Abstract
The genes for the protein synthesis elongation factors Tu (EF-Tu) and G (EF-G) are the products of an ancient gene duplication, which appears to predate the divergence of all extant organismal lineages. Thus, it should be possible to root a universal phylogeny based on either protein using the second protein as an outgroup. This approach was originally taken independently with two separate gene duplication pairs, (i) the regulatory and catalytic subunits of the proton ATPases and (ii) the protein synthesis elongation factors EF-Tu and EF-G. Questions about the orthology of the ATPase genes have obscured the former results, and the elongation factor data have been criticized for inadequate taxonomic representation and alignment errors. We have expanded the latter analysis using a broad representation of taxa from all three domains of life. All phylogenetic methods used strongly place the root of the universal tree between two highly distinct groups, the archaeons/eukaryotes and the eubacteria. We also find that a combined data set of EF-Tu and EF-G sequences favors placement of the eukaryotes within the Archaea, as the sister group to the Crenarchaeota. This relationship is supported by bootstrap values of 60-89% with various distance and maximum likelihood methods, while unweighted parsimony gives 58% support for archaeal monophyly.
Full text
PDFSelected References
These references are in PubMed. This may not be the complete list of references from this article.
- 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]
- Benachenhou-Lahfa N., Forterre P., Labedan B. Evolution of glutamate dehydrogenase genes: evidence for two paralogous protein families and unusual branching patterns of the archaebacteria in the universal tree of life. J Mol Evol. 1993 Apr;36(4):335–346. doi: 10.1007/BF00182181. [DOI] [PubMed] [Google Scholar]
- Bourne H. R., Sanders D. A., McCormick F. The GTPase superfamily: conserved structure and molecular mechanism. Nature. 1991 Jan 10;349(6305):117–127. doi: 10.1038/349117a0. [DOI] [PubMed] [Google Scholar]
- Brown J. R., Doolittle W. F. Root of the universal tree of life based on ancient aminoacyl-tRNA synthetase gene duplications. Proc Natl Acad Sci U S A. 1995 Mar 28;92(7):2441–2445. doi: 10.1073/pnas.92.7.2441. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brown J. R., Masuchi Y., Robb F. T., Doolittle W. F. Evolutionary relationships of bacterial and archaeal glutamine synthetase genes. J Mol Evol. 1994 Jun;38(6):566–576. doi: 10.1007/BF00175876. [DOI] [PubMed] [Google Scholar]
- Chien Y. T., Zinder S. H. Cloning, DNA sequencing, and characterization of a nifD-homologous gene from the archaeon Methanosarcina barkeri 227 which resembles nifD1 from the eubacterium Clostridium pasteurianum. J Bacteriol. 1994 Nov;176(21):6590–6598. doi: 10.1128/jb.176.21.6590-6598.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Clark A. J., Sandler S. J. Homologous genetic recombination: the pieces begin to fall into place. Crit Rev Microbiol. 1994;20(2):125–142. doi: 10.3109/10408419409113552. [DOI] [PubMed] [Google Scholar]
- Clark B. F., Kjeldgaard M., la Cour T. F., Thirup S., Nyborg J. Structural determination of the functional sites of E. coli elongation factor Tu. Biochim Biophys Acta. 1990 Aug 27;1050(1-3):203–208. doi: 10.1016/0167-4781(90)90167-z. [DOI] [PubMed] [Google Scholar]
- Creti R., Ceccarelli E., Bocchetta M., Sanangelantoni A. M., Tiboni O., Palm P., Cammarano P. Evolution of translational elongation factor (EF) sequences: reliability of global phylogenies inferred from EF-1 alpha(Tu) and EF-2(G) proteins. Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):3255–3259. doi: 10.1073/pnas.91.8.3255. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Czworkowski J., Wang J., Steitz T. A., Moore P. B. The crystal structure of elongation factor G complexed with GDP, at 2.7 A resolution. EMBO J. 1994 Aug 15;13(16):3661–3668. doi: 10.1002/j.1460-2075.1994.tb06675.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- De Rijk P., Van de Peer Y., Van den Broeck I., De Wachter R. Evolution according to large ribosomal subunit RNA. J Mol Evol. 1995 Sep;41(3):366–375. doi: 10.1007/BF01215184. [DOI] [PubMed] [Google Scholar]
- Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Doolittle R. F., Feng D. F., Anderson K. L., Alberro M. R. A naturally occurring horizontal gene transfer from a eukaryote to a prokaryote. J Mol Evol. 1990 Nov;31(5):383–388. doi: 10.1007/BF02106053. [DOI] [PubMed] [Google Scholar]
- Felsenstein J. Phylogenies from molecular sequences: inference and reliability. Annu Rev Genet. 1988;22:521–565. doi: 10.1146/annurev.ge.22.120188.002513. [DOI] [PubMed] [Google Scholar]
- Forterre P., Benachenhou-Lahfa N., Confalonieri F., Duguet M., Elie C., Labedan B. The nature of the last universal ancestor and the root of the tree of life, still open questions. Biosystems. 1992;28(1-3):15–32. doi: 10.1016/0303-2647(92)90004-i. [DOI] [PubMed] [Google Scholar]
- Garrett R. A., Dalgaard J., Larsen N., Kjems J., Mankin A. S. Archaeal rRNA operons. Trends Biochem Sci. 1991 Jan;16(1):22–26. doi: 10.1016/0968-0004(91)90011-j. [DOI] [PubMed] [Google Scholar]
- Gogarten J. P., Kibak H., Dittrich P., Taiz L., Bowman E. J., Bowman B. J., Manolson M. F., Poole R. J., Date T., Oshima T. Evolution of the vacuolar H+-ATPase: implications for the origin of eukaryotes. Proc Natl Acad Sci U S A. 1989 Sep;86(17):6661–6665. doi: 10.1073/pnas.86.17.6661. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gouy M., Li W. H. Phylogenetic analysis based on rRNA sequences supports the archaebacterial rather than the eocyte tree. Nature. 1989 May 11;339(6220):145–147. doi: 10.1038/339145a0. [DOI] [PubMed] [Google Scholar]
- Gupta R. S., Golding G. B. Evolution of HSP70 gene and its implications regarding relationships between archaebacteria, eubacteria, and eukaryotes. J Mol Evol. 1993 Dec;37(6):573–582. doi: 10.1007/BF00182743. [DOI] [PubMed] [Google Scholar]
- Hashimoto T., Hasegawa M. Origin and early evolution of eukaryotes inferred from the amino acid sequences of translation elongation factors 1alpha/Tu and 2/G. Adv Biophys. 1996;32:73–120. doi: 10.1016/0065-227x(96)84742-3. [DOI] [PubMed] [Google Scholar]
- Hilario E., Gogarten J. P. Horizontal transfer of ATPase genes--the tree of life becomes a net of life. Biosystems. 1993;31(2-3):111–119. doi: 10.1016/0303-2647(93)90038-e. [DOI] [PubMed] [Google Scholar]
- Hori H., Osawa S. Origin and evolution of organisms as deduced from 5S ribosomal RNA sequences. Mol Biol Evol. 1987 Sep;4(5):445–472. doi: 10.1093/oxfordjournals.molbev.a040455. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Jones D. T., Taylor W. R., Thornton J. M. The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci. 1992 Jun;8(3):275–282. doi: 10.1093/bioinformatics/8.3.275. [DOI] [PubMed] [Google Scholar]
- Kuhner M. K., Felsenstein J. A simulation comparison of phylogeny algorithms under equal and unequal evolutionary rates. Mol Biol Evol. 1994 May;11(3):459–468. doi: 10.1093/oxfordjournals.molbev.a040126. [DOI] [PubMed] [Google Scholar]
- Lake J. A. Origin of the eukaryotic nucleus determined by rate-invariant analysis of rRNA sequences. Nature. 1988 Jan 14;331(6152):184–186. doi: 10.1038/331184a0. [DOI] [PubMed] [Google Scholar]
- Lake J. A. Reconstructing evolutionary trees from DNA and protein sequences: paralinear distances. Proc Natl Acad Sci U S A. 1994 Feb 15;91(4):1455–1459. doi: 10.1073/pnas.91.4.1455. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Leffers H., Kjems J., Ostergaard L., Larsen N., Garrett R. A. Evolutionary relationships amongst archaebacteria. A comparative study of 23 S ribosomal RNAs of a sulphur-dependent extreme thermophile, an extreme halophile and a thermophilic methanogen. J Mol Biol. 1987 May 5;195(1):43–61. doi: 10.1016/0022-2836(87)90326-3. [DOI] [PubMed] [Google Scholar]
- Martin W., Brinkmann H., Savonna C., Cerff R. Evidence for a chimeric nature of nuclear genomes: eubacterial origin of eukaryotic glyceraldehyde-3-phosphate dehydrogenase genes. Proc Natl Acad Sci U S A. 1993 Sep 15;90(18):8692–8696. doi: 10.1073/pnas.90.18.8692. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nei M., Chakraborty R., Fuerst P. A. Infinite allele model with varying mutation rate. Proc Natl Acad Sci U S A. 1976 Nov;73(11):4164–4168. doi: 10.1073/pnas.73.11.4164. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Olsen G. J., Woese C. R., Overbeek R. The winds of (evolutionary) change: breathing new life into microbiology. J Bacteriol. 1994 Jan;176(1):1–6. doi: 10.1128/jb.176.1.1-6.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Potter S., Durovic P., Dennis P. P. Ribosomal RNA precursor processing by a eukaryotic U3 small nucleolar RNA-like molecule in an archaeon. Science. 1995 May 19;268(5213):1056–1060. doi: 10.1126/science.7538698. [DOI] [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]
- Rivera M. C., Lake J. A. Evidence that eukaryotes and eocyte prokaryotes are immediate relatives. Science. 1992 Jul 3;257(5066):74–76. doi: 10.1126/science.1621096. [DOI] [PubMed] [Google Scholar]
- Tateno Y., Takezaki N., Nei M. Relative efficiencies of the maximum-likelihood, neighbor-joining, and maximum-parsimony methods when substitution rate varies with site. Mol Biol Evol. 1994 Mar;11(2):261–277. doi: 10.1093/oxfordjournals.molbev.a040108. [DOI] [PubMed] [Google Scholar]
- Wolters J., Erdmann V. A. The structure and evolution of archaebacterial ribosomal RNAs. Can J Microbiol. 1989 Jan;35(1):43–51. doi: 10.1139/m89-007. [DOI] [PubMed] [Google Scholar]