Cafeteria roenbergensis virus

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Cafeteria roenbergensis virus
Giant virus CroV with its virophage Mavirus.png
The giant virus CroV with its virophage Mavirus at the lower left [1]
Virus classification OOjs UI icon edit-ltr.svg
(unranked): Virus
Realm: Varidnaviria
Kingdom: Bamfordvirae
Phylum: Nucleocytoviricota
Class: Megaviricetes
Order: Imitervirales
Family: Mimiviridae
Genus: Cafeteriavirus
Species:
Cafeteria roenbergensis virus

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

Contents

History

The virus was isolated from seawater samples collected from the Gulf of Mexico during 1989 to 1991, on a flagellate host that was misidentified as belonging to the genus Bodo; hence the original designation of the virus as BV-PW1. The virus was shown to be about 300 nm in diameter and have a complex internal structure, as well as evidence of a putative tail-like structure [2] Further work on the virus indicated that the host was an isolate of the genus Cafeteria and that the genome had a G+C content of ~34%. Further analysis suggested that the helicase of the virus was phylogenetically related to those found in the family Asfarviridae , and that the virus shared properties with members of the Nucleocytoplasmic large DNA viruses group. [3] CroV has one of the largest genomes of all marine viruses known, consisting of ~730,000 base pairs of double-stranded DNA. [4] Among its 544 predicted protein-coding genes are several that are usually restricted to cellular organisms, such as translation factors and enzymes for DNA repair and carbohydrate synthesis. CroV is distantly related to Mimivirus and belongs to a group of viruses known as Nucleocytoplasmic large DNA viruses. [5] CroV is itself parasitized by a virophage named "Mavirus". [6] [7]

Viral protein composition and structure

Cryo-EM images of CroV compared to APMV. (A) Cryo-electron micrograph of four CroV particles. (B) Single CroV particle with concave core depression (white arrow). (C) Single APMV particle. Scale bars in (A-C) represent 2,000 A. CroV TEM.jpg
Cryo-EM images of CroV compared to APMV. (A) Cryo-electron micrograph of four CroV particles. (B) Single CroV particle with concave core depression (white arrow). (C) Single APMV particle. Scale bars in (A–C) represent 2,000 Å.
Cryo-EM reconstruction of the CroV virion and capsomer arrangements of other giant icosahedral viruses. (A) Reconstruction of the CroV capsid. The isosurface of the map was colored by pentasymmetrons (purple) and trisymmetrons (blue, red, green, cyan and orange). One of the 30 edges of the icosahedron is marked by a cyan line. Two surface areas (a,b) are magnified and selected capsomers are labeled by yellow triangles to show their orientations. (B-E) Isolated icosahedral faces of CroV, PBCV-1, CIV and PpV01 capsids are shown schematically. Their T-numbers, asymmetric unit capsomer numbers, and trisymmetron capsomer numbers are listed. 5-fold, 3-fold, and 2-fold symbols are indicated in red and ASUs are outlined in blue. CroV reconstruction.jpg
Cryo-EM reconstruction of the CroV virion and capsomer arrangements of other giant icosahedral viruses. (A) Reconstruction of the CroV capsid. The isosurface of the map was colored by pentasymmetrons (purple) and trisymmetrons (blue, red, green, cyan and orange). One of the 30 edges of the icosahedron is marked by a cyan line. Two surface areas (a,b) are magnified and selected capsomers are labeled by yellow triangles to show their orientations. (B–E) Isolated icosahedral faces of CroV, PBCV-1, CIV and PpV01 capsids are shown schematically. Their T-numbers, asymmetric unit capsomer numbers, and trisymmetron capsomer numbers are listed. 5-fold, 3-fold, and 2-fold symbols are indicated in red and ASUs are outlined in blue.

Viral protein composition includes 141 encoded proteins that have been identified in CroV, a number believed to be in close proximity to the entirety of the virion proteome. The virus packages several distinct groups of proteins, including a presumably complete base excision repair (BER) pathway. This is the most extensive DNA repair machinery that has yet been observed in a virus. It is also the first virus to be found with a mechanosensitive ion channel protein, which may protect the genome from osmotic damage. [8] Mature CroV consists of a 300 nm diameter outer protein shell with icosahedral symmetry, an underlying lipid membrane, and an inner core that contains the genome. [9] Resolution of the virus structure by cryo-electron microscopy yielded an icosahedral virus capsid with a T number of 499 and a new model for capsid assembly for giant viruses.[ citation needed ]

Viral genome

A diagram of CroV's genome, showing the functional categories of what the genome encodes for, when in the viral life the genes are expressed, the types of promoters, as well as the types of repeats. CroV Phylogenetics.jpg
A diagram of CroV's genome, showing the functional categories of what the genome encodes for, when in the viral life the genes are expressed, the types of promoters, as well as the types of repeats.

CroV is the sole member of the genus Cafeteriavirus in the family Mimiviridae within the proposed order Megavirales. [10] Phylogenetic analysis indicates that the virus is a nucleocytoplasmic large DNA virus (NCLD virus). Acanthamoeba polyphaga mimivirus is its closest known relative, although the two viruses share less than one-third of homologous genes. [4]

The viral genome is primarily a 618,000 base pair strand flanked by large and highly repetitive repeats on both ends of the genome. These large caps are theorized to protect the ends of the protein-coding region, similar to telomeres in eukaryotes. Due to production of transcriptional genes, like that of tRNA synthetase, the virus is able to modify and regulate host translational machinery that results in CroV being less dependent on host-cell components. 5% of the genome consists of repetitive elements that serve a yet unknown purpose. A region of 38,000 bases was observed that is believed to be involved with carbohydrate metabolism. The virus contains pathways that help assist in the biosynthesis of KDO (3-deoxy-d-manno-octulosonate). The presence and expression of 10 genes involved in glycoprotein synthesis were identified, suggesting that CroV is able to potentially partake in virion-cell recognition. [4]

CroV also encodes several other interesting proteins. It encodes an entire biosynthetic pathway for the creation of 3-Deoxy-D-manno-oct-2-ulosonic acid, or KDO, which is a component of the cell walls of gram-negative bacteria. It also encodes two different photolyases, which repair DNA damage from UV radiation. CroV also encodes proteins that can carry out ubiquitination, which is a post-translational modification of proteins that functions in cellular signaling. [11]

Viral replication

VF is the "virus factory," where replication of CroV occurs. The white arrowhead indicates newly formed CroV particles. The white long-stem arrows indicate mavirus, a virophage that infects CroV. CroV.jpg
VF is the “virus factory,” where replication of CroV occurs. The white arrowhead indicates newly formed CroV particles. The white long-stem arrows indicate mavirus, a virophage that infects CroV.

Viral reproduction occurs in large constructs known as large cytoplasmic factories or viral factories. This is the site where DNA replication, transcription, and particle assembly are thought to take place. These factories are also the primary targets of the virophage Mavirus, which utilizes CroV machinery to replicate. Mavirus is a 19,000 kb circular double stranded DNA virus. Maviral infection reduces host cell death by interfering with CroV infection and replication. [12] Mavirus integrates into the genome of cells of Cafeteria roenbergensis , and thereby confers immunity to the population. [13]

CroV enters cells via phagocytosis. Once inside the cell, the CroV capsid disassembles and the viral proteins and genome are released. CroV does not use the transcription or translation machinery of the host cell. It remains in the cytoplasm, where a “virus factory” forms and replicates independent of the host cell nucleus. The CroV genome is not integrated into the host cell genome. CroV encodes eight subunits of DNA-dependent RNA polymerase and it also encodes at least six transcription factors, which allows the DNA genome to be transcribed into mRNA without the use of the cell’s proteins. CroV can then translate the mRNAs into proteins with help of the cell's translation machine and by using its own tRNA synthetase, tRNA, and translation initiation factors to fine-tune the translation to its own advantage. [4]

Host interaction

CroV infects Cafeteria roenbergensis , which is a marine zooflagellate. CroV is fatal to the host cell. This impacts coastal ecology because Cafeteria roenbergensis feeds on bacteria found in the water. When there are low numbers of Cafeteria roenbergensis due to extensive CroV infections, the bacterial populations rise exponentially. [4]

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.

<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.

Cauliflower mosaic virus (CaMV) is a member of the genus Caulimovirus, one of the six genera in the family Caulimoviridae, which are pararetroviruses that infect plants. Pararetroviruses replicate through reverse transcription just like retroviruses, but the viral particles contain DNA instead of RNA.

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).

<span class="mw-page-title-main">Viral protein</span>

The term viral protein refers to both the products of the genome of a virus and any host proteins incorporated into the viral particle. Viral proteins are grouped according to their functions, and groups of viral proteins include structural proteins, nonstructural proteins, regulatory proteins, and accessory proteins. Viruses are non-living and do not have the means to reproduce on their own, instead depending on their host cell's machinery to do this. Thus, viruses do not code for most of the proteins required for their replication and the translation of their mRNA into viral proteins, but use proteins encoded by the host cell for this purpose.

Lentivirus is a genus of retroviruses that cause chronic and deadly diseases characterized by long incubation periods, in humans and other mammalian species. The genus includes the human immunodeficiency virus (HIV), which causes AIDS. Lentiviruses are distributed worldwide, and are known to be hosted in apes, cows, goats, horses, cats, and sheep as well as several other mammals.

<i>Cafeteria roenbergensis</i> Species of single-celled organism

Cafeteria roenbergensis is a small bacterivorous marine flagellate. It was discovered by Danish marine ecologist Tom Fenchel and named by him and taxonomist David J. Patterson in 1988. It is in one of three genera of bicosoecids, and the first discovered of two known Cafeteria species. Bicosoecids belong to a broad group, the stramenopiles, also known as heterokonts (Heterokonta) that includes photosynthetic groups such as diatoms, brown, and golden algae, and non-photosynthetic groups such as opalinids, actinophryid "heliozoans", and oomycetes. The species is found primarily in coastal waters where there are high concentrations of bacteria on which it grazes. Its voracious appetite plays a significant role in regulating bacteria populations.

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.

<span class="mw-page-title-main">Virophage</span> Viral parasites of giant viruses

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.

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

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.

A giant virus, sometimes referred to as a girus, is a very large virus, some of which are larger than typical bacteria. All known giant viruses belong to the phylum Nucleocytoviricota.

<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

This glossary of virology is a list of definitions of terms and concepts used in virology, the study of viruses, particularly in the description of viruses and their actions. Related fields include microbiology, molecular biology, and genetics.

<i>Klosneuvirus</i> Genus of viruses

Klosneuvirus is a new type of giant virus found by the analysis of low-complexity metagenomes from a wastewater treatment plant in Klosterneuburg, Austria. It has a 1.57-Mb genome coding unusually high number of genes typically found in cellular organisms, including aminoacyl transfer RNA synthetases with specificities for 19 different amino acids, over 10 translation factors and several tRNA-modifying enzymes. Klosneuvirus, Indivirus, Catovirus and Hokovirus, are part of a group of giant viruses denoted as Klosneuviruses or Klosneuvirinae, a proposed subfamily of the Mimiviridae.

Hokovirus (HokV) is a genus of giant double-stranded DNA-containing viruses (NCLDV). This genus was detected during the analysis of metagenome samples of bottom sediments of reservoirs at the wastewater treatment plant in Klosterneuburg, Austria. New Klosneuvirus (KNV), Catovirus and Indivirus genera were also described together with Hokovirus, building up a putative virus subfamily Klosneuvirinae (Klosneuviruses) with KNV as type genus. Hokovirus has a large genome of 1.33 million base pairs. This is the third largest genome among known Klosneuviruses after KNV and Catovirus. GC content is 21.4 % Classification of metagenome, made by analyzing 18S rRNA indicate that their hosts are relate to the simple Cercozoa.

Catovirus (CatV) is a genus of giant double-stranded DNA-containing viruses. This genus was detected during the analysis of metagenome samples of bottom sediments of reservoirs at the wastewater treatment plant in Klosterneuburg, Austria. New Klosneuvirus (KNV), Hokovirus and Indivirus genera were also described together with Catovirus, building up a putative virus subfamily Klosneuvirinae (Klosneuviruses) with KNV as type genus. Catovirus has a large genome of 1.53 million base pairs. This is the second largest genome among known Klosneuviruses after KNV. GC content is 26.4 % Classification of metagenome, made by analyzing 18S rRNA indicate that their hosts are relate to the simple Cercozoa.

<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.

<span class="mw-page-title-main">Varidnaviria</span> 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.

References

  1. ↑ 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.
  2. ↑ D.R. Garza; C.A. Suttle (1995). "Large double-stranded DNA viruses which cause the lysis of a marine heterotrophic nanoflagellate (Bodo sp.) occur in natural marine viral communities". Aquatic Microbial Ecology. 9 (3): 203–210. doi: 10.3354/ame009203 .
  3. ↑ St. John, Tanya Marie (May 2003). Characterization of a large DNA virus (BV-PW1) infecting the heterotrophic marine nanoflagellate Cafeteria sp (MSc). Vancouver, Canada: University of British Columbia. doi:10.14288/1.0090960. hdl:2429/14364.
  4. 1 2 3 4 5 Matthias G. Fischer; Michael J. Allen; William H. Wilson; Curtis A. Suttle (2010). "Giant virus with a remarkable complement of genes infects marine zooplankton" (PDF). Proceedings of the National Academy of Sciences. 107 (45): 19508–19513. Bibcode:2010PNAS..10719508F. doi: 10.1073/pnas.1007615107 . PMC   2984142 . PMID   20974979.
  5. ↑ Matthias Fischer. "Suttle Laboratory Marine Virology and Microbiology: Profile: Matthias Fischer". Suttle Laboratory. Retrieved 2010-10-26.
  6. ↑ John Timmer. "A virus so large it gets viruses". Ars Technica. Retrieved 2010-03-05.
  7. ↑ Fischer, M. G.; Suttle, C. A. (2011). "A Virophage at the Origin of Large DNA Transposons". Science. 332 (6026): 231–234. Bibcode:2011Sci...332..231F. doi:10.1126/science.1199412. PMID   21385722. S2CID   206530677.
  8. ↑ Fischer, Matthias; Kelly, Isabelle; Foster, Leonard; Suttle, Curtis (October 2014). "The virion Catereria roenbergensis virus (CroV) contains a complex suite of proteins for transcription and DNA repair". Virology. 466–467: 82–94. doi: 10.1016/j.virol.2014.05.029 . PMID   24973308.
  9. ↑ Xiao, C.; Fischer, M.G.; Bolotaulo, D.M.; Ulloa-Rondeau, N.; Avila, G.A.; Suttle, C.A. (July 2017). "Cryo-EM reconstruction of the Cafeteria roenbergensis virus capsid suggests novel assembly pathway for giant viruses". Scientific Reports. 7 (1): 5484. Bibcode:2017NatSR...7.5484X. doi:10.1038/s41598-017-05824-w. PMC   5511168 . PMID   28710447.>
  10. ↑ Colson, P; De Lamballerie, X; Yutin, N; Asgari, S; Bigot, Y; Bideshi, BK; Cheng, XW; Federici, BA; Van Etten, JL; Koonin, EV; La Scola, B; Raoult, D (December 2013). ""Megavirales", a proposed new order for nucleocytoplasmic large DNA viruses". Archives of Virology. 158 (12): 2517–21. doi:10.1007/s00705-013-1768-6. PMC   4066373 . PMID   23812617.
  11. ↑ Van Etten, James (2011). "Another Really, Really Big Virus". Viruses. 3 (12): 32–46. doi: 10.3390/v3010032 . PMC   3187590 . PMID   21994725.
  12. ↑ Fischer, Matthias; Suttle, Curtis (April 2011). "A Virophage at the Origin of Large DNA Transposons". Science. 332 (6026): 231–234. Bibcode:2011Sci...332..231F. doi:10.1126/science.1199412. PMID   21385722. S2CID   206530677.
  13. ↑ 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.
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