Life Cycle

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Coccolithovirus

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In 2009, MacKinder et al. elucidated the entry mechanism of the genera Coccolithovirus. Using confocal and electron microscopy, the researchers demonstrated that the virus strain EhV-86 uses a unique infection mechanism, which differs from other algal viruses, showing a greater similarity to the entry and exit strategies seen in animal-like nucleocytoplasmic large dsDNA viruses (NCLDVs).[1]

In this study the researchers found that EhV-86 entered cells by either endocytosis, (the process by which food or liquid particles are taken into the cell by a vesicle), or direct fusion (the viral envelope fuses with the host membrane). Regardless of the mechanism of entry, the capsid enters the cytoplasm intact. This is unique, as most enveloped viruses after fusion of the viral membrane with a host-cell membrane inject their DNA into the cytoplasm. After entering the cell, the viral capsid disassembles and the DNA is released into the host cytoplasm or directly into the nucleus. Copies of the viral DNA are made by viral DNA polymerase. The viral DNA is then transcribed into RNA which is then converted into viral proteins by the host’s ribosomes via translation. In the cytoplasm, virions are assembled and transported to the plasma membrane and released from the host via a budding mechanism. In this budding mechanism, EhV-86 gains an outer membrane from the host membrane.[1]

A cluster of sphingolipid producing genes have been identified in EhV-86. Researchers have found that the production of viral sphingolipids produced during the lytic stage are involved in programmed cell death in coccolithophore populations. A high correlation was found between glycosphingolipid (GSL) production and caspase activity during the lytic stage in infected cells. Caspases are a family of protease enzymes involved in programmed cell death.[2] The researchers also found that a critical concentration of GSLs (>0.06 mg/ml) is required to initiate cell lysis. Thus, the authors suggest that the production of GSLs to a critical concentration may be part of a timing mechanism for the lytic cycle. The authors also suggest that these biomolecules may be able to induce programmed cell death in other unaffected cells, thus serving as an algal bloom termination signal.[3]

Phaeovirus

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Phaeoviruses infect the Ectocarpales brown algae, which is an order of filamentous brown algae. One of the most studied phaeoviruses is Ectocarpus siliculosus virus, most commonly known as EsV-1[4]. The EsV-1 virus only infects the single-celled gametes or spores of E. siliculosus. Vegetative cells are immune to infection, as they are protected by a rigid cell wall[5]. Following infection, one copy of the viral DNA is incorporated into the host genome. The EsV-1 viral genome is then replicated and virions are assembled in the sporangia or gametangia of infected plants[6]. Viruses are subsequently released via lysis of reproductive cells, stimulated by changes in environmental conditions, such as increase in temperature[7]. In healthy plants, environmental stimuli synchronizes the release of gametes and zoospores into the surrounding water[7]. Free virus particles can then re-infect free-swimming gametes or spores of healthy plants. Infected gametes or spores undergo mitosis, forming infected plants and all cells of the progeny plant contain viral DNA. However, viral particles are only produced in the reproductive cells of the algae, while viruses remain latent in vegetative cells. In infected sporophytes, cells undergo meiosis and produce haploid spores. The EsV genome is transmitted in a Mendelian manner, where half of the progeny contain viral DNA. Often, algae from infected spores are indistinguishable from algae derived from healthy spores, but are partially or fully incapable of reproduction[5][6].

Coccolithoviruses and phaeoviruses have opposing life strategies. The coccolithovirus possesses an Acute life strategy characterized by high reproduction and mutation rates and greater dependency on dense host populations for transmission. Phaeoviruses possess a Persistent life strategy where infection may or may not cause disease, and the genome is passed from parent to offspring[4].

Prasinovirus

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Prasinoviruses infect small unicellular green algae in the order Mamiellales, commonly found in coastal marine waters.[8] Common hosts of prasinoviruses include members from the genus Ostreococcus. Three potential species of Ostreococcus have been identified and differ based on their light requirements.[9] One of the most widely studied prasinoviruses, strain OtV5 whose genome is fully sequenced infects Ostreococcus tauri, the smallest free-living eukaryotes currently known.[10]

Prasinoviruses employ a nucleo-cytoplasmic replication strategy where virions adhere to the host-cell surface, followed by injection of DNA into the host cytoplasm. Researchers found that ‘empty’ OtV5 viruses, or viruses with only the capsid attached to the host membrane, were rarely seen at any stage of the infection, suggesting that virions detach from the host membrane after injection of their DNA. The authors also found that a high proportion of viruses did not attach to cells after inoculation and suggest that viral attachment may be a limiting step in the infection. The viral DNA is then replicated inside the nucleus by the host cell’s machinery. Virus particles are assembled in the cytoplasm, usually occupying a space near the inner face of the nucleus. Due to the extremely small size of the algae cells, the average burst size was found to be 25 virus particles per cell.[10]

Viral production without cell lysis has recently been observed in O. tauri cells. Thomas et al. (2011) found that in resistant host cells, the viral genome was replicated and viruses were released via a budding mechanism.[11] This low rate of viral release through budding allows for the host and virus to be preserved and thus a stable co-existence is achieved.[12]

Prymnesiovirus

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The genus Prymnesiovirus currently contains only one species, known as Chrysochromulina brevifilum virus PW1 (CbV-PW1).[13] CbV-PW1 infects two species of marine phytoplankton, Chrysochromulina brevifilum and C. strobilus, belonging to the genus Chrysochromulina.[14] According to the AlgaeBase database, there are currently 63 marine and freshwater species names in the genus, of which 48 are recognized as taxonomically acceptable names.[15] Chrysochromulina is a particularly important genus as it can comprise more than 50% of the photosynthetic nanoplanktonic cells in the ocean.[16]

Little is known about the life cycle of the virus infecting these flagellate-containing planktonic species, Chrysochromulina brevifilum and C. strobilus. Suttle and Chan (1995) were the first to isolate viruses which infect Prymnesiophytes or haptophytes. In this study, ultrathin sections of viruses within Chyrsochromulina brevifilum were prepared and viewed using transmission electron microscopy.[16] Electron micrographs in the early stage of infection suggest that virus replication occurs in the cytoplasm within a viroplasm. A viroplasm is a localized area in the cytoplasm, or around the nucleus of the cell which serves as a ‘viral replication factory’. The viroplasm contains components such as virus genetic material, host proteins and ribosomes necessary for replication.[17] Virosomes are often surrounded by a membrane;[17] the membrane surrounding the virosome contained in the infected cells in the study was found to consist of a fibrillar matrix.[16] Virions are released from infected cells following disruption of the organelles and lysis of the host cell membrane. Curtis and Chan counted more than 320 viruses in an ultrathin section of an infection cell.[16] Estimates for burst sizes range from 320 to 600 viruses per cell.[18].

Rhaphidovirus

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In Rhaphidovirus, there is only one species known as the Heterosigma akashiwo virus (HaV) which infects the unicellular alga, Heterosigma akashiwo. H. akashiwo is a member of the class Raphidophyceae, a bloom forming species and is widely distributed in temperate and neritic waters.[19] Several other types of viruses infecting H. akashiwo have been isolated and are not to be confused with HaV, such as the H. akashiwo RNA virus (HaRNAV) and H. akashiwo nuclear inclusion virus (HaNIV).[20] As this virus was first isolated and characterized in 1997,[20] information about the life cycle is limited.

The HaV specifically infects H. akashiwo and does not infect other marine phytoplankton species tested.[20] The mechanisms determining the virus-host specificity is not well understood. Tomaru et al. (2008) suggest that virus-host specificity maybe caused by unique interactions between a viral ligand and a host receptor.[20] In a study by Nagaski et al., virus particles were found inside the host cytoplasm at 24 hours post-infection. The latent period or lysogenic cycle was estimated to be 30-33 h with an average burst size (number of viruses produced after lysis) of 770 per cell. Virus particles were found in the subsurface area and in the viroplasm area.[21]

Encoded proteins

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Ectocarpus siliculosus virus (EsV-1) (belongs to Phaeovirus) and Paramecium bursaria chlorella virus (PBCV-1) (belongs to Chlorovirus) are two well-studied viruses, whose genomes have been found to encode many proteins. These proteins impact on virus stability, DNA synthesis, transcription, and other important interactions with host.

Enzymes for glycosylation

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PBCV-1 has a glycosylated major capsid protein, weighted as 54-kDa, which comprises about 40% of the total virus protein.[22] Unlike most of the viral structural proteins are glycosylated in the endoplasmic reticulum (ER) and Golgi apparatus by host-encoded glycosyltransferases,[23] PBCV-1 glycosylates its major capsid protein independently by encoding most of the enzymes that necessary for constructing the complex oligosaccharides, which then attach to the major capsid protein of PBCV-1 to form the glycoprotein. Therefore, the glycosylation of major capsid protein of PBCV-1 happens independently of ER and Golgi apparatus in host cells.[24]

Ion channel protein

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The first know viral protein that functions as potassium-selective ion channel was found in PBCV-1.[25] The protein (called Kcv) consists of 94 amino acids is encoded from a small ORF (ORF A250R) in PBCV-1, which can produce potassium-selective and voltage-sensitive conductance in Xenopus oocytes.[25] The putative PBCV-1 protein has a short cytoplasmic N-terminus (12 amino acids) containing one consensus protein kinase C site and it has 2 transmembrane domains. Whereas, the different amino acid sequence and lacking of COOH-terminal cytoplasmic tail make Kcv differ from other potassium channel.[25][26]

EsV-1 encodes a 124 codon ORF that has significant amino acid identity to PBCV-1 Kcv (41% amino acid identity).[26] However, the putative EsV-1 protein has a longer N-terminus (35 amino acids) containing two consensus protein kinase C sites and it has three transmembrane domains.[26] It is unknown that if the EsV-1 protein can form a functional channel in heterologous cells. The EsV-1 genome also encodes several proteins with hydrophobic amino acid rich regions that resemble helical transmembrane domains. Among these proteins, the input domain of the putative hybrid His-kinase 186 and the ORF 188 resemble ion channel proteins.[27]

DNA replication-associated proteins

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Both of EsV-1 and PBCV-1 encode DNA polymerase that belongs to the DNA polymerase-δ family, and they all contain a proof-reading 3’-5’ exonuclease domain.[28] Besides, both PBCV-1 and EsV-1 encode a sliding clamp processivity factor protein (PCNA), which interacts with proteins involved in DNA replication as well as proteins involved in DNA repair and postreplicative processing (e.g. DNA methylases and DNA transposases).[29]

Heteropentameric replication factor C (RFC) is a complex which responsible for the ATP-dependent loading of PCNA onto DNA;[30][31] EsV-1 encodes five proteins which can form a RFC complex. While, PBCV-1 encodes a single protein, the protein is resemble to the protein found in Archae RFC complex.[27] PBCV-1 also encodes other proteins involved in DNA replication including an ATP-dependent DNA ligase,[32] a type II DNA topoisomerase, and RNase H.[26] Although both EsV-1 and PBCV-1 own genes for essential elements of eukaryotic replication system, none has the complete replicative genes, since they all lack genes for primase.[22][26]

Transcription-associated proteins

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Neither EsV-1 nor PBSV-1 encodes a complete RNA polymerase, but they produce several transcription factor-like proteins to assist host transcription system.

EsV-1 encodes two small polypeptides (ORF 193 and ORF 196) for transcriptional regulation, the proteins resemble to α/β/α domain of TFIID-18 subunit.[27]The TFIID complex is necessasry for transcription of eukaryotes, as it binds to the TATA box in the core promoter of the gene to initiate the assembly of RNA polymerase. Besides, polypeptides resemble to the SET, BTB/POZ (i.e. Broad Complex, Tramtrack, and Bric-a-brac/poxvirus and zinc finger) (ORF 40), and BAF60b (ORF 129) domains are also encoded by ESV-1 to regulate chromatin remodeling and transcription repression.[27][22][33]

Four transcription factor-like proteins have been found in PBSV-1, including TFIIB (A107L), TFIID (A552R), TFIIS (A125L), and a VLTF-2 type transcription factor (A482R).[26] In addition, PBCV-1 also encodes two enzymes involved in forming a mRNA cap structure, an RNA triphosphatase[34] and a mRNA guanylyltransferase.[35] The PBCV-1 enzymes are more closely related to yeast enzymes than to poxvirus multifunctional RNA capping enzymes according to its size, amino acid sequence, and biochemical properties.[36][37] PBCV-1 also encodes RNase III, which is involved in virus mRNAs processing.[26]

Nucleotide metabolism-associated proteins

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To supply deoxynucleotides for viral production in the low proliferating host cells, large DNA viruses own genes to encode deoxynucleotide synthesis enzymes themselves.[26] Thirteen nucleotide metabolic enzymes have been found in PBCV-1, among them two are dUTP pyrophosphatase and dCMP deaminase, which can produce dUMP (i.e. the substrate for thymidylate synthetase).[38] In opposite, EsV-1 was found only encodes an ATPase (ORF 26) as well as both subunits of ribonucleotide reductase (ORF 128 and 180), which is a key enzyme in deoxynucleotide synthesis. [27]

Other enzymes

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Other enzymes like methyltransferases, DNA restriction endonucleases, and integrase were also found in PBCV-1.[22][26] Besides, PBCV-1 encodes a 187-amino-acid protein that resembles to the Cu-Zn SOD with all of the conserved amino acid residues for binding copper and zinc, which can decompose the rapid accumulated superoxide in host cell during infection, thereby benefits virus replication.[39]

Phylogeny

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Viruses belonged to Phycodnaviridae harbor double-stranded DNA genomes with sizes of several 100kbp, which together with other Megavirales (e.g. Iridoviridae, Pandoraviridae and Mimiviridae) named as Nucleocytoplasmic large DNA viruses (NCLDV). Because the large genome sizes and various proteins that can be encoded by, viruses of Phycodnaviridae are challenging the traditional concepts that viruses are small and simple “organisms at the edge of life”. Phylogenetic analyses of core genes based on gene concatenation,[40] individual phylogenies of the DNA polymerase,[41] and the major capsid protein,[42] indicate the close evolutionary relationships among members of Phycodnaviridae and between Phycodnaviridae with other families of NCLDV.

Ecological implications

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Coccolithovirus

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The coccolithovirus (EhV) infects the coccolithophore Emiliania huxleyi (E. huxleyi). Coccolithophores are marine haptophytes which are surrounded by microscopic plates made of calcium carbonate.[43] They live in the upper layers of the world’s oceans and represent the third most abundant group of phytoplankton, containing about 300 species.[44] E. huxleyi is recognized as the most prominent and ecologically important of the coccolithophores. E. huxleyi has a global distribution from the tropics to subarctic waters and occasionally forms dense blooms which can cover 100,000s of square kilometers.[44] These trillions of coccolithophores produced, then die and sink to the bottom of oceans, contributing to sediment formation, and are the biggest producers of calcite in the oceans.[43] Thus, coccoliths have significant roles in global carbon fixation and the carbon cycle as well as sulfur cycling.[44] Over time, coccolithophores have shaped geological features of our planet. For example, the White Cliffs of Dover are formed from white chalk, or calcium carbonate produced by coccolithophores over millions of years.

Coccolithophore blooms are typically not harmful to marine life in the ocean. As these organisms thrive in nutrient-poor conditions, the coccolithophores offer a source of nutrition for small fish and zooplankton.[43] E. huxylei viruses (EhVs) have been shown to be linked to the termination of these blooms. The termination stage of the bloom is indicated by a color change in the water. When large amounts of coccoliths (carbonate shell surrounding E. huxylei) are shed from E. huxylei cells from cell death or lysis, the water turns white or turquoise. In areas of dense bloom termination, the white color is reflective and can be seen in satellite imagery.[44] Wilson et al. (2002) used analytical flow cytometry to measure the abundance of viruses at different locations in and around the bloom area. The researchers found that the concentrations of viruses were higher inside the ‘high reflectance area’, suggesting that virus-induced lysis of E. huxleyi cells resulted in coccolith detachment.[45] Other studies by Martinez et al. (2007) and Bratbak et al. (1993) found higher concentrations of EhV viruses as the E. huxleyi bloom declined, indicating that lytic viral infection was the main cause of bloom termination.[46][47] EhV viruses therefore have important roles in regulating biomass production in marine environments and ecological succession. This regulation of coccolithophore populations by EhV viruses therefore has significant effects on biogeochemical cycles, particularly the carbon cycle.

Phaeovirus

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One of the most well studied phaeoviruses, EsV-1, infects the small, filamentous brown algae E. siliculosus, which has a cosmopolitan distribution (found in most of the world’s oceans).[48] E. siliculosus has been cited as a suitable genomic and genetic model organism for the brown algae. This species was chosen as a model organism because of its several features such as its small size, high fertility and rapid growth, as well as the ability to observe its full life cycle in the laboratory. Furthermore, the Ectocarpales are closely related to the brown algal group, the Laminariales, which are the most economically important group of brown algae, having a wide range of applications in the cosmetics and food industry.[49]

Muller et al. (1990) were one of the first to explore the causes of gametangium defects in E. siliculosus originating from New Zealand. The researchers identified reproductive cells of E. siliculosus filled with hexagonal particles which were then released into culture medium when the cells burst. Following release of these particles, sporophytes became infected, shown by pathological symptoms, suggesting that the particles are viruses.[50] Such studies allowed for the evaluation of infection potential of E. siliculosus viruses. Using PCR amplification of a viral gene fragment, Muller et al. (2005) monitored levels of pathogen infection in Ectocarpus samples from the Gran Canaria Island, North Atlantic and southern Chile. The researchers found high levels of pathogen prevalence; 40-100% of Ectocarpus specimens contained viral DNA.[51] Similar estimates have been given by Sengco et al. (1996) who estimated that at least 50% of Ectocarpus plants in the world contain viral DNA.[52] This high frequency of viral infection among globally distributed Ectocarpus plants has interesting ecological implications. Viral infection by EsV-1 in E. siliculosus plants, as mentioned, limits reproductive success of infected plants. Thus, the EsV-1 virus plays a key role in regulating populations of E. siliculosus, having further effects on local ecosystem dynamics.

Prasinovirus

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A commonly studied prasinovirus, OtV5, as mentioned, infects the smallest currently known eukaryote, Ostreococcus tauri. O. tauri is about 0.8 micrometers in diameter and is within the picosize fraction (0.2-2 micrometers).[53] Picoeukaryotes, such as Ostreococcus tauri, Synechococcus and Prochlorococcus are widely distributed and contribute significantly to microbial biomass and total primary productivity. In oligotrophic environments, marine picophytoplankton account for up to 90% of the autotrophic biomass and thus are an important food source for nanoplanktonic and phagotrophic protists.[54] As picoeukaryotes serve as the base for marine microbial food webs, they are intrinsic to the survival of higher trophic levels. Ostreococcus tauri has a rapid growth rate and dense blooms have been observed off the coasts of Long Island and California.[54] Samples collected from Long Island bay were found to contain many virus-like particles, a likely cause for the decline of the bloom.[55] Despite the large abundances of picoeukaryotes, these unicellular organisms are outnumbered by viruses by about ten to one.[56] Viruses such as OtV5, play important roles in regulating phytoplankton populations, and through lysis of cells contribute to the recycling of nutrients back towards other microorganisms, otherwise known as the viral shunt.[57]

Prymnesiovirus

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Prymnesiovirus, CbV-PW1, as mentioned infects the algal genus Chyrsochromulina. Chyrsochromulina, found in global fresh and marine waters, occasionally forms dense blooms which can produce harmful toxins, having negative effects on fisheries.[58] A particularly toxic species called C. polylepis has caused enormous damage to commercial fisheries in Scandinavia. In 1988, this bloom caused a loss of 500 tons of caged fish, worth 5 million US.[59] Given that Chyrsochromulina is a widespread species, and is of significant ecological importance, viral infection and lysis of genus members is likely to have significant impacts on biogeochemical cycles, such as nutrient recycling in aquatic environments. Curtis and Chan suggest that the presence of viruses should have a strong regulatory effect on Chyrsochromulina populations, thus preventing bloom formation or enabling bloom termination, explaining why persistent blooms are an unusual phenomenon in nature.[58]

Rhaphidovirus

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Heterosigma akashiwo forms dense, harmful blooms in temperate and subarctic waters, occurring at densities up to 5 ×106 cells/ml.[60] These algal blooms can be extremely harmful to aquatic life, causing mortality in wild and cultured fish, such as salmon, yellowtail and sea bream.[61] The severity and duration of these blooms varies from year, and damage to aquaculture by H.akashiwo has been increasing. In 1989, a noxious algal bloom off the coast of New Zealand resulted in the loss of seventeen million New Zealand dollars worth of chinook salmon. In 1995 and 1997 in Japanese coastal waters in Kagoshimo Bay, 1,090 million and 327 million Yen worth of fish were killed, respectively.[61]

The HaV virus, infecting H. akashiwo has been shown to be a factor in bloom termination. Suttle et al. (1990) suggested that viral infection of algae could have a role in regulating population densities of phytoplankton communities, thus having significant roles in shaping the dynamics of oceans.[62] Earlier studies, such as the study by Nagasaki et al. (1993), explored the dynamics between HaV and H. akashiwo. Algal samples were obtained in the middle or final stages of a red tide in Hiroshima Bay, Japan. Using transmission electron microscopy, Nagaski et al. identified the HaV virus in and around the nuclear area of H. akashiwo cells.[62] Further support for the role of the HaV virus in bloom termination was provided by a study conducted by Nagaski et al. (1994). Nagaski et al. (1994) found that proportion of virus-containing cells increased quickly before termination of the red tide; no virus-containing cells were detected three days before termination of the red tide and the sample collected on the last day revealed a high frequency (11.5%) of virus-containing cells.[63]

Further studies by Tarutani et al. (2000) also found an association between a decrease in cell density of H. akashiwo with an increase in the abundance of HaV. Interestingly, the researchers found that HaV not only plays in important role in controlling biomass, but also influences the clonal composition or characteristics of H. akashiwo cells. The researchers found that most isolates following bloom termination were resistant to HaV clonal isolates, while during bloom formation resistant cells were a minor component. The authors suggest that viral infection, during the bloom termination period influences the properties of dominant cells in H. akashiwo populations.[64] Selective pressure exerted by the viruses in the later stage of infection may promote genetic diversity, allowing the H. akashiwo population to thrive after bloom termination.

As mentioned, H. akashiwo blooms are detrimental to fish populations in temperate and subarctic waters, and continue to pose serious threats for aquaculture. Nagasaki et al. (1999) examined the growth characteristics of HaV and suggested that HaV could be used as a microbial agent against H. akashiwo red tides. The advantages of using HaV if that it specifically infects H. akashiwo even when other microorganisms are present. Additionally, it has a high growth rate and can be produced at a low cost. Using HaV as a microbial agent is a promising solution for eliminating red tides to protect fisheries and marine life, but as the authors concluded, the effects of various HaV clones on H. akashiwo populations should be explored in greater detail before the virus is used for wide-scale applications.[61]

References

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  1. ^ a b Mackinder, Luke C. M.; Worthy, Charlotte A.; Biggi, Gaia; Hall, Matthew; Ryan, Keith P.; Varsani, Arvind; Harper, Glenn M.; Wilson, William H.; Brownlee, Colin (2009-01-01). "A unicellular algal virus, Emiliania huxleyi virus 86, exploits an animal-like infection strategy". Journal of General Virology. 90 (9): 2306–2316. doi:10.1099/vir.0.011635-0.
  2. ^ "Caspase". Wikipedia. 2017-02-26.
  3. ^ Vardi, Assaf; Mooy, Benjamin A. S. Van; Fredricks, Helen F.; Popendorf, Kimberly J.; Ossolinski, Justin E.; Haramaty, Liti; Bidle, Kay D. (2009-11-06). "Viral Glycosphingolipids Induce Lytic Infection and Cell Death in Marine Phytoplankton". Science. 326 (5954): 861–865. Bibcode:2009Sci...326..861V. doi:10.1126/science.1177322. ISSN 0036-8075. PMID 19892986.
  4. ^ a b Stevens, Kim; Weynberg, Karen; Bellas, Christopher; Brown, Sonja; Brownlee, Colin; Brown, Murray T.; Schroeder, Declan C. (2014-01-21). "A Novel Evolutionary Strategy Revealed in the Phaeoviruses". PLoS ONE. 9 (1): e86040. Bibcode:2014PLoSO...986040S. doi:10.1371/journal.pone.0086040. ISSN 1932-6203. PMC 3897601. PMID 24465858.{{cite journal}}: CS1 maint: unflagged free DOI (link)
  5. ^ a b Klein, M.; Lanka, S. T.; Knippers, R.; Müller, D. G. (1995-01-10). "Coat protein of the Ectocarpus siliculosus virus". Virology. 206 (1): 520–526. ISSN 0042-6822. PMID 7831806.
  6. ^ a b Charrier, Bénédicte; Coelho, Susana M.; Le Bail, Aude; Tonon, Thierry; Michel, Gurvan; Potin, Philippe; Kloareg, Bernard; Boyen, Catherine; Peters, Akira F. (2008-01-01). "Development and physiology of the brown alga Ectocarpus siliculosus: two centuries of research". The New Phytologist. 177 (2): 319–332. doi:10.1111/j.1469-8137.2007.02304.x. ISSN 0028-646X. PMID 18181960.
  7. ^ a b Muller, Dieter G. (1991). "Marine virioplankton produced by infected Ectocarpus siliculosus (Phaeophyceae)" (PDF). Marine Ecology. 76: 101–102.
  8. ^ Clerissi, Camille; Desdevises, Yves; Grimsley, Nigel (2012-04-15). "Prasinoviruses of the Marine Green Alga Ostreococcus tauri Are Mainly Species Specific". Journal of Virology. 86 (8): 4611–4619. doi:10.1128/JVI.07221-11. ISSN 0022-538X. PMC 3318615. PMID 22318150.
  9. ^ "Home - Ostreococcus lucimarinus". genome.jgi.doe.gov. Retrieved 2017-02-28.
  10. ^ a b Derelle, Evelyne; Ferraz, Conchita; Escande, Marie-Line; Eychenié, Sophie; Cooke, Richard; Piganeau, Gwenaël; Desdevises, Yves; Bellec, Laure; Moreau, Hervé (2008-05-28). "Life-Cycle and Genome of OtV5, a Large DNA Virus of the Pelagic Marine Unicellular Green Alga Ostreococcus tauri". PLoS ONE. 3 (5): e2250. Bibcode:2008PLoSO...3.2250D. doi:10.1371/journal.pone.0002250. ISSN 1932-6203. PMC 2386258. PMID 18509524.{{cite journal}}: CS1 maint: unflagged free DOI (link)
  11. ^ Thomas, Rozenn; Grimsley, Nigel; Escande, Marie-Line; Subirana, Lucie; Derelle, Evelyne; Moreau, Hervé (2011-06-01). "Acquisition and maintenance of resistance to viruses in eukaryotic phytoplankton populations". Environmental Microbiology. 13 (6): 1412–1420. doi:10.1111/j.1462-2920.2011.02441.x. ISSN 1462-2920. PMID 21392198.
  12. ^ Sime-Ngando, Télesphore (2014-01-01). "Environmental bacteriophages: viruses of microbes in aquatic ecosystems". Aquatic Microbiology. 5: 355. doi:10.3389/fmicb.2014.00355. PMC 4109441. PMID 25104950.{{cite journal}}: CS1 maint: unflagged free DOI (link)
  13. ^ "Prymnesiovirus". Wikipedia. 2015-06-29.
  14. ^ Suttle, Curtis A.; Chan, Amy M. (2002-01-01). Tidona, Christian A.; MD, Gholamreza Darai; Büchen-Osmond, Cornelia (eds.). The Springer Index of Viruses. Springer Berlin Heidelberg. pp. 741–743. doi:10.1007/3-540-31042-8_128. ISBN 9783540671671.
  15. ^ "Chrysochromulina Lackey, 1939 :: Algaebase". www.algaebase.org. Retrieved 2017-02-28.
  16. ^ a b c d Suttle; A, C.; Chan; M, A. (1995-03-09). "Viruses infecting the marine Prymnesiophyte Chrysochromulina spp.: isolation, preliminary characterization and natural abundance". Marine Ecology Progress Series. 118: 275–282. doi:10.3354/meps118275.
  17. ^ a b "Viroplasm". Wikipedia. 2017-01-20.
  18. ^ King, Andrew M. Q. (2012-01-01). Virus Taxonomy: Classification and Nomenclature of Viruses : Ninth Report of the International Committee on Taxonomy of Viruses. Elsevier. ISBN 9780123846846.
  19. ^ "Evolution and Phylogeny of Large DNA Viruses, Mimiviridae and Phycodnaviridae Including Newly Characterized Heterosigma akashiwo Virus (PDF Download Available)". ResearchGate. Retrieved 2017-03-01.
  20. ^ a b c d Tomaru, Yuji; Shirai, Yoko; Nagasaki, Keizo (2008-08-01). "Ecology, physiology and genetics of a phycodnavirus infecting the noxious bloom-forming raphidophyte Heterosigma akashiwo". Fisheries Science. 74 (4): 701–711. doi:10.1111/j.1444-2906.2008.01580.x. ISSN 1444-2906.
  21. ^ Nagasaki, Keizo; Tarutani, Kenji; Yamaguchi, Mineo (1999-03-01). "Growth Characteristics of Heterosigma akashiwo Virus and Its Possible Use as a Microbiological Agent for Red Tide Control". Applied and Environmental Microbiology. 65 (3): 898–902. ISSN 0099-2240. PMC 91120. PMID 10049839.
  22. ^ a b c d "Phycodnaviridae: A peek at genetic diversity (PDF Download Available)". ResearchGate. Retrieved 2017-03-03.
  23. ^ "Host cell glycosylation of viral glycoproteins - a battlefield for host defence and viral resistance". ResearchGate. Retrieved 2017-03-03.
  24. ^ "Glycosyltransferases encoded by viruses (PDF Download Available)". ResearchGate. Retrieved 2017-03-03.
  25. ^ a b c Plugge, B.; Gazzarrini, S.; Nelson, M.; Cerana, R.; van Etten, J. L.; Derst, C.; DiFrancesco, D.; Moroni, A.; Thiel, G. (2000-01-01). "A Potassium Channel Protein Encoded by Chlorella Virus PBCV-1". Science. 287 (5458): 1641–1644. JSTOR 3074650.
  26. ^ a b c d e f g h i "Phycodnaviridae - Large DNA algal viruses (PDF Download Available)". ResearchGate. Retrieved 2017-03-03.
  27. ^ a b c d e Delaroque, Nicolas (2001). "The Complete DNA Sequence of the Ectocarpus siliculosus Virus EsV-1 Genome". Virology. 287: 112–132.
  28. ^ "Eukaryotic DNA polymerases, a growing family (PDF Download Available)". ResearchGate. Retrieved 2017-03-03.
  29. ^ "The puzzle of PCNA's many partners (PDF Download Available)". ResearchGate. Retrieved 2017-03-03.
  30. ^ "Opening of the clamp: An intimate view of an ATP-driven biological machine (PDF Download Available)". ResearchGate. Retrieved 2017-03-03.
  31. ^ "Clamping down on clamps and clamp loaders. The eukaryotic replication factor C". ResearchGate. Retrieved 2017-03-03.
  32. ^ "Characterization of an ATP-dependent DNA ligase encoded by Chlorella virus PBCV-1 (PDF Download Available)". ResearchGate. Retrieved 2017-03-03.
  33. ^ "The LAZ3/BCL6 Oncogene Encodes a Sequence-Specific Transcriptional Inhibitor: A Novel Function for the BTB/POZ Domain as an Autonomous Repressing Domain". PubMed Journals. Retrieved 2017-03-04.
  34. ^ "RNA Triphosphatase Component of the mRNA Capping Apparatus of Paramecium bursaria Chlorella Virus 1 (PDF Download Available)". ResearchGate. Retrieved 2017-03-03.
  35. ^ "Expression and Characterization of an RNA Capping Enzyme Encoded by Chlorella Virus PBCV-1 (PDF Download Available)". ResearchGate. Retrieved 2017-03-03.
  36. ^ Shuman, Stewart (2000). "Structure, mechanism, and evolution of the mRNA capping apparatus". Progress in Nucleic Acid Research and Molecular Biology. 66: 1–40.
  37. ^ Ho, C. K.; Van Etten, J. L.; Shuman, S. (1996-10-01). "Expression and characterization of an RNA capping enzyme encoded by Chlorella virus PBCV-1". Journal of Virology. 70 (10): 6658–6664. ISSN 0022-538X. PMC 190707. PMID 8794301.{{cite journal}}: CS1 maint: PMC format (link)
  38. ^ Van Etten, James L.; Meints, Russel H. (2003-11-28). "Giant Viruses Infecting Algae". Annual Review of Microbiology. 53 (1): 447–494. doi:10.1146/annurev.micro.53.1.447.
  39. ^ Kang, Ming; Duncan, Garry A.; Kuszynski, Charles; Oyler, George; Zheng, Jiayin; Becker, Donald F.; Etten, James L. Van (2014-11-01). "Chlorovirus PBCV-1 Encodes an Active Copper-Zinc Superoxide Dismutase". Journal of Virology. 88 (21): 12541–12550. doi:10.1128/JVI.02031-14. ISSN 0022-538X. PMC 4248938. PMID 25142578.
  40. ^ Maruyama, Fumito; Ueki, Shoko (2016-11-30). "Evolution and Phylogeny of Large DNA Viruses, Mimiviridae and Phycodnaviridae Including Newly Characterized Heterosigma akashiwo Virus". Frontiers in Microbiology. 7. doi:10.3389/fmicb.2016.01942. ISSN 1664-302X. PMC 5127864. PMID 27965659.{{cite journal}}: CS1 maint: unflagged free DOI (link)
  41. ^ Fischer, Matthias G.; Allen, Michael J.; Wilson, William H.; Suttle, Curtis A. (2010-11-09). "Giant virus with a remarkable complement of genes infects marine zooplankton". Proceedings of the National Academy of Sciences. 107 (45): 19508–19513. doi:10.1073/pnas.1007615107. ISSN 0027-8424. PMC 2984142. PMID 20974979.
  42. ^ Yau, Sheree; Lauro, Federico M.; DeMaere, Matthew Z.; Brown, Mark V.; Thomas, Torsten; Raftery, Mark J.; Andrews-Pfannkoch, Cynthia; Lewis, Matthew; Hoffman, Jeffrey M. (2011-04-12). "Virophage control of antarctic algal host–virus dynamics". Proceedings of the National Academy of Sciences. 108 (15): 6163–6168. doi:10.1073/pnas.1018221108. ISSN 0027-8424. PMC 3076838. PMID 21444812.
  43. ^ a b c John, Weier, (1999-04-26). "What is a Coccolithophore? Fact Sheet : Feature Articles". earthobservatory.nasa.gov. Retrieved 2017-03-03.{{cite web}}: CS1 maint: extra punctuation (link) CS1 maint: multiple names: authors list (link)
  44. ^ a b c d "Home - Emiliania huxleyi". genome.jgi.doe.gov. Retrieved 2017-03-03.
  45. ^ Wilson, William H.; Tarran, Glen A.; Schroeder, Declan; Cox, Michael; Oke, Joanne; Malin, Gillian (2002-06-01). "Isolation of viruses responsible for the demise of an Emiliania huxleyi bloom in the English Channel". Journal of the Marine Biological Association of the United Kingdom. 82 (3): 369–377. doi:10.1017/S002531540200560X. ISSN 1469-7769.
  46. ^ Martínez, Joaquín Martínez; Schroeder, Declan C.; Larsen, Aud; Bratbak, Gunnar; Wilson, William H. (2007-01-15). "Molecular Dynamics of Emiliania huxleyi and Cooccurring Viruses during Two Separate Mesocosm Studies". Applied and Environmental Microbiology. 73 (2): 554–562. doi:10.1128/AEM.00864-06. ISSN 0099-2240. PMC 1796978. PMID 17098923.
  47. ^ "Viral mortality of the marine alga Emiliania huxleyi (Haptophyceae) and termination of algal blooms (PDF Download Available)". ResearchGate. Retrieved 2017-03-03.
  48. ^ Klein, M.; Lanka, S. T.; Knippers, R.; Müller, D. G. (1995-01-10). "Coat protein of the Ectocarpus siliculosus virus". Virology. 206 (1): 520–526. ISSN 0042-6822. PMID 7831806.
  49. ^ CEA (2016-10-24). "Ectocarpus siliculosus a genetic and genomic model organism for the brown algae". CEA/Institute of Genomics. Retrieved 2017-03-05.
  50. ^ "A Virus Infection in the Marine Brown Alga Ectocarpus siliculosus (Phaeophyceae)". ResearchGate. Retrieved 2017-03-05.
  51. ^ G., Müller, D.; R., Westermeier,; J., Morales,; Garcia, Reina, G.; E., del Campo,; A., Correa, J.; E., Rometscha, (2000-03-08). "Massive Prevalence of Viral DNA in Ectocarpus (Phaeophyceae, Ectocarpales) from Two Habitats in the North Atlantic and South Pacific". Botanica Marina. 43 (2). doi:10.1515/BOT.2000.016. ISSN 0006-8055.{{cite journal}}: CS1 maint: extra punctuation (link) CS1 maint: multiple names: authors list (link)
  52. ^ Sengco, M. R.; Bräutigam, M.; Kapp, M.; Müller, D. G. (1996-02-01). "Detection of virus DNA in Ectocarpus siliculosus and E. fasciculatus (Phaeophyceae) from various geographic areas". European Journal of Phycology. 31 (1): 73–78. doi:10.1080/09670269600651221. ISSN 0967-0262.
  53. ^ "Ostreococcus tauri". Wikipedia. 2016-11-21.
  54. ^ a b Derelle, Evelyne; Ferraz, Conchita; Rombauts, Stephane; Rouzé, Pierre; Worden, Alexandra Z.; Robbens, Steven; Partensky, Frédéric; Degroeve, Sven; Echeynié, Sophie (2006-08-01). "Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features". Proceedings of the National Academy of Sciences. 103 (31): 11647–11652. doi:10.1073/pnas.0604795103. ISSN 0027-8424. PMC 1544224. PMID 16868079.
  55. ^ O'Kelly, Charles J.; Sieracki, Michael E.; Thier, Edward C.; Hobson, Ilana C. (2003-10-01). "A Transient Bloom of Ostreococcus (chlorophyta, Prasinophyceae) in West Neck Bay, Long Island, New York". Journal of Phycology. 39 (5): 850–854. doi:10.1046/j.1529-8817.2003.02201.x. ISSN 1529-8817.
  56. ^ Yau, Sheree; Hemon, Claire; Derelle, Evelyne; Moreau, Hervé; Piganeau, Gwenaël; Grimsley, Nigel (2016-10-27). "A Viral Immunity Chromosome in the Marine Picoeukaryote, Ostreococcus tauri". PLOS Pathogens. 12 (10): e1005965. doi:10.1371/journal.ppat.1005965. ISSN 1553-7374. PMC 5082852. PMID 27788272.{{cite journal}}: CS1 maint: unflagged free DOI (link)
  57. ^ "An Ocean of Viruses | The Scientist Magazine®". The Scientist. Retrieved 2017-03-05.
  58. ^ a b "Viruses infected the marine prymnesiophyte Chrysochromulina spp.: Isolation, preliminary characterization and natural abundance (PDF Download Available)". ResearchGate. Retrieved 2017-03-01.
  59. ^ "Toxic Algal Bloom in Scandinavian Waters, May–June 1988 | Oceanography". tos.org. Retrieved 2017-03-01.
  60. ^ Lawrence, Janice E.; Brussaard, Corina P. D.; Suttle, Curtis A. (2017-03-01). "Virus-Specific Responses of Heterosigma akashiwo to Infection". Applied and Environmental Microbiology. 72 (12): 7829–7834. doi:10.1128/AEM.01207-06. ISSN 0099-2240. PMC 1694243. PMID 17041155.
  61. ^ a b c Nagasaki, Keizo; Tarutani, Kenji; Yamaguchi, Mineo (1999-03-01). "Growth Characteristics of Heterosigma akashiwo Virus and Its Possible Use as a Microbiological Agent for Red Tide Control". Applied and Environmental Microbiology. 65 (3): 898–902. ISSN 0099-2240. PMC 91120. PMID 10049839.
  62. ^ a b Nagasaki, K.; Ando, M.; Imai, I.; Itakura, S.; Ishida, Y. (1994). "Virus-like particles in Heterosigma akashiwo (Raphidophyceae): a possible red tide disintegration mechanism". Marine Biology. 119 (2): 307–312. doi:10.1007/BF00349570. ISSN 0025-3162.
  63. ^ Nagasaki, Keizo; Ando, Masashi; Itakura, Shigeru; Imai, Ichiro; Ishida, Yuzaburo (1994-01-01). "Viral mortality in the final stage of Heterosigma akashiwo (Raphidophyceae) red tide". Journal of Plankton Research. 16 (11): 1595–1599. doi:10.1093/plankt/16.11.1595. ISSN 0142-7873.
  64. ^ Tarutani, Kenji; Nagasaki, Keizo; Yamaguchi, Mineo (2017-03-01). "Viral Impacts on Total Abundance and Clonal Composition of the Harmful Bloom-Forming Phytoplankton Heterosigma akashiwo". Applied and Environmental Microbiology. 66 (11): 4916–4920. ISSN 0099-2240. PMC 92399. PMID 11055943.