1887

Abstract

For most archaeal viruses, the mechanisms of genome replication are poorly understood, while the nature and provenance of their replication proteins are usually unknown. Here we show that replication of the circular double-stranded DNA genome of the halophilic virus SNJ1, a member of the family , is associated with the accumulation of single-stranded replicative intermediates, which is typical of rolling-circle replication. The homologues of RepA, the only enzyme that is indispensable for SNJ1 genome replication, are widespread in archaea and are most closely related to bacterial transposases of the IS and IS family insertion sequences, as opposed to other viral rolling-circle replication initiation proteins. Our results provide insights into the replication mechanism of archaeal viruses and emphasize the evolutionary connection between viruses and other types of mobile genetic elements.

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2018-03-01
2024-03-28
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References

  1. Prangishvili D, Bamford DH, Forterre P, Iranzo J, Koonin EV et al. The enigmatic archaeal virosphere. Nat Rev Microbiol 2017; 15:724–739 [View Article][PubMed]
    [Google Scholar]
  2. Snyder JC, Bolduc B, Young MJ. 40 Years of archaeal virology: expanding viral diversity. Virology 2015; 479-480:369–378 [View Article][PubMed]
    [Google Scholar]
  3. Iranzo J, Krupovic M, Koonin EV. The double-stranded DNA virosphere as a modular hierarchical network of gene sharing. MBio 2016; 7:e00978-16 [View Article][PubMed]
    [Google Scholar]
  4. Krupovic M, Cvirkaite-Krupovic V, Iranzo J, Prangishvili D, Koonin EV. Viruses of archaea: Structural, functional, environmental and evolutionary genomics. Virus Res 2018; 244:181–193 [View Article][PubMed]
    [Google Scholar]
  5. Iranzo J, Koonin EV, Prangishvili D, Krupovic M. Bipartite network analysis of the archaeal virosphere: evolutionary connections between viruses and capsidless mobile elements. J Virol 2016; 90:11043–11055 [View Article][PubMed]
    [Google Scholar]
  6. Krupovic M, Béguin P, Koonin EV. Casposons: mobile genetic elements that gave rise to the CRISPR-Cas adaptation machinery. Curr Opin Microbiol 2017; 38:36–43 [View Article][PubMed]
    [Google Scholar]
  7. Martínez-Alvarez L, Bell SD, Peng X. Multiple consecutive initiation of replication producing novel brush-like intermediates at the termini of linear viral dsDNA genomes with hairpin ends. Nucleic Acids Res 2016; 44:8799–8809 [View Article][PubMed]
    [Google Scholar]
  8. Pina M, Basta T, Quax TE, Joubert A, Baconnais S et al. Unique genome replication mechanism of the archaeal virus AFV1. Mol Microbiol 2014; 92:1313–1325 [View Article][PubMed]
    [Google Scholar]
  9. Wang Y, Sima L, Lv J, Huang S, Liu Y et al. Identification, characterization, and application of the replicon region of the halophilic temperate sphaerolipovirus SNJ1. J Bacteriol 2016; 198:1952–1964 [View Article][PubMed]
    [Google Scholar]
  10. Gardner AF, Bell SD, White MF, Prangishvili D, Krupovic M. Protein-protein interactions leading to recruitment of the host DNA sliding clamp by the hyperthermophilic Sulfolobus islandicus rod-shaped virus 2. J Virol 2014; 88:7105–7108 [View Article][PubMed]
    [Google Scholar]
  11. Zhang Z, Liu Y, Wang S, Yang D, Cheng Y et al. Temperate membrane-containing halophilic archaeal virus SNJ1 has a circular dsDNA genome identical to that of plasmid pHH205. Virology 2012; 434:233–241 [View Article][PubMed]
    [Google Scholar]
  12. Pawlowski A, Rissanen I, Bamford JK, Krupovic M, Jalasvuori M. Gammasphaerolipovirus, a newly proposed bacteriophage genus, unifies viruses of halophilic archaea and thermophilic bacteria within the novel family Sphaerolipoviridae. Arch Virol 2014; 159:1541–1554 [View Article][PubMed]
    [Google Scholar]
  13. Demina TA, Pietilä MK, Svirskaitė J, Ravantti JJ, Atanasova NS et al. Archaeal Haloarcula californiae Icosahedral virus 1 highlights conserved elements in icosahedral membrane-containing DNA viruses from extreme environments. MBio 2016; 7:e00699-16 [View Article][PubMed]
    [Google Scholar]
  14. Porter K, Kukkaro P, Bamford JK, Bath C, Kivelä HM et al. SH1: a novel, spherical halovirus isolated from an Australian hypersaline lake. Virology 2005; 335:22–33 [View Article][PubMed]
    [Google Scholar]
  15. Porter K, Tang SL, Chen CP, Chiang PW, Hong MJ et al. PH1: an archaeovirus of Haloarcula hispanica related to SH1 and HHIV-2. Archaea 2013; 2013:1–17 [View Article][PubMed]
    [Google Scholar]
  16. Jaakkola ST, Penttinen RK, Vilén ST, Jalasvuori M, Rönnholm G et al. Closely related archaeal Haloarcula hispanica icosahedral viruses HHIV-2 and SH1 have nonhomologous genes encoding host recognition functions. J Virol 2012; 86:4734–4742 [View Article][PubMed]
    [Google Scholar]
  17. Mei Y, Chen J, Sun D, Chen D, Yang Y et al. Induction and preliminary characterization of a novel halophage SNJ1 from lysogenic Natrinema sp. F5. Can J Microbiol 2007; 53:1106–1110 [View Article][PubMed]
    [Google Scholar]
  18. Chandler M, de La Cruz F, Dyda F, Hickman AB, Moncalian G et al. Breaking and joining single-stranded DNA: the HUH endonuclease superfamily. Nat Rev Microbiol 2013; 11:525–538 [View Article][PubMed]
    [Google Scholar]
  19. Krupovic M. Networks of evolutionary interactions underlying the polyphyletic origin of ssDNA viruses. Curr Opin Virol 2013; 3:578–586 [View Article][PubMed]
    [Google Scholar]
  20. Khan SA. Plasmid rolling-circle replication: highlights of two decades of research. Plasmid 2005; 53:126–136 [View Article][PubMed]
    [Google Scholar]
  21. Metcalf WW, Zhang JK, Apolinario E, Sowers KR, Wolfe RS. A genetic system for Archaea of the genus Methanosarcina: liposome-mediated transformation and construction of shuttle vectors. Proc Natl Acad Sci USA 1997; 94:2626–2631 [View Article][PubMed]
    [Google Scholar]
  22. Zhou L, Zhou M, Sun C, Xiang H, Tan H. Genetic analysis of a novel plasmid pZMX101 from Halorubrum saccharovorum: determination of the minimal replicon and comparison with the related haloarchaeal plasmid pSCM201. FEMS Microbiol Lett 2007; 270:104–108 [View Article][PubMed]
    [Google Scholar]
  23. Forterre P, Krupovic M, Raymann K, Soler N. Plasmids from Euryarchaeota. Microbiol Spectr 2014; 2:PLAS-0027-2014 [View Article][PubMed]
    [Google Scholar]
  24. Te Riele H, Michel B, Ehrlich SD. Single-stranded plasmid DNA in Bacillus subtilis and Staphylococcus aureus. Proc Natl Acad Sci USA 1986; 83:2541–2545 [View Article][PubMed]
    [Google Scholar]
  25. Zhou M, Xiang H, Sun C, Li Y, Liu J et al. Complete sequence and molecular characterization of pNB101, a rolling-circle replicating plasmid from the haloalkaliphilic archaeon Natronobacterium sp. strain AS7091. Extremophiles 2004; 8:91–98 [View Article][PubMed]
    [Google Scholar]
  26. Ilyina TV, Koonin EV. Conserved sequence motifs in the initiator proteins for rolling circle DNA replication encoded by diverse replicons from eubacteria, eucaryotes and archaebacteria. Nucleic Acids Res 1992; 20:3279–3285 [View Article][PubMed]
    [Google Scholar]
  27. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997; 25:3389–3402 [View Article][PubMed]
    [Google Scholar]
  28. van der Wielen PW, Bolhuis H, Borin S, Daffonchio D, Corselli C et al. The enigma of prokaryotic life in deep hypersaline anoxic basins. Science 2005; 307:121–123 [View Article][PubMed]
    [Google Scholar]
  29. Makarova KS, Wolf YI, Forterre P, Prangishvili D, Krupovic M et al. Dark matter in archaeal genomes: a rich source of novel mobile elements, defense systems and secretory complexes. Extremophiles 2014; 18:877–893 [View Article][PubMed]
    [Google Scholar]
  30. Gorlas A, Krupovic M, Forterre P, Geslin C. Living side by side with a virus: characterization of two novel plasmids from Thermococcus prieurii, a host for the spindle-shaped virus TPV1. Appl Environ Microbiol 2013; 79:3822–3828 [View Article][PubMed]
    [Google Scholar]
  31. Pietilä MK, Roine E, Sencilo A, Bamford DH, Oksanen HM. Pleolipoviridae, a newly proposed family comprising archaeal pleomorphic viruses with single-stranded or double-stranded DNA genomes. Arch Virol 2016; 161:249–256 [View Article][PubMed]
    [Google Scholar]
  32. Erauso G, Marsin S, Benbouzid-Rollet N, Baucher MF, Barbeyron T et al. Sequence of plasmid pGT5 from the archaeon Pyrococcus abyssi: evidence for rolling-circle replication in a hyperthermophile. J Bacteriol 1996; 178:3232–3237 [View Article][PubMed]
    [Google Scholar]
  33. Holmes ML, Pfeifer F, Dyall-Smith ML. Analysis of the halobacterial plasmid pHK2 minimal replicon. Gene 1995; 153:117–121 [View Article][PubMed]
    [Google Scholar]
  34. Sencilo A, Paulin L, Kellner S, Helm M, Roine E. Related haloarchaeal pleomorphic viruses contain different genome types. Nucleic Acids Res 2012; 40:5523–5534 [View Article][PubMed]
    [Google Scholar]
  35. Siguier P, Filée J, Chandler M. Insertion sequences in prokaryotic genomes. Curr Opin Microbiol 2006; 9:526–531 [View Article][PubMed]
    [Google Scholar]
  36. Garcillán-Barcia MP, de La Cruz F. Distribution of IS91 family insertion sequences in bacterial genomes: evolutionary implications. FEMS Microbiol Ecol 2002; 42:303–313 [View Article][PubMed]
    [Google Scholar]
  37. del Pilar Garcillán-Barcia M, Bernales I, Mendiola MV, de La Cruz F. Single-stranded DNA intermediates in IS91 rolling-circle transposition. Mol Microbiol 2001; 39:494–502 [View Article][PubMed]
    [Google Scholar]
  38. Mendiola MV, de La Cruz F. IS91 transposase is related to the rolling-circle-type replication proteins of the pUB110 family of plasmids. Nucleic Acids Res 1992; 20:3521 [View Article][PubMed]
    [Google Scholar]
  39. Ilyina TS. Mobile ISCR elements: structure, functions, and role in the emergence, increasing and spreading of blocks of bacterial genes of multiple antibiotic resistance. Mol Gen Mikrobiol Virusol 2012; 4:135–146 [View Article][PubMed]
    [Google Scholar]
  40. Toleman MA, Bennett PM, Walsh TR. ISCR elements: novel gene-capturing systems of the 21st century?. Microbiol Mol Biol Rev 2006; 70:296–316 [View Article][PubMed]
    [Google Scholar]
  41. He S, Corneloup A, Guynet C, Lavatine L, Caumont-Sarcos A et al. The IS200/IS605 family and "Peel and Paste" single-strand transposition mechanism. Microbiol Spectr 2015; 3:MDNA3-0039-2014 [View Article][PubMed]
    [Google Scholar]
  42. Filée J, Siguier P, Chandler M. Insertion sequence diversity in archaea. Microbiol Mol Biol Rev 2007; 71:121–157 [View Article][PubMed]
    [Google Scholar]
  43. Frickey T, Lupas A. CLANS: a Java application for visualizing protein families based on pairwise similarity. Bioinformatics 2004; 20:3702–3704 [View Article][PubMed]
    [Google Scholar]
  44. Henckaerts E, Dutheil N, Zeltner N, Kattman S, Kohlbrenner E et al. Site-specific integration of adeno-associated virus involves partial duplication of the target locus. Proc Natl Acad Sci USA 2009; 106:7571–7576 [View Article][PubMed]
    [Google Scholar]
  45. Liu H, Fu Y, Li B, Yu X, Xie J et al. Widespread horizontal gene transfer from circular single-stranded DNA viruses to eukaryotic genomes. BMC Evol Biol 2011; 11:276 [View Article][PubMed]
    [Google Scholar]
  46. Krupovic M, Forterre P. Single-stranded DNA viruses employ a variety of mechanisms for integration into host genomes. Ann N Y Acad Sci 2015; 1341:41–53 [View Article][PubMed]
    [Google Scholar]
  47. Crooks GE, Hon G, Chandonia JM, Brenner SE. WebLogo: a sequence logo generator. Genome Res 2004; 14:1188–1190 [View Article][PubMed]
    [Google Scholar]
  48. Katoh K, Rozewicki J, Yamada KD. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 2017 [View Article][PubMed]
    [Google Scholar]
  49. Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 2009; 25:1972–1973 [View Article][PubMed]
    [Google Scholar]
  50. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010; 59:307–321 [View Article][PubMed]
    [Google Scholar]
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