Abstract
Archaea (archaebacteria) constitute a domain of life that is distinct from Bacteria (eubacteria) and Eucarya (eukaryotes). Although archaeal cells share many morphological features with eubacteria, their transcriptional apparatus is more akin to eukaryotic RNA polymerases I, II and III than it is to eubacterial transcription systems. Thus, in addition to possessing a 10 subunit RNA polymerase and a homologue of the TATA-binding protein (TBP), Archaea possess a polypeptide termed TFB that is homologous to eukaryotic TFIIB. Here, we investigate the factor requirements for transcription of several promoters of the archaeon Sulfolobus shibatae and its associated virus SSV. Through in vitro transcription and immunodepletion, we demonstrate that S. shibatae TBP, TFB and RNA polymerase are not complexed tightly with one another and that each is required for efficient transcription of all promoters tested. Furthermore, full transcription is restored by supplementing respective depleted extracts with recombinant TBP or TFB, indicating that TBP-associated factors or TFB-associated factors are not required. Indeed, gel-filtration suggests that Sulfolobus TBP and TFB are not associated stably with other proteins. Finally, all promoters analysed are transcribed accurately and efficiently in an in vitro system comprising recombinant TBP and TFB, together with essentially homogeneous preparation of RNA polymerase. Transcription in Archaea is therefore fundamentally homologous to that in eukaryotes, although factor requirements appear to be much less complex.
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- Baumann P., Qureshi S. A., Jackson S. P. Transcription: new insights from studies on Archaea. Trends Genet. 1995 Jul;11(7):279–283. doi: 10.1016/s0168-9525(00)89075-7. [DOI] [PubMed] [Google Scholar]
- Berghöfer B., Kröckel L., Körtner C., Truss M., Schallenberg J., Klein A. Relatedness of archaebacterial RNA polymerase core subunits to their eubacterial and eukaryotic equivalents. Nucleic Acids Res. 1988 Aug 25;16(16):8113–8128. doi: 10.1093/nar/16.16.8113. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Creti R., Londei P., Cammarano P. Complete nucleotide sequence of an archaeal (Pyrococcus woesei) gene encoding a homolog of eukaryotic transcription factor IIB (TFIIB). Nucleic Acids Res. 1993 Jun 25;21(12):2942–2942. doi: 10.1093/nar/21.12.2942. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Eick D., Wedel A., Heumann H. From initiation to elongation: comparison of transcription by prokaryotic and eukaryotic RNA polymerases. Trends Genet. 1994 Aug;10(8):292–296. doi: 10.1016/0168-9525(90)90013-v. [DOI] [PubMed] [Google Scholar]
- Fox G. E., Stackebrandt E., Hespell R. B., Gibson J., Maniloff J., Dyer T. A., Wolfe R. S., Balch W. E., Tanner R. S., Magrum L. J. The phylogeny of prokaryotes. Science. 1980 Jul 25;209(4455):457–463. doi: 10.1126/science.6771870. [DOI] [PubMed] [Google Scholar]
- Frey G., Thomm M., Brüdigam B., Gohl H. P., Hausner W. An archaebacterial cell-free transcription system. The expression of tRNA genes from Methanococcus vannielii is mediated by a transcription factor. Nucleic Acids Res. 1990 Mar 25;18(6):1361–1367. doi: 10.1093/nar/18.6.1361. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goodrich J. A., Tjian R. Transcription factors IIE and IIH and ATP hydrolysis direct promoter clearance by RNA polymerase II. Cell. 1994 Apr 8;77(1):145–156. doi: 10.1016/0092-8674(94)90242-9. [DOI] [PubMed] [Google Scholar]
- Hausner W., Frey G., Thomm M. Control regions of an archaeal gene. A TATA box and an initiator element promote cell-free transcription of the tRNA(Val) gene of Methanococcus vannielii. J Mol Biol. 1991 Dec 5;222(3):495–508. doi: 10.1016/0022-2836(91)90492-o. [DOI] [PubMed] [Google Scholar]
- Hausner W., Thomm M. Purification and characterization of a general transcription factor, aTFB, from the archaeon Methanococcus thermolithotrophicus. J Biol Chem. 1993 Nov 15;268(32):24047–24052. [PubMed] [Google Scholar]
- Hempel W. M., Cavanaugh A. H., Hannan R. D., Taylor L., Rothblum L. I. The species-specific RNA polymerase I transcription factor SL-1 binds to upstream binding factor. Mol Cell Biol. 1996 Feb;16(2):557–563. doi: 10.1128/mcb.16.2.557. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hernandez N. TBP, a universal eukaryotic transcription factor? Genes Dev. 1993 Jul;7(7B):1291–1308. doi: 10.1101/gad.7.7b.1291. [DOI] [PubMed] [Google Scholar]
- Hethke C., Geerling A. C., Hausner W., de Vos W. M., Thomm M. A cell-free transcription system for the hyperthermophilic archaeon Pyrococcus furiosus. Nucleic Acids Res. 1996 Jun 15;24(12):2369–2376. doi: 10.1093/nar/24.12.2369. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hüdepohl U., Reiter W. D., Zillig W. In vitro transcription of two rRNA genes of the archaebacterium Sulfolobus sp. B12 indicates a factor requirement for specific initiation. Proc Natl Acad Sci U S A. 1990 Aug;87(15):5851–5855. doi: 10.1073/pnas.87.15.5851. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kassavetis G. A., Braun B. R., Nguyen L. H., Geiduschek E. P. S. cerevisiae TFIIIB is the transcription initiation factor proper of RNA polymerase III, while TFIIIA and TFIIIC are assembly factors. Cell. 1990 Jan 26;60(2):235–245. doi: 10.1016/0092-8674(90)90739-2. [DOI] [PubMed] [Google Scholar]
- Khoo B., Brophy B., Jackson S. P. Conserved functional domains of the RNA polymerase III general transcription factor BRF. Genes Dev. 1994 Dec 1;8(23):2879–2890. doi: 10.1101/gad.8.23.2879. [DOI] [PubMed] [Google Scholar]
- Klenk H. P., Palm P., Lottspeich F., Zillig W. Component H of the DNA-dependent RNA polymerases of Archaea is homologous to a subunit shared by the three eucaryal nuclear RNA polymerases. Proc Natl Acad Sci U S A. 1992 Jan 1;89(1):407–410. doi: 10.1073/pnas.89.1.407. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Langer D., Hain J., Thuriaux P., Zillig W. Transcription in archaea: similarity to that in eucarya. Proc Natl Acad Sci U S A. 1995 Jun 20;92(13):5768–5772. doi: 10.1073/pnas.92.13.5768. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Marsh T. L., Reich C. I., Whitelock R. B., Olsen G. J. Transcription factor IID in the Archaea: sequences in the Thermococcus celer genome would encode a product closely related to the TATA-binding protein of eukaryotes. Proc Natl Acad Sci U S A. 1994 May 10;91(10):4180–4184. doi: 10.1073/pnas.91.10.4180. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Orphanides G., Lagrange T., Reinberg D. The general transcription factors of RNA polymerase II. Genes Dev. 1996 Nov 1;10(21):2657–2683. doi: 10.1101/gad.10.21.2657. [DOI] [PubMed] [Google Scholar]
- Ouzounis C., Sander C. TFIIB, an evolutionary link between the transcription machineries of archaebacteria and eukaryotes. Cell. 1992 Oct 16;71(2):189–190. doi: 10.1016/0092-8674(92)90347-f. [DOI] [PubMed] [Google Scholar]
- Parvin J. D., Sharp P. A. DNA topology and a minimal set of basal factors for transcription by RNA polymerase II. Cell. 1993 May 7;73(3):533–540. doi: 10.1016/0092-8674(93)90140-l. [DOI] [PubMed] [Google Scholar]
- Pühler G., Leffers H., Gropp F., Palm P., Klenk H. P., Lottspeich F., Garrett R. A., Zillig W. Archaebacterial DNA-dependent RNA polymerases testify to the evolution of the eukaryotic nuclear genome. Proc Natl Acad Sci U S A. 1989 Jun;86(12):4569–4573. doi: 10.1073/pnas.86.12.4569. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Qureshi S. A., Khoo B., Baumann P., Jackson S. P. Molecular cloning of the transcription factor TFIIB homolog from Sulfolobus shibatae. Proc Natl Acad Sci U S A. 1995 Jun 20;92(13):6077–6081. doi: 10.1073/pnas.92.13.6077. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Reiter W. D., Hüdepohl U., Zillig W. Mutational analysis of an archaebacterial promoter: essential role of a TATA box for transcription efficiency and start-site selection in vitro. Proc Natl Acad Sci U S A. 1990 Dec;87(24):9509–9513. doi: 10.1073/pnas.87.24.9509. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Reiter W. D., Palm P., Voos W., Kaniecki J., Grampp B., Schulz W., Zillig W. Putative promoter elements for the ribosomal RNA genes of the thermoacidophilic archaebacterium Sulfolobus sp. strain B12. Nucleic Acids Res. 1987 Jul 24;15(14):5581–5595. doi: 10.1093/nar/15.14.5581. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Reiter W. D., Palm P., Zillig W. Analysis of transcription in the archaebacterium Sulfolobus indicates that archaebacterial promoters are homologous to eukaryotic pol II promoters. Nucleic Acids Res. 1988 Jan 11;16(1):1–19. doi: 10.1093/nar/16.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Roeder R. G. The role of general initiation factors in transcription by RNA polymerase II. Trends Biochem Sci. 1996 Sep;21(9):327–335. [PubMed] [Google Scholar]
- Rowlands T., Baumann P., Jackson S. P. The TATA-binding protein: a general transcription factor in eukaryotes and archaebacteria. Science. 1994 May 27;264(5163):1326–1329. doi: 10.1126/science.8191287. [DOI] [PubMed] [Google Scholar]
- Schleper C., Kubo K., Zillig W. 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 U S A. 1992 Aug 15;89(16):7645–7649. doi: 10.1073/pnas.89.16.7645. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Taggart A. K., Pugh B. F. Dimerization of TFIID when not bound to DNA. Science. 1996 May 31;272(5266):1331–1333. doi: 10.1126/science.272.5266.1331. [DOI] [PubMed] [Google Scholar]
- Tanese N., Pugh B. F., Tjian R. Coactivators for a proline-rich activator purified from the multisubunit human TFIID complex. Genes Dev. 1991 Dec;5(12A):2212–2224. doi: 10.1101/gad.5.12a.2212. [DOI] [PubMed] [Google Scholar]
- Verrijzer C. P., Tjian R. TAFs mediate transcriptional activation and promoter selectivity. Trends Biochem Sci. 1996 Sep;21(9):338–342. [PubMed] [Google Scholar]
- Werner M., Chaussivert N., Willis I. M., Sentenac A. Interaction between a complex of RNA polymerase III subunits and the 70-kDa component of transcription factor IIIB. J Biol Chem. 1993 Oct 5;268(28):20721–20724. [PubMed] [Google Scholar]
- White R. J., Jackson S. P. The TATA-binding protein: a central role in transcription by RNA polymerases I, II and III. Trends Genet. 1992 Aug;8(8):284–288. doi: 10.1016/0168-9525(92)90255-3. [DOI] [PubMed] [Google Scholar]
- Woese C. R., Fox G. E. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci U S A. 1977 Nov;74(11):5088–5090. doi: 10.1073/pnas.74.11.5088. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Woese C. R., Kandler O., Wheelis M. L. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci U S A. 1990 Jun;87(12):4576–4579. doi: 10.1073/pnas.87.12.4576. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zillig W., Stetter K. O., Janeković D. DNA-dependent RNA polymerase from the archaebacterium Sulfolobus acidocaldarius. Eur J Biochem. 1979 Jun 1;96(3):597–604. doi: 10.1111/j.1432-1033.1979.tb13074.x. [DOI] [PubMed] [Google Scholar]