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.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.039545-0
2010-11-01
2020-08-11
Loading full text...

Full text loading...

/deliver/fulltext/micro/156/11/3243.html?itemId=/content/journal/micro/10.1099/mic.0.039545-0&mimeType=html&fmt=ahah

References

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J.. 1990; Basic local alignment search tool. J Mol Biol215:403–410
    [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. Plasmid57:165–174
    [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 Bacteriol191:4144–4151
    [Google Scholar]
  4. Bentley S.. 2009; Sequencing the species pan-genome. Nat Rev Microbiol7:258–259
    [Google Scholar]
  5. Canchaya C., Proux C., Fournous G., Bruttin A., Brussow H.. 2003; Prophage genomics. Microbiol Mol Biol Rev67:238–276
    [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. Microbiology152:3185–3196
    [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 Microbiol38:229–232
    [Google Scholar]
  8. Chan C. X., Beiko R. G., Ragan M. A.. 2006; Detecting recombination in evolving nucleotide sequences. BMC Bioinformatics7:412
    [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 Res33: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 Microbiol73:7858–7866
    [Google Scholar]
  11. Daubin V., Perriere G.. 2003; G+C3 structuring along the genome: a common feature in prokaryotes. Mol Biol Evol20:471–483
    [Google Scholar]
  12. Dessau R. B., Pipper C. B.. 2008; “R” – project for statistical computing. Ugeskr Laeger170:328–330
    [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. Science308:1635–1638
    [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 Biol1: RESEARCH0011
    [Google Scholar]
  15. Fitch W. M.. 1970; Distinguishing homologous from analogous proteins. Syst Zool19:99–113
    [Google Scholar]
  16. Guindon S., Gascuel O.. 2003; A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol52:696–704
    [Google Scholar]
  17. Henz S. R., Huson D. H., Auch A. F., Nieselt-Struwe K., Schuster S. C.. 2005; Whole-genome prokaryotic phylogeny. Bioinformatics21:2329–2335
    [Google Scholar]
  18. Huson D. H.. 1998; SplitsTree: analyzing and visualizing evolutionary data. Bioinformatics14:68–73
    [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 Bacteriol191:678–679
    [Google Scholar]
  20. Klappenbach J. A., Dunbar J. M., Schmidt T. M.. 2000; rRNA operon copy number reflects ecological strategies of bacteria. Appl Environ Microbiol66:1328–1333
    [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 Biol5:R12
    [Google Scholar]
  22. Lapierre P., Gogarten J. P.. 2009; Estimating the size of the bacterial pan-genome. Trends Genet25:107–110
    [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 Microbiol72:527–535
    [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 Genomics9:247
    [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 A103:15611–15616
    [Google Scholar]
  26. Marco M. L., Pavan S., Kleerebezem M.. 2006; Towards understanding molecular modes of probiotic action. Curr Opin Biotechnol17:204–210
    [Google Scholar]
  27. Medini D., Donati C., Tettelin H., Masignani V., Rappuoli R.. 2005; The microbial pan-genome. Curr Opin Genet Dev15:589–594
    [Google Scholar]
  28. O'Hara A. M., Shanahan F.. 2007; Mechanisms of action of probiotics in intestinal diseases. Scientific World Journal7:31–46
    [Google Scholar]
  29. Pearson W. R.. 2000; Flexible sequence similarity searching with the fasta3 program package. Methods Mol Biol132:185–219
    [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 Bacteriol190:6881–6893
    [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. Plasmid58:140–147
    [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 A99:14422–14427
    [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 A105:18964–18969
    [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 Microbiol52:1043–1047
    [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. Science296:2376–2379
    [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 A102:13950–13955
    [Google Scholar]
  37. Tettelin H., Riley D., Cattuto C., Medini D.. 2008; Comparative genomics: the bacterial pan-genome. Curr Opin Microbiol11:472–477
    [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
  39. Tillier E. R., Collins R. A.. 2000; Genome rearrangement by replication-directed translocation. Nat Genet26:195–197
    [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 Microbiol75:1534–1545
    [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 J3:745–751
    [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. Science304:66–74
    [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 Microbiol56:2783–2792
    [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 Rev71:495–548
    [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 Microbiol7:61–71
    [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 Genet5:e1000785
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.039545-0
Loading
/content/journal/micro/10.1099/mic.0.039545-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error