Adnaviria

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Adnaviria
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Acidianus filamentous virus 3 (AFV3) virion
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(unranked): Virus
Realm: Adnaviria
Kingdom: Zilligvirae
Phylum: Taleaviricota
Class:Tokiviricetes
Subtaxa

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Adnaviria is a realm of viruses that includes archaeal viruses that have a filamentous virion (i.e. body) and a linear, double-stranded DNA genome. [1] The genome exists in A-form (A-DNA) and encodes a dimeric major capsid protein (MCP) that contains the SIRV2 fold, a type of alpha-helix bundle containing four helices. The virion consists of the genome encased in capsid proteins to form a helical nucleoprotein complex. For some viruses, this helix is surrounded by a lipid membrane called an envelope. Some contain an additional protein layer between the nucleoprotein helix and the envelope. Complete virions are long and thin and may be flexible or a stiff like a rod.

Contents

Adnaviria was established in 2020 after cryogenic electron microscopy showed that the viruses in the realm were related due to a shared MCP, A-DNA, and general virion structure. Viruses in Adnaviria infect hyperthermophilic archaea, i.e. archaea that inhabit very high temperature environments such as hot springs. Their A-DNA genome may be an adaptation to this extreme environment. Viruses in Adnaviria have potentially existed for a long time, as it is thought that they may have infected the last archaeal common ancestor. In general, they show no genetic relation to any viruses outside the realm.

Etymology

Adnaviria takes the first part of its name, Adna-, from A-DNA, referring to the A-form genomic DNA of all viruses in the realm. The second part, -viria is the suffix used for virus realms. The sole kingdom in the realm, Zilligvirae, is named after Wolfram Zillig (1925–2005) for his research on hyperthermophilic archaea, with the virus kingdom suffix -virae. The name of the sole phylum, Taleaviricota, is derived from Latin talea, meaning "rod", referring to the morphology of viruses in the realm, and the virus phylum suffix -viricota. Lastly, the sole class in the realm, Tokiviricetes, is constructed from Georgian toki (თოკი), meaning "thread", and the suffix used for virus classes, -viricetes. [2]

Characteristics

Viruses in Adnaviria infect hyperthermophilic archaea and have linear, double-stranded DNA (dsDNA) genomes ranging from about 16 to 56 kilobase pairs in length. The ends of their genomes contain inverted terminal repeats. [3] [4] [5] Notably, their genomes exist in A-form, also called A-DNA. [1] A-form is proposed to be an adaptation allowing DNA survival under extreme conditions since their hosts are hyperthermophiles and acidophiles microorganisms from the archaea domain. [6] Furthermore, Adnaviria viruses have high genome redundancy, an adaptation mechanism to survive such extreme environments. [7]

The creation of genomic A-DNA is caused by an interaction with major capsid protein (MCP) dimers, which, during virion assembly, cover pre-genomic B-DNA to form a helical nucleoprotein complex containing genomic A-DNA. [2]

The nucleoprotein helix is composed of asymmetric units of two MCPs. For rudiviruses, this is a homodimer, whereas for lipothrixviruses and tristromaviruses, [8] it is a heterodimer of paralogous MCPs. The MCPs of viruses in Adnaviria contain a folded structure consisting of a type of alpha-helix bundle that contains four helices [4] called the SIRV2 fold, named after the virus of the same name, Sulfolobus islandicus rod-shaped virus 2 (SIRV2). Variations in the protein structure exist, but the same base structure is retained in all adnaviruses. [2]

Adnaviruses have filamentous virions, i.e. they are long, thin, and cylindrical. Lipothrixviruses have flexible virions about 900 nanometers (nm) in length and 24 nm in width in which the nucleoprotein helix is surrounded by a lipid envelope. [3] Tristromaviruses, about 400 by 32 nm, likewise have flexible virions with an envelope, and they contain an additional protein sheath layer between the nucleoprotein complex and the envelope. [5] [9] Rudviruses have stiff, rod-like virions about 600–900 by 23 nm. [4] At both ends of the virion, lipothrixviruses have mop- or claw-like structures connected to a collar, whereas rudiviruses and tristromaviruses have plugs at each end from which bundles of thin filaments emanate. [3] [5] [10]

Phylogenetics

Viruses in Adnaviria have potentially existed for a long time, as it is thought that they may have infected the last archaeal common ancestor. [11] In general, they show no genetic relation to viruses outside the realm. The only genes that are shared with other viruses are glycosyltransferases, ribbon-helix-helix transcription factors, and anti-CRISPR proteins. Adnaviruses are morphologically similar to non-archaeal filamentous viruses but their virions are built from different capsid proteins. Viruses of Clavaviridae , a family of filamentous archaeal viruses morphologically similar to adnaviruses, likewise possess MCPs that show no relation to the MCPs of viruses in Adnaviria and for that reason are excluded from the realm. [2]

Classification

Adnaviria is monotypic down to the rank of its sole class, Tokiviricetes, which has three orders. This taxonomy is shown hereafter: [2] [12]

History

Viruses of Adnaviria began to be discovered in the 1980s by Wolfram Zillig and his colleagues. [13] To discover these viruses, Zillig developed the methods used to culture their hosts. [14] The first of these to be described were TTV1, TTV2, and TTV3 in 1983. [15] TTV1 was classified as the first lipothrixvirus but is now classified as a tristromavirus. [16] SIRV2, a rudivirus, became a model for studying virus-host interactions [13] after its discovery in 1998. [17] The families Lipothrixviridae and Rudiviridae were then united under the order Ligamenvirales in 2012 based on evidence of their relation. [18] [19] Cryogenic electron microscopy would later show in 2020 that the MCPs of tristromaviruses contained a SIRV2-like fold like ligamenviruses, providing justification for establishing Adnaviria in the same year. [8] [20]

See also

Related Research Articles

<span class="mw-page-title-main">A-DNA</span>

A-DNA is one of the possible double helical structures which DNA can adopt. A-DNA is thought to be one of three biologically active double helical structures along with B-DNA and Z-DNA. It is a right-handed double helix fairly similar to the more common B-DNA form, but with a shorter, more compact helical structure whose base pairs are not perpendicular to the helix-axis as in B-DNA. It was discovered by Rosalind Franklin, who also named the A and B forms. She showed that DNA is driven into the A form when under dehydrating conditions. Such conditions are commonly used to form crystals, and many DNA crystal structures are in the A form. The same helical conformation occurs in double-stranded RNAs, and in DNA-RNA hybrid double helices.

Icerudivirus is a genus of viruses in the family Rudiviridae. These viruses are non-enveloped, stiff-rod-shaped viruses with linear dsDNA genomes, that infect hyperthermophilic archaea of the species Sulfolobus islandicus. There are three species in the genus.

<i>Lipothrixviridae</i> Family of viruses

Lipothrixviridae is a family of viruses in the order Ligamenvirales. Thermophilic archaea in the phylum Thermoproteota serve as natural hosts. There are 11 species in this family, assigned to 4 genera. The genus

<i>Ampullaviridae</i> Family of viruses

Ampullaviridae is a family of viruses that infect archaea of the genus Acidianus. Only one genus in this family has been described, Bottigliavirus, which contains three species. The name of the family and genus is derived from the Latin word for bottle, ampulla, due to the virions having the shape of a bottle. The family was first described during an investigation of the microbial flora of hot springs in Italy.

<i>Bicaudaviridae</i> Family of viruses

Bicaudaviridae is a family of hyperthermophilic archaeal viruses. Members of the genus Acidianus serve as natural hosts. There is only one genus (Bicaudavirus) and one species in this family: Acidianus two-tailed virus. However, Sulfolobus tengchongensis spindle-shaped viruses 1 and 2 are regarded to belong to this family also.

<i>Clavaviridae</i> Family of viruses

Clavaviridae is a family of double-stranded viruses that infect archaea. This family was first described by the team led by D. Prangishvili in 2010. There is one genus in this family (Clavavirus). Within this genus, a single species has been described to date: Aeropyrum pernix bacilliform virus 1 (APBV1).

Ligamenvirales is an order of linear viruses that infect archaea of the phylum Thermoproteota and have double-stranded DNA genomes. The order was proposed by David Prangishvili and Mart Krupovic in 2012 and subsequently created by the International Committee on Taxonomy of Viruses (ICTV).

<span class="mw-page-title-main">David Prangishvili</span>

David Prangishvili is a virologist, Professor at the Pasteur Institute of Paris, and foremost authority on viruses infecting Archaea.

Yingchengvirus is a genus of double stranded DNA viruses that infect haloarchaea. The genus was previously named Betasphaerolipovirus.

Tristromaviridae is a family of viruses. Archaea of the genera Thermoproteus and Pyrobaculum serve as natural hosts. Tristromaviridae is the sole family in the order Primavirales. There are two genera and three species in the family.

Betalipothrixvirus is a genus of viruses in the family Lipothrixviridae. Archaea serve as natural hosts. The genus contains six species.

Spiraviridae is a family of viruses that replicate in hyperthermophilic archaea of the genus Aeropyrum, specifically Aeropyrum pernix. The family contains one genus, Alphaspiravirus, which contains one species, Aeropyrum coil-shaped virus. The virions of Aeropyrum coil-shaped virus (ACV) are non-enveloped and in the shape of hollow cylinders that are formed by a coiling fiber that consists of two intertwining halves of the circular DNA strand inside a capsid. An appendage protrudes from each end of the cylindrical virion. The viral genome is positive-sense, single-stranded DNA ( ssDNA) and encodes for significantly more genes than other known ssDNA viruses. ACV is also unique in that it appears to lack its own enzymes to aid replication, instead likely using the host cell's replisomes. ACV has no known relation to any other archaea-infecting viruses, but it does share its coil-like morphology with some other archaeal viruses, suggesting that such viruses may be an ancient lineage that only infect archaea.

Sulfolobus islandicus rod-shaped virus 2, also referred to as SIRV2, is an archaeal virus whose only known host is the archaeon Sulfolobus islandicus. This virus belongs to the family Rudiviridae. Like other viruses in the family, it is common in geothermal environments.

Stygiolobus rod-shaped virus (SRV), scientific name Azorudivirus SRV, is an archaeal virus and the sole species in the genus Azorudivirus. Its only known host is Stygiolobus archaea.

Sulfolobus islandicus filamentous virus (SIFV) is an archaeal virus, classified in the family Lipothrixviridae within the order Ligamenvirales. The virus infects hypethermophilic and acidophilic archaeon Sulfolobus islandicus.

In virology, realm is the highest taxonomic rank established for viruses by the International Committee on Taxonomy of Viruses (ICTV), which oversees virus taxonomy. Six virus realms are recognized and united by specific highly conserved traits:

<i>Duplodnaviria</i> Realm of viruses

Duplodnaviria is a realm of viruses that includes all double-stranded DNA viruses that encode the HK97 fold major capsid protein. The HK97 fold major capsid protein is the primary component of the viral capsid, which stores the viral deoxyribonucleic acid (DNA). Viruses in the realm also share a number of other characteristics, such as an icosahedral capsid, an opening in the viral capsid called a portal, a protease enzyme that empties the inside of the capsid prior to DNA packaging, and a terminase enzyme that packages viral DNA into the capsid.

<i>Varidnaviria</i> Realm of viruses

Varidnaviria is a realm of viruses that includes all DNA viruses that encode major capsid proteins that contain a vertical jelly roll fold. The major capsid proteins (MCP) form into pseudohexameric subunits of the viral capsid, which stores the viral deoxyribonucleic acid (DNA), and are perpendicular, or vertical, to the surface of the capsid. Apart from this, viruses in the realm also share many other characteristics, such as minor capsid proteins (mCP) with the vertical jelly roll fold, an ATPase that packages viral DNA into the capsid, and a DNA polymerase that replicates the viral genome.

<span class="mw-page-title-main">Archaeal virus</span>

An archaeal virus is a virus that infects and replicates in archaea, a domain of unicellular, prokaryotic organisms. Archaeal viruses, like their hosts, are found worldwide, including in extreme environments inhospitable to most life such as acidic hot springs, highly saline bodies of water, and at the bottom of the ocean. They have been also found in the human body. The first known archaeal virus was described in 1974 and since then, a large diversity of archaeal viruses have been discovered, many possessing unique characteristics not found in other viruses. Little is known about their biological processes, such as how they replicate, but they are believed to have many independent origins, some of which likely predate the last archaeal common ancestor (LACA).

<span class="mw-page-title-main">Portogloboviridae</span> Family of viruses

Portogloboviridae is a family of DNA viruses that infect archaea. It is a proposed family of the realm Varidnaviria. Viruses in the family are related to Halopanivirales. The capsid proteins of these viruses and their characteristics are of evolutionary importance for the origin of the other Varidnaviria viruses since they seem to retain primordial characters.

References

  1. 1 2 Krupovic, M; Kuhn, JH; Wang, F; Baquero, DP; Dolja, VV; Egelman, EH; Prangishvili, D; Koonin, EV (12 July 2021). "Adnaviria: a new realm for archaeal filamentous viruses with linear A-form double-stranded DNA genomes". Journal of Virology. 95 (15): e0067321. doi:10.1128/JVI.00673-21. PMC   8274609 . PMID   34011550.
  2. 1 2 3 4 5 Krupovic M, Kuhn JH, Wang F, Baquero DP, Egelman EH, Koonin EV, Prangishvili D (31 July 2020). "Create one new realm (Adnaviria) for classification of filamentous archaeal viruses with linear dsDNA genomes" (docx). International Committee on Taxonomy of Viruses (ICTV). Retrieved 20 July 2021.
  3. 1 2 3 "Lipothrixviridae". International Committee on Taxonomy of Viruses (ICTV). Retrieved 20 July 2021.[ dead link ]
  4. 1 2 3 "Rudiviridae". International Committee on Taxonomy of Viruses (ICTV). Retrieved 20 July 2021.[ dead link ]
  5. 1 2 3 Prangishvili D, Rensen E, Mochizuki T, Krupovic M (February 2019). "ICTV Taxonomy Profile: Tristromaviridae" (PDF). J Gen Virol. 100 (2): 135–136. doi:10.1099/jgv.0.001190. PMID   30540248. S2CID   54475961.
  6. ↑ Krupovic, Mart; Kuhn, Jens H.; Wang, Fengbin; Baquero, Diana P.; Dolja, Valerian V.; Egelman, Edward H.; Prangishvili, David; Koonin, Eugene V. (2021-07-12). Sandri-Goldin, Rozanne M. (ed.). "Adnaviria : a New Realm for Archaeal Filamentous Viruses with Linear A-Form Double-Stranded DNA Genomes". Journal of Virology. 95 (15): e00673–21. doi:10.1128/JVI.00673-21. ISSN   0022-538X. PMC   8274609 . PMID   34011550.
  7. ↑ Silva, Jorge Miguel; Pratas, Diogo; Caetano, Tânia; Matos, Sérgio (2022-08-11). "The complexity landscape of viral genomes". GigaScience. 11: giac079. doi:10.1093/gigascience/giac079. ISSN   2047-217X. PMC   9366995 . PMID   35950839.
  8. 1 2 Wang F, Baquero DP, Su Z, Osinski T, Prangishvili D, Egelman EH, Krupovic M (29 April 2020). "Structure of a filamentous virus uncovers familial ties within the archaeal virosphere". Virus Evol. 6 (1): veaa023. doi:10.1093/ve/veaa023. PMC   7189273 . PMID   32368353.
  9. ↑ Prangshvili D, Krupovic M (July 2016). "Create genus Alphatristromavirus within the new family Tristromaviridae and remove genus Alphalipothrixvirus from the family Lipothrixviridae" (PDF). International Committee on Taxonomy of Viruses (ICTV). Retrieved 20 July 2021.
  10. ↑ Lawrence CM, Menon S, Eilers BJ, Bothner B, Khayat R, Douglas T, Young MJ (8 May 2009). "Structural and functional studies of archaeal viruses". J Biol Chem. 284 (19): 12599–12603. doi: 10.1074/jbc.R800078200 . PMC   2675988 . PMID   19158076.
  11. ↑ Krupovic M, Dolja VV, Koonin EV (November 2020). "The LUCA and its complex virome" (PDF). Nat Rev Microbiol. 18 (11): 661–670. doi:10.1038/s41579-020-0408-x. PMID   32665595. S2CID   220516514.
  12. ↑ "Virus Taxonomy: 2022 Release". International Committee on Taxonomy of Viruses (ICTV). March 2021. Retrieved 20 July 2021.
  13. 1 2 Snyder JC, Buldoc B, Young MJ (May 2015). "40 Years of archaeal virology: Expanding viral diversity". Virology. 479–480: 369–378. doi: 10.1016/j.virol.2015.03.031 . PMID   25866378.
  14. ↑ Stedman K. "Wolfram ASM Letter" (PDF). Portland State University. Retrieved 20 July 2021.
  15. ↑ Janekovic D, Wunderl S, Holz I, Zillig W, Gierl A, Neumann H (1983). "TTV1, TTV2 and TTV3, a family of viruses of the extremely thermophilic, anaerobic, sulfur reducing archaebacterium Thermoproteus tenax". Mol Gen Genet. 192 (1–2): 39–45. doi:10.1007/BF00327644. S2CID   46094905.
  16. ↑ "ICTV Taxonomy history: Betatristromavirus TTV1". International Committee on Taxonomy of Viruses (ICTV). Retrieved 20 July 2021.
  17. ↑ Prangishvili D, Arnold HP, Gotz D, Ziese U, Holz I, Kristjansson JK, Zillig W (August 1999). "A novel virus family, the Rudiviridae: Structure, virus-host interactions and genome variability of the sulfolobus viruses SIRV1 and SIRV2". Genetics. 152 (4): 1387–1396. doi:10.1093/genetics/152.4.1387. PMC   1460677 . PMID   10430569.
  18. ↑ "ICTV Taxonomy history: Ligamenvirales". International Committee on Taxonomy of Viruses (ICTV). Retrieved 20 July 2021.
  19. ↑ Prangishvili D, Krupovic M (21 June 2012). "Create the order Ligamenvirales containing the families Rudiviridae and Lipothrixviridae" (PDF). International Committee on Taxonomy of Viruses (ICTV). Retrieved 20 July 2021.
  20. ↑ "ICTV Taxonomy history: Adnaviria". International Committee on Taxonomy of Viruses (ICTV). Retrieved 20 July 2021.
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