The complete genome sequence of Lactobacillus bulgaricus reveals extensive and ongoing reductive evolution

  1. M. van de Guchte*,,
  2. S. Penaud*,
  3. C. Grimaldi*,
  4. V. Barbe,
  5. K. Bryson§,,
  6. P. Nicolas§,
  7. C. Robert,
  8. S. Oztas,
  9. S. Mangenot,
  10. A. Couloux,
  11. V. Loux§,
  12. R. Dervyn*,
  13. R. Bossy§,
  14. A. Bolotin*,
  15. J.-M. Batto*,
  16. T. Walunas,
  17. J.-F. Gibrat§,
  18. P. Bessières§,
  19. J. Weissenbach,**,
  20. S. D. Ehrlich*, and
  21. E. Maguin*
  1. *Génétique Microbienne and
  2. §Mathématique, Informatique et Génome, Institut National de la Recherche Agronomique, 78352 Jouy en Josas Cedex, France;
  3. Genoscope, 2 Rue Gaston Crémieux, 91057 Evry Cedex, France;
  4. Integrated Genomics Inc., 2201 West Campbell Park Drive, Chicago, IL 60612; and
  5. **Centre National de la Recherche Scientifique, Unité Mixte de Recherche 8030, 2 Rue Gaston Crémieux, 91057 Evry Cedex, France
  1. Communicated by Todd R. Klaenhammer, North Carolina State University, Raleigh, NC, April 14, 2006 (received for review October 14, 2005)

Abstract

Lactobacillus delbrueckii ssp. bulgaricus (L. bulgaricus) is a representative of the group of lactic acid-producing bacteria, mainly known for its worldwide application in yogurt production. The genome sequence of this bacterium has been determined and shows the signs of ongoing specialization, with a substantial number of pseudogenes and incomplete metabolic pathways and relatively few regulatory functions. Several unique features of the L. bulgaricus genome support the hypothesis that the genome is in a phase of rapid evolution. (i) Exceptionally high numbers of rRNA and tRNA genes with regard to genome size may indicate that the L. bulgaricus genome has known a recent phase of important size reduction, in agreement with the observed high frequency of gene inactivation and elimination; (ii) a much higher GC content at codon position 3 than expected on the basis of the overall GC content suggests that the composition of the genome is evolving toward a higher GC content; and (iii) the presence of a 47.5-kbp inverted repeat in the replication termination region, an extremely rare feature in bacterial genomes, may be interpreted as a transient stage in genome evolution. The results indicate the adaptation of L. bulgaricus from a plant-associated habitat to the stable protein and lactose-rich milk environment through the loss of superfluous functions and protocooperation with Streptococcus thermophilus.

Footnotes

  • To whom correspondence should be addressed. E-mail: maarten.vandeguchte{at}jouy.inra.fr
  • Present address: Department of Computer Science, University College London, London WC1E 6BT, United Kingdom.

  • Author contributions: M.v.d.G., S.P., C.G., V.B., C.R., S.O., S.M., R.D., S.D.E., and E.M. designed research; M.v.d.G., S.P., C.G., V.B., C.R., S.O., S.M., and R.D. performed research; K.B., P.N., A.C., V.L., R.B., J.-M.B., T.W., J.-F.G., P.B., and J.W. contributed new reagents/analytic tools; M.v.d.G., S.P., C.G., V.B., P.N., C.R., S.O., S.M., R.D., A.B., S.D.E., and E.M. analyzed data; and M.v.d.G. and E.M. wrote the paper.

  • †† Sasaki, T., Ito, Y. & Sasaki, Y. (1993) FEMS Microbiol. Rev. 12, P8.

  • Conflict of interest statement: No conflicts declared.

  • Data deposition: The L. bulgaricus genome sequence has been submitted to the European Molecular Biology Laboratory database (accession no. CR954253).

  • Abbreviations:

    Abbreviations:

    CDS,
    coding sequences;
    IS,
    insertion sequence.
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