Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Genome rearrangement by replication-directed translocation

Abstract

Gene order in bacteria is poorly conserved during evolution1,2,3. For example, although many homologous genes are shared by the proteobacteria Escherichia coli, Haemophilus influenzae and Helicobacter pylori, their relative positions are very different in each genome, except local functional clusters such as operons3,4,5,6. The complete sequences of the more closely related bacterial genomes, such as pairs of Chlamydia7,8,9, H. pylori10,11 and Mycobacterium species12, now allow identification of the processes and mechanisms involved in genome evolution. Here we provide evidence that a substantial proportion of rearrangements in gene order results from recombination sites that are determined by the positions of the replication forks. Our observations suggest that replication has a major role in directing genome evolution.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Plots of the position of genes in related genomes.
Figure 2: Rearrangement of gene order by translocation of genes across the replication axis.
Figure 3: Examples of translocated genes in Chlamydia.

Similar content being viewed by others

Accession codes

Accessions

GenBank/EMBL/DDBJ

References

  1. Mushegian, A.R. & Koonin, E.V. Gene order is not conserved in bacterial evolution. Trends Genet. 12, 289–290 (1996).

    Article  CAS  Google Scholar 

  2. Huynen, M.A. & Bork, P. Measuring genome evolution. Proc. Natl Acad. Sci. USA 95, 5849–5856 (1998).

    Article  CAS  Google Scholar 

  3. Casjens, S. The diverse and dynamic structures of bacterial genomes. Annu. Rev. Genet. 32, 339–377 (1998).

    Article  CAS  Google Scholar 

  4. Tatusov, R.L. et al. Metabolism and evolution of Hemophilus influenzae deduced from a whole genome comparison with Escherichia coli. Current Biol. 3, 279–291 (1996).

    Article  Google Scholar 

  5. Kolsko, A.B. Dynamic bacterial genome organization. Mol. Microbiol. 24, 241–248 (1997).

    Article  Google Scholar 

  6. Tamames, J., Casari, G., Ouzounis, C. & Valencia, A. Conserved clusters of functionally related genes in two bacterial genomes. J. Mol. Evol. 44, 66–73 (1997).

    Article  CAS  Google Scholar 

  7. Kalman, S. et al. Comparative genomes of Chlamydia pneumoniae and C. trachomatis. Nature Genet. 21, 385–389 (1999).

    Article  CAS  Google Scholar 

  8. Stephens, R.S. et al. Genome sequence of an obligate intracellular pathogen of humans, Chlamydia trachomatis. Science 282, 754–759 (1998).

    Article  CAS  Google Scholar 

  9. Read, T.D. et al. Genome sequences of Chlamydia trachomatis MoPn and Chlamydia pneumoniae AR39. Nucleic Acids Res. 28, 1397–1406 (2000).

    Article  CAS  Google Scholar 

  10. Tomb, J.F. et al. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388, 539–547 (1997).

    Article  CAS  Google Scholar 

  11. Alm, R.A. et al. Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 397, 176–180 (1999).

    Article  Google Scholar 

  12. Cole, S.T. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393, 537–544 (1998).

    Article  CAS  Google Scholar 

  13. Parkhill, J. et al. The genome sequence of the food-borne pathogen Campylobacter jejuna reveals hypervariable sequences. Nature 403, 665–668 (2000).

    Article  CAS  Google Scholar 

  14. Shapiro, J.A. Molecular model for the transposition and replication of bacteriophage Mu and other transposable elements. Proc. Natl Acad. Sci. USA 76, 1933–1937 (1979).

    Article  CAS  Google Scholar 

  15. Liu, S.-H. & Sanderson, K.E. Rearrangements in the genome of the bacterium Salmonella typhi. Proc. Natl Acad. Sci. USA 92, 1018–1022 (1995).

    Article  CAS  Google Scholar 

  16. Shmid, M.B. & Roth, J.R. Selection and endpoint distribution of bacterial inversion mutations. Genetics 105, 539–557 (1983).

    Google Scholar 

  17. Rebollo, J.-E., François, V. & Louar, J.-M. Detection and possible role of two large nondivisible zones on the Escherichia coli chromosome. Proc. Natl Acad. Sci. USA 85, 9391–9395 (1988).

    Article  CAS  Google Scholar 

  18. Itaya, M. Physical map of the Bacillus subtilis 166 genome: evidence for the inversion of an approximately 1900 kb continuous DNA segment, the translocation of an approximately 100kb segment and the duplication of a 5kb segment. Microbiology 143, 3723–3732 (1997).

    Article  CAS  Google Scholar 

  19. Caro, L.G. & Berg, C.M. Chromosome replication in some strains of Escherichia coli K12. Cold Spring Harb. Symp. Quant. Biol. 33, 559–573 (1968).

    Article  CAS  Google Scholar 

  20. Schmid, M.B & Roth, J.R. Gene location affects expression level in Salmonella typhimurium. J. Bacteriol. 169, 2872–2875 (1987).

    Article  CAS  Google Scholar 

  21. Brewer, B.J. When polymerases collide: replication and the transcriptional organization of the E. coli chromosome. Cell 53, 679–686 (1988).

    Article  CAS  Google Scholar 

  22. Ikeda H., Moriya, K. & Matsumoto, T. In vitro study of illegitimate recombination: involvement of DNA gyrase. Cold Spring Harb. Symp. Quant. Biol. 45, 399–408 (1980).

    Article  Google Scholar 

  23. Michel, B., Ehrlich, S.D. & Uzest, M. DNA double-strand breaks caused by replication arrest. EMBO J. 16, 430–438 (1997).

    Article  CAS  Google Scholar 

  24. Bierne H., Ehrlich, S.D. & Michel, B. Deletions at stalled replication forks occur by two different pathways. EMBO J. 16, 3332–3340 (1997).

    Article  CAS  Google Scholar 

  25. Kuzminov, A. & Stahl, F.W. Double-strand end repair via the RecBC pathway in Escherichia coli primes DNA replication. Genes Dev. 13, 345–356 (1999).

    Article  CAS  Google Scholar 

  26. Newport, J. & Yan, H. Organization of DNA into foci during replication. Curr. Opin. Cell Biol. 8, 365–368 (1996).

    Article  CAS  Google Scholar 

  27. Lemon, K.P. & Grossman, A.D. Localization of bacterial DNA polymerase: evidence for a factory model of replication. Science 28, 1516–1519 (1998).

    Article  Google Scholar 

  28. Pearson, W.R. Rapid and sensitive sequence comparison with FASTP and FASTA. Methods Enzymol. 183, 63 (1990).

    Article  CAS  Google Scholar 

  29. Lobry, J.R. Origin of replication of Mycoplasma genitalium. Science 272, 745–746 (1996).

    Article  CAS  Google Scholar 

  30. Tillier, E.R.M. & Collins, R.A. The contributions of replication orientation, gene direction and signal sequences to base-composition asymmetries in bacterial genomes. J. Mol. Evol. 50, 249–257 (2000).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank W.F. Doolittle for discussion and B. Funnell for critical reading of the manuscript. R.A.C. is a fellow of the Canadian Institute for Advanced Research (CIAR). This work was funded by the National Sciences and Engineering Research Council (NSERC) grant to R.A.C.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Elisabeth R.M. Tillier.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tillier, E., Collins, R. Genome rearrangement by replication-directed translocation. Nat Genet 26, 195–197 (2000). https://doi.org/10.1038/79918

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/79918

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing