Virophage

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Lavidaviridae
Sputnik virofago.jpg
Sputnik virophage
Virus classification OOjs UI icon edit-ltr.svg
(unranked): Virus
Realm: Varidnaviria
Kingdom: Bamfordvirae
Phylum: Preplasmiviricota
Class: Maveriviricetes
Order: Priklausovirales
Family:Lavidaviridae
Genera and species
The parasitic lifestyle of virophages (A) When the host cell is only infected by a giant virus, the latter establishes a cytoplasmic virus factory to replicate and generates new virions, and the host cell is most likely lysed at the end of its replication cycle. (B) When the host cell is co-infected with a giant virus and its virophage, the latter parasitizes the giant virus factory. The presence of virophages could seriously impact the infectivity of the giant virus by decreasing its replication efficiency and increasing the survival of the host cell. (C) When the giant virus genome is parasitized by a provirophage, the latter is expressed during the giant virus replication. The virophage is produced from the giant virus factory and inhibits the giant virus replication, thus increasing the host cell survival. VF: Virus factory Parasitic lifestyle of virophages.png
The parasitic lifestyle of virophages
(A) When the host cell is only infected by a giant virus, the latter establishes a cytoplasmic virus factory to replicate and generates new virions, and the host cell is most likely lysed at the end of its replication cycle.
(B) When the host cell is co-infected with a giant virus and its virophage, the latter parasitizes the giant virus factory. The presence of virophages could seriously impact the infectivity of the giant virus by decreasing its replication efficiency and increasing the survival of the host cell.
(C) When the giant virus genome is parasitized by a provirophage, the latter is expressed during the giant virus replication. The virophage is produced from the giant virus factory and inhibits the giant virus replication, thus increasing the host cell survival.
VF: Virus factory
Virophages and satellite virus' lifestyle (A) The replication of virophages is supposed to occur entirely in the virus factory of its giant virus host, depending on the giant virus expression/replication complex. (B) The concept of satellite virus implicates that the virus initiates the expression and replication of its genome in the nucleus using the host cell machinery and then goes to the cytoplasm. In the cytoplasm, the satellite virus hijacks the morphogenesis machinery of its helper virus to produce its progeny. Virophages and satellite virus lifestyle.png
Virophages and satellite virus’ lifestyle
(A) The replication of virophages is supposed to occur entirely in the virus factory of its giant virus host, depending on the giant virus expression/replication complex.
(B) The concept of satellite virus implicates that the virus initiates the expression and replication of its genome in the nucleus using the host cell machinery and then goes to the cytoplasm. In the cytoplasm, the satellite virus hijacks the morphogenesis machinery of its helper virus to produce its progeny.

Virophages are small, double-stranded DNA viral phages that require the co-infection of another virus. The co-infecting viruses are typically giant viruses. Virophages rely on the viral replication factory of the co-infecting giant virus for their own replication. One of the characteristics of virophages is that they have a parasitic relationship with the co-infecting virus. Their dependence upon the giant virus for replication often results in the deactivation of the giant viruses. The virophage may improve the recovery and survival of the host organism.

Contents

All known virophages are grouped into the family Lavidaviridae (from "large virus dependent or associated" + -viridae). [2]

Discovery

The first virophage was discovered in a cooling tower in Paris in 2008. It was discovered with its co-infecting giant virus, Acanthamoeba castellanii mamavirus (ACMV). The virophage was named Sputnik and its replication relied entirely on the co-infection of ACMV and its cytoplasmic replication machinery. Sputnik was also discovered to have an inhibitory effect on ACMV and improved the survival of the host. Other characterised virophages include Sputnik 2, Sputnik 3, Zamilon and Mavirus. [3] [4] [5] [6]

A majority of these virophages are being discovered by analyzing metagenomic data sets. In metagenomic analysis, DNA sequences are run through multiple bioinformatic algorithms which pull out certain important patterns and characteristics. In these data sets are giant viruses and virophages. They are separated by looking for sequences around 17 to 20  kbp long which have similarities to already sequenced virophages. These virophages can have linear or circular double-stranded DNA genomes. [7] Known virophages in culture have icosahedral capsid particles that measure around 40 to 80 nanometers long, [8] and virophage particles are so small that electron microscopy must be used to view them. Metagenomic sequence-based analyses have been used to predict around 57 complete and partial virophage genomes [9] and in December 2019 to identify 328 high-quality (complete or near-complete) genomes from diverse habitats including the human gut, plant rhizosphere, and terrestrial subsurface, from 27 distinct taxonomic clades. [10]

Host range and replication

Virophages need to have a co-infecting virus in order for them to replicate. The virophages do not have the necessary enzymes to replicate on their own. Virophages use the giant viral replication machinery to replicate their own genomes and continue their existence. The host range for virophages include giant viruses with double stranded DNA genomes. Virophages use the transcriptional machinery of these giant viruses for their own replication instead of the host's transcriptional machinery. For example, the discovery of the virophage associated with the Samba virus decreased the viruses concentration in the host while the virophage was replicating using the giant virus. The host amoeba also showed a partial recovery from the infection by the Samba virus. [7]

Genome

Virophages have small double-stranded DNA genomes that are either circular or linear in shape. The size of these genomes can vary depending on the giant virus it infects. Most virophages have genomes around 17–30 kbp (kilobasepairs). [8] [9] Their genome is protected by an icosahedral capsid measuring approximately 40–80 nm in length. [8] In contrast, their co-infecting giant virus counterparts can have genomes as large as 1–2  Mbp (megabasepairs). [7] Some of the largest genomes of virophages are similar to the genome size of an adenovirus. [8]

Genome

Size (kbp)

Particle Size

(diameter, in nm)

Virus: Poliovirus 730
Virus: Adenoviridae 26–4890–100
Virophage: Zamilon Virophage1750–60
Virophage: Sputnik Virophage1874
Giant virus: Cafeteria roenbergensis virus 70075
Giant virus: Mimivirus 1,181400–800

All virophages known so far have four core genes. They are the virophage-specific major and minor capsid proteins (MCP and mCP), PRO (cysteine protease), and a DNA-packaging ATPase. The two capsids are almost universally found in a conserved block. [10] The MCP has two vertical jelly roll fold domain typical of Bamfordvirae, while the mCP (penton) has a regular jelly roll fold domain. [11]

Taxonomy

The family Lavidaviridae with the two genera, Sputnikvirus and Mavirus, has been established by the International Committee on Taxonomy of Viruses for classification of virophages. It is the sole family under order Priklausovirales (from Lithuanian priklausomas, "dependent"), which in turn is the sole order under class Maveriviricetes (from Maverick transposons). [8] [12]

Additionally, virophage genomes identified from metagenomes have been classified together with the isolate virophages into 27 distinct clades with consistent genome length, gene content, and habitat distribution. [10] Some fragmentary virophage sequences were additionally reported in a Loki's Castle metagenome. [13]

Genome organization of cultured virophages Genome representation of the virophages Sputnik, Zamilon, and Mavirus. Homologous genes are colored identically. Genome organization of cultured virophages.jpg
Genome organization of cultured virophages
Genome representation of the virophages Sputnik , Zamilon , and Mavirus . Homologous genes are colored identically.
The parasites of the giants are giants Plot comparing the virion and genome sizes for known virophages and some traditional satellite viruses. The ball sizes are proportional to the capsid sizes. Virion and genome sizes for virophages.png
The parasites of the giants are giants
Plot comparing the virion and genome sizes for known virophages and some traditional satellite viruses. The ball sizes are proportional to the capsid sizes.
Timeline of virophage discoveries 2003-2019 Timeline showing the chronological order of description of virophages isolated by co-culture and the major discoveries in the virophage field. RNV: Rio Negro Virophage. OLV: Organic Lake Virophage. Virophage timeline.png
Timeline of virophage discoveries 2003–2019
Timeline showing the chronological order of description of virophages isolated by co-culture and the major discoveries in the virophage field.
RNV: Rio Negro Virophage. OLV: Organic Lake Virophage.

Related Research Articles

<span class="mw-page-title-main">DNA virus</span> Virus that has DNA as its genetic material

A DNA virus is a virus that has a genome made of deoxyribonucleic acid (DNA) that is replicated by a DNA polymerase. They can be divided between those that have two strands of DNA in their genome, called double-stranded DNA (dsDNA) viruses, and those that have one strand of DNA in their genome, called single-stranded DNA (ssDNA) viruses. dsDNA viruses primarily belong to two realms: Duplodnaviria and Varidnaviria, and ssDNA viruses are almost exclusively assigned to the realm Monodnaviria, which also includes some dsDNA viruses. Additionally, many DNA viruses are unassigned to higher taxa. Reverse transcribing viruses, which have a DNA genome that is replicated through an RNA intermediate by a reverse transcriptase, are classified into the kingdom Pararnavirae in the realm Riboviria.

<span class="mw-page-title-main">RNA virus</span> Subclass of viruses

An RNA virus is a virus—other than a retrovirus—that has ribonucleic acid (RNA) as its genetic material. The nucleic acid is usually single-stranded RNA (ssRNA) but it may be double-stranded (dsRNA). Notable human diseases caused by RNA viruses include the common cold, influenza, SARS, MERS, COVID-19, Dengue virus, hepatitis C, hepatitis E, West Nile fever, Ebola virus disease, rabies, polio, mumps, and measles.

<i>Mimivirus</i> Genus of viruses

Mimivirus is a genus of giant viruses, in the family Mimiviridae. Amoeba serve as their natural hosts. This genus contains a single identified species named Acanthamoeba polyphaga mimivirus (APMV). It also refers to a group of phylogenetically related large viruses.

<span class="mw-page-title-main">Satellite (biology)</span> Subviral agent which depends on a helper virus for its replication

A satellite is a subviral agent that depends on the coinfection of a host cell with a helper virus for its replication. Satellites can be divided into two major classes: satellite viruses and satellite nucleic acids. Satellite viruses, which are most commonly associated with plants, are also found in mammals, arthropods, and bacteria. They encode structural proteins to enclose their genetic material, which are therefore distinct from the structural proteins of their helper viruses. Satellite nucleic acids, in contrast, do not encode their own structural proteins, but instead are encapsulated by proteins encoded by their helper viruses. The genomes of satellites range upward from 359 nucleotides in length for satellite tobacco ringspot virus RNA (STobRV).

Phycodnaviridae is a family of large (100–560 kb) double-stranded DNA viruses that infect marine or freshwater eukaryotic algae. Viruses within this family have a similar morphology, with an icosahedral capsid. As of 2014, there were 33 species in this family, divided among 6 genera. This family belongs to a super-group of large viruses known as nucleocytoplasmic large DNA viruses. Evidence was published in 2014 suggesting that specific strains of Phycodnaviridae might infect humans rather than just algal species, as was previously believed. Most genera under this family enter the host cell by cell receptor endocytosis and replicate in the nucleus. Phycodnaviridae play important ecological roles by regulating the growth and productivity of their algal hosts. Algal species such Heterosigma akashiwo and the genus Chrysochromulina can form dense blooms which can be damaging to fisheries, resulting in losses in the aquaculture industry. Heterosigma akashiwo virus (HaV) has been suggested for use as a microbial agent to prevent the recurrence of toxic red tides produced by this algal species. Phycodnaviridae cause death and lysis of freshwater and marine algal species, liberating organic carbon, nitrogen and phosphorus into the water, providing nutrients for the microbial loop.

<i>Marnaviridae</i> Family of viruses

Marnaviridae is a family of positive-stranded RNA viruses in the order Picornavirales that infect various photosynthetic marine protists. Members of the family have non-enveloped, icosahedral capsids. Replication occurs in the cytoplasm and causes lysis of the host cell. The first species of this family that was isolated is Heterosigma akashiwo RNA virus (HaRNAV) in the genus Marnavirus, which infects the toxic bloom-forming Raphidophyte alga, Heterosigma akashiwo. As of 2021, there are twenty species across seven genera in this family, as well as many other related virus sequences discovered through metagenomic sequencing that are currently unclassified.

<span class="mw-page-title-main">Virus</span> Infectious agent that replicates in cells

A virus is a submicroscopic infectious agent that replicates only inside the living cells of an organism. Viruses infect all life forms, from animals and plants to microorganisms, including bacteria and archaea. Viruses are found in almost every ecosystem on Earth and are the most numerous type of biological entity. Since Dmitri Ivanovsky's 1892 article describing a non-bacterial pathogen infecting tobacco plants and the discovery of the tobacco mosaic virus by Martinus Beijerinck in 1898, more than 11,000 of the millions of virus species have been described in detail. The study of viruses is known as virology, a subspeciality of microbiology.

<span class="mw-page-title-main">Sputnik virophage</span> Subviral agent

Mimivirus-dependent virus Sputnik is a subviral agent that reproduces in amoeba cells that are already infected by a certain helper virus; Sputnik uses the helper virus's machinery for reproduction and inhibits replication of the helper virus. It is known as a virophage, in analogy to the term bacteriophage.

<i>Mimiviridae</i> Family of viruses

Mimiviridae is a family of viruses. Amoeba and other protists serve as natural hosts. The family is divided in up to 4 subfamilies. Viruses in this family belong to the nucleocytoplasmic large DNA virus clade (NCLDV), also referred to as giant viruses.

Mamavirus is a large and complex virus in the Group I family Mimiviridae. The virus is exceptionally large, and larger than many bacteria. Mamavirus and other mimiviridae belong to nucleocytoplasmic large DNA virus (NCLDVs) family. Mamavirus can be compared to the similar complex virus mimivirus; mamavirus was so named because it is similar to but larger than mimivirus.

<i>Cafeteria roenbergensis virus</i> Species of virus

Cafeteria roenbergensis virus (CroV) is a giant virus that infects the marine bicosoecid flagellate Cafeteria roenbergensis, a member of the microzooplankton community.

<span class="mw-page-title-main">Megavirus</span> Genus of viruses

Megavirus is a viral genus containing a single identified species named Megavirus chilense, phylogenetically related to Acanthamoeba polyphaga Mimivirus (APMV). In colloquial speech, Megavirus chilensis is more commonly referred to as just “Megavirus”. Until the discovery of pandoraviruses in 2013, it had the largest capsid diameter of all known viruses, as well as the largest and most complex genome among all known viruses.

Organic Lake virophage (OLV) is a double-stranded DNA virophage. It was detected metagenomically in samples from Organic Lake, Antarctica.

<span class="mw-page-title-main">Mavirus</span> Genus of viruses

Mavirus is a genus of double stranded DNA virus that can infect the marine phagotrophic flagellate Cafeteria roenbergensis, but only in the presence of the giant CroV virus. The genus contains only one species, Cafeteriavirus-dependent mavirus. Mavirus can integrate into the genome of cells of C. roenbergensis, and thereby confer immunity to the population

<span class="mw-page-title-main">Zamilon virophage</span> Virus type

Mimivirus-dependent virus Zamilon, or Zamilon, is a virophage, a group of small DNA viruses that infect protists and require a helper virus to replicate; they are a type of satellite virus. Discovered in 2013 in Tunisia, infecting Acanthamoeba polyphaga amoebae, Zamilon most closely resembles Sputnik, the first virophage to be discovered. The name is Arabic for "the neighbour". Its spherical particle is 50–60 nm in diameter, and contains a circular double-stranded DNA genome of around 17 kb, which is predicted to encode 20 polypeptides. A related strain, Zamilon 2, has been identified in North America.

<i>Faustovirus</i> Genus of viruses

Faustovirus is a genus of giant virus which infects amoebae associated with humans. The virus was first isolated in 2015 and shown to be around 0.2 micrometers in diameter with a double stranded DNA genome of 466 kilobases predicted to encode 451 proteins. Although classified as a nucleocytoplasmic large DNA virus (NCLDV), faustoviruses share less than a quarter of their genes with other NCLDVs; however, ~46% are homologous to bacterial genes and the remainder are orphan genes (ORFans). Specifically, the gene encoding the major capsid protein (MCP) of faustovirus is different than that of its most closely related giant virus, asfivirus, as well as other NCLDVs. In asfivirus, the gene encoding MCP is a single genomic fragment of ~2000 base pairs (bp), however, in faustovirus the MCP is encoded by 13 exons separated by 12 large introns. The exons have a mean length of 149 bp and the introns have a mean length of 1,273 bp. The presence of introns in faustovirus genes is highly unusual for viruses.

<span class="mw-page-title-main">Jelly roll fold</span> Type of beta barrel protein domain structure

The jelly roll or Swiss roll fold is a protein fold or supersecondary structure composed of eight beta strands arranged in two four-stranded sheets. The name of the structure was introduced by Jane S. Richardson in 1981, reflecting its resemblance to the jelly or Swiss roll cake. The fold is an elaboration on the Greek key motif and is sometimes considered a form of beta barrel. It is very common in viral proteins, particularly viral capsid proteins. Taken together, the jelly roll and Greek key structures comprise around 30% of the all-beta proteins annotated in the Structural Classification of Proteins (SCOP) database.

<span class="mw-page-title-main">Marine viruses</span> Viruses found in marine environments

Marine viruses are defined by their habitat as viruses that are found in marine environments, that is, in the saltwater of seas or oceans or the brackish water of coastal estuaries. Viruses are small infectious agents that can only replicate inside the living cells of a host organism, because they need the replication machinery of the host to do so. They can infect all types of life forms, from animals and plants to microorganisms, including bacteria and archaea.

<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.

Nucleocytoviricota is a phylum of viruses. Members of the phylum are also known as the nucleocytoplasmic large DNA viruses (NCLDV), which serves as the basis of the name of the phylum with the suffix -viricota for virus phylum. These viruses are referred to as nucleocytoplasmic because they are often able to replicate in both the host's cell nucleus and cytoplasm.

References

  1. 1 2 3 4 Mougari, S., Sahmi-Bounsiar, D., Levasseur, A., Colson, P. and La Scola, B. (2019) "Virophages of Giant Viruses: An Update at Eleven". Viruses, 11(8): 733. doi:10.3390/v11080733. CC-BY icon.svg Material was copied from this source, which is available under a Creative Commons Attribution 4.0 International License
  2. ↑ Duponchel, S; Fischer, MG (March 2019). "Viva lavidaviruses! Five features of virophages that parasitize giant DNA viruses". PLOS Pathogens. 15 (3): e1007592. doi: 10.1371/journal.ppat.1007592 . PMC   6428243 . PMID   30897185.
  3. ↑ Fischer MG, Suttle CA (April 2011). "A virophage at the origin of large DNA transposons". Science. 332 (6026): 231–4. Bibcode:2011Sci...332..231F. doi:10.1126/science.1199412. PMID   21385722. S2CID   206530677.
  4. ↑ Fischer MG, Hackl (December 2016). "Host genome integration and giant virus-induced reactivation of the virophage mavirus". Nature. 540 (7632): 288–91. Bibcode:2016Natur.540..288F. doi:10.1038/nature20593. PMID   27929021. S2CID   4458402.
  5. ↑ taxonomy. "Taxonomy browser (Lavidaviridae)". www.ncbi.nlm.nih.gov. Retrieved 2023-09-20.
  6. ↑ taxonomy. "Taxonomy browser (Preplasmiviricota)". www.ncbi.nlm.nih.gov. Retrieved 2023-09-20.
  7. 1 2 3 Katzourakis, Aris; Aswad, Amr (2014). "The origins of giant viruses, virophages and their relatives in host genomes". BMC Biology. 12: 2–3. doi: 10.1186/s12915-014-0051-y . PMC   4096385 . PMID   25184667.
  8. 1 2 3 4 5 Krupovic, Mart; Kuhn, Jens; Fischer, Metthias (Fall 2015). "A classification system for virophages and satellite viruses" (PDF). Archives of Virology. 161 (1): 233–247. doi:10.1007/s00705-015-2622-9. PMID   26446887. S2CID   14196910 – via Springer.
  9. 1 2 Roux, Simon; Chan, Leong-Keat; Egan, Rob; Malmstrom, Rex R.; McMahon, Katherine D.; Sullivan, Matthew B. (2017-10-11). "Ecogenomics of virophages and their giant virus hosts assessed through time series metagenomics". Nature Communications. 8 (1): 858. Bibcode:2017NatCo...8..858R. doi:10.1038/s41467-017-01086-2. ISSN   2041-1723. PMC   5636890 . PMID   29021524.
  10. 1 2 3 Paez-Espino, David; Zhou, Jinglie; Roux, Simon; Nayfach, Stephen; Pavlopoulos, Georgios A.; Schulz, Frederik; McMahon, Katherine D.; Walsh, David; Woyke, Tanja; Ivanova, Natalia N.; Eloe-Fadrosh, Emiley A.; Tringe, Susannah G.; Kyrpides, Nikos C. (2019-12-10). "Diversity, evolution, and classification of virophages uncovered through global metagenomics". Microbiome. 7 (1): 157. doi: 10.1186/s40168-019-0768-5 . PMC   6905037 . PMID   31823797.
  11. ↑ Born, D; Reuter, L; Mersdorf, U; Mueller, M; Fischer, MG; Meinhart, A; Reinstein, J (10 July 2018). "Capsid protein structure, self-assembly, and processing reveal morphogenesis of the marine virophage mavirus". Proceedings of the National Academy of Sciences of the United States of America. 115 (28): 7332–7337. Bibcode:2018PNAS..115.7332B. doi: 10.1073/pnas.1805376115 . PMC   6048507 . PMID   29941605.
  12. ↑ Koonin EV, Dolja VV, Krupovic M, Varsani A, Wolf YI, Yutin N, Zerbini M, Kuhn JH (October 2019). "Create a megataxonomic framework, filling all principal taxonomic ranks, for DNA viruses encoding vertical jelly roll-type major capsid proteins". ICTV Proposal (Taxoprop): 2019.003G. doi:10.13140/RG.2.2.14886.47684.
  13. ↑ Bäckström D, Yutin N, Jørgensen SL, Dharamshi J, Homa F, Zaremba-Niedwiedzka K, Spang A, Wolf YI, Koonin EV, Ettema TJ (2019). "Virus genomes from deep sea sediments expand the ocean megavirome and support independent origins of viral gigantism". mBio. 10 (2): e02497-18. doi:10.1128/mBio.02497-18. PMC   6401483 . PMID   30837339. PDF
  14. ↑ Duponchel, S. and Fischer, M.G. (2019) "Viva lavidaviruses! Five features of virophages that parasitize giant DNA viruses". PLoS pathogens, 15(3). doi : 10.1371/journal.ppat.1007592. CC-BY icon.svg Material was copied from this source, which is available under a Creative Commons Attribution 4.0 International License.
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