Evolution of an archaeal virus nucleocapsid protein from the CRISPR-associated Cas4 nuclease

Biology Direct

Eugene V. Koonin²  David Prangishvili¹  Virginija Cvirkaite-Krupovic¹  Mart Krupovic¹ 

[1]Department of Microbiology, Unité Biologie Moléculaire du Gène chez les Extrêmophiles, Institut Pasteur, Paris 75015, France

[2]National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda 20894, MD, USA

关键词: Archaea viruses;    Virus origin;    Nucleocapsid;    Capsid proteins;    Virus evolution;   

Others  :  1230607
DOI  :  10.1186/s13062-015-0093-2

 received in 2015-09-04, accepted in 2015-10-26,  发布年份 2015

【 摘 要 】

Many proteins of viruses infecting hyperthermophilic Crenarchaeota have no detectable homologs in current databases, hampering our understanding of viral evolution. We used sensitive database search methods and structural modeling to show that a nucleocapsid protein (TP1) of Thermoproteus tenax virus 1 (TTV1) is a derivative of the Cas4 nuclease, a component of the CRISPR-Cas adaptive immunity system that is encoded also by several archaeal viruses. In TTV1, the Cas4 gene was split into two, with the N-terminal portion becoming TP1, and lost some of the catalytic amino acid residues, apparently resulting in the inactivation of the nuclease. To our knowledge, this is the first described case of exaptation of an enzyme for a virus capsid protein function.

【 授权许可】

   
2015 Krupovic et al.

【 图 表 】

Fig. 1.

【 参考文献 】

• [1]Koonin EV, Senkevich TG, Dolja VV: The ancient Virus World and evolution of cells. Biol Direct 2006, 1:29. BioMed Central Full Text
• [2]Krupovic M, Bamford DH: Order to the viral universe. J Virol 2010, 84(24):12476-12479.
• [3]Raoult D, Forterre P: Redefining viruses: lessons from Mimivirus. Nat Rev Microbiol 2008, 6(4):315-319.
• [4]Forterre P, Krupovic M, Prangishvili D: Cellular domains and viral lineages. Trends Microbiol 2014, 22(10):554-558.
• [5]Jalasvuori M, Koonin EV: Classification of prokaryotic genetic replicators: between selfishness and altruism. Ann N Y Acad Sci 2015, 1341:96-105.
• [6]Krupovic M, Bamford DH, Koonin EV: Conservation of major and minor jelly-roll capsid proteins in Polinton (Maverick) transposons suggests that they are bona fide viruses. Biol Direct 2014, 9(1):6. BioMed Central Full Text
• [7]Jalasvuori M, Mattila S, Hoikkala V: Chasing the origin of viruses: capsid-forming genes as a life-saving preadaptation within a community of early replicators. PLoS One 2015, 10(5):e0126094.
• [8]Krupovic M, Bamford DH: Double-stranded DNA viruses: 20 families and only five different architectural principles for virion assembly. Curr Opin Virol 2011, 1(2):118-124.
• [9]Krupovic M, Quemin ER, Bamford DH, Forterre P, Prangishvili D: Unification of the globally distributed spindle-shaped viruses of the Archaea. J Virol 2014, 88(4):2354-2358.
• [10]Abrescia NG, Bamford DH, Grimes JM, Stuart DI: Structure unifies the viral universe. Annu Rev Biochem 2012, 81:795-822.
• [11]DiMaio F, Yu X, Rensen E, Krupovic M, Prangishvili D, Egelman EH: Virology. A virus that infects a hyperthermophile encapsidates A-form DNA. Science 2015, 348(6237):914-917.
• [12]Koonin EV, Dolja VV, Krupovic M: Origins and evolution of viruses of eukaryotes: the ultimate modularity. Virology 2015, 479–480:2-25.
• [13]Janekovic D, Wunderl S, Holz I, Zillig W, Gierl A, Neumann H: TTV1, TTV2 and TTV3, a family of viruses of the extremely thermophilic, anaerobic, sulfur reducing archaebacterium Thermoproteus tenax. Mol Gen Genet 1983, 192:39-45.
• [14]Reiter WD, Zillig W, Palm P: Archaebacterial viruses. Adv Virus Res 1988, 34:143-188.
• [15]Neumann H, Schwass V, Eckerskorn C, Zillig W: Identification and characterization of the genes encoding three structural proteins of the Thermoproteus tenax virus TTV1. Mol Gen Genet 1989, 217(1):105-110.
• [16]Neumann H, Zillig W: Coat protein TP4 of the virus TTV1: primary structure of the gene and the protein. Nucleic Acids Res 1989, 17(22):9475.
• [17]Prangishvili D, Krupovic M: A new proposed taxon for double-stranded DNA viruses, the order “Ligamenvirales”. Arch Virol 2012, 157(4):791-795.
• [18]Prangishvili D: Archaeal viruses: living fossils of the ancient virosphere? Ann N Y Acad Sci 2015, 1341:35-40.
• [19]Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25(17):3389-3402.
• [20]Söding J: Protein homology detection by HMM-HMM comparison. Bioinformatics 2005, 21(7):951-960.
• [21]Makarova KS, Haft DH, Barrangou R, Brouns SJ, Charpentier E, Horvath P, Moineau S, Mojica FJ, Wolf YI, Yakunin AF, et al.: Evolution and classification of the CRISPR-Cas systems. Nat Rev Microbiol 2011, 9(6):467-477.
• [22]Makarova KS, Wolf YI, Koonin EV: The basic building blocks and evolution of CRISPR-CAS systems. Biochem Soc Trans 2013, 41(6):1392-1400.
• [23]Koonin EV, Krupovic M: Evolution of adaptive immunity from transposable elements combined with innate immune systems. Nat Rev Genet 2015, 16(3):184-192.
• [24]Koonin EV, Makarova KS: CRISPR-Cas: evolution of an RNA-based adaptive immunity system in prokaryotes. RNA Biol 2013, 10(5):679-686.
• [25]Makarova KS, Aravind L, Wolf YI, Koonin EV: Unification of Cas protein families and a simple scenario for the origin and evolution of CRISPR-Cas systems. Biol Direct 2011, 6:38. BioMed Central Full Text
• [26]Lemak S, Beloglazova N, Nocek B, Skarina T, Flick R, Brown G, Popovic A, Joachimiak A, Savchenko A, Yakunin AF: Toroidal structure and DNA cleavage by the CRISPR-associated [4Fe-4S] cluster containing Cas4 nuclease SSO0001 from Sulfolobus solfataricus. J Am Chem Soc 2013, 135(46):17476-17487.
• [27]Lemak S, Nocek B, Beloglazova N, Skarina T, Flick R, Brown G, Joachimiak A, Savchenko A, Yakunin AF: The CRISPR-associated Cas4 protein Pcal_0546 from Pyrobaculum calidifontis contains a [2Fe-2S] cluster: crystal structure and nuclease activity. Nucleic Acids Res 2014, 42(17):11144-11155.
• [28]Krupovic M, Makarova KS, Forterre P, Prangishvili D, Koonin EV: Casposons: a new superfamily of self-synthesizing DNA transposons at the origin of prokaryotic CRISPR-Cas immunity. BMC Biol 2014, 12:36. BioMed Central Full Text
• [29]Guo Y, Kragelund BB, White MF, Peng X: Functional characterization of a conserved archaeal viral operon revealing single-stranded DNA binding, annealing and nuclease activities. J Mol Biol 2015, 427(12):2179-2191.
• [30]Hooton SP, Connerton IF: Campylobacter jejuni acquire new host-derived CRISPR spacers when in association with bacteriophages harboring a CRISPR-like Cas4 protein. Front Microbiol 2014, 5:744.
• [31]Prangishvili D, Koonin EV, Krupovic M: Genomics and biology of Rudiviruses, a model for the study of virus-host interactions in Archaea. Biochem Soc Trans 2013, 41(1):443-450.
• [32]Gardner AF, Prangishvili D, Jack WE: Characterization of Sulfolobus islandicus rod-shaped virus 2 gp19, a single-strand specific endonuclease. Extremophiles 2011, 15(5):619-624.
• [33]Gould SJ, Vrba ES: Exaptation - a missing term in the science of form. Paleobiology 1982, 8(1):4-15.
• [34]Kazlauskas D, Venclovas C: Herpesviral helicase-primase subunit UL8 is inactivated B-family polymerase. Bioinformatics 2014, 30(15):2093-2097.
• [35]Yutin N, Faure G, Koonin EV, Mushegian AR: Chordopoxvirus protein F12 implicated in enveloped virion morphogenesis is an inactivated DNA polymerase. Biol Direct 2014, 9(1):22. BioMed Central Full Text
• [36]Pei J, Grishin NV: PROMALS3D: multiple protein sequence alignment enhanced with evolutionary and three-dimensional structural information. Methods Mol Biol 2014, 1079:263-271.
• [37]Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ: Jalview Version 2--a multiple sequence alignment editor and analysis workbench. Bioinformatics 2009, 25(9):1189-1191.
• [38]Marti-Renom MA, Stuart AC, Fiser A, Sanchez R, Melo F, Sali A: Comparative protein structure modeling of genes and genomes. Annu Rev Biophys Biomol Struct 2000, 29:291-325.
• [39]Wiederstein M, Sippl MJ: ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Res 2007, 35(Web Server issue):W407-410.
• [40]Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE: UCSF Chimera—a visualization system for exploratory research and analysis. J Comput Chem 2004, 25(13):1605-1612.