Skip to main content
SpringerLink
Log in

Selection for Highly Biased Amino Acid Frequency in the TolA Cell Envelope Protein of Proteobacteria

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

Abstract

The bacterial cell envelope protein TolA functions to maintain the integrity of the cell membrane. This protein contains high levels of alanine and lysine that are used in the formation of alpha helices, which are required for normal protein function. The neutral model of molecular evolution predicts that amino acid composition and nucleotide composition are driven by the underlying GC content, as a result of mutation bias. However, this study shows that selection has acted to maintain high levels of alanine and lysine in the TolA protein of Proteobacteria, which in turn has biased nucleotide composition in the corresponding tolA gene.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2

Similar content being viewed by others

References

  1. H Akashi T Gojobori (2002) ArticleTitleMetabolic efficiency and amino acid composition in the proteomes of Escherichia coli and Bacillus subtilis. Proc Natl Acad Sci USA 99 3695–3700 Occurrence Handle10.1073/pnas.062526999 Occurrence Handle1:CAS:528:DC%2BD38Xis1Kltr4%3D Occurrence Handle11904428

    Article  CAS  PubMed  Google Scholar 

  2. SF Altschul TL Madden AA Schaffer J Zhang Z Zhang W Miller DJ Lipman (1997) ArticleTitleGapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res 25 3389–3402 Occurrence Handle9254694

    PubMed  Google Scholar 

  3. G Bernardi (2000) ArticleTitleThe compositional evolution of vertebrate genomes. Gene 259 31–43 Occurrence Handle10.1016/S0378-1119(00)00441-8 Occurrence Handle1:CAS:528:DC%2BD3MXitV2msg%3D%3D Occurrence Handle11163959

    Article  CAS  PubMed  Google Scholar 

  4. G Bernardi G Bernardi (1986) ArticleTitleCompositional constraints and genome evolution. J Mol Evol 24 1–11 Occurrence Handle1:CAS:528:DyaL2sXhvFWgtr8%3D Occurrence Handle3104608

    CAS  PubMed  Google Scholar 

  5. L Chao BR Levin (1981) ArticleTitleStructured habitats and the evolution of anticompetitor toxins in bacteria. Proc Natl Acad Sci USA 78 6324–6328 Occurrence Handle1:CAS:528:DyaL3MXlvVersL8%3D Occurrence Handle7031647

    CAS  PubMed  Google Scholar 

  6. MA Clark NA Moran P Baumann (1999) ArticleTitleSequence evolution in bacterial endosymbionts having extreme base compositions. Mol Biol Evol 16 1586–1598 Occurrence Handle1:CAS:528:DyaK1MXntlKjs70%3D Occurrence Handle10555290

    CAS  PubMed  Google Scholar 

  7. JJ Dennis ER Lafontaine PA Sokol (1996) ArticleTitleIdentification and characterization of the tolQRA genes of Pseudomonas aeruginosa. J Bacteriol 178 7059–7068 Occurrence Handle1:CAS:528:DyaK2sXhtlSguw%3D%3D Occurrence Handle8955385

    CAS  PubMed  Google Scholar 

  8. J Felsenstein (1985) ArticleTitlePhylogenies and the comparative method. Am Nat 125 1–15 Occurrence Handle10.1086/284325

    Article  Google Scholar 

  9. PG Foster LS Jermiin DA Hickey (1997) ArticleTitleNucleotide composition bias affects amino acid content in proteins coded by animal mitochondria. J Mol Evol 44 282–288 Occurrence Handle1:CAS:528:DyaK2sXhs1Gls70%3D Occurrence Handle9060394

    CAS  PubMed  Google Scholar 

  10. X Gu D Hewett-Emmett WH Li (1998) ArticleTitleDirectional mutational pressure affects the amino acid composition and hydrophobicity of proteins in bacteria. Genetica 102–103 383–391 Occurrence Handle10.1023/A:1017028102013

    Article  Google Scholar 

  11. PH Harvey MD Pagel (1991) The comparative methods in evolutionary biology. Oxford University Press Oxford

    Google Scholar 

  12. AJ Heilpern MK Waldor (2000) ArticleTitleCTXφ infection of Vibrio cholerae requires the tolQRA gene products. J Bacteriol 182 1739–1747 Occurrence Handle10.1128/JB.182.6.1739-1747.2000 Occurrence Handle1:CAS:528:DC%2BD3cXhsVGltLc%3D Occurrence Handle10692381

    Article  CAS  PubMed  Google Scholar 

  13. TH Jukes V Bhushan (1986) ArticleTitleSilent nucleotide substitutions and G + C content of some mitochondrial and bacterial genes. J Mol Evol 24 39–44 Occurrence Handle1:CAS:528:DyaL2sXhtFClsbw%3D Occurrence Handle3104617

    CAS  PubMed  Google Scholar 

  14. TH Jukes CR Cantor (1969) Evolution of protein molecules. HN Munro (Eds) Mammalian protein metabolism. Academic Press New York 21–132

    Google Scholar 

  15. S Karlin BE Blaisdell P Bucher (1992) ArticleTitleQuantile distributions of amino acid usage in protein classes. Protein Eng 5 729–738 Occurrence Handle1:CAS:528:DyaK3sXhsVajtr8%3D Occurrence Handle1287653

    CAS  PubMed  Google Scholar 

  16. M Kimura (1968) ArticleTitleEvolutionary rate at the molecular level. Nature 217 624–626 Occurrence Handle5637732

    PubMed  Google Scholar 

  17. M Kimura (1980) ArticleTitleA simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16 111–120 Occurrence Handle7463489

    PubMed  Google Scholar 

  18. M Kimura (1983) The neutral theory of molecular evolution. Cambridge University Press Cambridge

    Google Scholar 

  19. JL King TH Jukes (1969) ArticleTitleNon-Darwinian evolution. Science 164 788–798 Occurrence Handle1:CAS:528:DyaF1MXktFyks7s%3D Occurrence Handle5767777

    CAS  PubMed  Google Scholar 

  20. S Kumar K Tamura IB Jakobsen M Nei (2001) ArticleTitleMEGA2: Molecular evolutionary genetics analysis software. Bioinformatics 17 1244–1245 Occurrence Handle1:CAS:528:DC%2BD38XmtVCktQ%3D%3D Occurrence Handle11751241

    CAS  PubMed  Google Scholar 

  21. JC Lazzaroni P Germon MC Ray A Vianney (1999) ArticleTitleThe Tol proteins of Escherichia coli and their involvement in the uptake of biomolecules and outer membrane stability. FEMS Microbiol Lett 177 191–197 Occurrence Handle10.1016/S0378-1097(99)00293-1 Occurrence Handle1:CAS:528:DyaK1MXkvVequrk%3D Occurrence Handle10474183

    Article  CAS  PubMed  Google Scholar 

  22. SK Levengood RE Webster (1989) ArticleTitleNucleotide sequences of the tolA and tolB genes and localization of their products, components of a multistep translocation system in Escherichia coli. J Bacteriol 171 6600–6609 Occurrence Handle1:CAS:528:DyaK3cXhsFalsbk%3D Occurrence Handle2687247

    CAS  PubMed  Google Scholar 

  23. SK Levengood WF Beyer Jr RE Webster (1991) ArticleTitleTolA: A membrane protein involved in colicin uptake contains an extended helical region. Proc Natl Acad Sci USA 88 5939–5943 Occurrence Handle1:CAS:528:DyaK3MXkvVOku7o%3D Occurrence Handle2068069

    CAS  PubMed  Google Scholar 

  24. WH Li (1997) Molecular evolution. Sinauer Sunderland, MA

    Google Scholar 

  25. MA Llamas JL Ramos JJ Rodríguez-Herva (2000) ArticleTitleMutations in each of the tol genes of Pseudomonas putida reveal that they are critical for maintenance of outer membrane stability. J Bacteriol 182 4764–4772 Occurrence Handle10.1128/JB.182.17.4764-4772.2000 Occurrence Handle1:CAS:528:DC%2BD3cXlvFajt78%3D Occurrence Handle10940016

    Article  CAS  PubMed  Google Scholar 

  26. R Lloubès E Cascales A Walburger E Bouveret C Lazdunski A Bernadac L Journet (2001) ArticleTitleThe Tol-Pal proteins of the Escherichia coli envelope: An energized system required for outer membrane integrity? Res Microbiol 152 523–529 Occurrence Handle10.1016/S0923-2508(01)01226-8 Occurrence Handle11501670

    Article  PubMed  Google Scholar 

  27. S Marqusee RL Baldwin (1987) ArticleTitleHelix stabilization by Glu−...Lys+ salt bridges in short peptides of de novo design. Proc Natl Acad Sci USA 84 8898–8902 Occurrence Handle1:CAS:528:DyaL1cXhs1ent7Y%3D Occurrence Handle3122208

    CAS  PubMed  Google Scholar 

  28. S Marqusee VH Robbins RL Baldwin (1989) ArticleTitleUnusually stable helix formation in short alanine-based peptides. Proc Natl Acad Sci USA 86 5286–5290 Occurrence Handle1:CAS:528:DyaK3cXhsFyqsbw%3D Occurrence Handle2748584

    CAS  PubMed  Google Scholar 

  29. M Nei (1987) Molecular evolutionary genetics. Columbia University Press New York

    Google Scholar 

  30. M Nei S Kumar (2000) Molecular evolution and phylogenetics. Oxford University Press Oxford

    Google Scholar 

  31. M Nishizawa K Nishizawa (1998) ArticleTitleBiased usage of arginines and lysines in proteins are correlated with local-scale fluctuations of the G + C content of DNA sequences. J Mol Evol 47 385–393 Occurrence Handle1:CAS:528:DyaK1cXms1WlsL8%3D Occurrence Handle9767684

    CAS  PubMed  Google Scholar 

  32. S Osawa TH Jukes K Watanabe A Muto (1992) ArticleTitleRecent evidence for evolution of the genetic code. Microbiol Rev 56 229–264 Occurrence Handle1:CAS:528:DyaK38Xit12jtrw%3D Occurrence Handle1579111

    CAS  PubMed  Google Scholar 

  33. C Palacios JJ Wernegreen (2002) ArticleTitleA strong effect of AT mutational bias on amino acid usage in Buchnera is mitigated at high-expression genes. Mol Biol Evol 19 1575–1584 Occurrence Handle1:CAS:528:DC%2BD38XntVyhtLg%3D Occurrence Handle12200484

    CAS  PubMed  Google Scholar 

  34. MA Riley DM Gordon (1999) ArticleTitleThe ecological role of bacteriocins in bacterial competition. Trends Microbiol 7 129–133 Occurrence Handle10.1016/S0966-842X(99)01459-6 Occurrence Handle1:STN:280:DyaK1M3is1ejsg%3D%3D Occurrence Handle10203843

    Article  CAS  PubMed  Google Scholar 

  35. MA Riley JE Wertz (2002) ArticleTitleBacteriocins: Evolution, ecology, and application. Annu Rev Microbiol 56 117–137 Occurrence Handle10.1146/annurev.micro.56.012302.161024 Occurrence Handle1:CAS:528:DC%2BD38Xos1Gis78%3D Occurrence Handle12142491

    Article  CAS  PubMed  Google Scholar 

  36. JJ Rodríguez-Herva MI Ramos-González JL Ramos (1996) ArticleTitleThe Pseudomonas putida peptidoglycan-associated outer membrane lipoprotein is involved in maintenance of the integrity of the cell envelope. J Bacteriol 178 1699–16706 Occurrence Handle8626299

    PubMed  Google Scholar 

  37. AP Rooney J Zhang M Nei (2000) ArticleTitleAn unusual form of purifying selection in a sperm DNA-binding protein. Mol Biol Evol 17 278–283 Occurrence Handle1:CAS:528:DC%2BD3cXosFynsw%3D%3D Occurrence Handle10677850

    CAS  PubMed  Google Scholar 

  38. RP Ross S Morgan C Hill (2002) ArticleTitlePreservation and fermentation: Past, present and future. Int J Food Microbiol 79 3–16 Occurrence Handle10.1016/S0168-1605(02)00174-5 Occurrence Handle12382680

    Article  PubMed  Google Scholar 

  39. N Saitou M Nei (1987) ArticleTitleThe neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol 4 406–425 Occurrence Handle1:STN:280:BieC1cbgtVY%3D Occurrence Handle3447015

    CAS  PubMed  Google Scholar 

  40. GA Singer DA Hickey (2000) ArticleTitleNucleotide bias causes a genome-wide bias in the amino acid composition of proteins. Mol Biol Evol 17 1581–1588 Occurrence Handle1:CAS:528:DC%2BD3cXnvFyqsbY%3D Occurrence Handle11070046

    CAS  PubMed  Google Scholar 

  41. N Sueoka (1961) ArticleTitleCorrelation between base composition of deoxyribonucleotic acid and amino acid composition of protein. Proc Natl Acad Sci USA 47 1141–1149 Occurrence Handle1:CAS:528:DyaF38XjsVGh

    CAS  Google Scholar 

  42. N Sueoka (1962) ArticleTitleOn the genetic basis of variation and heterogeneity of DNA base composition. Proc Natl Acad Sci USA 48 582–592 Occurrence Handle1:CAS:528:DyaF38XktlSqtbY%3D Occurrence Handle13918161

    CAS  PubMed  Google Scholar 

  43. N Sueoka (1988) ArticleTitleDirectional mutation pressure and neutral molecular evolution. Proc Natl Acad Sci USA 85 2653–2657 Occurrence Handle1:CAS:528:DyaL1cXktF2isbc%3D Occurrence Handle3357886

    CAS  PubMed  Google Scholar 

  44. TP Sun RE Webster (1987) ArticleTitleNucleotide sequence of a gene cluster involved in entry of E colicins and single-stranded DNA of infecting filamentous bacteriophages into Escherichia coli. J Bacteriol 169 2667–2674 Occurrence Handle1:CAS:528:DyaL2sXls12lsb0%3D Occurrence Handle3294803

    CAS  PubMed  Google Scholar 

  45. JD Thompson TJ Gibson F Plewniak F Jeanmougin DG Higgins (1997) ArticleTitleThe CLUSTAL_X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25 4876–4882 Occurrence Handle1:CAS:528:DyaK1cXntFyntQ%3D%3D Occurrence Handle9396791

    CAS  PubMed  Google Scholar 

  46. A Tibor V Weynants P Denoel B Lichtfouse X De Bolle E Saman JN Limet JJ Letesson (1994) ArticleTitleMolecular cloning, nucleotide sequence, and occurrence of a 16.5-kilodalton outer membrane protein of Brucella abortus with similarity to pal lipoproteins. Infect Immun 62 3633–3639 Occurrence Handle1:CAS:528:DyaK2MXlvVaqsQ%3D%3D Occurrence Handle8063379

    CAS  PubMed  Google Scholar 

  47. HC Wang DA Hickey (2002) ArticleTitleEvidence for strong selective constraint acting on the nucleotide composition of 16S ribosomal RNA genes. Nucleic Acids Res 30 2501–2507 Occurrence Handle10.1093/nar/30.11.2501 Occurrence Handle1:CAS:528:DC%2BD38XkvV2hs7Y%3D Occurrence Handle12034839

    Article  CAS  PubMed  Google Scholar 

  48. J Zhang HF Rosenberg M Nei (1998) ArticleTitlePositive Darwinian selection after gene duplication in primate ribonuclease genes. Proc Natl Acad Sci USA 95 3708–3713 Occurrence Handle10.1073/pnas.95.7.3708 Occurrence Handle1:CAS:528:DyaK1cXitlKjtrc%3D Occurrence Handle9520431

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Helpful comments were provided by C.P. Kurtzman, D.P. Labeda, T.J. Ward, J. Zhang, and two anonymous reviewers.

Author information

Authors and Affiliations

  1. Microbial Genomics and Bioprocessing Research Unit, National Center for Agricultural Utilization Research, Agricultural Research Service, U.S. Department of Agriculture, Peoria, IL 61604, USA

    Alejandro P. Rooney

Authors
  1. Alejandro P. Rooney
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alejandro P. Rooney.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rooney, A.P. Selection for Highly Biased Amino Acid Frequency in the TolA Cell Envelope Protein of Proteobacteria . J Mol Evol 57, 731–736 (2003). https://doi.org/10.1007/s00239-003-2530-6

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-003-2530-6

Keywords

Search

Navigation