Tupanvirus

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Tupanvirus
Tupanvirus.jpeg
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(unranked): Virus
Realm: Varidnaviria
Kingdom: Bamfordvirae
Phylum: Nucleocytoviricota
Class: Megaviricetes
Order: Imitervirales
Family: Mimiviridae (?)
Genus:Tupanvirus
Species

Tupanvirus is a genus of viruses first described in 2018. [1] The genus is composed of two species of virus that are in the giant virus group. [2] [3] Researchers discovered the first isolate in 2012 from deep water sediment samples taken at 3,000 m depth off the coast of Brazil. [1] The second isolate was collected from a soda lake in Southern Nhecolândia, Brazil in 2014. [1] 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. [1] [4] [5]

Contents

Classification

The genus Tupanvirus was first described in 2018 with the discovery of the two isolates of tupanviruses found in soda lake and deep oceanic sediments samples collected in Brazil. [1] The genus is currently unassigned but hypothesized to be a member of the family Mimiviridae , along with the other amoeba-infecting viruses. Members of the family Mimiviridae includes Acanthamoeba polyphaga mimivirus (APMV) that is known for its large size of ~500 nm in diameter. [6] In contrast, the typical virus size range is approximately 20-200 nm. [7] Mimiviruses also possess fibril structures on the capsid as well as genes encoding proteins for nucleotide synthesis and various metabolisms that are not found in other viruses. [8]

Unlike the other mimiviruses in the Mimiviridae, Tupanvirus has a ~550 nm long cylindrical tail covered with fibrils that is attached to the base of the capsid. [6] This morphological feature makes Tupanvirus the largest described virus (approximately ~ 1.2 μm in length with the tail) with the longest tail ever observed a in virus. [1] [6] Tupanviruses are also capable of infecting a wider range of amoebae than other mimiviruses, and produce a cytotoxic effect in host and non-host organisms that is not observed in APMV. In addition, phylogenomic results revealed that the genus Tupanvirus is separate from the other viruses in the family Mimiviridae. [6]

Morphology

The morphology of Tupanvirus is similar to that of other amoeba-infecting mimiviruses. [6] This is because of similarities between the capsid of Tupanvirus and that of other amoebae-infecting mimiviruses. [1] The capsid of Tupanvirus measures approximately 450 nm. [6] One major difference is that the Tupanvirus virion presents a large cylindrical tail (~550 nm × 450 nm diameter) attached to the base of the capsid. [1] Both the capsid and cylindrical tail are covered in fibrils. [6] Tupanvirus can measure up to 1.2 μm in length, and some particles can reach up to 2.3 μm because of the “high degree of plasticity in the size of the tail”. [1] [6] Also to note is a lipid membrane within the capsid. Additionally, their capsid is described as having a ‘stargate structure’. [6] This star-shaped vertex is present in other mimivurises, and acts as a seal for the apex of the capsid. [9] It has also been stated that the tail of Tupanvirus is less electron dense than the capsid. [6]

Genome

Tupanvirus genome-translation-related factors. a Circular representation of Tupanvirus soda lake genome highlighting its translation-related factors (aaRS, tRNAs and PSF). The box (upright) summarizes this information and considers the Tupanvirus deep ocean data set. b Network of shared categories of translation-related genes (not considering ribosomal proteins) present in tupanviruses, Mimivirus (APMV), Klosneuvirus, Catovirus, Hokovirus, Indivirus and cellular world organism--Encephalitozoon cuniculi (Eukaryota), Nanoarchaeum equitans (Archaea) and Candidatus Carsonella ruddii (Bacteria). The diameter of the organism's circles (numbers) is proportional to the number of translation-related genes present in those genomes. CDS coding sequences, tRNA transfer RNA, aaRS aminoacyl tRNA synthetase, PSF protein synthesis factors. Tupanvirus-Translational-Factors.png
Tupanvirus genome-translation-related factors. a Circular representation of Tupanvirus soda lake genome highlighting its translation-related factors (aaRS, tRNAs and PSF). The box (upright) summarizes this information and considers the Tupanvirus deep ocean data set. b Network of shared categories of translation-related genes (not considering ribosomal proteins) present in tupanviruses, Mimivirus (APMV), Klosneuvirus, Catovirus, Hokovirus, Indivirus and cellular world organism—Encephalitozoon cuniculi (Eukaryota), Nanoarchaeum equitans (Archaea) and Candidatus Carsonella ruddii (Bacteria). The diameter of the organism’s circles (numbers) is proportional to the number of translation-related genes present in those genomes. CDS coding sequences, tRNA transfer RNA, aaRS aminoacyl tRNA synthetase, PSF protein synthesis factors.

The genome contains roughly 1.5 million base pairs of double-stranded DNA, coding for 1276–1425 predicted proteins, making it the fourth largest among viral genomes. [4] While 30% of the genes are new and not found in other viruses, genomic analysis shows most of the known genes can be related to amoeba-infecting mimiviruses, with the rest corresponding to eukaryotes and bacteria. The shared genes of tupanvirus with different lineages of amoeba-infecting mimiviruses indicate it as a separate genus within family Mimiviridae. [1] For example, its A/T rich genome resembles that of other amoebal mimiviruses and suggests a preference for codons formed by A/T-rich sequences. As well, the frequent occurrence of the “AAAATTGA” promoter motif is also similar to that of other mimiviruses. [1] [10]

As a giant virus, tupanvirus presents the largest translational apparatus within the known virosphere, carrying 20 aminoacyl tRNA synthetase (aaRS) and 70 transfer RNAs (tRNA), while the rest are involved in RNA maturation and splicing, as well as ribosomal protein modification. [1] Moreover, tupanviruses contain a number of DNA-independent RNA synthesizing polymerases and enzymes as well as transcription factors that are involved in viral transcription. [10] Furthermore, many genes that encode for processes found in cellular organisms are also found in the Tupanvirus genome, which contains a richer gene set than some bacteria and archaea, and even some eukaryotes. [1] As a result, the analysis of tupanviruses constitutes a new step towards understanding the evolution of giant viruses, because such diverse and complete gene sets not only surpass that of other viral genomes, but also rival that of bacteria and even eukaryotes. In fact, tupanvirus is the only known virus to host all 20 aaRS, exceeding other giant viruses like Klosneuvirus; yet, there is no agreement on whether these genes are host-derived or passed down from an ancestral mimivirus. [6] One such extraordinary example are two copies of an 18 S rRNA intronic region that are highly expressed during viral replication. Although these intronic regions also exist in other mimiviruses, the tupanvirus 18S rRNA is phylogenetically different with their function still unknown. [1]

Host

Tupanvirus-induced clustering (as seen in A. castellani). Amoebal-Clustering-Tupanvirus.jpeg
Tupanvirus-induced clustering (as seen in A. castellani).

Tupanviruses have the ability to infect a wider range of hosts than other giant viruses, including many amoeba e of the genus Acanthameoba (as well as members of the species Vermamoeba vermiformis, Dictyostelium discoideum and Willartia magna), [6] and may also infect other protists. There are no documented threats to humans. [4] The tupanvirus’ generalist approach may be attributed to the low species richness and abundance of the virus’ habitat. [12]

Tupanvirus-infected amoebas also present a new virus-host interaction not previously observed among other amoebae. Infected cells were found to aggregate with non-infected cells, a mechanism suggested to be mediated by mannose binding protein gene expression (MBP). The clusters of affected cells were shown to increase viral dissemination within the host, thus increasing virulence of the virus. [11] The generalist approach, in conjunction with aggregation behaviour, decreases the dilution effect and increases host-encounter rates.

Life cycle and host interaction

Attachment

Viral particles attach directly to the host cell surface. The attachment process occurs very rapidly. Virions can be visibly attached at 0 hours past infection. The specific mechanism is still unknown. [11]

Entry

Virions enter via phagocytosis. Generally only one particle will be present in each phagosome, although several particles may enter the intracellular matrix in different phagosomes at the same time. [13] This Tupanvirus uses membrane fusion in order to release its genome. The viral capsid contains a lipid membrane that facilitates fusion with the phagosome membrane to release the viral genome. The virus also releases the contents kept in the tail after an invagination of the phagosome between the two tail components results in fusion. [1]

Replication

The viral genome is released from the phagosome into the amoeba’s cytoplasm. [1] This virus facilitates aggregation of amoeba hosts in order to replicate rapidly and have a supply of hosts for progeny particles. Bunch formation happens rapidly after infection and will continue as long as host cells are living. Bunches can re-form after mechanical separation as long as host cells are living. [11] Replication factories are formed as early as 8 h.p.i. up to 12 h.p.i. [11] [13]

Assembly

Initially, when replication factories are still immature, new virions are assembled as soon as possible. Therefore, many particles at various stages of assembly may be present inside a single factory. Once the factory has matured capsid assembly is finished and the genome is incorporated. The tails are attached to the capsid following genome incorporation. [13] Assembly of particles happens on a loose timeline, resulting in particles at varying stages of assembly at the time of release.

Release

Viral particles are released, facilitated by cell lysis. When infecting the amoeba in the species Vermamoeba vermiformis many assembled particles are not functional at the time of release. As many as half of released particles are not infectious; this phenomenon is also present when infecting host amoeba Acanthamoeba castellanii. Although more research is required it is hypothesized that the production of non-infectious particles may be a normal part of the replication cycle. [13]

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.

Metaviridae is a family of viruses which exist as Ty3-gypsy LTR retrotransposons in a eukaryotic host's genome. They are closely related to retroviruses: members of the family Metaviridae share many genomic elements with retroviruses, including length, organization, and genes themselves. This includes genes that encode reverse transcriptase, integrase, and capsid proteins. The reverse transcriptase and integrase proteins are needed for the retrotransposon activity of the virus. In some cases, virus-like particles can be formed from capsid proteins.

Pseudoviridae is a family of viruses, which includes three genera.

<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>Vesivirus</i> Genus of viruses

Vesivirus is a genus of viruses, in the family Caliciviridae. Swine, sea mammals, and felines serve as natural hosts. There are two species in this genus. Diseases associated with this genus include: respiratory disease, Feline calicivirus (FCV); conjunctivitis, and respiratory disease.

<i>Lagovirus</i> Genus of viruses

Lagovirus is a genus of viruses, in the family Caliciviridae. Lagomorphs serve as natural hosts. There are two species in this genus. Diseases associated with this genus include: necrotizing hepatitis leading to fatal hemorrhages.

<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.

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.

<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.

Mason-Pfizer monkey virus (M-PMV), formerly Simian retrovirus (SRV), is a species of retroviruses that usually infect and cause a fatal immune deficiency in Asian macaques. The ssRNA virus appears sporadically in mammary carcinoma of captive macaques at breeding facilities which expected as the natural host, but the prevalence of this virus in feral macaques remains unknown. M-PMV was transmitted naturally by virus-containing body fluids, via biting, scratching, grooming, and fighting. Cross contaminated instruments or equipment (fomite) can also spread this virus among animals.

<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.

Spiraviridae is a family of incertae sedis 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 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 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.

<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.

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. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 Abrahão J, Silva L, Silva LS, Khalil JY, Rodrigues R, Arantes T, et al. (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.
  2. ↑ "Tupanvirus altamarinense". ictv.global (taxon details). International Committee on Taxonomy of Viruses (ICTV). Retrieved 2024-07-27.
  3. ↑ "Tupanvirus salinum". ictv.global (taxon details). International Committee on Taxonomy of Viruses (ICTV). Retrieved 2024-07-27.
  4. 1 2 3 Garisto, Dan (27 February 2018). "These giant viruses have more protein-making gear than any known virus". sciencenews.org. Science News. Retrieved 2021-04-07.
  5. ↑ Schulz, Frederik; Yutin, Natalya; Ivanova, Natalia N.; Ortega, Davi R.; Lee, Tae Kwon; Vierheilig, Julia; Daims, Holger; Horn, Matthias; Wagner, Michael; Jensen, Grant J.; Kyrpides, Nikos C.; Koonin, Eugene V.; Woyke, Tanja (2017-04-07). "Giant viruses with an expanded complement of translation system components". Science. 356 (6333). eScholarship, University of California: 82–85. Bibcode:2017Sci...356...82S. doi: 10.1126/science.aal4657 . OCLC   9579903013. PMID   28386012.
  6. 1 2 3 4 5 6 7 8 9 10 11 12 Rodrigues RA, Mougari S, Colson P, La Scola B, Abrahão JS (January 2019). ""Tupanvirus", a new genus in the family Mimiviridae". Archives of Virology. 164 (1): 325–331. doi: 10.1007/s00705-018-4067-4 . PMID   30291500.
  7. ↑ Fuhrman JA (June 1999). "Marine viruses and their biogeochemical and ecological effects". Nature. 399 (6736): 541–8. Bibcode:1999Natur.399..541F. doi:10.1038/21119. PMID   10376593.
  8. ↑ Colson P, La Scola B, Levasseur A, Caetano-Anollés G, Raoult D (April 2017). "Mimivirus: leading the way in the discovery of giant viruses of amoebae". Nature Reviews. Microbiology. 15 (4): 243–254. doi:10.1038/nrmicro.2016.197. PMC   7096837 . PMID   28239153.
  9. ↑ Pires de Souza GA, Rolland C, Nafeh B, La Scola B, Colson P (April 2021). "Giant virus-related sequences in the 5300-year-old Ötzi mummy metagenome". Virus Genes. 57 (2): 222–227. doi:10.1007/s11262-021-01823-2. ISSN   0920-8569. PMID   33566217.
  10. 1 2 Rodrigues RA, Arantes TS, Oliveira GP, Dos Santos Silva LK, Abrahão JS (January 2019). "Chapter four: The Complex Nature of Tupanviruses". In Kielian M, Mettenleiter TC, Roossinck MJ (eds.). Advances in Virus Research. Vol. 103. Academic Press. pp. 135–166. doi:10.1016/bs.aivir.2018.09.001. ISBN   9780128177228. PMID   30635075.
  11. 1 2 3 4 5 Oliveira G, Silva L, Leão T, Mougari S, da Fonseca FG, Kroon EG, et al. (January 2019). "Tupanvirus-infected amoebas are induced to aggregate with uninfected cells promoting viral dissemination". Scientific Reports. 9 (1): 183. Bibcode:2019NatSR...9..183O. doi: 10.1038/s41598-018-36552-4 . PMC   6336878 . PMID   30655573.
  12. ↑ Sergeev VN, Gerasimenko LM, Zavarzin GA (2002-11-01). "[Proterozoic history and present state of cyanobacteria]". Mikrobiologiia. 71 (6): 725–40. doi:10.1023/A:1021415503436. PMID   12526193.
  13. 1 2 3 4 Silva LC, Rodrigues RA, Oliveira GP, Dornas FP, La Scola B, Kroon EG, Abrahão JS (2019). "Microscopic Analysis of the Tupanvirus Cycle in Vermamoeba vermiformis". Frontiers in Microbiology. 10: 671. doi: 10.3389/fmicb.2019.00671 . PMC   6456662 . PMID   31001237.
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