DNA virus

A DNA virus is a virus that has DNA as its genetic material and replicates using a DNA-dependent DNA polymerase. The nucleic acid is usually double-stranded DNA (dsDNA) but may also be single-stranded DNA (ssDNA). DNA viruses belong to either Group I or Group II of the Baltimore classification system for viruses. Single-stranded DNA is usually expanded to double-stranded in infected cells. Although Group VII viruses such as hepatitis B contain a DNA genome, they are not considered DNA viruses according to the Baltimore classification, but rather reverse transcribing viruses because they replicate through an RNA intermediate.

Group I: dsDNA viruses

Genome organization within this group varies considerably. Some have circular genomes (Baculoviridae, Papovaviridae and Polydnaviridae) while others have linear genomes (Adenoviridae, Herpesviridae and some phages). Some families have have circularly permuted linear genomes (phage T4 and some Iridoviridae). Others have linear genomes with covalently closed ends (Poxviridae and Phycodnaviridae).

Orders within this group are defined on the basis of morphology rather than DNA sequence similarity. It is thought that morphology is more conserved in this group than sequence similarity or gene order which is extremely variable. Three orders and 32 families are currently recognised. Four genera are recognised that have not yet been assigned a family. The species Sulfolobus turreted icosahedral virus is so unlike any previously described virus that it will almost certainly be placed in a new family on the next revision of viral families.

Fifteen families are enveloped. These include all three families in the order Herpesvirales and the following families: Ascoviridae, Ampullaviridae, Asfarviridae, Baculoviridae, Fuselloviridae, Globuloviridae, Guttaviridae, Hytrosaviridae, Iridoviridae, Lipothrixviridae, Nimaviridae and Poxviridae.

Bacteriophages belonging to the families Tectiviridae and Corticoviridae have a lipid bilayer inside the icosahedral protein capsid and the membrane surrounds the genome. The crenarchaeal virus Sulfolobus turreted icosahedral virus has a similar structure.

The genomes in this group vary considerably from ~20 kilobases to over 1.2 megabases in length.

Host range

Species of the order Caudovirales and of the families Corticoviridae and Tectiviridae infect bacteria.

Species of the order Ligamenvirales and the families Ampullaviridae, Bicaudaviridae, Clavaviridae, Fuselloviridae, Globuloviridae and Guttaviridae infect hyperthermophilic archaea species of the Crenarchaeota.

Species of the order Herpesvirales and of the families Adenoviridae, Asfarviridae, Iridoviridae, Papillomaviridae, Polyomaviridae and Poxviridae infect vertebrates.

Species of the families Ascovirus, Baculovirus, Hytrosaviridae, Iridoviridae and Polydnaviruses and of the genus Nudivirus infect insects.

Species of the families Marseilleviridae, Megaviridae and Mimiviridae and the species Mavirus virophage and Sputnik virophage infect protozoa.

Species of the family Nimaviridae infect crustaceans.

Species of the family Phycodnaviridae and the species Organic Lake virophage infect algae. These are the only known dsDNA viruses that infect plants.

Species of the family Plasmaviridae infect species of the class Mollicutes.

Species of the genus Dinodnavirus infect dinoflagellates. These are the only known viruses that infect dinoflagellates.

Species of the genus Rhizidiovirus infect stramenopiles. These are the only known dsDNA viruses that infect stramenopiles.

Species of the genus Salterprovirus infect infect halophilic archaea species of the Euryarchaeota.

Taxonomy

• Order Caudovirales
  • Family Myoviridae - includes Enterobacteria phage T4
  • Family Podoviridae - includes Enterobacteria phage T7
  • Family Siphoviridae - includes Enterobacteria phage λ

• Order Herpesvirales
  • Family Alloherpesviridae
  • Family Herpesviridae - includes human herpesviruses, Varicella Zoster virus
  • Family Malacoherpesviridae

• Order Ligamenvirales
  • Family Lipothrixviridae
  • Family Rudiviridae

• Unassigned families
  • Family Ascoviridae
  • Family Adenoviridae - includes viruses which cause human adenovirus infection
  • Family Ampullaviridae
  • Family Asfarviridae - includes African swine fever virus
  • Family Baculoviridae
  • Family Bicaudaviridae
  • Family Clavaviridae
  • Family Corticoviridae
  • Family Fuselloviridae
  • Family Globuloviridae
  • Family Guttaviridae
  • Family Hytrosaviridae
  • Family Iridoviridae
  • Family Marseilleviridae
  • Family Megaviridae
  • Family Mimiviridae
  • Family Nimaviridae
  • Family Papillomaviridae
  • Family Phycodnaviridae
  • Family Plasmaviridae
  • Family Polydnaviruses
  • Family Polyomaviridae - includes Simian virus 40, JC virus, BK virus
  • Family Poxviridae - includes Cowpox virus, smallpox
  • Family Tectiviridae

• Unassigned genera
  • Dinodnavirus
  • Nudivirus
  • Salterprovirus
  • Rhizidiovirus

• Unassigned species
  • Mavirus virophage
  • Organic Lake virophage
  • Sputnik virophage
  • Sulfolobus turreted icosahedral virus

Group II: ssDNA viruses

Although bacteriophages were first described in 1927, it was only in 1959 that Sinshemer working with the phage X174 showed that they could posses single stranded DNA genomes.^[1][2] Despite this discovery until relatively recently it was believed that the majority of DNA viruses belonged to the double stranded clade. Recent work suggests that this may not be the case with single stranded viruses forming the majority of viruses found in sea water, fresh water, sediment, terrestrial, extreme, metazoan-associated and marine microbial mats.^[3][4] The majority of these viruses have yet to be classified and assigned to genera and higher taxa. Because most of these viruses do not appear to be related or are only distantly related to known viruses additional taxa will be created for these.

All viruses in this group require formation of a replicative form - a double stranded DNA intermediate - for genome replication. This is normally created from the viral DNA with the assistance of the host's own DNA polymerase.

The evolutionary history of this group is currently poorly understood. However the parvoviruses have frequently invaded the germ lines of diverse animal species including mammals, fishes, birds, tunicates, arthropods and flatworms.^[5][6] In particular they have been associated with the human genome for ~98 million years.

Host range

Families in this group have been assigned on the basis of the nature of the genome (circular or linear) and the host range. Eight families are currently recognised.

The family Parvoviridae all have linear genomes while the other families have circular genomes. The Inoviridae and Microviridae infect bacteria; the Anelloviridae and Circoviridae infect animals (mammals and birds respectively); and the Geminiviridae and Nanoviridae infect plants. In both the Geminiviridae and Nanoviridae the genome is composed of more than a single chromosome. The Bacillariodnaviridae infect diatoms and have a unique genome: the major chromosome is circular (~6 kilobases in length): the minor chromosome is linear (~1 kilobase in length) and complementary to part of the major chromosome.

Taxonomy

• • Family Anelloviridae
  • Family Bacillariodnaviridae
  • Family Circoviridae
  • Family Geminiviridae
  • Family Inoviridae
  • Family Microviridae
  • Family Nanoviridae
  • Family Parvoviridae - includes Parvovirus B19

Unassigned species

A number of additional single stranded DNA viruses are known but are as yet unclassified. Among these are the parvovirus like viruses. These have linear single stranded DNA genomes but unlike the parvoviruses the genome is bipartate. This group includes the Bombyx mori densovirus type 2, Hepatopancreatic parvo-like virus and Lymphoidal parvo-like virus. A new family Bidensoviridae has been proposed for this group but this proposal has not been ratified by the ICTV to date.^[7] Their closest relations appear to be the Brevidensoviruses.^[8]

Another new genus - as yet unnamed - has been recognised.^[9] This genus includes the species bovine stool associated circular virus and chimpanzee stool associated circular virus.^[10] The closest relations to this genus appear to be the Nanoviridae but further work will be needed to confirm this.

A virus with a circular genome - sea turtle tornovirus 1 - has been isolated from a sea turtle with fibropapillomatosis.^[11] It is sufficiently unrelated to any other known virus that it may belong to a new family. The closest relations seem to be the Gyrovirinae.

Although ~50 archaeal viruses are known all the DNA viruses infecting archaea, with one known exception, have double stranded genomes. This exception is the Halorubrum pleomorphic virus 1 which has a unique structure and a circular genome.^[12]

Most known fungal viruses have either double stranded DNA or RNA genomes. A single stranded DNA fungal virus - Sclerotinia sclerotiorum hypovirulence associated DNA virus 1 - has been described.^[13] This virus appears to be related to the Geminiviridae but is distinct from them.

An unusual virus has been isolated from the flatwom Girardia tigrina.^[14] Because of its genome organisation, this virus appears to belong to an entirely new family. This virus is the first to be isolated from a flatworm.

Satellite viruses

Satellite viruses are small viruses with either RNA or DNA as their genomic material that require another virus to replicate. There are two types of DNA satellite viruses - the alphasatellites and the betasatellites - both of which are dependent on begomaviruses. At present satellite viruses are not classified into genera or higher taxa.

Alphasatellites are small circular single strand DNA viruses that require a begomovirus for transmission. Betasatellites are small linear single stranded DNA viruses that require a begomovirus to replicate.

Notes

NCLDVs

Main article: Nucleocytoplasmic large DNA viruses

The asfarviruses, iridoviruses, mimiviruses, phycodnaviruses and poxviruses have been shown to belong to a single group.^[15] - the large nuclear and cytoplasmic DNA viruses. These are also abbreviated "NCLDV".^[16] This clade can be divided into two groups:

• the iridoviruses-phycodnaviruses-mimiviruses group. The phycodnaviruses and mimiviruses are sister clades.
• the poxvirus-asfarviruses group.

It is probable that these viruses evolved before the separation of eukaryoyes into the extant crown groups. The ancestral genome was complex with at least 41 genes including (1) the replication machinery (2) up to four RNA polymerase subunits (3) at least three transcription factors (4) capping and polyadenylation enzymes (5) the DNA packaging apparatus (6) and structural components of an icosahedral capsid and the viral membrane.

Bacteriophage evolution

Bacteriophages occur in over 140 bacterial or archaeal genera.^[17] They arose repeatedly in different hosts and there are at least 11 separate lines of descent. Over 5100 bacteriophages have been examined in the electron microscope since 1959. Of these at least 4950 phages (96%) have tails. Of the tailed phages 61% have long, noncontractile tails (Siphoviridae). Tailed phages appear to be monophyletic and are the oldest known virus group.

Phylogenetic relationships

The family Ascoviridae appear to have evolved from the Iridoviridae.^[18] The family Polydnaviridae may have evolved from the Ascoviridae. Molecular evidence suggests that the Iridoviridae may have evolved from the family Phycodnaviridae.

The families Adenoviridae and Tectiviridae appear to be related structurally.^[19]

Based on the genome organisation and DNA replication mechanism it seems that phylogenetic relationships may exist between the rudiviruses and the large eukaryal DNA viruses: poxviruses, the African swine fever virus and Chlorella viruses.^[20]

The nucleocytoplasmic large DNA virus group (Asfarviridae, Iridoviridae, Marseilleviridae, Mimiviridae, Phycodnaviridae and Poxviridae) along with the families Adenoviridae, the Cortiviridae, the Tectiviridae, the phage Sulfolobus turreted icosahedral virus and the satellite virus Sputnik all possess double β-barrel major capsid proteins suggesting a common origin.^[21]

Based on the analysis of the DNA polymerase the genus Dinodnavirus may be a member of the family Asfarviridae.^[22] Further work on this virus will required before a final assignment can be made.

Based on the analysis of the coat protein Sulfolobus turreted icosahedral virus may share a common ancestry with the Tectiviridae.

A protein common to the families Bicaudaviridae, Lipotrixviridae and Rudiviridae and the unclassified virus Sulfolobus turreted icosahedral virus is known possibly suggesting a common origin.^[23]

Only a single gene, encoding the putative ATPase subunit of the terminase is conserved among all herpesviruses. To a lesser extent this gene is also found also in T4-like bacteriophages suggesting a common ancestor for these two groups of viruses.^[24]

A common origin for the Herpesviruses and the Caudoviruses has been suggested on the basis of parallels in their capsid assembly pathways and similarities between their portal complexes, through which DNA enters the capsid. ^[25] These two groups of viruses share a distinctive 12-fold arrangement of subunits in the portal complex.

Nudiviruses are regarded as a sister clade to the Baculoviruses.

References

1. ^ Sinshemer RL (1959) J Mol Biol 1:37
2. ^ Sinshemer RL (1959) J Mol Biol 1:43
3. ^ Desnues C, Rodriguez-Brito B, Rayhawk S, Kelley S, Tran T, Haynes M, Liu H, Furlan M, Wegley L, Chau B, Ruan Y, Hall D, Angly FE, Edwards RA, Li L, Thurber RV, Reid RP, Siefert J, Souza V, Valentine DL, Swan BK, Breitbart M, Rohwer F (2008) Biodiversity and biogeography of phages in modern stromatolites and thrombolites.Nature 452(7185):340-343
4. ^ Angly FE, Felts B, Breitbart M, Salamon P, Edwards RA, Carlson C, Chan AM, Haynes M, Kelley S, Liu H, Mahaffy JM, Mueller JE, Nulton J, Olson R, Parsons R, Rayhawk S, Suttle CA, Rohwer F (2006) The marine viromes of four oceanic regions. PLoS Biol 4(11):e368.
5. ^ Belyi VA, Levine AJ, Skalka AM (2010) Sequences from ancestral single-stranded DNA viruses in vertebrate genomes: the parvoviridae and circoviridae are more than 40 to 50 million years old. J Virol 84(23):12458-12462
6. ^ Liu H, Fu Y, Xie J, Cheng J, Ghabrial SA, Li G, Peng Y, Yi X, Jiang D. (2011) Widespread endogenization of Densoviruses and Parvoviruses in animal and human genomes. J Virol 85(19):9863-9876
7. ^ Tijssen P, Bergoin M (1995) Densonucleosis viruses constitute an increasingly diversified subfamily among the parvoviruses. Seminars in Virology 6, 347-355.
8. ^ Sukhumsirichart W, Attasart P, Boonsaeng V, Panyim S (2006) Complete nucleotide sequence and genomic organization of hepatopancreatic parvovirus (HPV) of Penaeus monodon. Virology 346(2):266-277
9. ^ Kim HK, Park SJ, Nguyen VG, Song DS, Moon HJ, Kang BK, Park BK (2011) Identification of a novel single stranded circular DNA virus from bovine stool. J Gen Virol
10. ^ Blinkova O, Victoria J, Li Y, Keele BF, Sanz C, Ndjango JB, Peeters M, Travis D, Lonsdorf EV, Wilson ML, Pusey AE, Hahn BH, Delwart EL (2010) Novel circular DNA viruses in stool samples of wild-living chimpanzees. J Gen Virol 91(Pt 1):74-86
11. ^ Ng TF, Manire C, Borrowman K, Langer T, Ehrhart L, Breitbart M (2009) Discovery of a novel single-stranded DNA virus from a sea turtle fibropapilloma by using viral metagenomics. J Virol 83(6):2500-2509
12. ^ Pietilä MK, Laurinavicius S, Sund J, Roine E, Bamford DH (2010) The single-stranded DNA genome of novel archaeal virus Halorubrum pleomorphic virus 1 is enclosed in the envelope decorated with glycoprotein spikes. J Virol 84(2):788-798
13. ^ Yu X, Li B, Fu Y, Jiang D, Ghabrial SA, Li G, Peng Y, Xie J, Cheng J, Huang J, Yi X (2010) A geminivirus-related DNA mycovirus that confers hypovirulence to a plant pathogenic fungus. Proc Natl Acad Sci USA 107(18):8387-8392
14. ^ Rebrikov DV, Bulina ME, Bogdanova EA, Vagner LL, Lukyanov SA (2002) Complete genome sequence of a novel extrachromosomal virus-like element identified in planarian Girardia tigrina. BMC Genomics 13;3:15.
15. ^ Iyer LM, Balaji S, Koonin EV, Aravind L (2006) Evolutionary genomics of nucleo-cytoplasmic large DNA viruses. Virus Res. 117(1):156-184
16. ^ Yutin N, Wolf YI, Raoult D, Koonin EV (2009). "Eukaryotic large nucleo-cytoplasmic DNA viruses: clusters of orthologous genes and reconstruction of viral genome evolution". Virol. J. 6: 223. doi:10.1186/1743-422X-6-223. PMC 2806869. PMID 20017929. http://www.virologyj.com/content/6//223. 
17. ^ Ackermann HW (2003) Bacteriophage observations and evolution. Res Microbiol 154(4):245-251
18. ^ Federici BA, Bideshi DK, Tan Y, Spears T, Bigot Y (2009) Ascoviruses: superb manipulators of apoptosis for viral replication and transmission. Curr Top Microbiol Immunol 328:171-196.
19. ^ Benson SD, Bamford JK, Bamford DH, Burnett RM (1999) Viral evolution revealed by bacteriophage PRD1 and human adenovirus coat protein structures. Cell 98(6):825-833.
20. ^ Prangishvili D, Garrett RA (2004) Exceptionally diverse morphotypes and genomes of crenarchaeal hyperthermophilic viruses. Biochem Soc Trans 32(Pt 2):204-208
21. ^ Krupovi M, Bamford DH (2008) Virus evolution: how far does the double beta-barrel viral lineage extend? Nat. Rev. Microbiol 6:941-948
22. ^ Ogata H, Toyoda K, Tomaru Y, Nakayama N, Shirai Y, Claverie JM, Nagasaki K (2009) Remarkable sequence similarity between the dinoflagellate-infecting marine girus and the terrestrial pathogen African swine fever virus. Virol J 6:178
23. ^ Keller J, Leulliot N, Cambillau C, Campanacci V, Porciero S, Prangishvilli D, Forterre P, Cortez D, Quevillon-Cheruel S, van Tilbeurgh H (2007) Crystal structure of AFV3-109, a highly conserved protein from crenarchaeal viruses. Virol J 22;4:12
24. ^ Davison AJ (2002) Evolution of the herpesviruses. Vet Microbiol 22;86(1-2):69-88
25. ^ Baker ML, Jiang W, Rixon FJ, Chiu W (2005) Common ancestry of herpesviruses and tailed DNA bacteriophages. J. Virol. 79:14967-14970

Additional reading

• Fauquent, C. M.; Mayo, M. A.; Maniloff, J.; Desselberger, U.; Ball, L. A.; eds. (2005-05-27). "8th Reports of the International Committee on Taxonomy of Viruses". Academic Press. U.S. National Center for Biotechnology Information, National Library for Medicine, National Institutes of Health. http://www.ncbi.nlm.nih.gov/ICTVdb/Ictv/fr-fst-g.htm.