Skip to main content
Log in

DNA-dependent RNA polymerase subunit B as a tool for phylogenetic reconstructions: Branching topology of the archaeal domain

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

The branching topology of the archaeal (archaebacterial) domain was inferred from sequence comparisons of the largest subunit (B) of DNA-dependent RNA polymerases (RNAP). Both the nucleic acid sequences of the genes coding for RNAP subunit B and the amino acid sequences of the derived gene products were used for phylogenetic reconstructions. Individual analysis of the three nucleotide positions of codons revealed significant inequalities with respect to guanosine and cytosine (GC) content and evolutionary rates. Only the nucleotides at the second codon positions were found to be unbiased by varied GC contents and sufficiently conserved for reliable phylogenetic reconstructions. A decision matrix was used for the combination of the results of distance matrix, maximum parsimony, and maximum likelihood methods. For this purpose the original results (sums of squares, steps, and logarithms of likelihoods) were transformed into comparable effective values and analyzed with methods known from the theory of statistical decisions. Phylogenetic invariants and statistical analysis with resampling techniques (bootstrap and jackknife) confirmed the preferred branching topology, which is significantly different from the topology known from phylogenetic trees based on 16S rRNA sequences. The preferred topology reconstructed by this analysis shows a common stem for the Methanococcales and Methanobacteriales and a separation of the thermophilic sulfur archaea from the methanogens and halophiles. The latter coincides with a unique phylogenetic location of a characteristic splitting event replacing the largest RNAP subunit of thermophilic sulfur archaea by two fragments in methanogens and halophiles. This topology is in good agreement with physiological and structural differences between the various archaea and demonstrates RNAP to be a suitable phylogenetic marker molecule.

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

  • Adachi J, Hasegawa M (1992) MOLPHY: programs for molecular phylogenetics, I. PROTML: maximum likelihood inference of protein phylogeny. In: Komazawa T, Nakamura T, Takagi H, Tamura Y-H, Tanabe K, Ohsumi N (eds) Computer science monographs no. 27. The Institute of Statistical Mathematics, Minato-ku, Tokyo, Japan.

    Google Scholar 

  • Berghoefer B, Kroeckel L, Koertner C, Truss M, Schallenberg J, Klein A (1988) Relatedness of archaebacterial RNA polymerase core subunits to their eubacterial and eukaryotic equivalents. Nucleic Acids Res 16:8113–8128

    Google Scholar 

  • Bernardi G, Bernardi G (1986) Compositional constraints and genome evolution. J Mol Evol 24:1–11

    Google Scholar 

  • Burggraf S, Stetter KO, Rouviere P, Woese CR (1991) Methanopyrus kandleri: an archaeal methanogen unrelated to all other known methanogens. System Appl Microbiol 14:346–351

    Google Scholar 

  • Cammarano P, Palm P, Creti R, Ceccarelli E, Sanangelantoni AM, Tiboni O (1992) Early evolutionary relationships among known life firms inferred from elongation factor EF-2/EF-G sequences: phylogenetic coherence and structure of the archaeal domain. J Mol Evol 34:396–405

    Google Scholar 

  • Creti R, Citarella F, Tiboni O, Sanangelantoni A, Palm P, Cammarano P (1991) Nucleotide sequence of a DNA region comprising the gene for elongation factor la (EF-1α) from the ultrathermophilic archaeote Pyrococcus woesei: phylogenetic implications. J Mol Evol 33:332–342

    Google Scholar 

  • Dayhoff MO (1978) A model of evolutionary change in proteins. Matrices for detecting distant relationships. In: Dayhoff MO (ed) Atlas of protein sequence and structure, vol 5, suppl 3. Natl Biomed Res Found, Washington, DC, pp 345–358

    Google Scholar 

  • Efron B (1982) The jackknife, the bootstrap, and other resampling plans. CBMS-NSF regional conference series in applied mathematics, monograph 38. Society of Industrial and Applied Mathematics, Philadelphia

    Google Scholar 

  • Felsenstein J (1991). PHYLIP users manual V3.4, University of Washington, Seattle

    Google Scholar 

  • Feng DF, Johnson MS, Doolittle RF (1985) Aligning amino acid sequences: comparison of commonly used methods. J Mol Evol 21:112–125

    Google Scholar 

  • Fitch WM, Margoliash E (1967) Construction of phylogenetic trees. Science 15:279–284

    Google Scholar 

  • Garrett RA, Dalgaard J, Larsen N, Kjems J, Mankin AS (1991) Archaeal rRNA operons. Trends Biochem Sci 16:22–26

    Google Scholar 

  • George DG, Barker WC, Hunt LT (1986) The protein identification resource. Nucleic Acids Res 14:11–15

    Google Scholar 

  • Gropp F, Reiter W-D, Sentenac A, Zillig W, Schnabel R, Thomm M, Stetter KO (1986) Homologies of components of DNA-dependent RNA polymerases of archaebacteria, eukaryotes and eubacteria. System Appl Microbiol 7:95–101

    Google Scholar 

  • Hasegawa M, Kishino H, Saitou N (1991) On the maximum likelihood method in molecular phylogenies. J Mol Evol 32:443–445

    Google Scholar 

  • Higgins DG, Sharp PM (1989) Fast and sensitive multiple sequence alignments on a microcomputer. CAIBIOS 5:151–153

    Google Scholar 

  • Iwabe N, Kuma K-i, Kishino H, Hasegawa M, Miyata T (1991) Evolution of RNA polymerases and branching patterns of the three major groups of archaeabacteria. J Mol Evol 32:70–78

    Google Scholar 

  • Jensen RA (1985) Biochemical pathways in procaryotes can be traced backwards through evolutionary time. Mol Biol Evol 2:87–120

    Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism, vol 3. Academic Press, New York, pp 21–132

    Google Scholar 

  • Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, Cambridge, England

    Google Scholar 

  • Klenk H-P, Haas B, Schwass V, Zillig W (1986) Hybridization homology: a new parameter for the analysis of phylogenetic relations, demonstrated with the urkingdom of the archaebacteria. J Mol Evol 24:167–173

    Google Scholar 

  • Klenk H-P, Schwass V, Zillig W (1992a) Nucleotide sequence of the genes encoding the three largest subunits of the DNA-dependent RNA polymerase from the archaeum Thermococcus celer. Nucleic Acids Res 20:4659

    Google Scholar 

  • Klenk H-P, Renner O, Schwass V, Zillig W (1992b) Nucleotide sequence of the genes encoding the subunits H, B, A′ and A″ of the DNA-dependent RNA polymerase and the initiator tRNA from Thermoplasma acidophilum. Nucleic Acids Res 20:5226

    Google Scholar 

  • Lake JA (1987) Rate-independent technique for analysis of nucleic acid sequences evolutionary parsimony. Mol Biol Evol 4:167–191

    Google Scholar 

  • Lake JA (1991) Tracing origins with molecular sequences: metazoan and eukaryotic beginnings. Trends Biochem Sci 16:46–50

    Google Scholar 

  • Leffers H, Gropp F, Lottspeich F, Zillig W, Garrett RA (1989) Sequence, organization, transcription and evolution of RNA polymerase subunit genes from the archaebacterial extreme halophiles Halobacterium halobium and Halococcus morrhue. J Mol Biol 206:1–17

    Google Scholar 

  • Le Quesne WJ (1969) A method of selection of characters in numerical taxonomy. Syst Zool 18:201–205

    Google Scholar 

  • Niehans J (1948) Zur Preisbildung bei ungewissen Erwartungen. Schweizerische Zeitschrift für Volkswirtschaft und Statistik 84:433–456

    Google Scholar 

  • Pühler G, Leffers H, Gropp F, Palm P, Klenk H-P, Lottspeich F, Garrett RA, Zillig W (1989) Archaebacterial DNA-dependent RNA polymerases testify to the evolution of eukaryotic nuclear genome. Proc Natl Acad Sci USA 86:4569–4573

    Google Scholar 

  • Pühler G, Lottspeich F, Zillig W (1989b) 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 17:4517–4534

    Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    Google Scholar 

  • Saitou N (1988) Property and efficiency of the maximum likelihood method for molecular phylogeny. J Mol Evol 27:261–273

    Google Scholar 

  • Savage LJ (1951) The theory of statistical decisions. Am Statist Assoc 46:55–67

    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 

  • Sidow A, Wilson AC (1990) Compositional statistics: an improvement of evolutionary parsimony and its application to deep branches in the tree of life. J Mol Evol 31:51–68

    Google Scholar 

  • Sweetser D, Nonet M, Young RA (1987) Procaryotic and eukaryotic RNA polymerases have homologous core subunits. Proc Natl Acad Sci USA 84:1192–1196

    Google Scholar 

  • Swofford DL (1989) PAUP 3.0 user's manual. Illinois Natural History Survey, Champaign, IL

    Google Scholar 

  • Templeton AR (1983) Phylogenetic inference from restriction endonuclease cleavage site maps with particular reference to the evolution of humans and the apes. Evolution 37:221–244

    Google Scholar 

  • Tu J, Prangishvilli D, Huber H, Wildgruber G, Zillig W, Stetter KO (1982) Taxonomic relations between archaebacteria including 6 novel genera examined by cross hybridization of DNAs and 16S rRNAs. J Mol Evol 18:109–114

    Google Scholar 

  • Woese CR, Fox GE (1977) Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci USA 74:5088–5090

    Google Scholar 

  • Woese CR, Olsen GJ (1986) Archaebacterial phylogeny: perspectives on the Urkingdoms. System Appl Microbiol 7:161–177

    Google Scholar 

  • Woese CR (1987) Bacterial evolution. Microbiol Rev 51:221–271

    Google Scholar 

  • Woese CR, Kandler O, Wheelis M (1990) Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci USA 87:4576–4579

    Google Scholar 

  • Woese CR, Achenbach L, Rouviere P, Mandelco L (1991) Archaeal phylogeny: reexamination of the phylogenetic position of Archaeoglobus fulgidus in light of certain composition-induced artifacts. System Appl Microbiol 14:364–371

    Google Scholar 

  • Zillig W, Klenk H-P, Palm P, Pühler G, Gropp F, Garrett RA, Leffers H (1989) The phylogenetic relations of DNA-dependent RNA polymerases of archaebacteria, eukaryotes, and eubacteria. Can J Microbiol 35:73–80

    Google Scholar 

  • Zuckerkandl E (1987) On the molecular evolutionary clock. J Mol Evol 26:34–46

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Correspondence to: H.-P. Klenk

Rights and permissions

Reprints and permissions

About this article

Cite this article

Klenk, HP., Zillig, W. DNA-dependent RNA polymerase subunit B as a tool for phylogenetic reconstructions: Branching topology of the archaeal domain. J Mol Evol 38, 420–432 (1994). https://doi.org/10.1007/BF00163158

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00163158

key words

Navigation