1887

Microbiology Society logo

Volume 153, Issue 11

Exploring the evolution of the group repeat element by comparative genome analysis of closely related strains Free

Abstract

is a chromosomal ∼155 bp repeated element found uniquely and ubiquitously in the group of Gram-positive bacteria; it exhibits several features characteristic of mobile elements, including a variable distribution pattern between strains. Here, highly similar elements in non-conserved genomic loci are identified in a set of closely related and strains near the phylogenetic cluster. It is also shown that may be present on small RNA transcripts in the 100–400 bp size range. folding of at the RNA level indicated that transcripts may form a double-hairpin-like structure predicted to have high structural stability. A functional role of at the RNA level is supported by multiple cases of G–U base-pairing, and compensatory mutations maintaining structural stability of the RNA fold. folding at the DNA level produced similar predicted structures, with the potential to form a cruciform structure at open DNA complexes. The predicted structural stability was greater for elements showing high sequence identities to elements in non-conserved chromosomal loci in other strains, relative to other copies. mobility could thus be dependent on the formation of a stable DNA or RNA intermediate. Furthermore, elements potentially encoding structurally stable and less stable transcripts were phylogenetically intermixed, indicating that loss of mobility may have occurred multiple times during evolution. Repeated elements with similar features in other bacteria have been shown to provide functions such as mRNA stabilization, transcription termination and/or promoter function. Similarly, may constitute a mobile element which occasionally gains a function when it enters an appropriate chromosomal locus.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): DEPC, diethyl pyrocarbonate , MLEE, multilocus enzyme electrophoresis , MLST, multilocus sequence typing and TBE, Tris/borate/EDTA
SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2007/005504-0
2007-11-01
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/11/3894.html?itemId=/content/journal/micro/10.1099/mic.0.2007/005504-0&mimeType=html&fmt=ahah

References

  1. 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
     [Google Scholar]
  2. Bachellier S., Clement J. M., Hofnung M. 1999; Short palindromic repetitive DNA elements in enterobacteria: a survey. Res Microbiol 150:627–639
     [Google Scholar]
  3. Buisine N., Tang C. M., Chalmers R. 2002; Transposon-like Correia elements: structure, distribution and genetic exchange between pathogenic Neisseria sp. FEBS Lett 522:52–58
     [Google Scholar]
  4. Bureau T. E., Wessler S. R. 1994; Mobile inverted-repeat elements of the Tourist family are associated with the genes of many cereal grasses. Proc Natl Acad Sci U S A 91:1411–1415
     [Google Scholar]
  5. Castresana J. 2000; Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552
     [Google Scholar]
  6. Correia F. F., Inouye S., Inouye M. 1988; A family of small repeated elements with some transposon-like properties in the genome of Neisseria gonorrhoeae. J Biol Chem 263:12194–12198
     [Google Scholar]
  7. Drobniewski F. A. 1993; Bacillus cereus and related species. Clin Microbiol Rev 6:324–338
     [Google Scholar]
  8. Galtier N., Gouy M., Gautier C. 1996; seaview and phylo_win: two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci 12:543–548
     [Google Scholar]
  9. Griffiths-Jones S., Bateman A., Marshall M., Khanna A., Eddy S. R. 2003; Rfam: an RNA family database. Nucleic Acids Res 31:439–441
     [Google Scholar]
  10. Griffiths-Jones S., Moxon S., Marshall M., Khanna A., Eddy S. R., Bateman A. 2005; Rfam: annotating non-coding RNAs in complete genomes. Nucleic Acids Res 33:D121–D124
     [Google Scholar]
  11. Han C. S., Xie G., Challacombe J. F., Altherr M. R., Bhotika S. S., Brown N., Bruce D., Campbell C. S., Campbell M. L. other authors 2006; Pathogenomic sequence analysis of Bacillus cereus and Bacillus thuringiensis isolates closely related to Bacillus anthracis. J Bacteriol 188:3382–3390
     [Google Scholar]
  12. Helgason E., Caugant D. A., Olsen I., Kolstø A. B. 2000a; Genetic structure of population of Bacillus cereus and B. thuringiensis isolates associated with periodontitis and other human infections. J Clin Microbiol 38:1615–1622
     [Google Scholar]
  13. Helgason E., Økstad O. A., Caugant D. A., Johansen H. A., Fouet A., Mock M., Hegna I., Kolstø A. B. 2000b; Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis – one species on the basis of genetic evidence. Appl Environ Microbiol 66:2627–2630
     [Google Scholar]
  14. Helgason E., Tourasse N. J., Meisal R., Caugant D. A., Kolstø A. B. 2004; Multilocus sequence typing scheme for bacteria of the Bacillus cereus group. Appl Environ Microbiol 70:191–201
     [Google Scholar]
  15. Hernandez E., Ramisse F., Ducoureau J. P., Cruel T., Cavallo J. D. 1998; Bacillus thuringiensis subsp. konkukian (serotype H34) superinfection: case report and experimental evidence of pathogenicity in immunosuppressed mice. J Clin Microbiol 36:2138–2139
     [Google Scholar]
  16. Herron W. M. 1930 Rancidity in Cheddar cheese Master's Thesis, Queen's University; Kingston, Ontario, Canada:
  17. Hofnung M., Shapiro J. A. 1999; Introduction – special issue on repetitive DNA sequences in microbes. Res Microbiol 150:577–578
     [Google Scholar]
  18. Hohl M., Kurtz S., Ohlebusch E. 2002; Efficient multiple genome alignment. Bioinformatics 18:Suppl 1S312–S320
     [Google Scholar]
  19. Huelsenbeck J. P., Ronquist F. 2001; mrbayes: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755
     [Google Scholar]
  20. Ivanova N., Sorokin A., Anderson I., Galleron N., Candelon B., Kapatral V., Bhattacharyya A., Reznik G., Mikhailova N. other authors 2003; Genome sequence of Bacillus cereus and comparative analysis with Bacillus anthracis. Nature 423:87–91
     [Google Scholar]
  21. Izsvak Z., Ivics Z., Shimoda N., Mohn D., Okamoto H., Hackett P. B. 1999; Short inverted-repeat transposable elements in teleost fish and implications for a mechanism of their amplification. J Mol Evol 48:13–21
     [Google Scholar]
  22. Jernigan J. A., Stephens D. S., Ashford D. A., Omenaca C., Topiel M. S., Galbraith M., Tapper M., Fisk T. L., Zaki S. other authors 2001; Bioterrorism-related inhalational anthrax: the first 10 cases reported in the United States. Emerg Infect Dis 7:933–944
     [Google Scholar]
  23. Kimura M. 1980; A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
     [Google Scholar]
  24. Kiss T. 2002; Small nucleolar RNAs: an abundant group of noncoding RNAs with diverse cellular functions. Cell 109:145–148
     [Google Scholar]
  25. Kiss A. M., Jady B. E., Bertrand E., Kiss T. 2004; Human box H/ACA pseudouridylation guide RNA machinery. Mol Cell Biol 24:5797–5807
     [Google Scholar]
  26. Knutsen E., Johnsborg O., Quentin Y., Claverys J. P., Håvarstein L. S. 2006; BOX elements modulate gene expression in Streptococcus pneumoniae: impact on the fine-tuning of competence development. J Bacteriol 188:8307–8312
     [Google Scholar]
  27. Kozik A., Kochetkova E., Michelmore R. 2002; GenomePixelizer – a visualization program for comparative genomics within and between species. Bioinformatics 18:335–336
     [Google Scholar]
  28. Kumar S., Tamura K., Jakobsen I. B., Nei M. 2001; mega2: molecular evolutionary genetics analysis software. Bioinformatics 17:1244–1245
     [Google Scholar]
  29. Lombard V., Camon E. B., Parkinson H. E., Hingamp P., Stoesser G., Redaschi N. 2002; EMBL-Align: a new public nucleotide and amino acid multiple sequence alignment database. Bioinformatics 18:763–764
     [Google Scholar]
  30. Martin B., Humbert O., Camara M., Guenzi E., Walker J., Mitchell T., Andrew P., Prudhomme M., Alloing G. other authors 1992; A highly conserved repeated DNA element located in the chromosome of Streptococcus pneumoniae. Nucleic Acids Res 20:3479–3483
     [Google Scholar]
  31. Mathews D. H., Sabina J., Zuker M., Turner D. H. 1999; Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J Mol Biol 288:911–940
     [Google Scholar]
  32. Mazzone M., De Gregorio E., Lavitola A., Pagliarulo C., Alifano P., Di Nocera P. P. 2001; Whole-genome organization and functional properties of miniature DNA insertion sequences conserved in pathogenic Neisseriae. Gene 278:211–222
     [Google Scholar]
  33. Oggioni M. R., Claverys J. P. 1999; Repeated extragenic sequences in prokaryotic genomes: a proposal for the origin and dynamics of the RUP element in Streptococcus pneumoniae. Microbiology 145:2647–2653
     [Google Scholar]
  34. Økstad O. A., Hegna I., Lindbäck T., Rishovd A. L., Kolstø A. B. 1999; Genome organization is not conserved between Bacillus cereus and Bacillus subtilis. Microbiology 145:621–631
     [Google Scholar]
  35. Økstad O. A., Tourasse N. J., Stabell F. B., Sundfaer C. K., Egge-Jacobsen W., Risøen P. A., Read T. D., Kolstø A. B. 2004; The bcr1 DNA repeat element is specific to the Bacillus cereus group and exhibits mobile element characteristics. J Bacteriol 186:7714–7725
     [Google Scholar]
  36. Page R. D. 1996; TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358
     [Google Scholar]
  37. Rasko D. A., Ravel J., Økstad O. A., Helgason E., Cer R. Z., Jiang L., Shores K. A., Fouts D. E., Tourasse N. J. other authors 2004; The genome sequence of Bacillus cereus ATCC 10987 reveals metabolic adaptations and a large plasmid related to Bacillus anthracis pXO1. Nucleic Acids Res 32:977–988
     [Google Scholar]
  38. Rasko D. A., Altherr M. R., Han C. S., Ravel J. 2005; Genomics of the Bacillus cereus group of organisms. FEMS Microbiol Rev 29:303–329
     [Google Scholar]
  39. Read T. D., Peterson S. N., Tourasse N., Baillie L. W., Paulsen I. T., Nelson K. E., Tettelin H., Fouts D. E., Eisen J. A. other authors 2003; The genome sequence of Bacillus anthracis Ames and comparison to closely related bacteria. Nature 423:81–86
     [Google Scholar]
  40. Reyes-Ramirez A., Ibarra J. E. 2005; Fingerprinting of Bacillus thuringiensis type strains and isolates by using Bacillus cereus group-specific repetitive extragenic palindromic sequence-based PCR analysis. Appl Environ Microbiol 71:1346–1355
     [Google Scholar]
  41. Ronquist F., Huelsenbeck J. P. 2003; MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
     [Google Scholar]
  42. Rozen S., Skaletsky H. 2000; Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386
     [Google Scholar]
  43. Saitou N., Nei M. 1987; The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
     [Google Scholar]
  44. Schnepf E., Crickmore N., Van Rie J., Lereclus D., Baum J., Feitelson J., Zeigler D. R., Dean D. H. 1998; Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol Mol Biol Rev 62:775–806
     [Google Scholar]
  45. Sonnhammer E. L., Durbin R. 1994; A workbench for large-scale sequence homology analysis. Comput Appl Biosci 10:301–307
     [Google Scholar]
  46. Stern M. J., Ames G. F., Smith N. H., Robinson E. C., Higgins C. F. 1984; Repetitive extragenic palindromic sequences: a major component of the bacterial genome. Cell 37:1015–1026
     [Google Scholar]
  47. 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
     [Google Scholar]
  48. Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G. 1997; The clustal_x Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
     [Google Scholar]
  49. Tourasse N. J., Helgason E., Økstad O. A., Hegna I. K., Kolstø A. B. 2006; The Bacillus cereus group: novel aspects of population structure and genome dynamics. J Appl Microbiol 101:579–593
     [Google Scholar]
  50. Versalovic J., Lupski J. R. 1998; Interspersed repetitive sequences in bacterial genomes. In Bacterial Genomes—Physical Structure and Analysis pp 38–48 Edited by de Bruijn F. J., Lupski J. R., Weinstock G. M. New York: Chapman & Hall;
     [Google Scholar]
  51. Wessler S. R., Bureau T. E., White S. E. 1995; LTR-retrotransposons and MITEs: important players in the evolution of plant genomes. Curr Opin Genet Dev 5:814–821
     [Google Scholar]
  52. Zuker M. 2003; Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2007/005504-0
Loading
Exploring the evolution of the Bacillus cereus group repeat element bcr1 by comparative genome analysis of closely related strains
Microbiology 153, 3894 (2007); https://doi.org/10.1099/mic.0.2007/005504-0
/content/journal/micro/10.1099/mic.0.2007/005504-0
/content/journal/micro/10.1099/mic.0.2007/005504-0
Loading

Data & Media loading...

Most cited 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