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. 1995 Jun 20;92(13):5768–5772. doi: 10.1073/pnas.92.13.5768

Transcription in archaea: similarity to that in eucarya.

D Langer 1, J Hain 1, P Thuriaux 1, W Zillig 1
PMCID: PMC41582  PMID: 7597027

Abstract

We present homologies between archaeal and eucaryal DNA-dependent RNA polymerase (RNAP) subunits and transcription factors. The sequences of the Sulfolobus acidocaldarius subunits D, E, and N and alignments with eucaryal homologs are presented here. The similarities between archaeal transcription factors and their eucaryal homologs TFIIB and TBP have been established in other laboratories. The archaeal RNAP subunits H, K, and N, respectively, show high sequence similarity to ABC27, ABC23, and ABC10 beta (found in all three eucaryal RNAPs); subunit D, to AC40 (common to polymerase II and polymerase III) and B44 (polymerase II); and subunit L, to AC19 and B12.5. The similarity of subunit D and its eucaryal homologs to bacterial alpha is limited to the "alpha-motif," which is also present in subunit L and its eucaryal homologs. Genes encoding homologs of the related eucaryal RNAP subunits A12.2/B12.6 and also homologs of eucaryal transcription elongation factors of the TFIIS family have been detected in Sulfolobus acidocaldarius and Thermococcus celer. In archaea, the protein is not an RNAP subunit. Together with the sequence similarities between archaeal box A-containing and eucaryal TATA box-containing promoters, this shows that the archaeal and eucaryal transcription systems are truly homologous and that they differ structurally and functionally from the bacterial transcription machinery. In contrast, however, a number of genes for the archaeal transcription apparatus are organized in clusters resembling the clusters of transcription-associated genes in Bacteria.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Agarwal K., Baek K. H., Jeon C. J., Miyamoto K., Ueno A., Yoon H. S. Stimulation of transcript elongation requires both the zinc finger and RNA polymerase II binding domains of human TFIIS. Biochemistry. 1991 Aug 6;30(31):7842–7851. doi: 10.1021/bi00245a026. [DOI] [PubMed] [Google Scholar]
  2. Burgess R. R. RNA polymerase. Annu Rev Biochem. 1971;40:711–740. doi: 10.1146/annurev.bi.40.070171.003431. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Dequard-Chablat M., Riva M., Carles C., Sentenac A. RPC19, the gene for a subunit common to yeast RNA polymerases A (I) and C (III). J Biol Chem. 1991 Aug 15;266(23):15300–15307. [PubMed] [Google Scholar]
  5. 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]
  6. Gierl A., Zillig W., Stetter K. O. The role of the components sigma and y of the DNA-dependent RNA polymerase of Lactobacillus curvatus in promotor selection. Eur J Biochem. 1982 Jun 15;125(1):41–47. doi: 10.1111/j.1432-1033.1982.tb06648.x. [DOI] [PubMed] [Google Scholar]
  7. Hain J., Reiter W. D., Hüdepohl U., Zillig W. Elements of an archaeal promoter defined by mutational analysis. Nucleic Acids Res. 1992 Oct 25;20(20):5423–5428. doi: 10.1093/nar/20.20.5423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. 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]
  10. Huet J., Riva M., Sentenac A., Fromageot P. Yeast RNA polymerase C and its subunits. Specific antibodies as structural and functional probes. J Biol Chem. 1985 Dec 5;260(28):15304–15310. [PubMed] [Google Scholar]
  11. Huet J., Schnabel R., Sentenac A., Zillig W. Archaebacteria and eukaryotes possess DNA-dependent RNA polymerases of a common type. EMBO J. 1983;2(8):1291–1294. doi: 10.1002/j.1460-2075.1983.tb01583.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Iwabe N., Kuma K., Hasegawa M., Osawa S., Miyata T. Evolutionary relationship of archaebacteria, eubacteria, and eukaryotes inferred from phylogenetic trees of duplicated genes. Proc Natl Acad Sci U S A. 1989 Dec;86(23):9355–9359. doi: 10.1073/pnas.86.23.9355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Iwabe N., Kuma K., Kishino H., Hasegawa M., Miyata T. Evolution of RNA polymerases and branching patterns of the three major groups of Archaebacteria. J Mol Evol. 1991 Jan;32(1):70–78. doi: 10.1007/BF02099931. [DOI] [PubMed] [Google Scholar]
  15. Kaine B. P., Mehr I. J., Woese C. R. The sequence, and its evolutionary implications, of a Thermococcus celer protein associated with transcription. Proc Natl Acad Sci U S A. 1994 Apr 26;91(9):3854–3856. doi: 10.1073/pnas.91.9.3854. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Kolodziej P., Young R. A. RNA polymerase II subunit RPB3 is an essential component of the mRNA transcription apparatus. Mol Cell Biol. 1989 Dec;9(12):5387–5394. doi: 10.1128/mcb.9.12.5387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Krömer W. J., Arndt E. Halobacterial S9 operon. Three ribosomal protein genes are cotranscribed with genes encoding a tRNA(Leu), the enolase, and a putative membrane protein in the archaebacterium Haloarcula (Halobacterium) marismortui. J Biol Chem. 1991 Dec 25;266(36):24573–24579. [PubMed] [Google Scholar]
  19. Lalo D., Carles C., Sentenac A., Thuriaux P. Interactions between three common subunits of yeast RNA polymerases I and III. Proc Natl Acad Sci U S A. 1993 Jun 15;90(12):5524–5528. doi: 10.1073/pnas.90.12.5524. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Langer D., Lottspeich F., Zillig W. A subunit of an archaeal DNA-dependent RNA polymerase contains the S1 motif. Nucleic Acids Res. 1994 Feb 25;22(4):694–694. doi: 10.1093/nar/22.4.694. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Langer D., Zillig W. Putative tfIIs gene of Sulfolobus acidocaldarius encoding an archaeal transcription elongation factor is situated directly downstream of the gene for a small subunit of DNA-dependent RNA polymerase. Nucleic Acids Res. 1993 May 11;21(9):2251–2251. doi: 10.1093/nar/21.9.2251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Mann C., Buhler J. M., Treich I., Sentenac A. RPC40, a unique gene for a subunit shared between yeast RNA polymerases A and C. Cell. 1987 Feb 27;48(4):627–637. doi: 10.1016/0092-8674(87)90241-8. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. Martindale D. W. A conjugation-specific gene (cnjC) from Tetrahymena encodes a protein homologous to yeast RNA polymerase subunits (RPB3, RPC40) and similar to a portion of the prokaryotic RNA polymerase alpha subunit (rpoA). Nucleic Acids Res. 1990 May 25;18(10):2953–2960. doi: 10.1093/nar/18.10.2953. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. McKune K., Richards K. L., Edwards A. M., Young R. A., Woychik N. A. RPB7, one of two dissociable subunits of yeast RNA polymerase II, is essential for cell viability. Yeast. 1993 Mar;9(3):295–299. doi: 10.1002/yea.320090309. [DOI] [PubMed] [Google Scholar]
  26. McKune K., Richards K. L., Edwards A. M., Young R. A., Woychik N. A. RPB7, one of two dissociable subunits of yeast RNA polymerase II, is essential for cell viability. Yeast. 1993 Mar;9(3):295–299. doi: 10.1002/yea.320090309. [DOI] [PubMed] [Google Scholar]
  27. Musgrave D. R., Sandman K. M., Reeve J. N. DNA binding by the archaeal histone HMf results in positive supercoiling. Proc Natl Acad Sci U S A. 1991 Dec 1;88(23):10397–10401. doi: 10.1073/pnas.88.23.10397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Nogi Y., Yano R., Dodd J., Carles C., Nomura M. Gene RRN4 in Saccharomyces cerevisiae encodes the A12.2 subunit of RNA polymerase I and is essential only at high temperatures. Mol Cell Biol. 1993 Jan;13(1):114–122. doi: 10.1128/mcb.13.1.114. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. Ozeki H., Ohyama K., Inokuchi H., Fukuzawa H., Kohchi T., Sano T., Nakahigashi K., Umesono K. Genetic system of chloroplasts. Cold Spring Harb Symp Quant Biol. 1987;52:791–804. doi: 10.1101/sqb.1987.052.01.088. [DOI] [PubMed] [Google Scholar]
  31. Pero J., Nelson J., Fox T. D. Highly asymmetric transcription by RNA polymerase containing phage-SP01-induced polypeptides and a new host protein. Proc Natl Acad Sci U S A. 1975 Apr;72(4):1589–1593. doi: 10.1073/pnas.72.4.1589. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Pühler G., Lottspeich F., Zillig W. Organization and nucleotide sequence of the genes encoding the large subunits A, B and C of the DNA-dependent RNA polymerase of the archaebacterium Sulfolobus acidocaldarius. Nucleic Acids Res. 1989 Jun 26;17(12):4517–4534. doi: 10.1093/nar/17.12.4517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. 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]
  34. 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]
  35. Sadhale P. P., Woychik N. A. C25, an essential RNA polymerase III subunit related to the RNA polymerase II subunit RPB7. Mol Cell Biol. 1994 Sep;14(9):6164–6170. doi: 10.1128/mcb.14.9.6164. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Schnabel R., Thomm M., Gerardy-Schahn R., Zillig W., Stetter K. O., Huet J. Structural homology between different archaebacterial DNA-dependent RNA polymerases analyzed by immunological comparison of their components. EMBO J. 1983;2(5):751–755. doi: 10.1002/j.1460-2075.1983.tb01495.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Schneider G. J., Hasekorn R. RNA polymerase subunit homology among cyanobacteria, other eubacteria and archaebacteria. J Bacteriol. 1988 Sep;170(9):4136–4140. doi: 10.1128/jb.170.9.4136-4140.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Scholzen T., Arndt E. The alpha-operon equivalent genome region in the extreme halophilic archaebacterium Haloarcula (Halobacterium) marismortui. J Biol Chem. 1992 Jun 15;267(17):12123–12130. [PubMed] [Google Scholar]
  39. Sopta M., Burton Z. F., Greenblatt J. Structure and associated DNA-helicase activity of a general transcription initiation factor that binds to RNA polymerase II. Nature. 1989 Oct 5;341(6241):410–414. doi: 10.1038/341410a0. [DOI] [PubMed] [Google Scholar]
  40. Sparkowski J., Das A. The nucleotide sequence of greA, a suppressor gene that restores growth of an Escherichia coli RNA polymerase mutant at high temperature. Nucleic Acids Res. 1990 Nov 11;18(21):6443–6443. doi: 10.1093/nar/18.21.6443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Stetter K. O., Zillig W. Transcription in lactobacillaceae. DNA-dependent RNA polymerase from Lactobacillus curvatus. Eur J Biochem. 1974 Oct 2;48(2):527–540. doi: 10.1111/j.1432-1033.1974.tb03794.x. [DOI] [PubMed] [Google Scholar]
  42. Travers A. A., Burgessrr Cyclic re-use of the RNA polymerase sigma factor. Nature. 1969 May 10;222(5193):537–540. doi: 10.1038/222537a0. [DOI] [PubMed] [Google Scholar]
  43. Tyree C. M., George C. P., Lira-DeVito L. M., Wampler S. L., Dahmus M. E., Zawel L., Kadonaga J. T. Identification of a minimal set of proteins that is sufficient for accurate initiation of transcription by RNA polymerase II. Genes Dev. 1993 Jul;7(7A):1254–1265. doi: 10.1101/gad.7.7a.1254. [DOI] [PubMed] [Google Scholar]
  44. Woese C. R. Bacterial evolution. Microbiol Rev. 1987 Jun;51(2):221–271. doi: 10.1128/mr.51.2.221-271.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. 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]
  46. Woese C. R. There must be a prokaryote somewhere: microbiology's search for itself. Microbiol Rev. 1994 Mar;58(1):1–9. doi: 10.1128/mr.58.1.1-9.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Woychik N. A., Lane W. S., Young R. A. Yeast RNA polymerase II subunit RPB9 is essential for growth at temperature extremes. J Biol Chem. 1991 Oct 5;266(28):19053–19055. [PubMed] [Google Scholar]
  48. Woychik N. A., McKune K., Lane W. S., Young R. A. Yeast RNA polymerase II subunit RPB11 is related to a subunit shared by RNA polymerase I and III. Gene Expr. 1993;3(1):77–82. [PMC free article] [PubMed] [Google Scholar]
  49. Woychik N. A., McKune K., Lane W. S., Young R. A. Yeast RNA polymerase II subunit RPB11 is related to a subunit shared by RNA polymerase I and III. Gene Expr. 1993;3(1):77–82. [PMC free article] [PubMed] [Google Scholar]
  50. Woychik N. A., Young R. A. RNA polymerase II subunit RPB4 is essential for high- and low-temperature yeast cell growth. Mol Cell Biol. 1989 Jul;9(7):2854–2859. doi: 10.1128/mcb.9.7.2854. [DOI] [PMC free article] [PubMed] [Google Scholar]

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