Results

We sequenced the genome of a neurotropic virus linked to a fatal ganglioneuritis devastating parts of a valuable wild abalone fishery in Australia. We show that the newly identified virus forms part of an ancient clade with its nearest relatives being a herpesvirus infecting bivalves (oyster) and, unexpectedly, one we identified, from published data, apparently integrated within the genome of amphioxus, an invertebrate chordate. Predicted protein sequences from the abalone virus genome have significant similarity to several herpesvirus proteins including the DNA packaging ATPase subunit of (putative) terminase and DNA polymerase. Conservation of amino acid sequences in the terminase across all herpesviruses and phylogenetic analysis using the DNA polymerase and terminase proteins demonstrate that the herpesviruses infecting the molluscs, oyster and abalone, are distantly related. The terminase and polymerase protein sequences from the putative amphioxus herpesvirus share more sequence similarity with those of the mollusc viruses than with sequences from any of the vertebrate herpesviruses analysed.

Conclusions

A family of mollusc herpesviruses, Malacoherpesviridae, that was based on a single virus infecting oyster can now be further established by including a distantly related herpesvirus infecting abalone, which, like many vertebrate viruses is neurotropic. The genome of Branchiostoma floridae (amphioxus) provides evidence for the existence of a herpesvirus associated with this invertebrate chordate. The virus which likely infected amphioxus is, by molecular phylogenetic analysis, more closely related to the other 2 invertebrate viruses than to herpesviruses infecting vertebrates (ie chordates).

Findings

In 2005 there was an outbreak of acute ganglioneuritis in an Australian population of the edible gastropod mollusc, abalone or Haliotis spp[1]. Using transmission electron microscopy, herpes-like particles were observed in ganglia of affected abalone[2] and purified virions from moribund abalone nervous tissues were identified as resembling those of herpesviruses, having an icosohedral capsid approximately 100 nm in diameter surrounded by a 150 nm diameter spiked envelope[3]. Potential herpesvirus particles were also identified previously in Taiwan following mortalities in Haliotis diversicolor[4]. Recently a diagnostic PCR test has been developed to detect the abalone virus [5]. The test has detected viral DNA sequences in diseased abalone from separate geographical locations in Australia and in DNA isolated from a herpes-like virus found some time ago in Taiwan[4].

Three herpesvirus families have been described in the order Herpesvirales - the Herpesviridae which infect Mammalia, Aves and Reptilia, the Alloherpesviridae infecting Amphibia and Osteichthyes (bony fish), and the mollusc-infecting Malacoherpesviridae containing a single virus that infects an invertebrate class, Bivalvia[68]. The phylogenetic relationships of these herpesviruses have been well studied and their evolution over epochs is largely synchronous with host lineages [7, 8]. Gastropods separated early in the Cambrian period from all other known herpesvirus hosts. This unique evolutionary positioning[6] combined with our discovery of a related herpesvirus genome apparently integrated into the genome of another invertebrate, amphioxus, expands the Herpesvirales order and provides two key links to understanding the nature of the ancient ancestors of mollusc and vertebrate herpesviruses. To understand the structural and evolutionary relationships of the abalone virus to other herpesviruses, we purified abalone virus particles and isolated and sequenced genomic DNA using methods previously described[3, 9]. The DNA was subjected to multiple displacement amplification[10] and sequenced using the Roche 454 GS-FLX system followed by partial genome assembly using the Newbler algorithm (Roche).

Based on the assembled DNA sequences of the abalone virus, several protein coding sequences predicted using Artemis[11] showed varying distant homology to herpesvirus proteins, most notably those of Ostreid herpesvirus 1 (oyster herpesvirus 1, OsHV-1), a virus infecting bivalve mollusc species[12, 13]. BLAST analysis[14] of assembled sequence contigs based on predicted proteins identified 39 full length homologues of OsHV-1 genes (Table 1). These coding sequences, within partial genome scaffold sequences, or as individual coding sequences, have been submitted to Genbank. None of the coding sequences identified appear to be split by introns. Full-length sequences encoding homologues of DNA polymerase and the DNA packaging ATPase subunit of the (putative) terminase (henceforth referred to as the polymerase and terminase respectively), were identified and chosen for use in sequence alignments and phylogenetic analysis (Figures 1 & 2). Hereafter, we will refer to the new abalone virus as abalone herpesvirus or AbHV-1.
Table 1

OsHV-1 homologues of AbHV-1 coding sequences

AbHV-1

OsHV-1

BLASTP result

Gene

Genbank

Genbank

Description

Ident.

Score

E value

AbHVp002c

ADJ95315.1

YP_024647.1

ORF109 terminase

42%

620

3e-175

AbHVp003

ADL16651.1

YP_024565.1

ORF20 RNR2

37%

252

1e-64

AbHVp005c

ADL16652.1

YP_024602.1

ORF59

24%

90

1e-15

AbHVp006

ADL16653.1

YP_024573.1

ORF28

26%

239

2e-60

AbHVp013c

ADL16656.1

YP_024591.1

ORF47

27%

336

1e-89

AbHVp018c

ADL16657.1

YP_024590.1

ORF46

31%

48

6e-04

AbHVp019c

ADL16658.1

YP_024552.1

YP_024552.1

ORF49, ORF7

primase/helicase

24%, 24%

94, 74

5e-17, 1e-10

AbHVp024

ADL16662.1

YP_024567.1

ORF22

23%

234

7e-59

AbHVp031c

ADL16665.1

YP_024606.1

ORF66

27%

375

2e-101

AbHVp032

ADL16666.1

YP_024607.1

ORF67

32%

247

3e-63

AbHVp034

ADL16667.1

YP_024575.1

ORF30

27%

53

3e-05

AbHVp037c

ADL16668.1

YP_024616.1

ORF77

23%

170

1e-39

AbHVp038c

ADL16669.1

YP_024587.1

ORF43

27%

70

1e-10

AbHVp039c

ADL16670.1

YP_024634.1

ORF95

27%

94

2e-17

AbHVp043c

ADL16671.1

YP_024611.1

ORF71

23%

108

1e-21

AbHVp045c

ADL16672.1

YP_024604.1

ORF61

29%

185

1e-44

# AbHVp050

ADL16674.1

YP_024593.1,

YP_024552.1

ORF49, ORF7

primase/helicase

21% 20%

125, 90

4e-26, 1e-15

AbHVp057c

ADJ95314.1

YP_024639.1

ORF100 DNA

polymerase

31%

673

0.0

AbHVp064

HQ400676

YP_024619.1

ORF80

 

38.5

0.29

AbHVp070c

HQ400677

YP_024651.1

ORF113

25%

105

8e-21

AbHVp073c

HQ400678

YP_024650.1

ORF112

26%

119

7e-25

AbHVp075

HQ400679

YP_024649.1

ORF111

32%

198

6e-49

AbHVp086

HQ400681

YP_024645.1

ORF107

26%

134

4e-29

AbHVp093

HQ400682

YP_024622.1

ORF83

19%

49

3e-04

AbHVp102

HQ400683

YP_024630.1

ORF91

30%

151

1e-34

AbHVp104c

HQ400684

YP_024584.1

ORF40

30%

238

2e-60

AbHVp110

HQ400685

YP_024595.1

ORF52

34%

68

4e-10

AbHVp111

HQ400686

YP_024596.1

ORF53

23%

50

9e-04

AbHVp112

HQ400687

YP_024597.1,

YP_024608.1

ORF54, ORF68

43%

643

0.0

AbHVp113c

HQ400688

YP_024657.1

ORF115

32%

80

3e-13

AbHVp117c

HQ400689

YP_024635.1

ORF96

23%

53

4e-05

AbHVp121

HQ400690

YP_024633.1

ORF94

28%

114

2e-23

AbHVp130c

HQ400691

YP_024605.1

ORF64

36%

212

6e-53

AbHVp131

HQ400692

YP_024615.1

ORF76

29%

202

1e-59

AbHVp133

HQ400693

YP_024569.1

ORF24

23%

67

3e-09

AbHVp134c

HQ400694

YP_024608.1,

YP_024597.1

ORF68, ORF54

53%

784

0.0

AbHVp135c

HQ400695

YP_024624.1

ORF85

26%

225

1e-56

AbHVp136c

HQ400696

YP_024588.1

ORF44

32%

134

1e-29

AbHVp137

HQ400697

YP_024609.1

ORF69

29%

172

7e-41

Note: OsHV ORF49 & ORF7 are members of a gene family comprising ORF49, ORF7 & ORF115 OsHV ORF54 & ORF68 comprise a gene family.

AbHV Genbank accessions beginning with "AD" can also be found in scaffold sequences [Genbank:HM631981, Genbank:HM631982].

Figure 1

Alignment of ATP hydrolase domains from terminase protein sequences. ClustalW alignment of one of the conserved regions of the putative terminase gene - the ATP hydrolase (ATPase) domain from various herpesviruses taken from Table 3, identified using Interproscan. Grey background = >90% conserved amino acids.

Figure 2

Dendrogram of concatenated DNA polymerase and terminase protein sequences from 34 herpesviruses. Dendrogram illustrating the evolutionary relationship of abalone and amphioxus herpesviruses to 32 other herpesviruses based on the concatenated full length protein sequences of DNA polymerase and the ATPase subunit of the putative terminase for each virus. The tree was inferred with MEGA4[32] using the Minimum Evolution (ME) method and a model based on the number of amino acid differences detected after an alignment using ClustalW[19]. The percentage of replicate trees in which the associated taxa clustered together in the bootstrap test (2000 replicates) are shown next to the branches. The scale bar for the branch lengths = 100 amino acid sequence differences.

During the search for homologues of predicted AbHV-1 proteins using BLAST we identified, in the non-redundant (nr) Genbank protein sequence database, Branchiostoma floridae (amphioxus) coding sequences with significant homology to some of those in AbHV-1. The genome of amphioxus has been recently sequenced[15] although final assembly of chromosomes is not yet complete. On further analysis of amphioxus coding sequences using BLASTP with the predicted protein sequences of the oyster herpesvirus OsHV-1 genome (Genbank NC_005881), we identified 19 herpesvirus gene homologues. Consistent with this being an integrated virus, we found that 18 of these genes are clustered within a 150 kb region of a single amphioxus scaffold BRAFLscaffold_217, including the herpesvirus specific terminase gene[16] and all but 4 of these genes do not contain introns. These virus coding sequences appear to be legitimately assembled within published genome sequence scaffolds and are therefore probably integrated within the amphioxus genome. Further experiments such as fluorescence in situ hybridisation of chromosomes would confirm this. The 19 coding sequences identified are listed in Table 2 along with their OsHV-1 homologues and BLAST scores. We utilised the amphioxus virus terminase and polymerase protein sequence homologues in our analyses.
Table 2

Branchiostoma florida e (amphioxus) homologues of OsHV-1 coding sequences

OsHV-1

Branchiostoma floridae

BLASTP result

Accession/ORF

Accession

Location

Ident.

Score

E value

YP_024639.1 ORF100

DNA polymerase

XP_002591163.1

DNA polymerase

55013..60373

no introns

28%

379

e-102

YP_024567.1 ORF22

XP_002591166.1

67372..72375

no introns

24%

128

8e-27

YP_024552.1

YP_024593.1

ORF7, ORF49 family primase-helicase

XP_002591168.1

76325..79696

no introns

24%

122

3e-25

YP_024630.1 ORF91

XP_002591169.1

80230..85225

introns predicted

29%

114

2e-23

YP_024606.1 ORF66 AE_Prim_S_like primase

XP_002591170.1

86185..88995

no introns

24%

239

2e-60

YP_024573.1 ORF28

XP_002591172.1

94244..96667

no introns

22%

107

4e-21

YP_024641.1 ORF102

XP_002591174.1

99529..101919

no introns

20%

78

4e-12

YP_024645.1 ORF107

XP_002591175.1 contains PAT1 domain pfam09770

103007..105292

no introns

24%

65

2e-08

YP_024584.1 ORF40

XP_002591176.1

105441..107045

no introns

29%

180

4e-43

YP_024643.1 ORF104

XP_002591178.1

108452..110641

no introns

19%

101

4e-19

YP_024615.1 ORF76

XP_002591179.1

112401..114281

no introns

26%

71

4e-10

YP_024624.1 ORF85

XP_002591189.1

137878..148379

introns predicted

22%

70

1e-09

YP_024597.1

YP_024608.1

ORF54, ORF68 family membrane glycoprotein

XP_002591190.1 XP_002591197.1

(possible gene family)

148508..150751

174789..176912 no introns

30%

332

1e-88

YP_024591.1 ORF47

XP_002591194.1

163504..167571

no introns

23%

275

4e-71

YP_024647.1 ORF109 terminase

XP_002591195.1 terminase

168081..170354

no introns

31%

308

2e-81

YP_024650.1 ORF112

XP_002591198.1

177489..179961

introns predicted

23%

68

2e-09

YP_024609.1 ORF69

XP_002591200.1

187709..188944

no introns

25%

80

3e-13

YP_024600.1 ORF57

XP_002610653.1 chloride channel

BRAFLscaffold_25 2304811..2311488

introns predicted

30%

86

4e-15

Note: B. floridae OsHV homologue locations are all on scaffold BRAFLscaffold_217, except for OsHV ORF57. All OsHV and B. floridae predicted proteins listed are of unknown function unless stated otherwise. Four B. floridae genes are predicted to contain introns. Also 4 other B. floridae genes in the scaffold BRAFLscaffold_217 between 60 kb and 150 kb encode proteins similar to apoptosis regulators like IAP-3 often present in herpesvirus genomes (not listed and not detected using OsHV sequences).

The putative terminase, or DNA packaging ATPase, appears specific to herpesviruses and some bacteriophages, such as T4[16] and is thought to be an enzyme motor involved in packaging viral DNA into preformed capsids[17]. We used the ATPase motif from this protein to investigate the phylogeny of the herpesviruses.

The ATP hydrolase (ATPase) motif sequences from 20 of the 34 terminase proteins listed in Table 3, plus their T4 bacteriophage homologue and the amphioxus terminase homologue (XP_002591195.1, listed in Table 2), were identified using Interproscan[18] and aligned using ClustalW[19]. Figure 1 shows that 12 amino acids are conserved across all herpesvirus ATPase domain sequences, including those from the abalone, oyster and amphioxus virus genomes, indicating the placement of the abalone virus and putative amphioxus virus within the Herpesvirales order. A common ancestral origin for the mollusc and amphioxus viruses is confirmed by the absence of introns in the terminase gene and the presence of additional amino acid loops (Figure 1). Although being in the same clade (Figure 2), at a protein sequence level the mollusc viruses are only moderately related with 40% amino acid identity in this conserved viral protein, across their full length.
Table 3

Genbank Accessions of Herpesvirus Polymerase and Terminase protein sequences used for phylogenetic analysis

Virus

Polymerase

Terminase

Abalone_herpesvirus

ADJ95314.1

ADJ95315.1

Amphioxus_associated_virus

XP_002591163.1

XP_002591195.1

Anguillid_herpesvirus_1

YP_003358194.1

YP_003358149.1

Bovine_herpesvirus_1

NP_045328.1

NP_045342.1

Bovine_herpesvirus_5

NP_954917.1

NP_954931.1

Cercopithecine_herpesvirus_2

YP_164473.1

YP_164457.1

Cercopithecine_herpesvirus_9

NP_077443.1

NP_077457.1

Cyprinid_herpesvirus_3

YP_001096114.1

YP_001096069.1

Equid_herpesvirus_1

YP_053075.1

YP_053090.1

Equid_herpesvirus_4

NP_045247.1

NP_045262.1

Equid_herpesvirus_9

YP_002333511.1

YP_002333526.2

Gallid_herpesvirus_1

YP_182359.1

YP_182378.2

Gallid_herpesvirus_2

AAF66765.1

YP_001033943.1

Gallid_herpesvirus_3

NP_066862.1

NP_066845.1

Human_herpesvirus_1

NP_044632.1

NP_044616.1

Human_herpesvirus_2

P07918.1

NP_044484.1

Human_herpesvirus_3

NP_040151.1

NP_040165.1

Human_herpesvirus_4

YP_401712.1

YP_401690.1

Human_herpesvirus_5

P08546.2

P16732.1

Human_herpesvirus_6

NP_042931.1

NP_042953.2

Human_herpesvirus_7

P52342.1

YP_073802.1

Human_herpesvirus_8

AAC57086.1

YP_001129382.1

Ictalurid_herpesvirus_1

NP_041148.2

NP_041153.2

Macacine_herpesvirus_1

NP_851890.1

NP_851874.1

Meleagrid_herpesvirus_1

NP_073324.1

NP_073308.1

Murid_herpesvirus_4

NP_044849.1

NP_044866.2

Ostreid_herpesvirus_1

YP_024639.1

YP_024647.1

Ovine_herpesvirus_2

YP_438136.1

YP_438152.1

Panine_herpesvirus_2

NP_612698.1

NP_612722.1

Papiine_herpesvirus_2

YP_443877.1

YP_443861.1

Psittacid_herpesvirus_1

NP_944403.1

NP_944422.2

Ranid_herpesvirus_1

YP_656727.1

YP_656697.1

Ranid_herpesvirus_2

YP_656618.1

YP_656576.1

Suid_herpesvirus_1

YP_068333.1

YP_068358.1

The phylogenetic analysis comparing concatenated polymerase and terminase full-length proteins (Figure 2, Table 3), illustrates the evolutionary relationships within the Herpesvirales order. The five Alloherpesviridae viruses are clustered together, with separate clades for frog and fish viruses as found previously [8], and the Herpesviridae are clustered into separate major clades reflecting their taxonomic groupings of alpha-, beta- and gammaherpesvirinae sub-families. The phylogenetic analysis confirms a relationship between the amphioxus virus and the abalone and oyster viruses in a deep invertebrate clade. The level of divergence makes estimation of the relative divergence times of the 3 herpesvirus families difficult. Interestingly, the amphioxus virus is in the clade with mollusc viruses, which may not have been expected given the amphioxus chordate host lineage is more aligned with vertebrates than molluscs.

The invertebrate herpesvirus clade provides a unique branching point to inform the metazoan diversification of the herpesviruses. It is thought that during the Cambrian era, the Bilaterial species diverged to generate the Protostomes (evolving into such animals as flatworms, molluscs and arthropods) and the Deuterostomes (from which the chordates and then the vertebrates evolved)[20, 21]. Molluscs emerged more than 100 My before vertebrates with a bony skeleton (the current known range of herpesviruses in vertebrates). One hypothesis to explain the diversity of viruses within vertebrates and the positioning of the mollusc viruses among them, rather than as an ancestral outgroup, is the existence of diverse herpesviruses in Cambrian metazoans. Consistent with this hypothesis, previous estimates for the divergence of just the Herpesviridae in vertebrates indicate a divergence of alpha-, beta- and gammaherpesviruses to over 400 Mya, and longer times are predicted for divergence of Alloherpesviridae and Malacoherpesviridae[7]. An alternate hypothesis to explain the branching of the 3 herpesvirus families is that molluscs acquired herpesviruses by transmission in the aquatic environment, for example through association such as mollusc predation of early chordates. It appears that modern Malacoherpesviridae may have the ability to infect across species, a feature not typically observed in vertebrate herpesviruses, although the infection observed is restricted to related mollusc species[22].

As more sequence data and gene structure for Alloherpesviridae, Malacoherpesviridae and other invertebrate herpesviruses become available it will allow a more informative analysis of their evolution. Of particular interest will be new herpesviruses yet to be discovered in species which share bilateral symmetry such as amphioxus, sea squirts, flatworms or squid. Our discovery of clustered intact herpesvirus genes in amphioxus suggests an opportunistic integration has occurred in the amphioxus genome. This may not be a normal feature of infection and latency, but herpesviruses can occasionally integrate into the genome of their host[23]. Surprisingly, the nearest relatives of this chordate virus seem to be the viruses infecting molluscs rather than those of fish or frogs. Although herpesvirus particles have not been seen in the more primitive metazoan species, their existence is suspected; short herpes-like DNA sequences having been found in a metagenomic study of Hawaian coral[24]. Further metagenomic approaches similar to those described previously[25] and PCR-directed approaches[26] based on new sequences described here will enable these evolutionary questions to be addressed. The sequence information is also crucial for the development of molecular diagnostic tools to monitor and manage disease outbreaks.

The neurotropism of certain herpesviruses is well documented but this behaviour is not known outside the families of herpesviruses infecting terrestrial vertebrates[27, 28]. The neurotropic tissue infection profile of the new gastropod virus analysed here is shared with some viruses within the Herpesviridae family. Convergent evolution may have given rise to the neurotropism seen in some members of the Herpesviridae and now the Malacoherpesviridae families. The rooting of a neurotropic invertebrate virus near or before the divergence of alpha-, beta-, and gammaherpesviruses, may also suggest that early mammalian herpesvirus precursors were neurotropic and that some have retained this feature over time. It is interesting to speculate as to the earliest functional interactions between sensory cells and viruses, as the first sign of neurons appeared over 600 million years ago in "cnidarians," (eg: hydra), but organisms basal to them like sponges do not have neurons or synapses[29]. Recent evidence indicates sponges have gene networks in cells which were precursors to nerve cells including proteins related to virus nerve entry receptors[30]. Others[24] have speculated on a link between herpesvirus neurotropism and the evolution of modern herpesviruses from ancestors infecting invertebrates such as Cnidaria (for example, coral or sea anemones), thought to be related to the first species with sensory receptors[31]. Further, the discovery reported here of a putative herpesvirus integrated into the genome of amphioxus hints at a wide diversity of herpesviruses within the invertebrate community, perhaps dating back to before the divergence of arthropods, molluscs and chordates. It will be exciting to discover such invertebrate herpesviruses and explore their links to ancient herpesvirus ancestors.

To accommodate the new abalone virus, which we have suggested naming abalone herpesvirus or AbHV-1, within the Herpesvirales order, we suggest the creation of a new genus called Haliotivirus within the Malacoherpesviridae family and assignment of AbHV-1 as a species under Haliotivirus (as Haliotid herpesvirus 1).

We have referred to the putative virus genome integrated into the Branchiostomid species chromosome as amphioxus-associated virus, AaHV-1. We suggest the species name Branchiostomid herpesvirus 1. Given the unique nature of the virus revealed by phylogenetic analysis and the unique evolutionary positioning of amphioxus as an invertebrate chordate, we suggest this virus, if classified, could be a member of a new family, Aspondyloherpesviridae (from the Greek for "no spine").

Declarations

Acknowledgements

The authors wish to thank Fisheries Victoria for supplying infected abalone, German Spangenberg for facilitating the genome sequencing and Megan Vardy for technical assistance during generation of DNA sequence data. Funding was provided by the Department of Primary Industries, Victoria, Australia, The Commonwealth Scientific & Industrial Organisation, Australia and the Fisheries Research & Development Corp., Australia. The funding bodies had no role in the study design, data collection, analysis or interpretation, manuscript preparation or submission other than contributing to author salaries and experiment costs.

Authors’ Affiliations

(1)
Department of Primary Industries, Biosciences Research Division
(2)
Biosciences Research Division, Department of Primary Industries, Biosciences Research Division
(3)
Australian Animal Health Laboratory, CSIRO Livestock Industries
(4)
School of Plant Biology, University of Western Australia
(5)
La Trobe University

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This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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