1887

Abstract

The genus contains over 80 recognized species, and is characterized by a high level of diversity, reflected in its complex phylogeny. The authors' recent determination of the genome sequence of means that five complete genomes of species are available for comparative genomics: , , , and . This paper now shows that there is no extensive synteny of the genome sequences of these five lactobacilli. Phylogeny based on whole-genome alignments suggested that was closer to than to , which was closest to , in contrast to 16S rRNA gene relatedness. A total of 593 orthologues common to all five species were identified. Species relatedness based on this protein set was largely concordant with genome synteny-based relatedness. A supertree, combining individual phylogenetic trees from each of 354 core proteins, had four main branches, comprising ; ; ; and . The extreme divergence of the genomes analysed supports the recognition of new subgeneric divisions.

Keyword(s): GI, gastrointestinal
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2006-11-01
2024-12-03
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References

  1. Ahrne S, Nobaek S, Jeppsson B, Adlerberth I, Wold A. E, Molin G. 1998; The normal Lactobacillus flora of healthy human rectal and oral mucosa. J Appl Microbiol 85:88–94 [CrossRef]
    [Google Scholar]
  2. Altermann E, Russell W. M, Azcarate-Peril M. A. 11 other authors 2005; Complete genome sequence of the probiotic lactic acid bacterium Lactobacillus acidophilus NCFM. Proc Natl Acad Sci U S A 102:3906–3912 [CrossRef]
    [Google Scholar]
  3. Altschul S. F, Madden T. L, Schaffer A. A, Zhang J, Zhang Z, Miller W, Lipman D. J. 1997; Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402 [CrossRef]
    [Google Scholar]
  4. Beijerink M. W. 1901; Sur les ferments lactiques de l'industrie. Arch Néerl Sci Exactes Nat Série II:212–243
    [Google Scholar]
  5. Boekhorst J, Siezen R. J, Zwahlen M. C. 7 other authors 2004; The complete genomes of Lactobacillus plantarum and Lactobacillus johnsonii reveal extensive differences in chromosome organization and gene content. Microbiology 150:3601–3611 [CrossRef]
    [Google Scholar]
  6. Brussow H, Canchaya C, Hardt W. D. 2004; Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol Mol Biol Rev 68:560–602 [CrossRef]
    [Google Scholar]
  7. Cai Y, Benno Y, Ogawa M, Kumai S. 1999; Effect of applying lactic acid bacteria isolated from forage crops on fermentation characteristics and aerobic deterioration of silage. J Dairy Sci 82:520–526 [CrossRef]
    [Google Scholar]
  8. Candela M, Vitali B, Matteuzzi D, Brigidi P. 2004; Evaluation of the rrn operon copy number in Bifidobacterium using real-time PCR. Lett Appl Microbiol 38:229–232 [CrossRef]
    [Google Scholar]
  9. Chaillou S, Champomier-Verges M. C, Cornet M. 8 other authors 2005; The complete genome sequence of the meat-borne lactic acid bacterium Lactobacillus sakei 23K. Nat Biotechnol 23:1527–1533 [CrossRef]
    [Google Scholar]
  10. Chan P. Y, Lam T. W, Yiu S. M. 2006; A more accurate and efficient whole genome phylogeny. In Proceedings of 4th Asia-Pacific Bioinformatics Conference , Taipei, Taiwan pp  337–352 London: Imperial College Press;
    [Google Scholar]
  11. Claesson M. J, Li Y, Leahy S. 12 other authors 2006; Multireplicon genome architecture of Lactobacillus salivarius . Proc Natl Acad Sci U S A 103:6718–6723 [CrossRef]
    [Google Scholar]
  12. Cole J. R, Chai B, Farris R. J, Wang Q, Kulam S. A, McGarrell D. M, Garrity G. M, Tiedje J. M. 2005; The Ribosomal Database Project (RDP-II): sequences and tools for high-throughput rRNA analysis. Nucleic Acids Res 33:D294–D296
    [Google Scholar]
  13. Creevey C. J, McInerney J. O. 2005; Clann: investigating phylogenetic information through supertree analyses. Bioinformatics 21:390–392 [CrossRef]
    [Google Scholar]
  14. Creevey C. J, Fitzpatrick D. A, Philip G. K, Kinsella R. J, O'Connell M. J, Pentony M. M, Travers S. A, Wilkinson M, McInerney J. O. 2004; Does a tree-like phylogeny only exist at the tips in the prokaryotes?. Proc Biol Sci 271:2551–2558 [CrossRef]
    [Google Scholar]
  15. Daubin V, Perriere G. 2003; G+C3 structuring along the genome: a common feature in prokaryotes. Mol Biol Evol 20:471–483 [CrossRef]
    [Google Scholar]
  16. Dellaglio F, Felis G. E. 2005 Taxonomy of lactobacilli and bifidobacteria. Probiotics and Prebiotics: Scientific Aspects pp  25–49 Edited by Tannock G. W. Norfolk, UK: Caister Academic Press;
    [Google Scholar]
  17. Dellaglio F, Felis G. E, Torriani S. 2005; Is the genus Lactobacillus a single genus?. In LAB8 Symposium on Lactic Acid Bacteria Egmond aan Zee, Netherlands: FEMS;
    [Google Scholar]
  18. Dunne C, Murphy L, Flynn S. 12 other authors 1999; Probiotics: from myth to reality. Demonstration of functionality in animal models of disease and in human clinical trials. Antonie Van Leeuwenhoek 76:279–292 [CrossRef]
    [Google Scholar]
  19. Dunne C, O'Mahony L, Murphy L. 11 other authors 2001; In vitro selection criteria for probiotic bacteria of human origin correlation with in vivo findings. Am J Clin Nutr 73:386S–392S
    [Google Scholar]
  20. Eisen J. A, Heidelberg J. F, White O, Salzberg S. L. 2000; Evidence for symmetric chromosomal inversions around the replication origin in bacteria. Genome Biol 1: RESEARCH0011
    [Google Scholar]
  21. Fitch W. M. 1970; Distinguishing homologous from analogous proteins. Syst Zool 19:99–113 [CrossRef]
    [Google Scholar]
  22. Flynn S. 2001 Molecular characterisation of bacteriocin producing genes and plasmid encoded functions of the probiotic strain Lactobacillus salivarius subsp. salivarius UCC118 PhD thesis Department of Microbiology, University College Cork; Ireland:
    [Google Scholar]
  23. Guarner F, Schaafsma G. J. 1998; Probiotics. Int J Food Microbiol 39:237–238 [CrossRef]
    [Google Scholar]
  24. Guindon S, Gascuel O. 2003; A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704 [CrossRef]
    [Google Scholar]
  25. Hammes W. P, Hertel C. 2003; The Genera Lactobacillus and Carnobacterium. In The Prokaryotes , release 3.15 Edited by Dworkin M.
    [Google Scholar]
  26. Hancock J. M. 2005; Gene factories, microfunctionalization and the evolution of gene families. Trends Genet 11:591–595
    [Google Scholar]
  27. Heilig H. G, Zoetendal E. G, Vaughan E. E, Marteau P, Akkermans A. D, de Vos W. M. 2002; Molecular diversity of Lactobacillus spp. and other lactic acid bacteria in the human intestine as determined by specific amplification of 16S ribosomal DNA. Appl Environ Microbiol 68:114–123 [CrossRef]
    [Google Scholar]
  28. Henz S. R, Huson D. H, Auch A. F, Nieselt-Struwe K, Schuster S. C. 2005; Whole-genome prokaryotic phylogeny. Bioinformatics 21:2329–2335 [CrossRef]
    [Google Scholar]
  29. Huson D. H. 1998; SplitsTree: analyzing and visualizing evolutionary data. Bioinformatics 14:68–73 [CrossRef]
    [Google Scholar]
  30. Keane T. M, Page A. J, Naughton T. J, Travers S. A. A, McInerney J. O. 2006; Building large phylogenetic trees on coarse-grained parallel machines. Algorithmica 45:285–300 [CrossRef]
    [Google Scholar]
  31. Klaenhammer T. R, Russell W. M. 2000 In Encyclopedia of Food Microbiology pp  1151–1157 Amsterdam: Elsevier;
    [Google Scholar]
  32. Klaenhammer T. R, Barrangou R, Buck B. L, Azcarate-Peril M. A, Altermann E. 2005; Genomic features of lactic acid bacteria effecting bioprocessing and health. FEMS Microbiol Rev 29:393–409 [CrossRef]
    [Google Scholar]
  33. Kleerebezem M, Boekhorst J, van Kranenburg R. 17 other authors 2003; Complete genome sequence of Lactobacillus plantarum WCFS1. Proc Natl Acad Sci U S A 100:1990–1995 [CrossRef]
    [Google Scholar]
  34. Konings W. N, Kok J, Kuipers O. P, Poolman B. 2000; Lactic acid bacteria: the bugs of the new millennium. Curr Opin Microbiol 3:276–282 [CrossRef]
    [Google Scholar]
  35. Konstantinidis K. T, Tiedje J. M. 2004; Trends between gene content and genome size in prokaryotic species with larger genomes. Proc Natl Acad Sci U S A 101:3160–3165 [CrossRef]
    [Google Scholar]
  36. Korbel J. O, Snel B, Huynen M. A, Bork P. 2002; SHOT: a web server for the construction of genome phylogenies. Trends Genet 18:158–162 [CrossRef]
    [Google Scholar]
  37. Kullen M. J, Sanozky-Dawes R. B, Crowell D. C, Klaenhammer T. R. 2000; Use of the DNA sequence of variable regions of the 16S rRNA gene for rapid and accurate identification of bacteria in the Lactobacillus acidophilus complex. J Appl Microbiol 89:511–516 [CrossRef]
    [Google Scholar]
  38. Kurtz S, Phillippy A, Delcher A. L, Smoot M, Shumway M, Antonescu C, Salzberg S. L. 2004; Versatile and open software for comparing large genomes. Genome Biol 5:R12 [CrossRef]
    [Google Scholar]
  39. McCarthy J, O'Mahony L, O'Callaghan L. 8 other authors 2003; Double blind, placebo controlled trial of two probiotic strains in interleukin 10 knockout mice and mechanistic link with cytokine balance. Gut 52:975–980 [CrossRef]
    [Google Scholar]
  40. Molin G. 2001; Probiotics in foods not containing milk or milk constituents, with special reference to Lactobacillus plantarum 299v. Am J Clin Nutr 73:380S–385S
    [Google Scholar]
  41. Molin G, Jeppsson B, Johansson M. L, Ahrne S, Nobaek S, Stahl M, Bengmark S. 1993; Numerical taxonomy of Lactobacillus spp. associated with healthy and diseased mucosa of the human intestines. J Appl Bacteriol 74:314–323 [CrossRef]
    [Google Scholar]
  42. Nakamura C. E, Whited G. M. 2003; Metabolic engineering for the microbial production of 1,3-propanediol. Curr Opin Biotechnol 14:454–459 [CrossRef]
    [Google Scholar]
  43. Parkhill J, Sebaihia M, Preston A. 50 other authors 2003; Comparative analysis of the genome sequences of Bordetella pertussis , Bordetella parapertussis and Bordetella bronchiseptica . Nat Genet 35:32–40 [CrossRef]
    [Google Scholar]
  44. Pearson W. R. 2000; Flexible sequence similarity searching with the FASTA3 program package. Methods Mol Biol 132:185–219
    [Google Scholar]
  45. Pridmore R. D, Berger B, Desiere F. 12 other authors 2004; The genome sequence of the probiotic intestinal bacterium Lactobacillus johnsonii NCC 533. Proc Natl Acad Sci U S A 101:2512–2517 [CrossRef]
    [Google Scholar]
  46. Ranea J. A, Buchan D. W, Thornton J. M, Orengo C. A. 2004; Evolution of protein superfamilies and bacterial genome size. J Mol Biol 336:871–887 [CrossRef]
    [Google Scholar]
  47. Rogosa M, Wiseman R. F, Mitchell J. A, Disraely M. N, Beaman A. J. 1953; Species differentiation of oral lactobacilli from man including description of Lactobacillus salivarius nov spec and Lactobacillus cellobiosus nov spec. J Bacteriol 65:681–699
    [Google Scholar]
  48. Satokari R. M, Vaughan E. E, Smidt H, Saarela M, Matto J, de Vos W. M. 2003; Molecular approaches for the detection and identification of bifidobacteria and lactobacilli in the human gastrointestinal tract. Syst Appl Microbiol 26:572–584 [CrossRef]
    [Google Scholar]
  49. Schleifer K. H, Ludwig V. 1995; Phylogenetic relationships of lactic acid bacteria. In The Genera of Lactic Acid Bacteria pp  7–17 Edited by Wood B. J. B., Holzapfel W. H. Glasgow, UK: Chapman & Hall;
    [Google Scholar]
  50. Sheil B, McCarthy J, O'Mahony L, Bennett M. W, Ryan P, Fitzgibbon J. J, Kiely B, Collins J. K, Shanahan F. 2004; Is the mucosal route of administration essential for probiotic function? Subcutaneous administration is associated with attenuation of murine colitis and arthritis. Gut 53:694–700 [CrossRef]
    [Google Scholar]
  51. Skerman V. B. D, McGowan V, Sneath P. H. A. 1980; Approved Lists of Bacterial Names. Edited by Skerman V. B. D, McGowan V, Sneath P. H. A. and on behalf of the Ad Hoc Committee of the Judicial Commission of the International Committee on Systematic Bacteriology of the International Association of Microbiological Societies Washington, DC: American Society for Microbiology;
    [Google Scholar]
  52. Snel B, Bork P, Huynen M. A. 1999; Genome phylogeny based on gene content. Nat Genet 21:108–110 [CrossRef]
    [Google Scholar]
  53. Stiles M. E. 1996; Biopreservation by lactic acid bacteria. Antonie Van Leeuwenhoek 70:331–345 [CrossRef]
    [Google Scholar]
  54. Stover C. K, Pham X. Q, Erwin A. L. 28 other authors 2000; Complete genome sequence of Pseudomonas aeruginosa PA01, an opportunistic pathogen. Nature 406:959–964 [CrossRef]
    [Google Scholar]
  55. Takahashi T, Satoh I, Kikuchi N. 1999; Phylogenetic relationships of 38 taxa of the genus Staphylococcus based on 16S rRNA gene sequence analysis. Int J Syst Bacteriol 49:725–728 [CrossRef]
    [Google Scholar]
  56. Tannock G. W. 2004; A special fondness for lactobacilli. Appl Environ Microbiol 70:3189–3194 [CrossRef]
    [Google Scholar]
  57. Thompson J. D, Higgins D. G, Gibson T. J. 1994; clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight-matrix choice. Nucleic Acids Res 22:4673–4680 [CrossRef]
    [Google Scholar]
  58. Tillier E. R, Collins R. A. 2000; Genome rearrangement by replication-directed translocation. Nat Genet 26:195–197 [CrossRef]
    [Google Scholar]
  59. Vandamme P, Pot B, Gillis M, Kersters K, Swings J, de Vos P. 1996; Polyphasic taxonomy, a consensus approach to bacterial systematics. Microbiol Rev 60:407–438
    [Google Scholar]
  60. Van Dongen S. 2000 Graph clustering by flow simulation PhD thesis University of Utrecht;
    [Google Scholar]
  61. van Kranenburg R, Golic N, Bongers R, Leer R. J, Siezen R. J, Kleerebezem M, de Vos W. M. 2005; Functional analysis of three plasmids from Lactobacillus plantarum . Appl Environ Microbiol 71:1223–1230 [CrossRef]
    [Google Scholar]
  62. van Pijkeren J.-P, Canchaya C, Ryan K. A. 8 other authors 2006; Comparative and functional genomics of sortase-dependent proteins in the predicted secretome of Lactobacillus salivarius UCC118. Appl Environ Microbiol 72:4143–4153 [CrossRef]
    [Google Scholar]
  63. Vaughan E. E, Heilig H. G, Ben-Amor K, de Vos W. M. 2005; Diversity, vitality and activities of intestinal lactic acid bacteria and bifidobacteria assessed by molecular approaches. FEMS Microbiol Rev 29:477–490 [CrossRef]
    [Google Scholar]
  64. Ventura M, Canchaya C, Bernini V. 15 other authors 2006; Comparative genomics and transcriptional analysis of prophages identified in the genomes of Lactobacillus gasseri , Lactobacillus salivarius and Lactobacillus casei . Appl Environ Microbiol 72:3130–3146 [CrossRef]
    [Google Scholar]
  65. Wang T. T, Lee B. H. 1997; Plasmids in Lactobacillus . Crit Rev Biotechnol 17:227–272 [CrossRef]
    [Google Scholar]
  66. Zdobnov E. M, Lopez R, Apweiler R, Etzold T. 2002; The EBI SRS server – new features. Bioinformatics 18:1149–1150 [CrossRef]
    [Google Scholar]
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