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Characterization of the Sulfolobus host–SSV2 virus interaction

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Abstract

The Sulfolobus spindle virus, SSV2, encodes a tyrosine integrase which furthers provirus formation in host chromosomes. Consistently with the prediction made during sequence analysis, integration was found to occur in the downstream half of the tRNAGly (CCC) gene. In this paper we report the findings of a comparative study of SSV2 physiology in the natural host, Sulfolobus islandicus REY15/4, versus the foreign host, Sulfolobus solfataricus, and provide evidence of differently regulated SSV2 life cycles in the two hosts. In fact, whereas a significant induction of SSV2 replication takes place during the growth of the natural host REY15/4, the cellular content of SSV2 DNA remains fairly low throughout the incubation of the foreign host. The accumulation of episomal DNA in the former case cannot be traced to decreased packaging activity because of a simultaneous increase in the virus titre in the medium. In addition, the interaction between SSV2 and its natural host is characterized by the concurrence of host growth inhibition and the induction of viral DNA replication. When this virus–host interaction was investigated using S. islandicus REY15A, a strain which is closely related to the natural host, it was found that the SSV2 replication process was induced in the same way as in the natural host REY15/4.

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References

  • Ackermann HW, DuBow MS (1987) Viruses of prokaryotes: general properties of bacteriophages. CRC Press, Inc., Boca Raton

    Google Scholar 

  • Albers SV, Jonuscheit M, Dinkelaker S, Urich T, Kletzin A, Tampe R, Driessen AJ, Schleper C (2006) Production of recombinant and tagged proteins in the hyperthermophilic archaeon Sulfolobus solfataricus. Appl Environ Microbiol 72:102–111

    Article  PubMed  CAS  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  PubMed  CAS  Google Scholar 

  • Arnold HP, She Q, Phan H, Stedman KM, Prangishvili D, Holz I, Kristjansson JK, Garrett RA, Zillig W (1999a) The genetic element pSSVx of the extremely thermophilic crenarchaeon Sulfolobus is a hybrid between a plasmid and a virus. Mol Microbiol 34:217–226

    Article  PubMed  CAS  Google Scholar 

  • Arnold HP, Stedman KM, Zillig W (1999b) Archaeal phages. In: Webster RG, Granoff A (eds) Encyclopedia of virology. Academic, London, pp 76–89

    Google Scholar 

  • Bettstetter M, Peng X, Garrett RA, Prangishvili D (2003) AFV1, a novel virus infecting hyperthermophilic archaea of the genus Acidianus. Virology 315:68–79

    Article  PubMed  CAS  Google Scholar 

  • Blum H, Zillig W, Mallock S, Domday H, Prangishvili D (2001) The genome of the archaeal virus SIRV1 has features in common with genomes of eukaryal viruses. Virology 281:6–9

    Article  PubMed  CAS  Google Scholar 

  • Campbell AM (1992) Chromosomal insertion sites for phages and plasmids. J Bacteriol 174:7495–7499

    PubMed  CAS  Google Scholar 

  • Esposito D, Scocca JJ (1997) The integrase family of tyrosine recombinases: evolution of a conserved active site domain. Nucleic Acids Res 25:3605–3614

    Article  PubMed  CAS  Google Scholar 

  • Garrett RA, Redder P, Greve B, Brügger K, Chen L, She Q (2004) Archaeal plasmids. In: Funnell BE, Phillips GJ (eds) Plasmid Biology, ASM Press, Washington DC, pp 377–392

    Google Scholar 

  • Grogan D, Palm P, Zillig W (1990) Isolate B12, which harbours a virus-like element, represents a new species of the archaebacterial genus Sulfolobus, Sulfolobus shibatae, sp. nov. Arch Microbiol 154:594–599

    Article  PubMed  CAS  Google Scholar 

  • Jonuscheit M, Martusewitsch E, Stedman KM, Schleper C (2003) A reporter gene system for the hyperthermophilic archaeon Sulfolobus solfataricus based on a selectable and integrative shuttle vector. Mol Microbiol 48:1241–1252

    Article  PubMed  CAS  Google Scholar 

  • Lubelska JM, Jonuscheit M, Schleper C, Albers SV, Driessen AJ (2006) Regulation of expression of the arabinose and glucose transporter genes in the thermophilic archaeon Sulfolobus solfataricus. Extremophiles April 8 (Epub ahead of print)

  • Martin A, Yeats S, Janekovic D, Reiter WD, Aicher W, Zillig W (1984) SAV1, a temperate U. V. inducible DNA virus like particle from the archaebacterium Sulfolobus acidocaldarius isolate B12. EMBO J 3:2165–2168

    PubMed  CAS  Google Scholar 

  • Muskhelishvili G, Palm P, Zillig W (1993) SSV1-encoded site-specific recombination system in Sulfolobus shibatae. Mol Gen Genet 237:334–342

    PubMed  CAS  Google Scholar 

  • Nadal M, Mirambeau G, Forterre P, Reiter WD, Duguet M (1986) Positively supercoiled DNA in a virus-like particle of an archaebacterium. Nature 321:256–258

    Article  CAS  Google Scholar 

  • Nunes-Duby SE, Kwon HJ, Tirumalai RS, Ellenberger T, Landy A (1998) Similarities and differences among 105 members of the Int family of site-specific recombinases. Nucleic Acids Res 26:391–406

    Article  PubMed  CAS  Google Scholar 

  • Palm P, Schleper C, Grampp B, Yeats S, McWilliam P, Reiter WD, Zillig W (1991) Complete nucleotide sequence of the virus SSV1 of the archaebacterium Sulfolobus shibatae. Virology 185:242–250

    Article  PubMed  CAS  Google Scholar 

  • Peng X, Blum H, She Q, Mallok S, Brügger K, Garrett RA, Zillig W, Prangishvili D (2001) Sequences and replication of genomes of the archaeal rudiviruses SIRV1 and SIRV2: relationships to the archaeal lipothrixvirus SIFV and some eukaryal viruses. Virology 291:226–234

    Article  PubMed  CAS  Google Scholar 

  • Prangishvili D, Stedman K, Zillig W (2001) Viruses of the extremely thermophilic archaeon Sulfolobus. Trends Microbiol 9:39–43

    Article  PubMed  CAS  Google Scholar 

  • Prangishvili D, Garrett RA, Koonin EV (2006a) Evolutionary genomics of archaeal viruses: unique viral genomes in the third domain of life. Virus Res 117:52–67

    Article  PubMed  CAS  Google Scholar 

  • Prangishvili D, Vestergaard G, Haring M, Aramayo R, Basta T, Rachel R, Garrett RA (2006b) Structural and genomic properties of the hyperthermophilic archaeal virus ATV with an extracellular stage of the reproductive cycle. J Mol Biol April 27 (pub ahead)

  • Reiter WD, Palm P (1990) Identification and characterization of a defective SSV1 genome integrated into a tRNA gene in the archaebacterium Sulfolobus sp. B12. Mol Gen Genet 221:65–71

    Article  PubMed  CAS  Google Scholar 

  • Reiter WD, Palm P, Henschen A, Lottspeich F, Zillig W, Grampp B (1987a) Identification and characterization of the genes encoding three structural proteins of the Sulfolobus virus-like particle SSV1. Mol Gen Genet 206:144–153

    Article  CAS  Google Scholar 

  • Reiter WD, Palm P, Yeats S, Zillig W (1987b) Gene expression in archaebacteria: physical mapping of constitutive and UV-inducible transcripts from the Sulfolobus virus-like particle SSV1. Mol Gen Genet 209:270–275

    Article  CAS  Google Scholar 

  • Reiter WD, Palm P, Zillig W (1988) Analysis of transcription in the archaebacterium Sulfolobus indicates that archaebacterial promoters are homologous to eukaryotic pol II promoters. Nucleic Acids Res 16:1–19

    PubMed  CAS  Google Scholar 

  • Reiter WD, Palm P, Yeats S (1989) Transfer RNA genes frequently serve as integration sites for prokaryotic genetic elements. Nucleic Acids Res 17:1907–1914

    PubMed  CAS  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning, a laboratory manual. 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Schleper C, Kubo K, Zillig W (1992) The particle SSV1 from the extremely thermophilic archaeon Sulfolobus is a virus: demonstration of infectivity and of transfection with viral DNA. Proc Natl Acad Sci USA 89:7645–7649

    Article  PubMed  CAS  Google Scholar 

  • Serre MC, Letzelter C, Garel JR, Duguet M (2002) Cleavage properties of an archaeal site-specific recombinase, the SSV1 integrase. J Biol Chem 277:16758–16767

    Article  PubMed  CAS  Google Scholar 

  • She Q, Peng X, Zillig W, Garrett RA (2001a) Gene capture in archaeal chromosomes. Nature 409:478

    Article  PubMed  CAS  Google Scholar 

  • She Q, Singh RK, Confalonieri F, Zivanovic Y, Allard G, Awayez MJ, Chan-Weiher CC-Y, Clausen IG, Curtis BA, Moors AD, Erauso G, Fletcher C, Gordon PMK, Jong IH-D, Jeffries AC, Kozera CJ, Medina N, Peng X, Thi-Ngoc HP, Redder P, Schenk ME, Theriault C, Tolstrup N, Charlebois RL, Doolittle WF, Duguet M, Gaasterland T, Garrett RA, Ragan M A, Sensen CW, van der Oost J (2001b) The complete genome of the crenarchaeon Sulfolobus solfataricus P2. Proc Natl Acad Sci USA 98:7835–7840

    Article  PubMed  CAS  Google Scholar 

  • She Q, Brugger K, Chen L (2002) Archaeal integrative elements and their impact on evolution. Res Microbiol 153:325–332

    Article  PubMed  CAS  Google Scholar 

  • She Q, Shen B, Chen L (2004) Archaeal integrases and mechanisms of gene capture. Biochem Soc Trans 32:222–226

    Article  PubMed  CAS  Google Scholar 

  • Snyder JC, Stedman K, Rice G, Wiedenheft B, Spuhler J, Young MJ (2003) Viruses of hyperthermophilic Archaea. Res Microbiol 154:474–482

    Article  PubMed  CAS  Google Scholar 

  • Stedman KM, She Q, Phan H, Arnold HP, Holz I, Garrett RA, Zillig W (2003) Relationships between fuselloviruses infecting the extremely thermophilic archaeon Sulfolobus: SSV1 and SSV2. Res Microbiol 154:295–302

    Article  PubMed  CAS  Google Scholar 

  • Wiedenheft B, Stedman KM, Roberto F, Willits D, Gleske AK, Zoeller L, Snyder J, Douglas T, Young M (2004) Comparative genomic analysis of hyperthermophilic archaeal Fuselloviridae viruses. J Virol 78:1954–1961

    Article  PubMed  CAS  Google Scholar 

  • Weinbauer MG (2004) Ecology of prokaryotic viruses. FEMS Microbiol Rev 28:127–181

    Article  PubMed  CAS  Google Scholar 

  • Williams KP (2002) Integration sites for genetic elements in prokaryotic tRNA and tmRNA genes: sublocation preference of integrase subfamilies. Nucleic Acids Res 30:866–875

    Article  PubMed  CAS  Google Scholar 

  • Xiang X, Chen L, Huang X, Luo Y, She Q, Huang L (2005) Sulfolobus tengchongensis spindle-shaped virus STSV1: virus–host interactions and genomic features. J Virol 79:8677–8686

    Article  PubMed  CAS  Google Scholar 

  • Yeats S, McWilliam P, Zillig W (1982) A plasmid in the archaebacterium Sulfolobus acidocaldarius. EMBO J 1:1035–1038

    PubMed  CAS  Google Scholar 

  • Zillig W, Kletzin A, Schleper C, Holz I, Janekovi PD, Hain J, Lanzendorfer M, Kristjansson J (1994) Screening for Sulfolobales, their plasmids, and their viruses in Icelandic sulfataras. Syst Appl Microbiol 16:609–628

    CAS  Google Scholar 

  • Zillig W, Arnold HP, Holz I, Prangishvili D, Schweier A, Stedman KM, She Q, Phan H, Garrett RA, Kristjansson JK (1998) Genetic elements in the extremely thermophilic archaeon Sulfolobus. Extremophiles 2:131–140

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We thank Roger Garrett for encouraging discussion, Wolfram Zillig for providing a number of Sulfolobus strains and enrichment cultures, Raffaele Cannio and Kenneth Stedman for helpful discussion. We also acknowledge support from a Young Research Leader project of the Danish Research Council of Technology and Production (FTP), from the “Archaea Centre: Diversity and Evolution” of the Danish Natural Science Research Council (FNU) to the Copenhagen laboratory, from the National Competence Centre (CRdc ATIBB, Campania Region, Naples) and the European Union (Contract QLK3-CT-2000-00649) to the Naples laboratory.

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Authors and Affiliations

  1. Department of Biological Chemistry, Institute of Molecular Biology and Physiology, University of Copenhagen, Sølvgade 83H, 1307 , Copenhagen, Denmark

    Patrizia Contursi, Susanne Jensen & Qunxin She

  2. Dipartimento di Biologia Strutturale e Funzionale, Universitá degli Studi di Napoli Federico II, Complesso Universitario Monte S.Angelo, Via Cinthia, Naples, Italy

    Patrizia Contursi, Tiziana Aucelli, Mosé Rossi & Simonetta Bartolucci

  3. Istituto di Biochimica delle Proteine, CNR, via Pietro Castellino 111, 80131, Naples, Italy

    Mosé Rossi

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  1. Patrizia Contursi
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Correspondence to Qunxin She.

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Communicated by G. Antranikian

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Contursi, P., Jensen, S., Aucelli, T. et al. Characterization of the Sulfolobus host–SSV2 virus interaction. Extremophiles 10, 615–627 (2006). https://doi.org/10.1007/s00792-006-0017-2

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