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Characteristics of Virophages and Giant Viruses Beata Tokarz-Deptuła1*, Paulina Czupryńska2, Agata Poniewierska-Baran1 and Wiesław Deptuła2

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Characteristics of Virophages and Giant Viruses Beata Tokarz-Deptuła1*, Paulina Czupryńska2, Agata Poniewierska-Baran1 and Wiesław Deptuła2 Vol. 65, No 4/2018 487–496 https://doi.org/10.18388/abp.2018_2631 Review Characteristics of virophages and giant viruses Beata Tokarz-Deptuła1*, Paulina Czupryńska2, Agata Poniewierska-Baran1 and Wiesław Deptuła2 1Department of Immunology, 2Department of Microbiology, Faculty of Biology, University of Szczecin, Szczecin, Poland Five years after being discovered in 2003, some giant genus, Mimiviridae family (Table 3). It was found in the viruses were demonstrated to play a role of the hosts protozoan A. polyphaga in a water-cooling tower in Brad- for virophages, their parasites, setting out a novel and ford (Table 1). Sputnik has a spherical dsDNA genome yet unknown regulatory mechanism of the giant virus- closed in a capsid with icosahedral symmetry, 50–74 nm es presence in an aqueous. So far, 20 virophages have in size, inside which there is a lipid membrane made of been registered and 13 of them have been described as phosphatidylserine, which probably protects the genetic a metagenomic material, which indirectly impacts the material of the virophage (Claverie et al., 2009; Desnues number of single- and multi-cell organisms, the environ- et al., 2012). Sputnik’s genome has 18343 base pairs with ment where giant viruses replicate. 21 ORFs that encode proteins of 88 to 779 amino ac- ids. They compose the capsids and are responsible for Key words: virophages, giant viruses, MIMIVIRE, Sputnik N-terminal acetylation of amino acids and transposases Received: 14 June, 2018; revised: 21 August, 2018; accepted: (Claverie et al., 2009; Desnues et al., 2012; Tokarz-Dep- 09 September, 2018; available on-line: 23 October, 2018 tula et al., 2015). Sputnik’s genome does not have an * RNA-dependent DNA polymerase. Hence, in infection, e-mail: [email protected] Sputnik uses Mamavirus – ACMV or Minivirus – APMV Abbreviations: ACMV, acanthamoeba castellanii mamavirus; ALM, ace lake mavirus; APMV, acanthamoeba polyphaga mimivirus; synthesized polymerase (La Scola et al., 2008; Desnues et CroV, cafateria roenbergensis virus; DNA, deoxyribonucleic acid; al., 2012). dsDNA, double stranded DNA; DSLV, Dishui Lake virophage; dsR- Mavirus (Table 1) is a virophage that was identified NA, double stranded RNA; IEM, independent entry mode; IRG1, im- in 2011 and infects a giant virus Cafateria roenbergensis mune responsive gene 1; NCLDV, nucleocytoplasmic large DNA vi- ruses; OLV, organic lake virophage; ORF, open reading frames; QLV, (CroV) of the genus Cafateriavirus, family Mimiviridae (Ta- Qinghai Lake virophage; PEM, paired entry mode; PCR, polymerase ble 3). Mavirus was isolated for the first time from the chain reaction; PGV, phaeocystis globosa virophage; RNA, ribonu- flagellate Cafateria roenbergensis that populates the coastal cleic acid; RNV, Rio Negro virophage; RVP, rumen virophage; SMBV, waters of Gulf of Mexico in Texas (Table 1). This vi- Samba virus; ssDNA, single-stranded DNA; ssRNA, single-stranded RNA; tRNA, transfer RNA; YSLV, Yellowstone Lake virophage rophage also has a spherical dsDNA genome, which probably encodes 20 proteins (Fischer et al., 2011; Sli- wa-Dominiak et al., 2016), and a capsid with icosahedral VIROPHAGES symmetry that is similar to that identified in Sputnik (Fischer et al., 2011). The Mavirus virophage’s genome Among the 20 virophages described so far, 13 are in is homologous to eukaryotic DNA transposons, which the form of a metagenomic material, and the hosts were suggests that the virophages could indeed have been in- revealed for 16 virophages (Table 1). Out of the group volved in their origin (Fischer et al., 2011; Desnues et al., of the 16 hosts, 8 giant viruses (items 1–6, 12 and 13 2012). Interestingly, virophages play an important role in in Table 1) were characterized, with the other 8 hosts the ecology of the protists’ natural populations (Fischer identified as the ‘probable’ giant viruses (items 7–11 and et al., 2011; Desnues et al., 2012; Sliwa-Dominiak et al., 18–20 in Table 1). Currently, the virophages are classi- 2016; Krupovic et al., 2016; Fischer et al., 2016). fied to belong to the Lavidaviridae family (Krupovic et al., The third discovered virophage was isolated in 2011 2016). Although they differ significantly between each in the salty waters of Antarctica. It was OLV (Organic other, they are considered to be satellite- or satellite-like lake virophage), which preyed on an algae- infecting giant viruses (Table 2). virus (no genus given), of a Phycodnaviridae family (Ta- Sputnik was the first virophage to be identified in ble 1). OLV, like the Sputnik, also has a double strand- 2008 in a Mamavirus – ACMV (Acanthamoeba castellanii ed DNA genome that is circular in shape and 26421 bp mamavirus), a giant virus (Table 1) of the Mimivirus genus in size and encodes 24 proteins which are 27–42% iden- of Mimiviridae family (Table 3). The virus was found tical with the Sputnik proteins (Yau et al., 2011; Beklitz inside the protozoan Acanthamoeba (A.) castellanii, in a et al., 2016). The OLVs’ effect on giant viruses infecting Paris water-cooling tower (Table 1). Research on ACMV algae impacts their count and regulates organic matter in Mamavirus revealed an eclipse phase, called Sputnik (from their aqueous environment (Yau et al., 2011). a Russian word meaning ‘a companion in a journey’), to Sputnik 2, which was discovered in 2012, has an celebrate the first artificial satellite of the Earth (Tay- 18338 bp, circular, double stranded DNA genome (Gaia lor et al., 2014). Given the analogy with the term bac- et al., 2013; Beklitz et al., 2016), with a capsid that has teriophages, it is also referred to as a virophage, which icosahedral symmetry (Beklitz et al., 2016). It infects Len- stands for a ‘virus eater’ (La Scola et al., 2008). Later, tille virus, a giant virus, genus Mimivirus, family Mimiviridae Sputnik virophage was demonstrated to infect the giant (Table 3), that was found in A. polyphaga eukaryote har- virus APMV (Acanthamoeba polyphaga) Mimivirus, that was vested from a contact lens fluid (Desnues et al., 2012). identified in 2003 (Table 1) and belongs to the Mimivirus 488 B. Tokarz-Deptuła and others 2018 Table 1. Virophages and their “host” – giant viruses The name of the Virophages and the Species, type or family Host and place of occurance of giant No. year of finding of giant viruses viruses Reference Amoeba Acanthamoeba (A.) castellanii – Mamavirus (ACMV) water of cooling tower in Paris (France) 1. Sputnik (2008) La Scola et al., 2008 Amoeba A. polyphaga – water of cooling Mimivirus (APMV) tower in Bradford (England). 2. Mavirus (2011) Cafateria roenbergensis Flagellate Cafateria roenbergensis Fischer & Suttle, virus (CroV) – sea water in Texas coast (USA) 2011 OLV (Organic Lake Virophage) Algae (no name) – saline waters of 3. (2011) Phycodnaviridae Antarctica Lake Yau et al., 2011 Amoeba A. polyphaga – contact lenses Desnues et al., 4. Sputnik 2 (2012) Lentille virus liquid (France) 2012 Mimiviridae, probably Amoeba A. polyphaga – soil samples 5. Sputnik 3 (2013) Mamavirus (France) Gaia et al., 2013 Algae Phaeocystis type – water of the 6. PGV (Phaeocystis globosa virophage) Phaeocystis globose North Sea samples (coast of the Nether- Santini et al., 2013 – metagenomic material (2013) virus (PgV-16T) lands) YSLV 1 (Yellowstone Lake Virophage 7. 1) – metagenomic material (2013) YSLV 2 (Yellowstone Lake Virophage 8. 2) – metagenomic material (2013) Probably Phycodnaviri- *Algae – water of the Yellowstone Lake dae or Mimivirus (USA) Zhou et al., 2013 YSLV 3 (Yellowstone Lake Virophage 9. 3) – metagenomic material (2013) YSLV 4 (Yellowstone Lake Virophage 10. 4) – metagenomic material (2013) ALM (Ace Lake Mavirus) – Probably *Protozoa (no name) – water of 11. metagenomic material (2013) Mimiviridae Antarctica Lake Zhou et al., 2013 Amoeba A. castellanii – water of Campos et al., 12. RNV (Rio Negro virophage) (2014) Samba wirus (SMBV) the Negro River (Brazil) 2014 Amoeba A. polyphaga – soil samples 13. Zamilon virophage (2014) Mont1 wirus (Tunisia) Gaia et al., 2014 YSLV 5 (Yellowstone Lake Virophage 14. 5) – metagenomic material (2015) YSLV 6 (Yellowstone Lake Virophage 15. 6) – metagenomic Not described No “host” for the virus-lake water in Yel- Zhou et al., 2015 material (2015) lowstone Park (USA) YSLV 7 (Yellowstone Lake Virophage 16. 7) – metagenomic material (2015) Probably amoeba Acanthamoeba 17. Zamilon 2 – metagenomic material Not described sp. – water in a poplar wood bioreactor Beklitz et al., 2015 (2015) (USA)) RVP (Rumen virophage) – Probably * Protozoa (no name) – sheep’s rumen 18. metagenomic material (2015) Mimiviridae (USA) Yutin et al., 2015 DSLV (Dishui Lake virophage) – Probably *Algae (no name) – water of the Dishui 19. metagenomic material (2016) Phycodnaviridae Lake (China) Gong et al., 2016 QLV (Qinghai Lake virophage) – Probably *Algae (no name) – water of the Qinghai 20. metagenomic material (2016) Phycodnaviridae Lake (Tibet) Oh et al., 2016 *supposed „host” for giant viruses Vol. 65 Characteristics of virophages and giant viruses 489 Table 2. Selected feature of virophages and satellite viruses (satellite-like) No. Feature Virophages Satellite viruses (satellite- like) Reference Mammals, plants in presence Fischer et al., 2011; 1. Host Giant viruses of helper viruses Taylor et al., 2014 Impact on giant viruses or viru- Negatively impact on giant No negatively impact on hel- 2. ses (helper viruses) viruses per viruses Taylor et al., 2014 Impact of virophages on host of giant viruses (protozoa, algae) Taylor et al., 2014; 3. and impact of satellite No interactions Negatively or no interactions Tokarz-Deptuła et al., viruses on host of viruses (mam- 2013 mals and plants) Cell nucleus of eukaryotic Colson et al., 2010; 4. Place of replication „Factories of giant viruses” organisms Abergel et al., 2015 5. Type of genetic material dsDNA ssRNA, dsRNA and ssDNA Krupovic et al., 2016 6. Genome size 18,0 -19,0 thousand bp 11,0 thousand nt Krupovic et al., 2016 High degree of diversity, be- cause they have sequences Fischer et al., 2011; 7. Differentiation in genome bu- from eukaryotes, Typical diversity - only viral Desnues et al., 2012; ilding including algae and giant sequences exist Krupovic et al., 2016 viruses 8.
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