1887

Abstract

The major outer-membrane protein of , OprF, is multifunctional. It is a non-specific porin that plays a role in maintenance of cell shape, in growth in a low-osmolarity environment, and in adhesion to various supports or molecules. OprF has been studied extensively for its utility as a vaccine component, its role in antimicrobial drug resistance, and its porin function. The authors have previously shown important differences between the OprF and 16S rDNA phylogenies: isolates split into two quite separate clusters, probably according to their ecological niche. In this study, the evolutionary history of the gene was investigated further. The study of G+C content at the third codon position, synonymous codon usage (codon adaptation index, CAI) and genomic context showed no evidence of horizontal transfer or gene duplication. Similarly, a robust likelihood test of incongruence showed no significant incongruence between the phylogeny and the species phylogeny. In addition, the ratio of nonsynonymous mutations to synonymous mutations ( / ) is high between the different clusters, especially between the two clusters containing isolates, highlighting important modifications in evolutionary constraints during the history of the gene. Since OprF is known as a pleiotropic protein, modifications in evolutionary constraints could have resulted from variations in cryptic functions, correlated with the ecological fingerprint. Finally, relaxed constraints and/or episodic positive evolution, especially for some strains, could have led to a phylogeny reconstruction artifact.

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2006-04-01
2024-03-28
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References

  1. Aagot N, Nybroe O, Nielsen P, Johnsen K. 2001; An altered Pseudomonas diversity is recovered from soil by using nutrient-poor Pseudomonas -selective soil extract media. Appl Environ Microbiol 67:5233–5239 [CrossRef]
    [Google Scholar]
  2. Ait Tayeb L, Ageron E, Grimont F, Grimont P. A. D. 2005; Molecular phylogeny of the genus Pseudomonas based on rpoB sequences and application for the identification of isolates. Res Microbiol 156:763–773 [CrossRef]
    [Google Scholar]
  3. Anzai Y, Kim H, Park J, Wakabayashi H, Oyaizu H. 2000; Phylogenetic affiliation of the pseudomonads based on 16S rRNA sequence. Int J Syst Evol Microbiol 50:1563–1589 [CrossRef]
    [Google Scholar]
  4. Bellido F, Martin N, Siehnel R, Hancock R. 1992; Reevaluation, using intact cells, of the exclusion limit and role of porin OprF in Pseudomonas aeruginosa outer membrane permeability. J Bacteriol 174:5196–5203
    [Google Scholar]
  5. Bodilis J, Calbrix R, Guerillon J, Merieau A, Pawlak B, Orange N, Barray S. 2004; Phylogenetic relationships between environmental and clinical isolates of Pseudomonas fluorescens and related species deduced from 16S rRNA gene and OprF protein sequences. Syst Appl Microbiol 27:93–108 [CrossRef]
    [Google Scholar]
  6. Brinkman F. S, Schoofs G, Hancock R. E, de Mot R. 1999; Influence of a putative ECF sigma factor on expression of the major outer membrane protein, OprF, in Pseudomonas aeruginosa and Pseudomonas fluorescens . J Bacteriol 181:4746–4754
    [Google Scholar]
  7. Brinkman F. S, Bains M, Hancock R. E. 2000; The amino terminus of Pseudomonas aeruginosa outer membrane protein OprF forms channels in lipid bilayer membranes: correlation with a three-dimensional model. J Bacteriol 182:5251–5255 [CrossRef]
    [Google Scholar]
  8. Dé E, de Mot R, Orange N, Saint N, Molle G. 1995; Channel-forming properties and structural homology of major outer membrane proteins from Pseudomonas fluorescens MFO and OE 28.3. FEMS Microbiol Let 127:267–272 [CrossRef]
    [Google Scholar]
  9. Dé E, Orange N, Saint N, Guerillon J, Molle G, de Mot R. 1997; Growth temperature dependence of channel size of the major outer- membrane protein (OprF) in psychrotrophic Pseudomonas fluorescens strains. Microbiology 143:1029–1035 [CrossRef]
    [Google Scholar]
  10. de Mot R., Vanderleyden J. 1994; A conserved surface-exposed domain in major outer membrane proteins of pathogenic Pseudomonas and Branhamella species shares sequence homology with the calcium-binding repeats of the eukaryotic extracellular matrix protein thrombospondin. Mol Microbiol 13:379–380 [CrossRef]
    [Google Scholar]
  11. de Mot R, Proost P, Vanderleyden J, van Damme J. 1992; Homology of the root adhesin of Pseudomonas fluorescens OE 28.3 with porin F of P. aeruginosa and P. syringae . Mol Gen Genet 231:489–493 [CrossRef]
    [Google Scholar]
  12. de Mot R, Schoofs G, Roelandt A, Declerck P, Proost P, Van Damme J, Vanderleyden J. 1994; Molecular characterization of the major outer-membrane protein OprF from plant root-colonizing Pseudomonas fluorescens . Microbiology 140:1377–1387 [CrossRef]
    [Google Scholar]
  13. Endo T, Ikeo K, Gojobori T. 1996; Large-scale search for genes on which positive selection may operate. Mol Biol Evol 13:685–690 [CrossRef]
    [Google Scholar]
  14. Herbeck J. T, Wall D. P, Wernegreen J. J. 2003; Gene expression level influences amino acid usage, but not codon usage, in the tsetse fly endosymbiont Wigglesworthia . Microbiology 149:2585–2596 [CrossRef]
    [Google Scholar]
  15. Hilario E, Buckley T, Young J. 2004; Improved resolution on the phylogenetic relationships among Pseudomonas by the combined analysis of atpD , carA , recA and 16S rDNA. Antonie van Leeuwenhoek 86:51–64 [CrossRef]
    [Google Scholar]
  16. Jaouen T, De E, Chevalier S, Orange N. 2004; Pore size dependence on growth temperature is a common characteristic of the major outer membrane protein OprF in psychrotrophic and mesophilic Pseudomonas species. Appl Environ Microbiol 70:6665–6669 [CrossRef]
    [Google Scholar]
  17. Jukes T, Cantor C. 1969; Evolution of Protein Molecules. Mammalian Protein Metabolism New York: Academic Press;
    [Google Scholar]
  18. Kersters K, Ludwig W, Vancanneyt M, Gillis M, Schleifer K.-H, de Vos P. 1996; Recent changes in the classification of the pseudomonads: an overview. Syst Appl Microbiol 19:465–477 [CrossRef]
    [Google Scholar]
  19. Kimura M. 1980; A simple method for estimation of evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120 [CrossRef]
    [Google Scholar]
  20. Kumar S, Tamura K, Jakobsen I. B, Nei M. 2001; mega2: molecular evolutionary genetics analysis software. Bioinformatics 17:1244–1245 [CrossRef]
    [Google Scholar]
  21. Lafay B, Atherton J. C, Sharp P. M. 2000; Absence of translationally selected synonymous codon usage bias in Helicobacter pylori . Microbiology 146:851–860
    [Google Scholar]
  22. Messier W, Stewart C.-B. 1997; Episodic adaptative evolution of primate lysozymes. Nature 385:151–154 [CrossRef]
    [Google Scholar]
  23. Moore E. R. B, Mau M, Arnscheidt A, Collins M, Wachter R, Timmis K. N, Böttger E, Hutson R, Van de Peer Y. 1996; The determination and comparison of the 16S rRNA gene sequences of species of the genus Pseudomonas (sensu stricto) and estimation of the natural intrageneric relationships. Syst Appl Microbiol 19:478–492 [CrossRef]
    [Google Scholar]
  24. Muto A, Osawa S. 1987; The guanine and cytosine content of genomic DNA and bacterial evolution. Proc Natl Acad Sci U S A 84:166–169 [CrossRef]
    [Google Scholar]
  25. Nikaido H. 2003; Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev 67:593–656 [CrossRef]
    [Google Scholar]
  26. Orange N. 1994; Growth temperature regulates the induction of beta-lactamase in Pseudomonas fluorescens through modulation of the outer membrane permeation of a beta-lactam-inducing antibiotic. Microbiology 140:3125–3130 [CrossRef]
    [Google Scholar]
  27. Palacios C, Wernegreen J. J. 2002; A strong effect of AT mutational bias on amino acid usage in Buchnera is mitigated at high-expression genes. Mol Biol Evol 19:1575–1584 [CrossRef]
    [Google Scholar]
  28. Pautsch A, Schlulz G. 1998; Structure of the outer membrane protein A transmembrane domain. Nat Struct Biol 5:1013–1017 [CrossRef]
    [Google Scholar]
  29. Ramette A, Moenne-Loccoz Y, Defago G. 2001; Polymorphism of the polyketide synthase gene phlD in biocontrol fluorescent pseudomonads producing 2,4-diacetylphloroglucinol and comparison of PhID with plant polyketide synthases. Mol Plant Microbe Interact 14:639–652 [CrossRef]
    [Google Scholar]
  30. Rawling E, Martin N, Hancock R. 1995; Epitope mapping of the Pseudomonas aeruginosa major outer membrane porin protein OprF. Infect Immun 63:38–42
    [Google Scholar]
  31. Rawling E. G, Brinkman F. S, Hancock R. E. 1998; Roles of the carboxy-terminal half of Pseudomonas aeruginosa major outer membrane protein OprF in cell shape, growth in low-osmolarity medium, and peptidoglycan association. J Bacteriol 180:3556–3562
    [Google Scholar]
  32. Rebière-Huët J, Di Martino P, Gallet O, Hulen C. 1999; Interaction of Pseudomonas aeruginosa outer membrane proteins with plasmatic fibronectin. A root for new bacterial adhesins. C R Acad Sci Paris 322:1071–1080 [CrossRef]
    [Google Scholar]
  33. Rediers H, Vanderleyden J, de Mot R. 2004; Azotobacter vinelandii : a Pseudomonas in disguise?. Microbiology 150:1117–1119 [CrossRef]
    [Google Scholar]
  34. Rice P, Longden I, Bleasby A. 2000; emboss: the European Molecular Biology Open Software Suite. Trends Genet 16:276–277 [CrossRef]
    [Google Scholar]
  35. Saitou N, Nei M. 1987; The neighbor-joining method: a new method for reconstructing phylogenetic tree. Mol Biol Evol 4:406–425
    [Google Scholar]
  36. Sharp P, Li W. 1987; The codon adaptation index – a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 15:1281–1295 [CrossRef]
    [Google Scholar]
  37. Shimodaira H, Hasegawa M. 1999; Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 16:1114–1116 [CrossRef]
    [Google Scholar]
  38. Tamber S, Hancock R. 2004; The outer membranes of pseudomonads. In Pseudomonas pp  575–601 Edited by Ramos J. L. New York: Plenum;
    [Google Scholar]
  39. Thompson J. D, Gibson T. J, Plewniak F, Jeanmougin F, Higgins D. G. 1997; The clustal_x windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882 [CrossRef]
    [Google Scholar]
  40. Vermeiren H, Willems A, Schoofs G, De Mot R, Keijers V, Hai W, Vanderleyden J. 1999; The rice inoculant strain Alcaligenes faecalis A15 is a nitrogen-fixing Pseudomonas stutzeri . Syst Appl Microbiol 22:215–224 [CrossRef]
    [Google Scholar]
  41. von Specht B, Knapp B, Muth G, Broker M, Hungerer K, Diehl K, Massarrat K, Seemann A, Domdey H. 1995; Protection of immunocompromised mice against lethal infection with Pseudomonas aeruginosa by active or passive immunization with recombinant P. aeruginosa outer membrane protein F and outer membrane protein I fusion proteins. Infect Immun 63:1855–1862
    [Google Scholar]
  42. Woese C. R. 1987; Bacterial evolution. Microbiol Rev 51:221–271
    [Google Scholar]
  43. Woodruff W, Hancock R. 1989; Pseudomonas aeruginosa outer membrane protein F: structural role and relationship to the Escherichia coli OmpA protein. J Bacteriol 171:3304–3309
    [Google Scholar]
  44. Worgall S, Krause A, Rivara M. 8 other authors 2005; Protection against P. aeruginosa with an adenovirus vector containing an OprF epitope in the capsid. J Clin Invest 115:1281–1289 [CrossRef]
    [Google Scholar]
  45. Wu L, Estrada O, Zaborina O. 12 other authors 2005; Recognition of host immune activation by Pseudomonas aeruginosa . Science 309:774–777 [CrossRef]
    [Google Scholar]
  46. Yamamoto S, Kasai H, Arnold D. L, Jackson R. W, Vivian A, Harayama S. 2000; Phylogeny of the genus Pseudomonas : intrageneric structure reconstructed from the nucleotide sequences of gyrB and rpoD genes. Microbiology 146:2385–2394
    [Google Scholar]
  47. Yang Z, Nielsen R. 2002; Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol Biol Evol 19:908–917 [CrossRef]
    [Google Scholar]
  48. Yang Z, Nielsen R, Goldman N, Pedersen A.-M. K. 2000; Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155:431–449
    [Google Scholar]
  49. Zhang J, Rosenberg H. F, Nei M. 1998; Positive Darwinian selection after gene duplication in primate ribonuclease genes. Proc Natl Acad Sci U S A 95:3708–3713 [CrossRef]
    [Google Scholar]
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