Skip to main content
Log in

Identification and characterization of the genes encoding three structural proteins of the Sulfolobus virus-like particle SSV1

  • Published:
Molecular and General Genetics MGG Aims and scope Submit manuscript

Summary

Three structural proteins, VP1, VP2 and VP3, of the virus-like particle SSV1 of the thermoacidophilic archaebacterium Sulfolobus sp. strain B12 were purified. VP1 and VP3 are very hydrophobic and show a high degree of homology. They consist of 73 and 92 amino acid residues, respectively. The third protein, VP2, is extremely basic containing 29 basic amino acids but only 4 acidic ones in a total of 74 amino acid residues. The genes encoding these three proteins were mapped within the genome by comparison of N-terminal amino acid sequences with the SSV1 DNA sequence. The three genes are closely linked in the order VP1-VP3-VP2 and the coding strand is the same in all three genes. Ten nucleotides separate the stop codon for VP1 from the initiation codon for VP3 and one nucleotide separates the genes encoding VP3 and VP2. Duplicate putative ribosome binding sites are found upstream of the initiation codons for VP2 and VP3. The major coat protein VP1 does not start with a methionine residue and appears to be the result of proteolytic cleavage of a precursor molecule. Transcription of the region encoding VP1, VP2 and VP3 results in the formation of two mRNAs of 0.5 kb and 1.0 kb, the shorter one only encoding VP1, the longer one spanning all three genes. A 61 bp sequence encoding part of VP1 is exactly repeated within the gene for VP3 and these identical sequences are translated into stretches of identical amino acids in the two proteins. A function of this repeated DNA sequence beyond its coding properties is very likely.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Aebersold RH, Teplow DB, Hood LE, Kent SBH (1986) Electroblotting ontoo activated glass. High efficiency preparation of proteins from analytical sodium dodecyl sulfate-polyacrylamide gels for direct sequence analysis. J Biol Chem 261:4229–4238

    Google Scholar 

  • Baresi L, Bertani G (1984) Isolation of a bacteriophage for a methanogenic bacterium. Abstr Annu Meet Am Soc Microbiol 84: Abstract I 74

  • Bollschweiler C, Klein A (1982) Polypeptide synthesis in Escherichia coli directed by cloned Methanobrevibacter arboriphilus DNA. Zentralbl Bakteriol Mikrobiol Hyg [C] 3:101–109

    Google Scholar 

  • Bollschweiler C, Kühn R, Klein A (1985) Non-repetitive AT-rich sequences are found in intergenic regions of Methanococcus voltae DNA. EMBO J 4:805–809

    Google Scholar 

  • Cue D, Beckler GS, Reeve JN, Konisky J (1985) Structure and sequence divergence of two archaebacterial genes. Proc Natl Acad Sci USA 82:4207–4211

    Google Scholar 

  • Daniels LL, Wais AC (1984) Restriction and modification of halophage S45 in Halobacterium. Curr Microbiol 10:133–136

    Google Scholar 

  • Deininger PL (1983) Random subcloning of sonicated DNA: Application to shotgun DNA sequence analysis. Anal Biochem 129:216–223

    Google Scholar 

  • Devereux J, Haeberli P, Smithies O (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12:387–395

    Google Scholar 

  • Dorsch-Häsler K, Keil GM, Weber F, Jasin M, Schaffner W, Koszinowski UH (1985) A long and complex enhancer activates transcription of the gene coding for the highly abundant immediate early mRNA in murine cytomegalovirus. Proc Natl Acad Sci USA 82:8325–8329

    Google Scholar 

  • Fox GE, Stackebrandt E, Hespell RB, Gibson J, Maniloff J, Dyer TA, Wolfe RS, Balch WE, Tanner RS, Magrum LJ, Zablen LB, Blakemore R, Gupta R, Bonen L, Lewis BJ, Stahl DA, Luehrsen KR, Chen KN, Woese CR (1980) The phylogeny of prokaryotes. Science 209:457–463

    Google Scholar 

  • Gluzman Y (ed) (1985) Eukaryotic transcription: The role of cis- and trans-acting elements in initiation. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY

    Google Scholar 

  • Hamilton PT, Reeve JN (1985) Structure of genes and an insertion element in the methane producing archaebacterium Methanobrevibacter smithii. Mol Gen Genet 200:47–59

    Google Scholar 

  • Hu N, Messing J (1982) The making of strand-specific M13 probes. Gene 17:271–277

    Google Scholar 

  • Huet J, Schnabel R, Sentenac A, Zillig W (1983) Archaebacteria and eukaryotes possess DNA-dependent RNA polymerases of a common type. EMBO J 2:1291–1294

    Google Scholar 

  • Janekovic D, Wunderl S, Holz I, Zillig W, Gierl A, Neumann H (1983) TTV1, TTV2 and TTV3, a family of viruses of the extremely thermophilic, anaerobic, sulfur reducing archaebacterium Thermoproteus tenas. Mol Gen Genet 192:39–45

    Google Scholar 

  • Konheiser U, Pasti G, Bollschweiler C, Klein A (1984) Physical mapping of genes coding for two subunits of methyl CoM reductase component C of Methanococcus voltae. Mol Gen Genet 198:146–152

    Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Google Scholar 

  • Lottspeich F, Kellermann J, Henschen A, Rauth G, Müller-Esterl W (1984) Human low-molecular-mass kininogen. Amino-acid sequence of the light chain: homology with other protein sequences. Eur J Biochem 142:227–232

    Google Scholar 

  • Lottspeich F (1985) Microscale isocratic separation of phenylthio-hydantoin amino acid derivatives. J Chromatogr 326:321–327

    Google Scholar 

  • Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning, a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY

    Google Scholar 

  • 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

    Google Scholar 

  • Messing J, Vieira J (1982) A new pair of M13 vectors for selecting either DNA strand of double-digest restriction fragments. Gene 19:269–276

    Google Scholar 

  • Mirault ME, Scherrer K, Hansen L (1971) Isolation of preribosomes from HeLa cells and their characterization by electrophoresis on uniform and exponential-gradient-polyacrylamide gels. Eur J Biochem 23:372–386

    Google Scholar 

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

    Google Scholar 

  • Olsen GJ, Pace N, Nuell M, Kaine BP, Gupta R, Woese CR (1985) Sequence of the 16S rRNA gene from the thermoacidophilic archaebacerium Sulfolobus solfataricus and its evolutionary implications. J Mol Evol 22:301–307

    Google Scholar 

  • Pauling C (1982) Bacteriophages of Halobacterium halobium: isolation from fermented fish sauce and primary characterization. Can J Microbiol 28:916–921

    Google Scholar 

  • Reeve JN, Hamilton PT, Beckler GS, Morris CJ, Clarke CH (1986) Structure of methanogen genes. Syst Appl Microbiol 7:5–12

    Google Scholar 

  • Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467

    Google Scholar 

  • Sanger F, Coulson AR, Barrell BG, Smith AJH, Roe BA (1980) Cloning in single-stranded bacteriophage as an aid to rapid DNA sequencing. J Mol Biol 143:161–178

    Google Scholar 

  • Sather S, Agabian N (1985) A 5′ spliced leader is added in trans to both α- and β-tubulin transcripts in Trypanosoma brucei. Proc Natl Acad Sci USA 82:5695–5699

    Google Scholar 

  • Schnabel H, Zillig W, Pfäffle M, Schnabel R, Michel H, Delius H (1982a) Halobacterium halobium phage ΦH. EMBO J 1:87–92

    Google Scholar 

  • Schnabel H, Schramm E, Schnabel R, Zillig W (1982b) Structural variability in the genome of phage ΦH of Halobacterium halobium. Mol Gen Genet 188:370–377

    Google Scholar 

  • Schnabel H (1984a) An immune strain of Halobacterium halobium carries the invertible L segment of phage ΦH as a plasmid. Proc Natl Acad Sci USA 81:1017–1020

    Google Scholar 

  • Schnabel H (1984b) Integration of plasmid pΦHL into phage genomes during infection of Halobacterium halobium R1-L with phage ΦHL1. Mol Gen Genet 197:19–23

    Google Scholar 

  • Schnabel H, Zillig W (1984) Circular structure of the genome of phage ΦH in a lysogenic Halobacterium halobium. Mol Gen Genet 193:422–426

    Google Scholar 

  • Schnabel H, Palm P, Dick K, Grampp B (1984) Sequence analysis of the insertion element ISH1.8 and of associated structural changes in the genome of phage ΦH of the archaebacterium Halobacterium halobium. EMBO J 3:1717–1722

    Google Scholar 

  • Schnabel R, Thomm M, Gerardy-Schahn R, Zillig W, Stetter KO, Huet J (1983) Structural homology between different archaebacterial DNA-dependent RNA polymerases analyzed by immunological comparison of their components. EMBO J 2:751–755

    Google Scholar 

  • Shine J, Dalgarno L (1974) The 3′-terminal sequence of Escherichia coli 16S ribosomal RNA: Complementarity to nonsense triplets and ribosome binding sites. Proc Natl Acad Sci USA 71:1342–1346

    Google Scholar 

  • Staden R (1980) A new computer method for the storage and manipulation of DNA gel reading data. Nucleic Acids Res 8:3673–3694

    Google Scholar 

  • Steitz JA (1978) Methanogenic bacterial. Nature 273:10

    Google Scholar 

  • Tandy NE, Dilley RA, Regnier FE (1983) High-performance liquid chromatographic purification of the hydrophobic ω subunit of the chloroplast energy coupling complex. J Chromatogr 266:599–607

    Google Scholar 

  • Thomas PS (1983) Hybridization of denatured RNA transferred or dotted to nitrocellulose paper. Methods Enzymol 100:255–266

    Google Scholar 

  • Torsvik T, Dundas ID (1974) Bacteriophage of Halobacterium salinarium. Nature 248:680–681

    Google Scholar 

  • Torsvik T, Dundas JD (1980) Persisting phage infection in Halobacterium salinarium str. 1. J Gene Virol 47:29–36

    Google Scholar 

  • Vogelsang-Wenke H, Oesterhelt D (1986) Halophage ΦN. In: Kandler O, Zillig W (eds) Archaebacteria 85. Gustav Fischer Verlag, Stuttgart New York, pp 403–405

    Google Scholar 

  • Wais AC, Kon M, MacDonald RE (1975) Salt-dependent bacteriophage infecting Halobacterium cutirubrum and H. halobium. Nature 256:314–315

    Google Scholar 

  • Woese CR, Olsen GJ (1986) Archabacterial phylogeny: Perspectives on the urkingdoms. Syst Appl Microbiol 7:161–177

    Google Scholar 

  • Wood AG, Redborg AH, Cue DR, Whitman WB, Konisky J (1983) Complementation of argG and hisA mutations of Escherichia coli by DNA cloned from the archaebacterium Methanococcus voltae. J Bacteriol 156:19–29

    Google Scholar 

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

    Google Scholar 

  • Zillig W, Schnabel R, Stetter KO (1985a) Archabacteria and the origin of the eukaryotic cytoplasm. Curr Top Microbiol Immunol 114:1–18

    Google Scholar 

  • Zillig W, Yeats S, Holz I, Böck A, Gropp F, Rettenberger M, Lutz S (1985b) Plasmid-related anaerobic autotrophy of the novel archaebacterium Sulfolobus ambivalens. Nature 313:789–791

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by A. Böck

Rights and permissions

Reprints and permissions

About this article

Cite this article

Reiter, WD., Palm, P., Henschen, A. et al. Identification and characterization of the genes encoding three structural proteins of the Sulfolobus virus-like particle SSV1. Mol Gen Genet 206, 144–153 (1987). https://doi.org/10.1007/BF00326550

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00326550

Key words

Navigation