Virosphere

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Virosphere (virus diversity, virus world, global virosphere) was coined to refer to all those places in which viruses are found or which are affected by viruses. [1] [2] However, more recently virosphere has also been used to refer to the pool of viruses that occurs in all hosts and all environments, [3] as well as viruses associated with specific types of hosts (prokaryotic virosphere, [4] archaeal virosphere, [5] Invertebrate  virosphere), [6] type of genome  (RNA virosphere, [7] dsDNA virosphere) [8] or ecological niche (marine virosphere). [9]

Contents

Viral genome diversity

The scope of viral genome diversity is enormous compared to cellular life. Cellular life including all known organisms have double stranded DNA genome. Whereas viruses have one of at least 7 different types of genetic information, namely dsDNA, ssDNA, dsRNA, ssRNA+, ssRNA-, ssRNA-RT, dsDNA-RT. Each type of genetic information has its specific manner of mRNA synthesis. Baltimore classification is a system providing overview on these mechanisms for each type of genome. Moreover, in contrast to cellular organisms, viruses don't have universally conserved sequences in their genomes to be compared by.[ citation needed ]

Viral genome size varies approximately 1000 fold. Smallest viruses may consist of only from 1–2 kb genome coding for 1 or 2 genes and it is enough for them to successfully evolve and travel through space and time by infecting and replicating (make copies of their own) in its host. Two most basic viral genes are replicase gene and capsid protein gene, as soon as virus has them it represents a biological entity able to evolve and reproduce in cellular life forms. Some viruses may have only replicase gene and use capsid gene of other e.g. endogenous virus. Most viral genomes are 10-100kb, whereas bacteriophages tend to have larger genomes carrying parts of genome translation machinery genes from their host. In contrast, RNA viruses have smaller genomes, with maximum 35kb by coronavirus. RNA genomes have higher mutation rate, that is why their genome has to be small enough in order not to harbour to many mutations, which would disrupt the essential genes or their parts. [10] The function of the vast majority of viral genes remain unknown und the approaches to study have to be developed. [11] The total number of viral genes is much higher, than the total number of genes of three domains of life all together, which practically means viruses encode most of the genetic diversity on the planet. [12]

Viral host diversity

Viruses are cosmopolites, they are able to infect every cell and every organism on planet earth. However different viruses infect different hosts. Viruses are host specific as they need to replicate (reproduce) within a host cell. In order to enter the cell viral particle needs to interact with a receptor on the surface of its host cell. For the process of replication many viruses use their own replicases, but for protein synthesis they are dependent on their host cell protein synthesis machinery. Thus, host specificity is a limiting factor for viral reproduction.[ citation needed ]

Some viruses have extremely narrow host range and are able to infect only 1 certain strain of 1 bacterial species, whereas others are able to infect hundreds or even thousands of different hosts. For example cucumber mosaic virus (CMV) can use more than 1000 different plant species as a host. [13] Members of viral families like Rhabdoviridae infect hosts from different kingdoms e.g. plants and vertebrates. [14] And members of genera Psimunavirus and Myohalovirus infect hosts from different domains of life e.g. bacteria and archaea. [15]

Viral capsid diversity

Capsid is the outer protecting shell or scaffold of a viral genome. Capsid enclosing viral nucleic acid make up viral particle or a virion. Capsid is made of protein and sometimes has lipid layer harboured from the host cell while exiting it. Capsid proteins are highly symmetrical and assemble within a host cell by their own due to the fact, that assembled capsid is more thermodynamically favourable state, than separate randomly floating proteins. The most viral capsids have icosahedral or helical symmetry, whereas bacteriophages have complex structure consisting of icosahedral head and helical tail including baseplate and fibers important for host cell recognition and penetration. [16] Viruses of archaea infecting hosts living in extreme environments like boiling water, highly saline or acidic environments have totally different capsid shapes and structures. The variety of capsid structures of Archaeal viruses includes lemon shaped viruses Bicaudaviridae of family and Salterprovirus genus, spindle form Fuselloviridae, bottle shaped Ampullaviridae, egg shaped Guttaviridae. [5]

Capsid size of a virus differs dramatically depending on its genome size and capsid type.Icosahedral capsids are measured by diameter, whereas helical and complex are measured by length and diameter. Viruses differ in capsid size in a spectrum from 10 to more than 1000 nm. The smallest viruses are ssRNA viruses like Parvovirus. They have icosahedral capsid approximately 14 nm in diameter. Whereas the biggest currently known viruses are Pithovirus, Mamavirus and Pandoravirus. Pithovirus is a flask-shaped virus 1500 nm long and 500 nm in diameter, Pandoravirus is an oval-shaped virus1000nm (1 micron) long and Mamavirus is an icosahedral virus reaching approximately 500 nm in diameter. [17] Example of how capsid size depends on the size of viral genome can be shown by comparing icosahedral viruses - the smallest viruses are 15-30 nm in diameter have genomes in range of 5 to 15 kb (kilo bases or kilo base pairs depending on type of genome), and the biggest are near 500 nm in diameter and their genomes are also the largest, they exceed1Mb (million base pairs).[ citation needed ]

Viral evolution

Viral evolution or evolution of viruses presumably started from the beginning of the second age of RNA world, when different types of viral genomes arose through the transition from RNA- RT –DNA, which also emphasises that viruses played a critical role in the emergence of DNA and predate LUCA [18] [19] The abundance and variety of viral genes also imply that their origin predates LUCA. [20] As viruses do not share unifying common genes they are considered to be polyphyletic or having multiple origins as opposed to one common origin as all cellular life forms have. [21] [22] Virus evolution is more complex as it is highly prone to horizontal gene transfer, genetic recombination and reassortment. Moreover viral evolution should always be considered as a process of co-evolution with its host, as a host cell is inevitable for virus reproduction and hence, evolution.[ citation needed ]

Viral abundance

Viruses are the most abundant biological entities, there are 10^31 viruses on our planet. [23] [24] Viruses are capable of infecting all organisms on earth and they are able to survive in much harsher environments, than any cellular life form. As viruses can not be included in the tree of life there is no separate structure illustrating viral diversity and evolutionary relationships. [25] However, viral ubiquity can be imagined as a virosphere covering the whole tree of life.[ citation needed ]

Nowadays we are entering the phase of exponential viral discovery. The genome sequencing technologies including high-throughput methods allow fast and cheap sequencing of environmental samples. The vast majority of the sequences from any environment, both from wild nature and human made, reservoirs are new. [26] [27] It practically means that during over a 100 years of virus research from the discovery of bacteriophages - viruses of bacteria in 1917 until current time we only scratched on a surface of a great viral diversity. The classic methods like viral culture used previously allowed to observe physical virions or viral particles using electron microscope, they also allowed to gathering information about their physical and molecular properties. New methods deal only with the genetic information of viruses.[ citation needed ]

See also

Related Research Articles

<span class="mw-page-title-main">Capsid</span> Protein shell of a virus

A capsid is the protein shell of a virus, enclosing its genetic material. It consists of several oligomeric (repeating) structural subunits made of protein called protomers. The observable 3-dimensional morphological subunits, which may or may not correspond to individual proteins, are called capsomeres. The proteins making up the capsid are called capsid proteins or viral coat proteins (VCP). The capsid and inner genome is called the nucleocapsid.

<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">Movement protein</span>

In order for a virus to infect a plant, it must be able to move between cells so it can spread throughout the plant. Plant cell walls make this moving/spreading quite difficult and therefore, for this to occur, movement proteins must be present. A movement protein (MP) is a specific virus-encoded protein that is considered to be a general feature of plant genomes. They allow for local and systemic viral spread throughout a plant. MPs were first studied in the Tobacco Mosaic Virus (TMV) where it was found that viruses were unable to spread without the presence of a specific protein. In general, the plant viruses first, move within the cell from replication sites to the plasmodesmata (PD). Then, the virus is able to go through the PD and spread to other cells. This process is controlled through MPs. Different MPs use different mechanisms and pathways to regulate this spread of some viruses. Nearly all plants express at least one MP, while some can encode many different MPs which help with cell to cell viral transmission. They serve to increase the size exclusion limits (SEL) of plasmodesmata to allow for greater spread of the virus.

Baltimore classification is a system used to classify viruses based on their manner of messenger RNA (mRNA) synthesis. By organizing viruses based on their manner of mRNA production, it is possible to study viruses that behave similarly as a distinct group. Seven Baltimore groups are described that take into consideration whether the viral genome is made of deoxyribonucleic acid (DNA) or ribonucleic acid (RNA), whether the genome is single- or double-stranded, and whether the sense of a single-stranded RNA genome is positive or negative.

<i>Lipothrixviridae</i> Family of viruses

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

<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">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.

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

<i>Bidensovirus</i> Genus of viruses

Bidensovirus is a genus of single stranded DNA viruses that infect invertebrates. The species in this genus were originally classified in the family Parvoviridae but were moved to a new genus because of significant differences in the genomes.

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

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">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.

<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 3000m 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.

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

<i>Monodnaviria</i> Realm of viruses

Monodnaviria is a realm of viruses that includes all single-stranded DNA viruses that encode an endonuclease of the HUH superfamily that initiates rolling circle replication of the circular viral genome. Viruses descended from such viruses are also included in the realm, including certain linear single-stranded DNA (ssDNA) viruses and circular double-stranded DNA (dsDNA) viruses. These atypical members typically replicate through means other than rolling circle replication.

<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.

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

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

<i>Portogloboviridae</i> Family of viruses

Portogloboviridae is a family of dsDNA viruses that infect archaea. It is a proposed family of the realm Varidnaviria, but ICTV officially puts it as incertae sedis virus. Viruses in the family are related to Helvetiavirae. The capsid proteins of these viruses and their characteristics are of evolutionary importance for the origin of the other Varidnaviria viruses since they seem to retain primordial characters.

<i>Adnaviria</i> Realm of viruses

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

References

  1. "World Wide Words: Virosphere". World Wide Words. Retrieved 2023-04-13.
  2. Suttle, Curtis (2005). "The viriosphere: the greatest biological diversity on Earth and driver of global processes". Environmental Microbiology. 7 (4): 481–482. Bibcode:2005EnvMi...7..481S. doi: 10.1111/j.1462-2920.2005.803_11.x . ISSN   1462-2912. PMID   15816923. S2CID   40555592.
  3. Abroi, Aare; Gough, Julian (2011). "Are viruses a source of new protein folds for organisms? – Virosphere structure space and evolution". BioEssays. 33 (8): 626–635. doi:10.1002/bies.201000126. ISSN   1521-1878. PMID   21633962. S2CID   6680980.
  4. Krupovic, Mart; Prangishvili, David; Hendrix, Roger W.; Bamford, Dennis H. (2011). "Genomics of Bacterial and Archaeal Viruses: Dynamics within the Prokaryotic Virosphere". Microbiology and Molecular Biology Reviews. 75 (4): 610–635. doi:10.1128/mmbr.00011-11. PMC   3232739 . PMID   22126996.
  5. 1 2 Prangishvili, David; Bamford, Dennis H.; Forterre, Patrick; Iranzo, Jaime; Koonin, Eugene V.; Krupovic, Mart (December 2017). "The enigmatic archaeal virosphere". Nature Reviews Microbiology. 15 (12): 724–739. doi:10.1038/nrmicro.2017.125. ISSN   1740-1534. PMID   29123227. S2CID   21789564.
  6. Shi, Mang; Lin, Xian-Dan; Tian, Jun-Hua; Chen, Liang-Jun; Chen, Xiao; Li, Ci-Xiu; Qin, Xin-Cheng; Li, Jun; Cao, Jian-Ping; Eden, John-Sebastian; Buchmann, Jan (December 2016). "Redefining the invertebrate RNA virosphere". Nature. 540 (7634): 539–543. Bibcode:2016Natur.540..539S. doi:10.1038/nature20167. ISSN   1476-4687. PMID   27880757. S2CID   1198891.
  7. Urayama, Syun-ichi; Takaki, Yoshihiro; Nishi, Shinro; Yoshida-Takashima, Yukari; Deguchi, Shigeru; Takai, Ken; Nunoura, Takuro (2018). "Unveiling the RNA virosphere associated with marine microorganisms". Molecular Ecology Resources. 18 (6): 1444–1455. doi: 10.1111/1755-0998.12936 . ISSN   1755-0998. PMID   30256532. S2CID   52821905.
  8. Iranzo, Jaime; Krupovic, Mart; Koonin, Eugene V. (2016). "The Double-Stranded DNA Virosphere as a Modular Hierarchical Network of Gene Sharing". mBio. 7 (4). doi:10.1128/mbio.00978-16. PMC   4981718 . PMID   27486193.
  9. Mizuno, Carolina Megumi; Rodriguez-Valera, Francisco; Kimes, Nikole E.; Ghai, Rohit (2013-12-12). "Expanding the Marine Virosphere Using Metagenomics". PLOS Genetics. 9 (12): e1003987. doi: 10.1371/journal.pgen.1003987 . ISSN   1553-7404. PMC   3861242 . PMID   24348267.
  10. Holmes, Edward C. (2010-01-26). "The comparative genomics of viral emergence". Proceedings of the National Academy of Sciences. 107 (suppl 1): 1742–1746. doi: 10.1073/pnas.0906193106 . PMC   2868293 . PMID   19858482.
  11. Hurwitz, Bonnie L.; U'Ren, Jana M.; Youens-Clark, Ken (May 2016). Millard, Andrew (ed.). "Computational prospecting the great viral unknown". FEMS Microbiology Letters. 363 (10): fnw077. doi: 10.1093/femsle/fnw077 . ISSN   1574-6968. PMID   27030726.
  12. Rohwer, Forest; Barott, Katie (2013-03-01). "Viral information". Biology & Philosophy. 28 (2): 283–297. doi:10.1007/s10539-012-9344-0. ISSN   1572-8404. PMC   3585991 . PMID   23482918.
  13. Palukaitis, Peter; Roossinck, Marilyn J.; Dietzgen, Ralf G.; Francki, Richard I.B. (1992-01-01). "Cucumber MOSAIC Virus". Advances in Virus Research. 41: 281–348. doi:10.1016/S0065-3527(08)60039-1. ISBN   9780120398416. ISSN   0065-3527. PMID   1575085.
  14. Hogenhout, Saskia A.; Redinbaugh, Margaret G.; Ammar, El-Desouky (June 2003). "Plant and animal rhabdovirus host range: a bug's view". Trends in Microbiology. 11 (6): 264–271. doi:10.1016/s0966-842x(03)00120-3. ISSN   0966-842X. PMID   12823943.
  15. Dyall-Smith, Mike; Palm, Peter; Wanner, Gerhard; Witte, Angela; Oesterhelt, Dieter; Pfeiffer, Friedhelm (March 2019). "Halobacterium salinarum virus ChaoS9, a Novel Halovirus Related to PhiH1 and PhiCh1". Genes. 10 (3): 194. doi: 10.3390/genes10030194 . PMC   6471424 . PMID   30832293.
  16. Kizziah, James L.; Manning, Keith A.; Dearborn, Altaira D.; Dokland, Terje (2020-02-18). "Structure of the host cell recognition and penetration machinery of a Staphylococcus aureus bacteriophage". PLOS Pathogens. 16 (2): e1008314. doi: 10.1371/journal.ppat.1008314 . ISSN   1553-7374. PMC   7048315 . PMID   32069326.
  17. Abergel, Chantal; Legendre, Matthieu; Claverie, Jean-Michel (2015-11-01). "The rapidly expanding universe of giant viruses: Mimivirus, Pandoravirus, Pithovirus and Mollivirus". FEMS Microbiology Reviews. 39 (6): 779–796. doi: 10.1093/femsre/fuv037 . ISSN   0168-6445. PMID   26391910.
  18. Holmes, Edward C. (2011). "What Does Virus Evolution Tell Us about Virus Origins?". Journal of Virology. 85 (11): 5247–5251. doi:10.1128/jvi.02203-10. PMC   3094976 . PMID   21450811.
  19. Krupovic, Mart; Dolja, Valerian V.; Koonin, Eugene V. (November 2020). "The LUCA and its complex virome". Nature Reviews Microbiology. 18 (11): 661–670. doi:10.1038/s41579-020-0408-x. ISSN   1740-1534. PMID   32665595. S2CID   220516514.
  20. Edwards, Robert A.; Rohwer, Forest (June 2005). "Viral metagenomics". Nature Reviews Microbiology. 3 (6): 504–510. doi:10.1038/nrmicro1163. ISSN   1740-1534. PMID   15886693. S2CID   8059643.
  21. Iranzo, Jaime; Krupovic, Mart; Koonin, Eugene V. (2017-03-04). "A network perspective on the virus world". Communicative & Integrative Biology. 10 (2): e1296614. doi:10.1080/19420889.2017.1296614. ISSN   1942-0889. PMC   5398231 . PMID   28451057.
  22. Krupovic, Mart; Dolja, Valerian V.; Koonin, Eugene V. (July 2019). "Origin of viruses: primordial replicators recruiting capsids from hosts". Nature Reviews Microbiology. 17 (7): 449–458. doi:10.1038/s41579-019-0205-6. ISSN   1740-1534. PMID   31142823. S2CID   169035711.
  23. Suttle, Curtis A. (October 2007). "Marine viruses — major players in the global ecosystem". Nature Reviews Microbiology. 5 (10): 801–812. doi:10.1038/nrmicro1750. ISSN   1740-1534. PMID   17853907. S2CID   4658457.
  24. Breitbart, Mya; Rohwer, Forest (June 2005). "Here a virus, there a virus, everywhere the same virus?". Trends in Microbiology. 13 (6): 278–284. doi:10.1016/j.tim.2005.04.003. ISSN   0966-842X. PMID   15936660.
  25. "V-table – the interactive structured virosphere" (PDF). dpublication.com. 6 December 2019. Retrieved 18 September 2021.
  26. Gulino, K.; Rahman, J.; Badri, M.; Morton, J.; Bonneau, R.; Ghedin, E. (2020-06-30). Gilbert, Jack A. (ed.). "Initial Mapping of the New York City Wastewater Virome". mSystems. 5 (3). doi:10.1128/mSystems.00876-19. ISSN   2379-5077. PMC   7300365 . PMID   32546676.
  27. Labonté, Jessica M.; Suttle, Curtis A. (November 2013). "Previously unknown and highly divergent ssDNA viruses populate the oceans". The ISME Journal. 7 (11): 2169–2177. Bibcode:2013ISMEJ...7.2169L. doi:10.1038/ismej.2013.110. ISSN   1751-7370. PMC   3806263 . PMID   23842650.