The rapidly expanding universe of giant viruses: Mimivirus, Pandoravirus, Pithovirus and Mollivirus

FEMS Microbiology Reviews

Volumn 39, Issue 6, 2015, Pages 779-796

  Abergel, Chantal ^a   Legendre, Matthieu ^a   Claverie, Jean Michel ^a,b  

^a CNRS   (France)

^b ASSISTANCE PUBLIQUE HÔPITAUX DE MARSEILLE   (France)

Author keywords

DNA virus; Giant virus; Mimiviridae; Mollivirus; Pandoraviridae; Pithoviridae

Indexed keywords

AQUATIC ENVIRONMENT; COOLING TOWER; COSMOS; DNA VIRUS; ELECTRON; GENETIC TRANSCRIPTION; GENOME; GENOME SIZE; MICROSCOPY; MIMIVIRIDAE; MIMIVIRUS; MOLLIVIRUS; NONHUMAN; PANDORAVIRUS; PHAGOTROPH; PITHOVIRUS; REVIEW; VIRION; VIRUS; VIRUS DETECTION; WASTE WATER MANAGEMENT; WATER SUPPLY; PHYSIOLOGY; ULTRASTRUCTURE; VIRAL PHENOMENA AND FUNCTIONS;

DNA VIRUS;

DNA VIRUSES; VIRION; VIRUS PHYSIOLOGICAL PHENOMENA;

EID: 84947549860     PISSN: 01686445     EISSN: 15746976     Source Type: Journal    
DOI: 10.1093/femsre/fuv037     Document Type: Review

References (141)

1. Abergel C, Rudinger-Thirion J, Giegé R, et al. Virus-encoded aminoacyl-tRNA synthetases: structural and functional characterization of mimivirus TyrRS and MetRS. J Virol 2007;81:12406-17.
2. Aherfi S, Boughalmi M, Pagnier I, et al. Complete genome sequence of Tunisvirus, a new member of the proposed family Marseilleviridae. Arch Virol 2014;159:2349-58.
3. Allen MJ, Schroeder DC, Wilson WH. Preliminary characterisation of repeat families in the genome of EhV-86, a giant algal virus that infects the marinemicroalga Emiliania huxleyi. Arch Virol 2006;151:525-35.
4. Antwerpen MH, Georgi E, Zoeller L, et al. Whole-genome sequencing of a pandoravirus isolated from keratitis-inducing acanthamoeba. Genome Announc 2015;3: pii: e00136-15.
5. Arslan D, Legendre M, Seltzer V, et al. Distant Mimivirus relative with a larger genome highlights the fundamental features of Megaviridae. P Natl Acad Sci USA 2011;108:17486-91.
6. Azza S, Cambillau C, Raoult D, et al. Revised Mimivirus major capsid protein sequence reveals intron-containing gene structure and extra domain. BMC Mol Biol 2009;10:39.
7. Bahar MW, Graham SC, Stuart DI, et al. Insights into the evolution of a complex virus from the crystal structure of vaccinia virus D13. Struct Lond Engl 1993 2011;19:1011-20.
8. Beijerinck MW. über ein contagium vivum fluidum als Ursache der Fleckenkrankheit der Tabaksblätter. in Verhandelingen Kon. Akademie van Wetenschappen, Amsterdam 1898, Deel VI, No. 5.
9. Benarroch D, Claverie J-M, Raoult D, et al. Characterization of mimivirus DNA topoisomerase IB suggests horizontal gene transfer between eukaryal viruses and bacteria. J Virol 2006;80:314-21.
10. Benarroch D, Qiu ZR, Schwer B, et al. Characterization of a mimivirus RNA cap guanine-N2 methyltransferase. RNA 2009;15:666-74.
11. Benarroch D, Shuman S. Characterization of mimivirus NAD+-dependent DNA ligase. Virology 2006;353:133-43.
12. Benarroch D, Smith P, Shuman S. Characterization of a trifunctional mimivirus mRNAcapping enzyme and crystal structure of the RNA triphosphatase domain. Structure 2008;16:501-12.
13. Boughalmi M, Pagnier I, Aherfi S, et al. First isolation of a giant virus from wild Hirudo medicinalis leech: Mimiviridae isolation in Hirudo medicinalis. Viruses 2013a;5:2920-30.
14. Boughalmi M, Saadi H, Pagnier I, et al. High-throughput isolation of giant viruses of the Mimiviridae and Marseilleviridae families in the Tunisian environment. Environ Microbiol 2013b;15:2000-7.
15. Boyer M, Azza S, Barrassi L, et al. Mimivirus shows dramatic genome reduction after intraamoebal culture. P Natl Acad Sci USA 2011;108:10296-301.
16. Boyer M, Madoui M-A, Gimenez G, et al. Phylogenetic and phyletic studies of informational genes in genomes highlight existence of a 4 domain of life including giant viruses. PloS One 2010;5:e15530.
17. Boyer M, Yutin N, Pagnier I, et al. Giant Marseillevirus highlights the role of amoebae as a melting pot in emergence of chimeric microorganisms. P Natl Acad Sci USA 2009;106:21848-53.
18. Breitbart M, Salamon P, Andresen B, et al. Genomic analysis of uncultured marine viral communities. P Natl Acad Sci USA 2002;99:14250-5.
19. Byrne D, Grzela R, Lartigue A, et al. The polyadenylation site of Mimivirus transcripts obeys a stringent 'hairpin rule'. Genome Res 2009;19:1233-42.
20. Campos RK, Boratto PV, Assis FL, et al. Samba virus: a novel mimivirus from a giant rain forest, the Brazilian Amazon. Virol J 2014;11:95.
21. Carter GC, Law M, Hollinshead M, et al. Entry of the vaccinia virus intracellular mature virion and its interactions with glycosaminoglycans. J Gen Virol 2005;86:1279-90.
22. Claverie J-M. Viruses take center stage in cellular evolution. Genome Biol 2006;7:110.
23. Claverie J-M, Abergel C. Mimivirus and its virophage. Annu Rev Genet 2009;43:49-66.
24. Claverie J-M, Abergel C. Mimivirus: the emerging paradox of quasi-autonomous viruses. Trends Genet 2010;26:431-7.
25. Claverie J-M, Abergel C. Open questions about giant viruses. Adv Virus Res 2013;85:25-56.
26. Claverie J-M, Abergel C. From extraordinary endocytobionts to Pandoraviruses. Comment on Scheid et al. some secrets are revealed: parasitic keratitis amoebae as vectors of the scarcely described pandoraviruses to humans. Parasitol Res 2015;114:1625-7.
27. Claverie JM, Abergel C, Ogata H. Mimivirus. Curr Top Microbiol Immunol 2009;328:89-121.
28. Claverie J-M, Ogata H, Audic S, et al. Mimivirus and the emerging concept of 'giant' virus. Virus Res 2006;117:133-44.
29. Colson P, De Lamballerie X, Yutin N, et al. 'Megavirales', a proposed neworder for eukaryotic nucleocytoplasmic largeDNA viruses. Arch Virol 2013a;158:2517-21.
30. Colson P, Gimenez G, Boyer M, et al. The giant Cafeteria roenbergensis virus that infects a widespread marine phagocytic protist is a new member of the fourth domain of Life. PloS One 2011a;6:e18935.
31. Colson P, Pagnier I, Yoosuf N, et al. 'Marseilleviridae', a new family of giant viruses infecting amoebae. Arch Virol 2013b;158:915-20.
32. Colson P, Yutin N, Shabalina SA, et al. Viruses with more than 1, 000 genes: Mamavirus, a new Acanthamoeba polyphaga mimivirus strain, and reannotation of Mimivirus genes. Genome Biol Evol 2011b;3:737-42.
33. Delhon G, Tulman ER, Afonso CL, et al. Genome of invertebrate iridescent virus type 3 (mosquito iridescent virus). J Virol 2006;80:8439-49.
34. Desnues C, Boyer M, Raoult D. Sputnik, a virophage infecting the viral domain of life. Adv Virus Res 2012;82:63-89.
35. Doutre G, Philippe N, Abergel C, et al. Genome analysis of the first Marseilleviridae representative from Australia indicates that most of its genes contribute to virus fitness. J Virol 2014;88:14340-9.
36. Dufresne A, Garczarek L, Partensky F. Accelerated evolution associated with genome reduction in a free-living prokaryote. Genome Biol 2005;6:R14.
37. Ekeberg T, Svenda M, Abergel C, et al. Three-dimensional reconstruction of the giant mimivirus particle with an x-ray freeelectron laser. Phys Rev Lett 2015;114:098102.
38. El Albani A, Bengtson S, Canfield DE, et al. Large colonial organisms with coordinated growth in oxygenated environments 2.1 Gyr ago. Nature 2010;466:100-4.
39. El Albani A, Bengtson S, Canfield DE, et al. The 2.1 Ga old Francevillian biota: biogenicity, taphonomy and biodiversity. PloS One 2014;9:e99438.
40. Filée J. Route of NCLDV evolution: the genomic accordion. Curr Opin Virol 2013;3:595-9.
41. Filée J, Siguier P, Chandler M. I am what I eat and I eat what I am: acquisition of bacterial genes by giant viruses. Trends Genet TIG 2007;23:10-5.
42. Fischer MG, Allen MJ, Wilson WH, et al. Giant virus with a remarkable complement of genes infects marine zooplankton. P Natl Acad Sci USA 2010;107:19508-13.
43. Fischer MG, Suttle CA. A virophage at the origin of large DNA transposons. Science 2011;332:231-4.
44. Fitzgerald LA, Graves MV, Li X, et al. Sequence and annotation of the 369-kb NY-2A and the 345-kb AR158 viruses that infect Chlorella NC64A. Virology 2007;358:472-84.
45. Forterre P. Giant viruses: conflicts in revisiting the virus concept. Intervirology 2010;53:362-78.
46. Forterre P. The virocell concept and environmentalmicrobiology. ISME J 2013;7:233-6.
47. Gaia M, Benamar S, Boughalmi M, et al. Zamilon, a novel virophage with Mimiviridae host specificity. PloS One 2014;9:e94923.
48. Geisen S, Fiore-Donno AM, Walochnik J, et al. Acanthamoeba everywhere: high diversity of Acanthamoeba in soils. Parasitol Res 2014;113:3151-8.
49. Hakim M, Fass D. Dimer interface migration in a viral sulfhydryl oxidase. J Mol Biol 2009;391:758-68.
50. Hingamp P, Grimsley N, Acinas SG, et al. Exploring nucleocytoplasmic large DNA viruses in Tara Oceans microbial metagenomes. ISME J 2013;7:1678-95.
51. Imamura K, Averill A, Wallace SS, et al. Structural characterization of viral ortholog of human DNA glycosylase NEIL1 bound to thymine glycol or 5-hydroxyuracil-containing DNA. J Biol Chem 2012;287:4288-98.
52. Ivanovski D. über die Mosaikkrankheit der Tabakspflanze. St Petersb Acad Imp Sci Bul 1892;35:67-70.
53. Iyer LM, Aravind L, Koonin EV. Common origin of four diverse families of large eukaryotic DNA viruses. J Virol 2001;75:11720-34.
54. Iyer LM, Balaji S, Koonin EV, et al. Evolutionary genomics of nucleo-cytoplasmic large DNA viruses. Virus Res 2006;117:156-84.
55. Jeanniard A, Dunigan DD, Gurnon JR, et al. Towards defining the chloroviruses: a genomic journey through a genus of large DNA viruses. BMC Genomics 2013;14:158.
56. Jeudy S, Abergel C, Claverie J-M, et al. Translation in giant viruses: a unique mixture of bacterial and eukaryotic termination schemes. PLoS Genet 2012;8:e1003122.
57. Jeudy S, Lartigue A, Claverie J-M, et al. Dissecting the unique nucleotide specificity of mimivirus nucleoside diphosphate kinase. J Virol 2009;83:7142-50.
58. Johannessen TV, Bratbak G, Larsen A, et al. Characterisation of three novel giant viruses reveals huge diversity among viruses infecting Prymnesiales (Haptophyta). Virology 2014;476C:180-8.
59. Kausche GA, Pfankuch E, Ruska H. Die Sichtbarmachung von pflanzlichem Virus im übermikroskop. Naturwissenschaften 1939;27:292-9.
60. Klose T, Herbst DA, Zhu H, et al. A mimivirus enzyme that participates in viral entry. Struct Lond Engl 1993 2015;23:1058-65.
61. Klose T, Kuznetsov YG, Xiao C, et al. The three-dimensional structure of Mimivirus. Intervirology 2010;53:268-73.
62. Korn ED, Weisman RA. Phagocytosis of latex beads by Acanthamoeba. II. Electron microscopic study of the initial events. J Cell Biol 1967;34:219-27.
63. Kuznetsov YG, Klose T, Rossmann M, et al. Morphogenesis of mimivirus and its viral factories: an atomic force microscopy study of infected cells. J Virol 2013;87:11200-13.
64. Kuznetsov YG, Xiao C, Sun S, et al. Atomic force microscopy investigation of the giant mimivirus. Virology 2010;404:127-37.
65. La Scola B, Audic S, Robert C, et al. A giant virus in amoebae. Science 2003;299:2033.
66. La Scola B, Campocasso A, N'Dong R, et al. Tentative characterization of new environmental giant viruses by MALDI-TOF mass spectrometry. Intervirology 2010;53:344-53.
67. La Scola B, Desnues C, Pagnier I, et al. The virophage as a unique parasite of the giant mimivirus. Nature 2008;455:100-4.
68. Larsen JB, Larsen A, Bratbak G, et al. Phylogenetic analysis of members of the Phycodnaviridae virus family, using amplified fragments of the major capsid protein gene. Appl Environ Microb 2008;74:3048-57.
69. Lartigue A, Burlat B, Coutard B, et al. The megavirus chilensis Cu, Zn-superoxide dismutase: the first viral structure of a typical cellular copper chaperone-independent hyperstable dimeric enzyme. J Virol 2015;89:824-32.
70. Legendre M, Arslan D, Abergel C, et al. Genomics of Megavirus and the elusive fourth domain of Life. Commun Integr Biol 2012;5:102-6.
71. Legendre M, Audic S, Poirot O, et al. mRNA deep sequencing reveals 75 new genes and a complex transcriptional landscape in Mimivirus. Genome Res 2010;20:664-74.
72. Legendre M, Bartoli J, Shmakova L, et al. Thirty-thousand-yearold distant relative of giant icosahedral DNA viruses with a pandoravirus morphology. P Natl Acad Sci USA 2014;111: 4274-9.
73. Legendre M, Lartigue A, Bertaux L, et al. In-depth study of Mollivirus sibericum, a new 30, 000-y-old giant virus infecting Acanthamoeba. Proc Natl Acad Sci USA 2015, pii: 201510795.
74. Legendre M, Santini S, Rico A, et al. Breaking the 1000-gene barrier for Mimivirus using ultra-deep genome and transcriptome sequencing. Virol J 2011;8:99.
75. Luther KB, Hülsmeier AJ, Schegg B, et al. Mimivirus collagen is modified by bifunctional lysyl hydroxylase and glycosyltransferase enzyme. J Biol Chem 2011;286:43701-9.
76. Lwoff A. The concept of virus. J Gen Microbiol 1957;17:239-53.
77. Lwoff A, Tournier P. The classification of viruses. Annu Rev Microbiol 1966;20:45-74.
78. Martínez-Cano DJ, Reyes-Prieto M, Martínez-Romero E, et al. Evolution of small prokaryotic genomes. Front Microbiol 2014;5:742.
79. Michel R, Müller KD, Schmid EN, et al. Endocytobiont KC5/2 induces transformation into sol-like cytoplasm of its host Acanthamoeba sp. as substrate for its own development. Parasitol Res 2003a;90:52-6.
80. Michel R, Schmid EN, Hoffmann R, et al. Endoparasite KC5/2 encloses large areas of sol-like cytoplasm within Acanthamoebae. Normal behavior or aberration? Parasitol Res 2003b;91:265-6.
81. Mira A, Ochman H, Moran NA. Deletional bias and the evolution of bacterial genomes. Trends Genet TIG 2001;17:589-96.
82. Mizuno CM, Rodriguez-Valera F, Kimes NE, et al. Expanding the marine virosphere using metagenomics. PLoS Genet 2013;9:e1003987.
83. Moran NA. Accelerated evolution and Muller's rachet in endosymbiotic bacteria. P Natl Acad Sci USA 1996;93:2873-8.
84. Moreira D, Brochier-Armanet C. Giant viruses, giant chimeras: the multiple evolutionary histories of Mimivirus genes. BMC Evol Biol 2008;8:12.
85. Moreira D, López-García P. Ten reasons to exclude viruses from the tree of life. Nat Rev Microbiol 2009;7:306-11.
86. Morris JJ, Lenski RE, Zinser ER. The Black Queen Hypothesis: evolution of dependencies through adaptive gene loss. mBio 2012;3: pii: e00036-12.
87. Mozar M, Claverie J-M. Expanding the Mimiviridae family using asparagine synthase as a sequence bait. Virology 2014;466-467:112-22.
88. Mutsafi Y, Fridmann-Sirkis Y, Milrot E, et al. Infection cycles of large DNA viruses: emerging themes and underlying questions. Virology 2014;466-467:3-14.
89. Mutsafi Y, Shimoni E, Shimon A, et al. Membrane assembly during the infection cycle of the giant Mimivirus. PLoS Pathog 2013;9:e1003367.
90. Mutsafi Y, Zauberman N, Sabanay I, et al. Vaccinia-like cytoplasmic replication of the giant Mimivirus. P Natl Acad Sci USA 2010;107:5978-82.
91. Ogata H, Raoult D, Claverie J-M. A new example of viral intein in Mimivirus. Virol J 2005;2:8.
92. Ogata H, Ray J, Toyoda K, et al. Two new subfamilies of DNA mismatch repair proteins (MutS) specifically abundant in the marine environment. ISME J 2011;5:1143-51.
93. Parakkottil Chothi M, Duncan GA, Armirotti A, et al. Identification of an L-rhamnose synthetic pathway in two nucleocytoplasmic large DNA viruses. J Virol 2010;84:8829-38.
94. Philippe N, Legendre M, Doutre G, et al. Pandoraviruses: amoeba viruses with genomes up to 2.5 Mb reaching that of parasitic eukaryotes. Science 2013;341:281-6.
95. Piacente F, Bernardi C, Marin M, et al. Characterization of a UDPN-acetylglucosamine biosynthetic pathway encoded by the giant DNA virus Mimivirus. Glycobiology 2014a;24:51-61.
96. Piacente F, De Castro C, Jeudy S, et al. Giant virus Megavirus chilensis encodes the biosynthetic pathway for uncommon acetamido sugars. J Biol Chem 2014b;289:24428-39.
97. Piacente F, Marin M, Molinaro A, et al. Giant DNA virus mimivirus encodes pathway for biosynthesis of unusual sugar 4-amino-4, 6-dideoxy-D-glucose (Viosamine). J Biol Chem 2012;287:3009-18.
98. Poulin R. Are there general laws in parasite ecology? Parasitology 2007;134:763-76.
99. Priet S, Lartigue A, Debart F, et al. mRNA maturation in giant viruses: variation on a theme. Nucleic Acids Res 2015; 43:3776-88.
100. Raoult D, Audic S, Robert C, et al. The 1.2-megabase genome sequence of Mimivirus. Science 2004;306:1344-50.
101. Raoult D, Forterre P. Redefining viruses: lessons from Mimivirus. Nat Rev Microbiol 2008;6:315-9.
102. Raoult D, La Scola B, Birtles R. The discovery and characterization of Mimivirus, the largest known virus and putative pneumonia agent. Clin Infect Dis 2007;45:95-102.
103. Renesto P, Abergel C, Decloquement P, et al. Mimivirus giant particles incorporate a large fraction of anonymous and unique gene products. J Virol 2006;80:11678-85.
104. Roberts KL, Smith GL Vaccinia virus morphogenesis and dissemination. Trends Microbiol 2008;16:472-9.
105. Rowbotham TJ. Isolation of Legionella pneumophila from clinical specimens via amoebae, and the interaction of those and other isolates with amoebae. J Clin Pathol 1983;36:978-86.
106. Ruiz-Saenz J, Rodas JD. Viruses, virophages, and their living nature. Acta Virol 2010;54:85-90.
107. Saadi H, Pagnier I, Colson P, et al. First isolation of Mimivirus in a patient with pneumonia. Clin Infect Dis 2013a;57:e127-34.
108. Saadi H, Reteno D-GI, Colson P, et al. Shan virus: a newmimivirus isolated from the stool of a Tunisian patient with pneumonia. Intervirology 2013b;56:424-9.
109. Santini S, Jeudy S, Bartoli J, et al. Genome of Phaeocystis globosa virus PgV-16T highlights the common ancestry of the largest known DNA viruses infecting eukaryotes. P Natl Acad Sci USA 2013;110:10800-5.
110. Sawyer TK, Visvesvara GS, Harke BA. Pathogenic amoebas from brackish and ocean sediments, with a description of Acanthamoeba hatchetti, n. sp. Science 1977;196:1324-5.
111. Scheid P, Balczun C, Schaub GA. Some secrets are revealed: parasitic keratitis amoebae as vectors of the scarcely described pandoraviruses to humans. Parasitol Res 2014;113:3759-64.
112. Scheid P, Hauröder B, Michel R. Investigations of an extraordinary endocytobiont in Acanthamoeba sp.: development and replication. Parasitol Res 2010;106:1371-7.
113. Scheid P, Zöller L, Pressmar S, et al. An extraordinary endocytobiont in Acanthamoeba sp. isolated from a patient with keratitis. Parasitol Res 2008;102:945-50.
114. Seibert MM, Ekeberg T, Maia FRNC, et al. Single mimivirus particles intercepted and imaged with an X-ray laser. Nature 2011;470:78-81.
115. Sloan DB, Nakabachi A, Richards S, et al. Parallel histories of horizontal gene transfer facilitated extreme reduction of endosymbiont genomes in sap-feeding insects. Mol Biol Evol 2014;31:857-71.
116. Suárez C, Welsch S, Chlanda P, et al. Open membranes are the precursors for assembly of large DNA viruses. Cell Microbiol 2013;15:1883-95.
117. Suhre K, Audic S, Claverie J-M. Mimivirus gene promoters exhibit an unprecedented conservation among all eukaryotes. P Natl Acad Sci USA 2005;102:14689-93.
118. Suzan-Monti M, La Scola B, Raoult D. Genomic and evolutionary aspects of Mimivirus. Virus Res 2006;117:145-55.
119. Suzan-Monti M, Scola BL, Barrassi L, et al. Ultrastructural characterization of the giant volcano-like virus factory of Acanthamoeba polyphaga Mimivirus. PLoS One 2007;2:e328.
120. Thai V, Renesto P, Fowler CA, et al. Structural, biochemical, and in vivo characterization of the first virally encoded cyclophilin from the Mimivirus. J Mol Biol 2008;378:71-86.
121. Thomas V, Bertelli C, Collyn F, et al. Lausannevirus, a giant amoebal virus encoding histone doublets. Environ Microbiol 2011;13:1454-66.
122. Thomas V, Loret J-F, Jousset M, et al. Biodiversity of amoebae and amoebae-resisting bacteria in a drinking water treatment plant. Environ Microbiol 2008;10:2728-45.
123. Tiwari R, Chakraborty S, Dhama K, et al. Wonder world of phages: potential biocontrol agents safeguarding biosphere and health of animals and humans-current scenario and perspectives. Pak J Biol Sci 2014;17:316-28.
124. Tulman ER, Afonso CL, Lu Z, et al. The genome of canarypox virus. J Virol 2004;78:353-66.
125. Tulman ER, Delhon GA, Ku BK, et al. African Swine fever virus. In: Etten JLV (ed.). Lesser Known Large dsDNA Viruses. Berlin, Heidelberg: Springer, 2009, 43-87.
126. Van Etten JL, Dunigan DD Chloroviruses: not your everyday plant virus. Trends Plant Sci 2012;17:1-8.
127. Vanspauwen MJ, Schnabel RM, Bruggeman CA, et al. Mimivirus is not a frequent cause of ventilator-associated pneumonia in critically ill patients. J Med Virol 2013;85:1836-41.
128. Villarreal LP, Witzany G. Viruses are essential agents within the roots and stem of the tree of life. J Theor Biol 2010;262:698-710.
129. Williams TA, Embley TM, Heinz E. Informational gene phylogenies do not support a fourth domain of life for nucleocytoplasmic large DNA viruses. PloS One 2011;6:e21080.
130. Wilson WH, Schroeder DC, Allen MJ, et al. Complete genome sequence and lytic phase transcription profile of a Coccolithovirus. Science 2005;309:1090-2.
131. Wilson WH, Gilg IC, Duarte A, et al. Development of DNA mismatch repair gene, MutS, as a diagnostic marker for detection and phylogenetic analysis of algal Megaviruses. Virology 2014;466-467:123-8.
132. Xiao C, Kuznetsov YG, Sun S, et al. Structural studies of the giant mimivirus. PLoS Biol 2009;7:e1000092.
133. Yau S, Lauro FM, DeMaere MZ, et al. Virophage control of antarctic algal host-virus dynamics. P Natl Acad Sci USA 2011;108:6163-8.
134. Yoosuf N, Pagnier I, Fournous G, et al. Complete genome sequence of Courdo11 virus, a member of the family Mimiviridae. Virus Genes 2014a;48:218-23.
135. Yoosuf N, Pagnier I, Fournous G, et al. Draft genome sequences of Terra1 and Terra2 viruses, new members of the family Mimiviridae isolated from soil. Virology 2014b;452-453:125-32.
136. Yoosuf N, Yutin N, Colson P, et al. Related giant viruses in distant locations and different habitats: Acanthamoeba polyphaga moumouvirus represents a third lineage of the Mimiviridae that is close to the megavirus lineage. Genome Biol Evol 2012;4:1324-30.
137. Yutin N, Koonin EV. Pandoraviruses are highly derived phycodnaviruses. Biol Direct 2013;8:25.
138. Yutin N, Wolf YI, Koonin EV. Origin of giant viruses from smaller DNA viruses not froma fourth domain of cellular life. Virology 2014;466-467:38-52.
139. Yutin N, Wolf YI, Raoult D, et al. Eukaryotic large nucleocytoplasmic DNA viruses: clusters of orthologous genes and reconstruction of viral genome evolution. Virol J 2009;6:223.
140. Zauberman N, Mutsafi Y, Halevy DB, et al. Distinct DNA exit and packaging portals in the virus Acanthamoeba polyphaga mimivirus. PLoS Biol 2008;6:e114.
141. Zhou J, Sun D, Childers A, et al. Three novel virophage genomes discovered from Yellowstone Lake metagenomes. J Virol 2015;89:1278-85.