1887

Abstract

Whole-genome sequencing efforts have revolutionized the study of bifidobacterial genetics and physiology. Unfortunately, the sequence of a single genome does not provide information on bifidobacterial genetic diversity and on how genetic variability supports improved adaptation of these bacteria to the environment of the human gastrointestinal tract (GIT). Analysis of nine genomes from bifidobacterial species showed that such genomes display an open pan-genome structure. Mathematical extrapolation of the data indicates that the genome reservoir available to the bifidobacterial pan-genome consists of more than 5000 genes, many of which are uncharacterized, but which are probably important to provide adaptive abilities pertinent to the human GIT. We also define a core bifidobacterial gene set which will undoubtedly provide a new baseline from which one can examine the evolution of bifidobacteria. Phylogenetic investigation performed on a total of 506 orthologues that are common to nine complete bifidobacterial genomes allowed the construction of a supertree which is largely concordant with the phylogenetic tree obtained using 16S rRNA genes. Moreover, this supertree provided a more robust phylogenetic resolution than the 16S rRNA gene-based analysis. This comparative study of the genus thus presents a foundation for future functional analyses of this important group of GIT bacteria.

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2010-11-01
2019-11-13
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References

  1. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. ( 1990; ). Basic local alignment search tool. J Mol Biol 215, 403–410.[CrossRef]
    [Google Scholar]
  2. Alvarez-Martín, P., Florez, A. B. & Mayo, B. ( 2007; ). Screening for plasmids among human bifidobacteria species: sequencing and analysis of pBC1 from Bifidobacterium catenulatum L48. Plasmid 57, 165–174.[CrossRef]
    [Google Scholar]
  3. Barrangou, R., Briczinski, E. P., Traeger, L. L., Loquasto, J. R., Richards, M., Horvath, P., Coûté-Monvoisin, A. C., Leyer, G., Rendulic, S. & other authors ( 2009; ). Comparison of the complete genome sequences of Bifidobacterium animalis subsp. lactis DSM 10140 and Bl-04. J Bacteriol 191, 4144–4151.[CrossRef]
    [Google Scholar]
  4. Bentley, S. ( 2009; ). Sequencing the species pan-genome. Nat Rev Microbiol 7, 258–259.[CrossRef]
    [Google Scholar]
  5. Canchaya, C., Proux, C., Fournous, G., Bruttin, A. & Brussow, H. ( 2003; ). Prophage genomics. Microbiol Mol Biol Rev 67, 238–276.[CrossRef]
    [Google Scholar]
  6. Canchaya, C., Claesson, M. J., Fitzgerald, G. F., van Sinderen, D. & O'Toole, P. W. ( 2006; ). Diversity of the genus Lactobacillus revealed by comparative genomics of five species. Microbiology 152, 3185–3196.[CrossRef]
    [Google Scholar]
  7. 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]
  8. Chan, C. X., Beiko, R. G. & Ragan, M. A. ( 2006; ). Detecting recombination in evolving nucleotide sequences. BMC Bioinformatics 7, 412.[CrossRef]
    [Google Scholar]
  9. 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]
  10. Cronin, M., Knobel, M., O'Connell-Motherway, M., Fitzgerald, G. F. & van Sinderen, D. ( 2007; ). Molecular dissection of a bifidobacterial replicon. Appl Environ Microbiol 73, 7858–7866.[CrossRef]
    [Google Scholar]
  11. 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]
  12. Dessau, R. B. & Pipper, C. B. ( 2008; ). “R” – project for statistical computing. Ugeskr Laeger 170, 328–330.
    [Google Scholar]
  13. Eckburg, P. B., Bik, E. M., Bernstein, C. N., Purdom, E., Dethlefsen, L., Sargent, M., Gill, S. R., Nelson, K. E. & Relman, D. A. ( 2005; ). Diversity of the human intestinal microbial flora. Science 308, 1635–1638.[CrossRef]
    [Google Scholar]
  14. 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]
  15. Fitch, W. M. ( 1970; ). Distinguishing homologous from analogous proteins. Syst Zool 19, 99–113.[CrossRef]
    [Google Scholar]
  16. 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]
  17. 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]
  18. Huson, D. H. ( 1998; ). SplitsTree: analyzing and visualizing evolutionary data. Bioinformatics 14, 68–73.[CrossRef]
    [Google Scholar]
  19. Kim, J. F., Jeong, H., Yu, D. S., Choi, S. H., Hur, C. G., Park, M. S., Yoon, S. H., Kim, D. W., Ji, G. E. & other authors ( 2009; ). Genome sequence of the probiotic bacterium Bifidobacterium animalis subsp. lactis AD011. J Bacteriol 191, 678–679.[CrossRef]
    [Google Scholar]
  20. Klappenbach, J. A., Dunbar, J. M. & Schmidt, T. M. ( 2000; ). rRNA operon copy number reflects ecological strategies of bacteria. Appl Environ Microbiol 66, 1328–1333.[CrossRef]
    [Google Scholar]
  21. 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]
  22. Lapierre, P. & Gogarten, J. P. ( 2009; ). Estimating the size of the bacterial pan-genome. Trends Genet 25, 107–110.[CrossRef]
    [Google Scholar]
  23. Lee, J. H. & O'Sullivan, D. J. ( 2006; ). Sequence analysis of two cryptic plasmids from Bifidobacterium longum DJO10A and construction of a shuttle cloning vector. Appl Environ Microbiol 72, 527–535.[CrossRef]
    [Google Scholar]
  24. Lee, J. H., Karamychev, V. N., Kozyavkin, S. A., Mills, D., Pavlov, A. R., Pavlova, N. V., Polouchine, N. N., Richardson, P. M., Shakhova, V. V. & other authors ( 2008; ). Comparative genomic analysis of the gut bacterium Bifidobacterium longum reveals loci susceptible to deletion during pure culture growth. BMC Genomics 9, 247.[CrossRef]
    [Google Scholar]
  25. Makarova, K., Slesarev, A., Wolf, Y., Sorokin, A., Mirkin, B., Koonin, E., Pavlov, A., Pavlova, N., Karamychev, V. & other authors ( 2006; ). Comparative genomics of the lactic acid bacteria. Proc Natl Acad Sci U S A 103, 15611–15616.[CrossRef]
    [Google Scholar]
  26. Marco, M. L., Pavan, S. & Kleerebezem, M. ( 2006; ). Towards understanding molecular modes of probiotic action. Curr Opin Biotechnol 17, 204–210.[CrossRef]
    [Google Scholar]
  27. Medini, D., Donati, C., Tettelin, H., Masignani, V. & Rappuoli, R. ( 2005; ). The microbial pan-genome. Curr Opin Genet Dev 15, 589–594.[CrossRef]
    [Google Scholar]
  28. O'Hara, A. M. & Shanahan, F. ( 2007; ). Mechanisms of action of probiotics in intestinal diseases. Scientific World Journal 7, 31–46.[CrossRef]
    [Google Scholar]
  29. Pearson, W. R. ( 2000; ). Flexible sequence similarity searching with the fasta3 program package. Methods Mol Biol 132, 185–219.
    [Google Scholar]
  30. Rasko, D. A., Rosovitz, M. J., Myers, G. S., Mongodin, E. F., Fricke, W. F., Gajer, P., Crabtree, J., Sebaihia, M., Thomson, N. R. & other authors ( 2008; ). The pangenome structure of Escherichia coli: comparative genomic analysis of E. coli commensal and pathogenic isolates. J Bacteriol 190, 6881–6893.[CrossRef]
    [Google Scholar]
  31. Sangrador-Vegas, A., Stanton, C., van Sinderen, D., Fitzgerald, G. F. & Ross, R. P. ( 2007; ). Characterization of plasmid pASV479 from Bifidobacterium pseudolongum subsp. globosum and its use for expression vector construction. Plasmid 58, 140–147.[CrossRef]
    [Google Scholar]
  32. Schell, M. A., Karmirantzou, M., Snel, B., Vilanova, D., Berger, B., Pessi, G., Zwahlen, M. C., Desiere, F., Bork, P. & other authors ( 2002; ). The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. Proc Natl Acad Sci U S A 99, 14422–14427.[CrossRef]
    [Google Scholar]
  33. Sela, D. A., Chapman, J., Adeuya, A., Kim, J. H., Chen, F., Whitehead, T. R., Lapidus, A., Rokhsar, D. S., Lebrilla, C. B. & other authors ( 2008; ). The genome sequence of Bifidobacterium longum subsp. infantis reveals adaptations for milk utilization within the infant microbiome. Proc Natl Acad Sci U S A 105, 18964–18969.[CrossRef]
    [Google Scholar]
  34. Stackebrandt, E., Frederiksen, W., Garrity, G. M., Grimont, P. A., Kämpfer, P., Maiden, M. C., Nesme, X., Rosselló-Mora, R., Swings, J. & other authors ( 2002; ). Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int J Syst Evol Microbiol 52, 1043–1047.[CrossRef]
    [Google Scholar]
  35. Tamas, I., Klasson, L., Canback, B., Naslund, A. K., Eriksson, A. S., Wernegreen, J. J., Sandstrom, J. P., Moran, N. A. & Andersson, S. G. ( 2002; ). 50 million years of genomic stasis in endosymbiotic bacteria. Science 296, 2376–2379.[CrossRef]
    [Google Scholar]
  36. Tettelin, H., Masignani, V., Cieslewicz, M. J., Donati, C., Medini, D., Ward, N. L., Angiuoli, S. V., Crabtree, J., Jones, A. L. & other authors ( 2005; ). Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial “pan-genome”. Proc Natl Acad Sci U S A 102, 13950–13955.[CrossRef]
    [Google Scholar]
  37. Tettelin, H., Riley, D., Cattuto, C. & Medini, D. ( 2008; ). Comparative genomics: the bacterial pan-genome. Curr Opin Microbiol 11, 472–477.[CrossRef]
    [Google Scholar]
  38. Thompson, J. D., Gibson, T. J. & Higgins, D. G. ( 2002; ). Multiple sequence alignment using clustal_w and clustal_x. Curr Protoc Bioinformatics Chapter 2, Unit 2.3.
    [Google Scholar]
  39. Tillier, E. R. & Collins, R. A. ( 2000; ). Genome rearrangement by replication-directed translocation. Nat Genet 26, 195–197.[CrossRef]
    [Google Scholar]
  40. Turroni, F., Foroni, E., Pizzetti, P., Giubellini, V., Ribbera, A., Merusi, P., Cagnasso, P., Bizzarri, B., de'Angelis, G. L. & other authors ( 2009a; ). Exploring the diversity of the bifidobacterial population in the human intestinal tract. Appl Environ Microbiol 75, 1534–1545.[CrossRef]
    [Google Scholar]
  41. Turroni, F., Marchesi, J. R., Foroni, E., Gueimonde, M., Shanahan, F., Margolles, A., van Sinderen, D. & Ventura, M. ( 2009b; ). Microbiomic analysis of the bifidobacterial population in the human distal gut. ISME J 3, 745–751.[CrossRef]
    [Google Scholar]
  42. van Dongen, S. ( 2000; ). Graph clustering by flow simulation. PhD thesis, University of Utrecht, Utrecht, The Netherlands.
  43. Venter, J. C., Remington, K., Heidelberg, J. F., Halpern, A. L., Rusch, D., Eisen, J. A., Wu, D., Paulsen, I., Nelson, K. E. & other authors ( 2004; ). Environmental genome shotgun sequencing of the Sargasso Sea. Science 304, 66–74.[CrossRef]
    [Google Scholar]
  44. Ventura, M., Canchaya, C., Del Casale, A., Dellaglio, F., Neviani, E., Fitzgerald, G. F. & van Sinderen, D. ( 2006; ). Analysis of bifidobacterial evolution using a multilocus approach. Int J Syst Evol Microbiol 56, 2783–2792.[CrossRef]
    [Google Scholar]
  45. Ventura, M., Canchaya, C., Tauch, A., Chandra, G., Fitzgerald, G. F., Chater, K. F. & van Sinderen, D. ( 2007; ). Genomics of Actinobacteria: tracing the evolutionary history of an ancient phylum. Microbiol Mol Biol Rev 71, 495–548.[CrossRef]
    [Google Scholar]
  46. Ventura, M., O'Flaherty, S., Claesson, M. J., Turroni, F., Klaenhammer, T. R., van Sinderen, D. & O'Toole, P. W. ( 2009a; ). Genome-scale analyses of health-promoting bacteria: probiogenomics. Nat Rev Microbiol 7, 61–71.[CrossRef]
    [Google Scholar]
  47. Ventura, M., Turroni, F., Zomer, A., Foroni, E., Giubellini, V., Bottacini, F., Canchaya, C., Claesson, M. J., He, F. & other authors ( 2009b; ). The Bifidobacterium dentium Bd1 genome sequence reflects its genetic adaptation to the human oral cavity. PLoS Genet 5, e1000785.[CrossRef]
    [Google Scholar]
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