Giant virus

Last updated

A giant virus, sometimes referred to as a girus, is a very large virus, some of which are larger than typical bacteria. [1] [2] All known giant viruses belong to the phylum Nucleocytoviricota . [3]

Contents

Description

While the exact criteria as defined in the scientific literature vary, giant viruses are generally described as viruses having large, pseudo-icosahedral capsids (200 to 400 nanometers in diameter) [4] that may be surrounded by a thick (approximately 100 nm) layer of filamentous protein fibers. The viruses have large, double-stranded DNA genomes (300 to >1000 kilobasepairs) that encode a large contingent of genes (of the order of 1000 genes). [3] [5] The best characterized giant viruses are the phylogenetically related mimivirus and megavirus, which belong to the family Mimiviridae (aka Megaviridae), and are distinguished by their large capsid diameters. [3] [5] Giant viruses from the deep ocean, terrestrial sources, and human patients contain genes encoding cytochrome P450 (CYP; P450) enzymes. The origin of these P450 genes in giant viruses remains unknown but may have been acquired from an ancient host. [6]

The genomes of many giant viruses encode many unusual genes that are not found in other viruses, including genes involved in glycolysis and the TCA cycle, [7] fermentation, [8] and the cytoskeleton. [9] [10] [11]

Cryo-EM images of the giant viruses CroV and 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 the giant viruses CroV and 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.
Phylogeny of Nucleocytoviricota Journal.pbio.3001430.g002.png
Phylogeny of Nucleocytoviricota

History

The first giant viruses to be described were chloroviruses of the family Phycodnaviridae. These were discovered in 1981 by Russel H. Meints, James L. Van Etten, Daniel Kuczmarski, Kit Lee, and Barbara Ang. The first chlorovirus was initially called HVCV (Hydra viridis Chlorella virus) since it was first found to infect Chlorella-like algae. [13] [14]

Other giant viruses that infected marine flagellates were described later. The first mimivirus (BV-PW1) was described in 1995, [15] but was not recognized as such until its sequenced genome was released as Cafeteria roenbergensis virus (CroV) in 2010. [16] Subsequently, the Giant Virus Acanthamoeba polyphaga Mimivirus was characterized [17] (which had been mistaken as a bacterium in 1993), [18] and then sequenced. [19] The term "girus" was coined to refer to the group in 2006. [20]

Genetics and evolution

The genomes of giant viruses are the largest known for viruses, and contain genes that encode for important elements of translation machinery, a characteristic that had previously been believed to be indicative of cellular organisms. These genes include multiple genes encoding a number of aminoacyl tRNA synthetases, enzymes that catalyze the esterification of specific amino acids or their precursors to their corresponding cognate tRNAs to form an aminoacyl tRNA that is then used during translation. [5] The presence of four aminoacyl tRNA synthetase encoding genes in mimivirus and mamavirus genomes, both species within the Mimiviridae family, as well as the discovery of seven aminoacyl tRNA synthetase genes in the megavirus genome (including those in Mimiviridae) provide evidence that these large DNA viruses may have evolved from a shared cellular genome ancestor by means of genome reduction. [5]

The discovery and subsequent characterization of giant viruses has triggered debate on their evolutionary origins. The two main hypotheses are that they evolved from small viruses by picking up DNA from host organisms; or that they evolved from very complicated organisms via genome reduction, losing various functions including self-reproduction. [21] The possible complicated ancestral organism is also a topic of debate: by one proposal, it might represent a fourth domain of life, [5] but this has been largely discounted. [22] [23] [24]

Comparison of largest known giant viruses

Largest giant viruses with complete sequenced genomes as of June 2018
Giant virus nameGenome LengthGenesCapsid diameter (nm)Hair coverGenbank #
Pandoravirus salinus [25] 2,473,8702500 proteins (predicted)~500KC977571
Tupanvirus [26] 1,500,0001276–1425 proteins≥450+550 [27] KY523104
MF405918 [28]
Bodo saltans virus [29] 1,385,8691227 proteins (predicted)~300yes (~40 nm)MF782455
Megavirus chilense [30] 1,259,1971120 proteins (predicted)440yes (75 nm)JN258408
Mamavirus [31] 1,191,6931023 proteins (predicted)500yes (120 nm)JF801956
Mimivirus [19] [32] 1,181,549979 proteins 39 non-coding500yes (120 nm)NC_014649
M4 [33] (Mimivirus "bald" variant)981,813756 proteins (predicted)390NoJN036606
Cafeteria roenbergensis virus [34] 617,453 (730 kb)544 proteins (predicted)300NoNC_014637

The whole list is in the Giant Virus Toplist created by the Giant Virus Finder software. [35] As of June 11, 2018, there were 183 listed. [36]

Specific common features among giant viruses
Giant virus nameAminoacyl-tRNA synthetaseOctocoral-like 1MutS2Stargate [37] Known virophage [38] Cytoplasmic virion factoryHost
Megavirus chilensis7 (Tyr, Arg, Met, Cys, Trp, Asn, Ile)yesyesnoyesAcanthamoeba (Unikonta, Amoebozoa)
Mamavirus4 (Tyr, Arg, Met, Cys)yesyesyesyesAcanthamoeba (Unikonta, Amoebozoa)
Mimivirus4 (Tyr, Arg, Met, Cys)yesyesyesyesAcanthamoeba (Unikonta, Amoebozoa)
M4 (Mimivirus "bald" variant)3 (Met, Cys, Arg)yesyesResistantyesAcanthamoeba (Unikonta, Amoebozoa)
Cafeteria roenbergensis virus1 (Ile)yesnoyesyesPhagotrophic protozoan (Heterokonta, Stramenopiles)

1Mutator S (MutS) and its homologs are a family of DNA mismatch repair proteins involved in the mismatch repair system that acts to correct point mutations or small insertion/deletion loops produced during DNA replication, increasing the fidelity of replication.2A stargate is a five-pronged star structure present on the viral capsid forming the portal through which the internal core of the particle is delivered to the host's cytoplasm.

See also

Related Research Articles

<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">Mobilome</span>

The mobilome is the entire set of mobile genetic elements in a genome. Mobilomes are found in eukaryotes, prokaryotes, and viruses. The compositions of mobilomes differ among lineages of life, with transposable elements being the major mobile elements in eukaryotes, and plasmids and prophages being the major types in prokaryotes. Virophages contribute to the viral mobilome.

<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> 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.

<i>Marseilleviridae</i> Family of viruses

Marseilleviridae is a family of viruses first named in 2012. The genomes of these viruses are double-stranded DNA. Amoeba are often hosts, but there is evidence that they are found in humans as well. The family contains one genus and four species, two of which are unassigned to a genus. It is a member of the nucleocytoplasmic large DNA viruses clade.

<i>Megavirus</i> Genus of viruses

Megavirus is a viral genus, phylogenetically related to Acanthamoeba polyphaga mimivirus (APMV). In colloquial speech, Megavirus chilense 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.

A transpoviron is a plasmid-like genetic element found in the genomes of giant DNA viruses.

<i>Pandoravirus</i> Genus of giant virus possessing a large double-stranded DNA genome

Pandoravirus is a proposed genus of giant virus, first discovered in 2013. It is the third largest in physical size of any known viral genus, behind Pithovirus and Megaklothovirus. Pandoraviruses have double stranded DNA genomes, with the largest genome size of any known viral genus.

<i>Alphapithovirus</i> Genus of viruses

Alphapithovirus, is a genus of giant virus known from two species, Alphapithovirus sibericum, which infects amoebas, and Alphapithovirus massiliense. It is DNA-based and is a member of the nucleocytoplasmic large DNA viruses clade. It was discovered in 2014, when a viable specimen was found in a 30,000-year-old ice core harvested from permafrost in Siberia, Russia.

<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.

Polintons are large DNA transposons which contain genes with homology to viral proteins and which are often found in eukaryotic genomes. They were first discovered in the mid-2000s and are the largest and most complex known DNA transposons. Polintons encode up to 10 individual proteins and derive their name from two key proteins, a DNA polymerase and a retroviral-like integrase.

<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.

<i>Tupanvirus</i> Proposed genus of viruses

Tupanvirus is a genus of viruses first described in 2018. The genus is composed of two species of virus that are in the giant virus group. Researchers discovered the first isolate in 2012 from deep water sediment samples taken at 3,000 m depth off the coast of Brazil. The second isolate was collected from a soda lake in Southern Nhecolândia, Brazil in 2014. They are named after Tupã (Tupan), a Guaraní thunder god, and the places they were found. These are the first viruses reported to possess genes for amino-acyl tRNA synthetases for all 20 standard amino acids.

<span class="mw-page-title-main">Chrysochromulina ericina virus</span> Giant virus

Chrysochromulina ericina virus 01B, or simply Chrysochromulina ericina virus (CeV) is a giant virus in the family Mimiviridae infecting Haptolina ericina, a marine microalgae member of the Haptophyta. CeV is a dsDNA virus.

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:

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.

Virosphere was coined to refer to all those places in which viruses are found or which are affected by viruses. However, more recently virosphere has also been used to refer to the pool of viruses that occurs in all hosts and all environments, as well as viruses associated with specific types of hosts, type of genome or ecological niche.

References

  1. ↑ Reynolds KA (2010). "Mysterious Microbe in Water Challenges the Very Definition of a Virus" (PDF). Water Conditioning & Purification. Archived from the original (PDF) on 2014-03-19.
  2. ↑ Ogata H, Toyoda K, Tomaru Y, Nakayama N, Shirai Y, Claverie JM, Nagasaki K (October 2009). "Remarkable sequence similarity between the dinoflagellate-infecting marine girus and the terrestrial pathogen African swine fever virus". Virology Journal. 6 (178): 178. doi: 10.1186/1743-422X-6-178 . PMC   2777158 . PMID   19860921.
  3. 1 2 3 Van Etten JL (July–August 2011). "Giant Viruses". American Scientist. 99 (4): 304–311. doi:10.1511/2011.91.304. Archived from the original on 2011-06-21.
  4. ↑ Xiao C, Fischer MG, Bolotaulo DM, Ulloa-Rondeau N, Avila GA, Suttle CA (14 July 2017). "Cryo-EM reconstruction of the Cafeteria roenbergensis virus capsid suggests novel assembly pathway for giant viruses". Scientific Reports. 7 (5484): 5484. Bibcode:2017NatSR...7.5484X. doi:10.1038/s41598-017-05824-w. PMC   5511168 . PMID   28710447.
  5. 1 2 3 4 5 Legendre M, Arslan D, Abergel C, Claverie JM (January 2012). "Genomics of Megavirus and the elusive fourth domain of Life". Communicative & Integrative Biology. 5 (1): 102–6. doi:10.4161/cib.18624. PMC   3291303 . PMID   22482024.
  6. ↑ Lamb DC, Follmer AH, Goldstone JV, Nelson DR, Warrilow AG, Price CL, et al. (June 2019). "On the occurrence of cytochrome P450 in viruses". Proceedings of the National Academy of Sciences of the United States of America. 116 (25): 12343–12352. Bibcode:2019PNAS..11612343L. doi: 10.1073/pnas.1901080116 . PMC   6589655 . PMID   31167942.
  7. ↑ Moniruzzaman M, Martinez-Gutierrez CA, Weinheimer AR, Aylward FO (2020). "Dynamic genome evolution and complex virocell metabolism of globally-distributed giant viruses". Nature Communications. 11 (1710): 1710. Bibcode:2020NatCo..11.1710M. doi:10.1038/s41467-020-15507-2. PMC   7136201 . PMID   32249765.
  8. ↑ Schvarcz CR, Steward GF (2018). "A giant virus infecting green algae encodes key fermentation genes". Virology. 518: 423–433. doi: 10.1016/j.virol.2018.03.010 . PMID   29649682.
  9. ↑ Da Cunha V, Gaia M, Ogata H, Jaillon O, Delmont TO, Patrick Forterre P (2020). "Giant viruses encode novel types of actins possibly related to the origin of eukaryotic actin: the viractins". bioRxiv. doi:10.1101/2020.06.16.150565. S2CID   219947620.
  10. ↑ Ha AD, Moniruzzaman M, Aylward FO (2021). "High Transcriptional Activity and Diverse Functional Repertoires of Hundreds of Giant Viruses in a Coastal Marine System". mSystems. 6 (4): e0029321. doi:10.1128/mSystems.00293-21. PMC   8407384 . PMID   34254826.
  11. ↑ Kijima S, Delmont TO, Miyazaki U, Gaia M, Endo H, Ogata H (7 June 2021). "Discovery of Viral Myosin Genes With Complex Evolutionary History Within Plankton". Frontiers in Microbiology. 12: 683294. doi: 10.3389/fmicb.2021.683294 . PMC   8215601 . PMID   34163457.
  12. ↑ Aylward FO, Moniruzzaman M, Ha AD, Koonin EV (2021). "A phylogenomic framework for charting the diversity and evolution of giant viruses". PLOS Biology. 19 (10): e3001430. doi: 10.1371/journal.pbio.3001430 . PMC   8575486 . PMID   34705818.
  13. ↑ Meints, Russel H.; Van Etten, James L.; Kuczmarski, Daniel; Lee, Kit; Ang, Barbara (September 1981). "Viral infection of the symbiotic chlorella-like alga present in Hydra viridis". Virology. 113 (2): 698–703. doi:10.1016/0042-6822(81)90198-7. PMID   18635088.
  14. ↑ Hoshina, Ryo; Shimizu, Mayumi; Makino, Yoichi; Haruyama, Yoshihiro; Ueda, Shin-ichiro; Kato, Yutaka; Kasahara, Masahiro; Ono, Bun-ichiro; Imamura, Nobutaka (13 September 2010). "Isolation and characterization of a virus (CvV-BW1) that infects symbiotic algae of Paramecium bursaria in Lake Biwa, Japan". Virology Journal. 7: 222. doi: 10.1186/1743-422X-7-222 . ISSN   1743-422X. PMC   2949830 . PMID   20831832.
  15. ↑ Garza, D. Randy; Suttle, Curtis A. (1995-12-31). "Large double-stranded DNA viruses which cause the lysis of a marine heterotrophic nanoflagellate (Bodo sp) occur in natural marine viral communities" (PDF). Aquatic Microbial Ecology. 9 (3): 133–144. doi: 10.3354/ame009203 .
  16. ↑ Fischer, M. G.; Allen, M. J.; Wilson, W. H.; Suttle, C. A. (2010). "Giant virus with a remarkable complement of genes infects marine zooplankton" (PDF). Proceedings of the National Academy of Sciences. 107 (45): 19508–13. Bibcode:2010PNAS..10719508F. doi: 10.1073/pnas.1007615107 . PMC   2984142 . PMID   20974979.
  17. ↑ La Scola B, Audic S, Robert C, Jungang L, de Lamballerie X, Drancourt M, Birtles R, Claverie JM, Raoult D (2003). "A giant virus in amoebae". Science. 299 (5615): 2033. doi:10.1126/science.1081867. PMID   12663918. S2CID   39606235.
  18. ↑ "Giant Viruses". American Scientist. 2017-02-06. Retrieved 2021-09-02.
  19. 1 2 Raoult D, Audic S, Robert C, Abergel C, Renesto P, Ogata H, La Scola B, Suzan M, Claverie JM (November 2004). "The 1.2-megabase genome sequence of Mimivirus". Science. 306 (5700): 1344–50. Bibcode:2004Sci...306.1344R. doi:10.1126/science.1101485. PMID   15486256. S2CID   84298461.
  20. ↑ Claverie, Jean-Michel; Ogata, Hiroyuki; Audic, Stéphane; Abergel, Chantal; Suhre, Karsten; Fournier, Pierre-Edouard (April 2006). "Mimivirus and the emerging concept of "giant" virus" (PDF). Virus Research. 117 (1): 133–144. arXiv: q-bio/0506007 . doi:10.1016/j.virusres.2006.01.008. PMID   16469402. S2CID   8791457.
  21. ↑ Bichell RE. "In Giant Virus Genes, Hints About Their Mysterious Origin". All Things Considered.
  22. ↑ Schulz F, Yutin N, Ivanova NN, Ortega DR, Lee TK, Vierheilig J, Daims H, Horn M, Wagner M, Jensen GJ, Kyrpides NC, Koonin EV, Woyke T (April 2017). "Giant viruses with an expanded complement of translation system components" (PDF). Science. 356 (6333): 82–85. Bibcode:2017Sci...356...82S. doi: 10.1126/science.aal4657 . PMID   28386012. S2CID   206655792.
  23. ↑ Bäckström D, Yutin N, Jørgensen SL, Dharamshi J, Homa F, Zaremba-Niedwiedzka K, Spang A, Wolf YI, Koonin EV, Ettema TJ (March 2019). "Virus Genomes from Deep Sea Sediments Expand the Ocean Megavirome and Support Independent Origins of Viral Gigantism". mBio. 10 (2): e02497-02418. doi:10.1128/mBio.02497-18. PMC   6401483 . PMID   30837339.
  24. ↑ Yutin N, Wolf Y, Koonin EV (2014). "Origin of giant viruses from smaller DNA viruses not from a fourth domain of cellular life". Virology. 466–467 (2014): 38–52. doi:10.1016/j.virol.2014.06.032. PMC   4325995 . PMID   25042053.
  25. ↑ Pereira Andrade, Ana Cláudia dos Santos; Victor de Miranda Boratto, Paulo; Rodrigues, Rodrigo Araújo Lima; Bastos, Talita Machado; Azevedo, Bruna Luiza; Dornas, Fábio Pio; Oliveira, Danilo Bretas; Drumond, Betânia Paiva; Kroon, Erna Geessien; Abrahão, Jônatas Santos (2019-02-19). "New Isolates of Pandoraviruses: Contribution to the Study of Replication Cycle Steps". Journal of Virology. 93 (5): 10.1128/jvi.01942–18. doi:10.1128/jvi.01942-18. PMC   6384056 . PMID   30541841.
  26. ↑ Abrahão J, Silva L, Silva LS, Khalil JY, Rodrigues R, Arantes T, Assis F, Boratto P, Andrade M, Kroon EG, Ribeiro B, Bergier I, Seligmann H, Ghigo E, Colson P, Levasseur A, Kroemer G, Raoult D, La Scola B (February 2018). "Tailed giant Tupanvirus possesses the most complete translational apparatus of the known virosphere". Nature Communications. 9 (1): 749. Bibcode:2018NatCo...9..749A. doi:10.1038/s41467-018-03168-1. PMC   5829246 . PMID   29487281.
  27. ↑ head and tail, respectively
  28. ↑ soda lake and deep ocean species of Tupanvirues, respectively
  29. ↑ Deeg CM, Chow CT, Suttle CA (March 2018). "The kinetoplastid-infecting Bodo saltans virus (BsV), a window into the most abundant giant viruses in the sea". eLife. 7: e33014. doi: 10.7554/eLife.33014 . PMC   5871332 . PMID   29582753.
  30. ↑ Arslan D, Legendre M, Seltzer V, Abergel C, Claverie JM (October 2011). "Distant Mimivirus relative with a larger genome highlights the fundamental features of Megaviridae". Proceedings of the National Academy of Sciences of the United States of America. 108 (42): 17486–91. Bibcode:2011PNAS..10817486A. doi: 10.1073/pnas.1110889108 . PMC   3198346 . PMID   21987820.
  31. ↑ Colson P, Yutin N, Shabalina SA, Robert C, Fournous G, La Scola B, Raoult D, Koonin EV (2011). "Viruses with more than 1,000 genes: Mamavirus, a new Acanthamoeba polyphaga mimivirus strain, and reannotation of Mimivirus genes". Genome Biology and Evolution. 3: 737–42. doi:10.1093/gbe/evr048. PMC   3163472 . PMID   21705471.
  32. ↑ Legendre M, Santini S, Rico A, Abergel C, Claverie JM (March 2011). "Breaking the 1000-gene barrier for Mimivirus using ultra-deep genome and transcriptome sequencing". Virology Journal. 8 (1): 99. doi: 10.1186/1743-422X-8-99 . PMC   3058096 . PMID   21375749.
  33. ↑ Boyer, M.; Azza, S.; Barrassi, L.; Klose, T.; Campocasso, A.; Pagnier, I.; Fournous, G.; Borg, A.; et al. (2011). "Mimivirus shows dramatic genome reduction after intraamoebal culture". Proceedings of the National Academy of Sciences. 108 (25): 10296–301. Bibcode:2011PNAS..10810296B. doi: 10.1073/pnas.1101118108 . PMC   3121840 . PMID   21646533.
  34. ↑ Fischer, M. G.; Allen, M. J.; Wilson, W. H.; Suttle, C. A. (2010). "Giant virus with a remarkable complement of genes infects marine zooplankton" (PDF). Proceedings of the National Academy of Sciences. 107 (45): 19508–13. Bibcode:2010PNAS..10719508F. doi: 10.1073/pnas.1007615107 . PMC   2984142 . PMID   20974979.
  35. ↑ "Giant Virus Toplist". PIT Bioinformatics Group, Department of Computer Science. Eötvös University. 2015-03-26.
  36. ↑ "Giant Virus Toplist". PIT Bioinformatics Group. 26 March 2015. Retrieved 10 May 2023.
  37. ↑ Zauberman N, Mutsafi Y, Halevy DB, Shimoni E, Klein E, Xiao C, Sun S, Minsky A (May 2008). Sugden B (ed.). "Distinct DNA exit and packaging portals in the virus Acanthamoeba polyphaga mimivirus". PLOS Biology. 6 (5): e114. doi: 10.1371/journal.pbio.0060114 . PMC   2430901 . PMID   18479185.
  38. ↑ 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.
This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.