Advertisement

Journal of Molecular Evolution

, Volume 65, Issue 3, pp 228–235 | Cite as

Molecular Evidence for the Ancient Origin of the Ribosomal Protection Protein That Mediates Tetracycline Resistance in Bacteria

  • Takeshi Kobayashi
  • Lisa NonakaEmail author
  • Fumito Maruyama
  • Satoru Suzuki
Article

Abstract

The ribosomal protection proteins (RPPs) mediate the resistance to tetracycline (TC) in Gram-positive and Gram-negative bacteria. The RPPs display sequence similarity to translation elongation factors, EF-G/EF-2 and EF-Tu/EF-1α. To determine the evolutionary origin of the RPPs, we constructed a composite phylogenetic tree of the RPPs, EF-G/EF-2 and EF-Tu/EF-1α. This tree includes two universal trees for the EF-G/EF-2 and EF-Tu/EF-1α, which form clusters corresponding to the respective two groups of proteins from three superkingdoms. The cluster of RPPs was placed at a point between the EF-G/EF-2 and EF-Tu/EF-1α clusters. The branch length (substitutions/site) between the node for the RPP cluster and the primary divergence of the RPPs was statistically shorter than that between the node for this cluster and the primary divergence in the EF-G/EF-2 cluster. This indicates that the RPPs derived through duplication and divergence of the ancient GTPase before the divergence of the three superkingdoms. Furthermore, this suggests the RPPs’ extant function occurred before the streptomycetes that include the TC-producing strains. Therefore, the RPPs evolved independent of the presence of TCs and serve a function other than antibiotic resistance. The RPPs may provide ribosomal protection against other chemical substances in the environment.

Keywords

Bacteria Antibiotic Tetracycline Resistance Ribosomal protection protein Evolution Origin EF-G/EF-2 EF-Tu/EF-1α Composite phylogenetic tree 

Notes

Acknowledgments

We thank Ms. Annie Marlow for proofreading the manuscript. This work was supported by the 21st Century COE Program from the Japanese Ministry of Education, Culture, Sports, Science and Technology (MEXT); by a Sasagawa Scientific Research Grant from The Japan Science Society; and by the Mitsubishi Foundation from the Mitsubishi Group.

References

  1. Adachi J, Hasegawa M (1996) MOLPHY version 2.3: Programs for molecular phylogenetics based on maximum likelihood. Comput Sci Monogr Inst Stat Math 28:1–150Google Scholar
  2. Aminov RI, Garrigues-Jeanjean N, Mackie RI (2001) Molecular ecology of tetracycline resistance: development and validation of primers for detection of tetracycline resistance genes encoding ribosomal protection proteins. Appl Environ Microbiol 67:22–32PubMedCrossRefGoogle Scholar
  3. Benveniste R, Davies J (1973) Aminoglycoside antibiotic-inactivation enzymes in actinomycetes similar to those present in clinical isolates of antibiotic resistant bacteria. Proc Natl Acad Sci U S A 172:3628–3632Google Scholar
  4. Bromhan L, Penny D (2003) The modern molecular clock. Nat Rev Genet 4:216–224CrossRefGoogle Scholar
  5. Chopra I, Roberts M (2001) Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol Mol Biol Rev 65:232–260PubMedCrossRefGoogle Scholar
  6. Connell SR, Tracz DM, Nierhaus KH, Taylor DE (2003) Ribosomal protection proteins and their mechanism of tetracycline resistance. Antimicrob Agents Chemother 47:3675–3681PubMedCrossRefGoogle Scholar
  7. Cundliffe E, Bate N, Butler A, Fish S, Gandecha A, Merson-Davies L (2001) The tylosin-biosynthetic genes of Streptomyces fradiae. Antonie Leeuwenhoek 79:229–234PubMedCrossRefGoogle Scholar
  8. Deckert G, Warren PV, Gaasterland T, Young WG, Lenox AL, Graham DE, Overbeek R, Snead MA, Keller M, Aujay M, Huber R, Feldman RA, Short JM, Olsen GJ, Swanson RV (1998) The complete genome of the hyperthermophilic bacterium Aquifex aeolicus. Nature 392:353–358PubMedCrossRefGoogle Scholar
  9. Hubbard BK, Walsh CT (2003) Vancomycin assembly: Nature’s way. Chem Int Ed Eng l42:730–765CrossRefGoogle Scholar
  10. Huelsenbeck JP, Ronquist F (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755PubMedCrossRefGoogle Scholar
  11. Iwabe N, Kuma K, Hasegawa M, Osawa S, Miyata T (1989) Evolutionary relationship of Archaebacteria, Eubacteria, and erukaryotes inferred from phylogenetic trees of duplicated genes. Proc Natl Acad Sci U S A 86:9355–9359PubMedCrossRefGoogle Scholar
  12. Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comp Appl Biosci 8:275–282PubMedGoogle Scholar
  13. Kim SR, Nonaka L, Suzuki S (2004) Occurrence of tetracycline resistance genes tet(M) and tet(S) in bacteria from marine aquaculture sites. FEMS Microbiol Lett 237:147–156PubMedCrossRefGoogle Scholar
  14. Kishino H, Miyata T, Hasegawa M (1990) Maximum likelihood inference of protein phylogeny, and the origin of chloroplasts. J Mol Evol 31:151–160CrossRefGoogle Scholar
  15. Leipe DD, Wolf YI, Koonin EV, Aravind L (2002) Classification and evolution of P-loop GTPases and related ATPases. J Mol Biol 317:41–72PubMedCrossRefGoogle Scholar
  16. Ronquist F, Huelsenbeck JP (2003) MyBayes 3: Bayesian phylogenetic inference under mixed modeles. Bioinformatics 19:1572–1574PubMedCrossRefGoogle Scholar
  17. Sanchez-Pescador R, Brown JT, Roberts M, Urdea MS (1988) Homology of the TetM with translational elongation factors: implications for potential modes of tetM-conferred tetracycline resistance. Nucleic Acids Res 16:1218PubMedCrossRefGoogle Scholar
  18. Taylor JS, Raes J (2004) Duplication and divergence: The evolution of new genes and old ideas. Annu Rev Gen 38:615–643CrossRefGoogle Scholar
  19. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680PubMedCrossRefGoogle Scholar
  20. Woese CR (1987) Bacterial evolution. Microbiol Rev 51:221–271PubMedGoogle Scholar
  21. Yamamoto H, Hiraishi A, Kato K, Chiura HX, Maki Y, Shimizu A (1998) Phylogenetic evidence for the existence of novel thermophilic bacteria in hot spring sulfur-turf microbial mats in Japan. Appl Environ Microbiol 64:1680–1687PubMedGoogle Scholar
  22. Zuckerkandl E, Pauling L (1965) Evolutionary divergence and convergence in proteins. In Bryson V, Vogel HJ (eds) Evolving genes and proteins. Acadmic Press, New York, pp 97–166Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • Takeshi Kobayashi
    • 1
  • Lisa Nonaka
    • 1
    Email author
  • Fumito Maruyama
    • 2
  • Satoru Suzuki
    • 1
  1. 1.Center for Marine Environmental Studies (CMES)Ehime UniversityEhimeJapan
  2. 2.The Institute of Medical ScienceThe University of TokyoTokyoJapan

Personalised recommendations