Lausannevirus, a giant amoebal virus encoding histone doublets

Summary Large viruses infecting algae or amoebae belong to the NucleoCytoplasmic Large DNA Viruses (NCLDV) and present genotypic and phenotypic characteristics that have raised major interest among microbiologists. Here, we describe a new large virus discovered in Acanthamoeba castellanii co‐culture...

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Veröffentlicht in:	Environmental microbiology Jg. 13; H. 6; S. 1454 - 1466
Hauptverfasser:	Thomas, Vincent, Bertelli, Claire, Collyn, François, Casson, Nicola, Telenti, Amalio, Goesmann, Alexander, Croxatto, Antony, Greub, Gilbert
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	Oxford, UK Blackwell Publishing Ltd 01.06.2011
Schlagworte:	Acanthamoeba castellanii Acanthamoeba castellanii - virology Amoeba Base Sequence Biological Evolution classification coculture DNA Viruses DNA Viruses - classification DNA Viruses - genetics DNA Viruses - isolation & purification genes genetics Genome, Viral histones Histones - genetics host range Host Specificity isolation & purification Mimivirus Molecular Sequence Data Phylogeny Rivers Rivers - virology virology viruses Water Microbiology
ISSN:	1462-2912, 1462-2920, 1462-2920
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Abstract	Summary Large viruses infecting algae or amoebae belong to the NucleoCytoplasmic Large DNA Viruses (NCLDV) and present genotypic and phenotypic characteristics that have raised major interest among microbiologists. Here, we describe a new large virus discovered in Acanthamoeba castellanii co‐culture of an environmental sample. The virus, referred to as Lausannevirus, has a very limited host range, infecting Acanthamoeba spp. but being unable to infect other amoebae and mammalian cell lines tested. Within A. castellanii, this icosahedral virus of about 200 nm exhibits a development cycle similar to Mimivirus, with an eclipse phase 2 h post infection and a logarithmic growth leading to amoebal lysis in less than 24 h. The 346 kb Lausannevirus genome presents similarities with the recently described Marseillevirus, sharing 89% of genes, and thus belongs to the same family as confirmed by core gene phylogeny. Interestingly, Lausannevirus and Marseillevirus genomes both encode three proteins with predicted histone folds, including two histone doublets, that present similarities to eukaryotic and archaeal histones. The discovery of Lausannevirus and the analysis of its genome provide some insight in the evolution of these large amoebae‐infecting viruses.
AbstractList	Large viruses infecting algae or amoebae belong to the NucleoCytoplasmic Large DNA Viruses (NCLDV) and present genotypic and phenotypic characteristics that have raised major interest among microbiologists. Here, we describe a new large virus discovered in Acanthamoeba castellanii co-culture of an environmental sample. The virus, referred to as Lausannevirus, has a very limited host range, infecting Acanthamoeba spp. but being unable to infect other amoebae and mammalian cell lines tested. Within A. castellanii, this icosahedral virus of about 200 nm exhibits a development cycle similar to Mimivirus, with an eclipse phase 2 h post infection and a logarithmic growth leading to amoebal lysis in less than 24 h. The 346 kb Lausannevirus genome presents similarities with the recently described Marseillevirus, sharing 89% of genes, and thus belongs to the same family as confirmed by core gene phylogeny. Interestingly, Lausannevirus and Marseillevirus genomes both encode three proteins with predicted histone folds, including two histone doublets, that present similarities to eukaryotic and archaeal histones. The discovery of Lausannevirus and the analysis of its genome provide some insight in the evolution of these large amoebae-infecting viruses. Summary Large viruses infecting algae or amoebae belong to the NucleoCytoplasmic Large DNA Viruses (NCLDV) and present genotypic and phenotypic characteristics that have raised major interest among microbiologists. Here, we describe a new large virus discovered in Acanthamoeba castellanii co‐culture of an environmental sample. The virus, referred to as Lausannevirus, has a very limited host range, infecting Acanthamoeba spp. but being unable to infect other amoebae and mammalian cell lines tested. Within A. castellanii, this icosahedral virus of about 200 nm exhibits a development cycle similar to Mimivirus, with an eclipse phase 2 h post infection and a logarithmic growth leading to amoebal lysis in less than 24 h. The 346 kb Lausannevirus genome presents similarities with the recently described Marseillevirus, sharing 89% of genes, and thus belongs to the same family as confirmed by core gene phylogeny. Interestingly, Lausannevirus and Marseillevirus genomes both encode three proteins with predicted histone folds, including two histone doublets, that present similarities to eukaryotic and archaeal histones. The discovery of Lausannevirus and the analysis of its genome provide some insight in the evolution of these large amoebae‐infecting viruses. Large viruses infecting algae or amoebae belong to the NucleoCytoplasmic Large DNA Viruses (NCLDV) and present genotypic and phenotypic characteristics that have raised major interest among microbiologists. Here, we describe a new large virus discovered in Acanthamoeba castellanii co-culture of an environmental sample. The virus, referred to as Lausannevirus, has a very limited host range, infecting Acanthamoeba spp. but being unable to infect other amoebae and mammalian cell lines tested. Within A. castellanii, this icosahedral virus of about 200 nm exhibits a development cycle similar to Mimivirus, with an eclipse phase 2 h post infection and a logarithmic growth leading to amoebal lysis in less than 24 h. The 346 kb Lausannevirus genome presents similarities with the recently described Marseillevirus, sharing 89% of genes, and thus belongs to the same family as confirmed by core gene phylogeny. Interestingly, Lausannevirus and Marseillevirus genomes both encode three proteins with predicted histone folds, including two histone doublets, that present similarities to eukaryotic and archaeal histones. The discovery of Lausannevirus and the analysis of its genome provide some insight in the evolution of these large amoebae-infecting viruses.Large viruses infecting algae or amoebae belong to the NucleoCytoplasmic Large DNA Viruses (NCLDV) and present genotypic and phenotypic characteristics that have raised major interest among microbiologists. Here, we describe a new large virus discovered in Acanthamoeba castellanii co-culture of an environmental sample. The virus, referred to as Lausannevirus, has a very limited host range, infecting Acanthamoeba spp. but being unable to infect other amoebae and mammalian cell lines tested. Within A. castellanii, this icosahedral virus of about 200 nm exhibits a development cycle similar to Mimivirus, with an eclipse phase 2 h post infection and a logarithmic growth leading to amoebal lysis in less than 24 h. The 346 kb Lausannevirus genome presents similarities with the recently described Marseillevirus, sharing 89% of genes, and thus belongs to the same family as confirmed by core gene phylogeny. Interestingly, Lausannevirus and Marseillevirus genomes both encode three proteins with predicted histone folds, including two histone doublets, that present similarities to eukaryotic and archaeal histones. The discovery of Lausannevirus and the analysis of its genome provide some insight in the evolution of these large amoebae-infecting viruses.
Author	Thomas, Vincent Greub, Gilbert Telenti, Amalio Collyn, François Casson, Nicola Croxatto, Antony Bertelli, Claire Goesmann, Alexander
Author_xml	– sequence: 1 givenname: Vincent surname: Thomas fullname: Thomas, Vincent organization: Institute of Microbiology, University Hospital Center and University of Lausanne, 1011 Lausanne, Switzerland – sequence: 2 givenname: Claire surname: Bertelli fullname: Bertelli, Claire organization: Institute of Microbiology, University Hospital Center and University of Lausanne, 1011 Lausanne, Switzerland – sequence: 3 givenname: François surname: Collyn fullname: Collyn, François organization: Institute of Microbiology, University Hospital Center and University of Lausanne, 1011 Lausanne, Switzerland – sequence: 4 givenname: Nicola surname: Casson fullname: Casson, Nicola organization: Institute of Microbiology, University Hospital Center and University of Lausanne, 1011 Lausanne, Switzerland – sequence: 5 givenname: Amalio surname: Telenti fullname: Telenti, Amalio organization: Institute of Microbiology, University Hospital Center and University of Lausanne, 1011 Lausanne, Switzerland – sequence: 6 givenname: Alexander surname: Goesmann fullname: Goesmann, Alexander organization: Center for Biotechnology (CeBiTec), Bielefeld University, 33501 Bielefeld, Germany – sequence: 7 givenname: Antony surname: Croxatto fullname: Croxatto, Antony organization: Institute of Microbiology, University Hospital Center and University of Lausanne, 1011 Lausanne, Switzerland – sequence: 8 givenname: Gilbert surname: Greub fullname: Greub, Gilbert email: gilbert.greub@chuv.ch organization: Institute of Microbiology, University Hospital Center and University of Lausanne, 1011 Lausanne, Switzerland
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J Mol Biol 194: 557-564. Fitzgerald, L.A., Graves, M.V., Li, X., Feldblyum, T., Nierman, W.C., and Van Etten, J.L. (2007a) Sequence and annotation of the 369-kb NY-2A and the 345-kb AR158 viruses that infect Chlorella NC64A. Virology 358: 472-484. La Scola, B., Desnues, C., Pagnier, I., Robert, C., Barrassi, L., Fournous, G., et al. (2008) The virophage as a unique parasite of the giant mimivirus. Nature 455: 100-104. Ronquist, F., and Huelsenbeck, J.P. (2003) MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574. Bendtsen, J.D., Nielsen, H., von Heijne, G., and Brunak, S. (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340: 783-795. La Scola, B., Campocasso, A., N'Dong, R., Fournous, G., Barrassi, L., Flaudrops, C., and Raoult, D. (2010) Tentative characterization of new environmental giant viruses by MALDI-TOF mass spectrometry. Intervirology 53: 344-353. Coulon, C., Collignon, A., McDonnell, G., and Thomas, V. (2010) Resistance of Acanthamoeba cysts to disinfection treatments used in health care settings. J Clin Microbiol 48: 2689-2697. Badger, J.H., and Olsen, G.J. (1999) CRITICA: coding region identification tool invoking comparative analysis. Mol Biol Evol 16: 512-524. Khan, M., La Scola, B., Lepidi, H., and Raoult, D. (2007) Pneumonia in mice inoculated experimentally with Acanthamoeba polyphaga mimivirus. Microb Pathog 42: 56-61. Thomas, V., and Greub, G. (2010) Amoebae/amoebal symbionts genetic transfers: lessons from giant viruses neighbours. Intervirology 53: 254-267. Tarutani, K., Nagasaki, K., Itakura, S., and Yamaguchi, M. (2001) Isolation of a virus infecting the novel shellfish-killing dinoflagellate Heterocapsa circularisquama. Aquat Microb Ecol 23: 103-111. Van Etten, J.L. (2003) Unusual life style of giant chlorella viruses. Annu Rev Genet 37: 153-195. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215: 403-410. Lamoth, F., and Greub, G. (2010) Amoebal pathogens as emerging causal agents of pneumonia. FEMS Microbiol Rev 34: 260-280. Guindon, S., and Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704. De Silva, F.S., and Moss, B. (2008) Effects of vaccinia virus uracil DNA glycosylase catalytic site and deoxyuridine triphosphatase deletion mutations individually and together on replication in active and quiescent cells and pathogenesis in mice. Virol J 5: 145. Perler, F.B. (2002) InBase: the Intein Database. Nucleic Acids Res 30: 383-384. Talbert, P.B., and Henikoff, S. (2010) Histone variants - ancient wrap artists of the epigenome. Nat Rev Mol Cell Biol 11: 264-275. Cheng, C.H., Liu, S.M., Chow, T.Y., Hsiao, Y.Y., Wang, D.P., Huang, J.J., and Chen, H.H. (2002) Analysis of the complete genome sequence of the Hz-1 virus suggests that it is related to members of the Baculoviridae. J Virol 76: 9024-9034. Gordon, D., Abajian, C., and Green, P. (1998) Consed: a graphical tool for sequence finishing. Genome Res 8: 195-202. Nagasaki, K., Shirai, Y., Tomaru, Y., Nishida, K., and Pietrokovski, S. (2005) Algal viruses with distinct intraspecies host specificities include identical intein elements. Appl Environ Microbiol 71: 3599-3607. de Souza, R.F., Iyer, L.M., and Aravind, L. (2010) Diversity and evolution of chromatin proteins encoded by DNA viruses. Biochim Biophys Acta 1799: 302-318. Raoult, D., Renesto, P., and Brouqui, P. (2006) Laboratory infection of a technician by mimivirus. Ann Intern Med 144: 702-703. Linke, B., McHardy, A.C., Neuweger, H., Krause, L., and Meyer, F. (2006) REGANOR: a gene prediction server for prokaryotic genomes and a database of high quality gene predictions for prokaryotes. Appl Bioinformatics 5: 193-198. Moreira, D., and Brochier-Armanet, C. (2008) Giant viruses, giant chimeras: the multiple evolutionary histories of Mimivirus genes. BMC Evol Biol 8: 12. Raoult, D., Audic, S., Robert, C., Abergel, C., Renesto, P., Ogata, H., et al. (2004) The 1.2-megabase genome sequence of Mimivirus. Science 306: 1344-1350. Moliner, C., Fournier, P.E., and Raoult, D. (2010) Genome analysis of microorganisms living in amoebae reveals a melting pot of evolution. FEMS Microbiol Rev 34: 281-294. Croxatto, A., and Greub, G. (2010) Early intracellular trafficking of Waddlia chondrophila in human macrophages. Microbiology 156: 340-355. Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797. Sogayar, M.I., and Gregorio, E.A. (1986) Cytoplasmic inclusions in Giardia: an electron microscopy study. Ann Trop Med Parasitol 80: 49-52. Greub, G., and Raoult, D. (2004) Microorganisms resistant to free-living amoebae. Clin Microbiol Rev 17: 413-433. Cubonova, L., Sandman, K., Hallam, S.J., Delong, E.F., and Reeve, J.N. (2005) Histones in crenarchaea. 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Nucleic Acids Res 31: 2187-2195. Sandman, K., and Reeve, J.N. (2006) Archaeal histones and the origin of the histone fold. Curr Opin Microbiol 9: 520-525. Suzan-Monti, M., La Scola, B., and Raoult, D. (2006) Genomic and evolutionary aspects of Mimivirus. V 2010; 11 2010; 53 2010; 18 2002; 56 2008; 8 2008; 5 2008; 3 2003; 19 2008; 4 2001; 305 2003; 52 2004; 32 2009; 11 1987; 194 1986; 80 1990; 215 2006; 23 2005; 187 1991; 45 2002; 83 1999; 16 2010; 156 2005; 71 1998; 93 2007; 23 2007; 24 2010; 34 1997; 179 2004; 340 2007a; 358 2002; 30 1997; 25 2002; 76 2006; 9 2010; 1799 2006; 5 2003; 37 1997; 27 2008; 10 2004; 306 2001; 23 2006; 117 2003; 299 2003; 31 2010; 48 2004; 17 2007b; 358 2008; 89 2005; 97 1962; 26 1999; 73 2008; 136 2008; 455 2007; 42 1998; 7 2006; 144 2001; 75 2009; 106 1998; 8 e_1_2_5_27_1 e_1_2_5_25_1 e_1_2_5_48_1 e_1_2_5_23_1 e_1_2_5_46_1 e_1_2_5_21_1 e_1_2_5_44_1 e_1_2_5_65_1 e_1_2_5_29_1 e_1_2_5_61_1 e_1_2_5_63_1 e_1_2_5_42_1 e_1_2_5_40_1 e_1_2_5_15_1 e_1_2_5_38_1 Sogayar M.I. (e_1_2_5_49_1) 1986; 80 e_1_2_5_17_1 e_1_2_5_36_1 e_1_2_5_59_1 e_1_2_5_9_1 e_1_2_5_11_1 e_1_2_5_34_1 e_1_2_5_57_1 e_1_2_5_7_1 e_1_2_5_13_1 e_1_2_5_32_1 e_1_2_5_55_1 e_1_2_5_3_1 e_1_2_5_19_1 e_1_2_5_30_1 e_1_2_5_53_1 Baldo A.M. (e_1_2_5_5_1) 1999; 73 e_1_2_5_51_1 e_1_2_5_28_1 e_1_2_5_26_1 e_1_2_5_47_1 e_1_2_5_24_1 e_1_2_5_45_1 e_1_2_5_22_1 e_1_2_5_43_1 e_1_2_5_60_1 e_1_2_5_62_1 e_1_2_5_64_1 e_1_2_5_20_1 e_1_2_5_41_1 e_1_2_5_14_1 e_1_2_5_39_1 e_1_2_5_16_1 e_1_2_5_37_1 e_1_2_5_58_1 e_1_2_5_8_1 e_1_2_5_10_1 e_1_2_5_35_1 e_1_2_5_56_1 e_1_2_5_6_1 e_1_2_5_12_1 e_1_2_5_33_1 e_1_2_5_54_1 e_1_2_5_4_1 e_1_2_5_2_1 e_1_2_5_18_1 e_1_2_5_31_1 e_1_2_5_52_1 e_1_2_5_50_1
References_xml	– reference: de Souza, R.F., Iyer, L.M., and Aravind, L. (2010) Diversity and evolution of chromatin proteins encoded by DNA viruses. Biochim Biophys Acta 1799: 302-318. – reference: Raoult, D., Audic, S., Robert, C., Abergel, C., Renesto, P., Ogata, H., et al. (2004) The 1.2-megabase genome sequence of Mimivirus. Science 306: 1344-1350. – reference: Fitzgerald, L.A., Graves, M.V., Li, X., Feldblyum, T., Hartigan, J., and Van Etten, J.L. (2007b) Sequence and annotation of the 314-kb MT325 and the 321-kb FR483 viruses that infect Chlorella Pbi. Virology 358: 459-471. – reference: Cheng, C.H., Liu, S.M., Chow, T.Y., Hsiao, Y.Y., Wang, D.P., Huang, J.J., and Chen, H.H. (2002) Analysis of the complete genome sequence of the Hz-1 virus suggests that it is related to members of the Baculoviridae. J Virol 76: 9024-9034. – reference: Derelle, E., Ferraz, C., Escande, M.L., Eychenie, S., Cooke, R., Piganeau, G., et al. (2008) Life-cycle and genome of OtV5, a large DNA virus of the pelagic marine unicellular green alga Ostreococcus tauri. PLoS ONE 3: e2250. – reference: Cubonova, L., Sandman, K., Hallam, S.J., Delong, E.F., and Reeve, J.N. (2005) Histones in crenarchaea. J Bacteriol 187: 5482-5485. – reference: Gogarten, J.P., Senejani, A.G., Zhaxybayeva, O., Olendzenski, L., and Hilario, E. (2002) Inteins: structure, function, and evolution. Annu Rev Microbiol 56: 263-287. – reference: Suzan-Monti, M., La Scola, B., and Raoult, D. (2006) Genomic and evolutionary aspects of Mimivirus. Virus Res 117: 145-155. – reference: Chen, R., Wang, H., and Mansky, L.M. (2002) Roles of uracil-DNA glycosylase and dUTPase in virus replication. J Gen Virol 83: 2339-2345. – reference: Delcher, A.L., Bratke, K.A., Powers, E.C., and Salzberg, S.L. (2007) Identifying bacterial genes and endosymbiont DNA with Glimmer. 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Snippet	Summary Large viruses infecting algae or amoebae belong to the NucleoCytoplasmic Large DNA Viruses (NCLDV) and present genotypic and phenotypic characteristics... Large viruses infecting algae or amoebae belong to the NucleoCytoplasmic Large DNA Viruses (NCLDV) and present genotypic and phenotypic characteristics that...
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SubjectTerms	Acanthamoeba castellanii Acanthamoeba castellanii - virology Amoeba Base Sequence Biological Evolution classification coculture DNA Viruses DNA Viruses - classification DNA Viruses - genetics DNA Viruses - isolation & purification genes genetics Genome, Viral histones Histones - genetics host range Host Specificity isolation & purification Mimivirus Molecular Sequence Data Phylogeny Rivers Rivers - virology virology viruses Water Microbiology
Title	Lausannevirus, a giant amoebal virus encoding histone doublets
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