Evolution of paralogous genes: Reconstruction of genome rearrangements through comparison of multiple genomes within Staphylococcus aureus

Molecular Biology and Evolution

Volumn 23, Issue 6, 2006, Pages 1269-1285

  Tsuru, Takeshi ^a   Kawai, Mikihiko ^a,b   Mizutani Ui, Yoko ^a   Uchiyama, Ikuo ^c   Kobayashi, Ichizo ^a,b  

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

Author keywords

Deletion; Genome comparison; Genome rearrangements; Recombination; Restriction modification

Indexed keywords

BACTERIAL DNA; BACTERIAL RNA;

ARTICLE; BACTERIAL GENOME; BACTERIAL STRAIN; DNA POLYMORPHISM; DNA SEQUENCE; EVOLUTION; GENE CLUSTER; GENE NUMBER; GENE REARRANGEMENT; GENE SEQUENCE; GENETIC CODE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; STAPHYLOCOCCUS AUREUS;

AMINO ACID SEQUENCE; BASE SEQUENCE; EVOLUTION, MOLECULAR; GENOME, BACTERIAL; MOLECULAR SEQUENCE DATA; POLYMORPHISM, GENETIC; RECOMBINATION, GENETIC; RRNA OPERON; STAPHYLOCOCCUS AUREUS;

BACTERIA (MICROORGANISMS); STAPHYLOCOCCUS AUREUS;

EID: 33646891724     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msk013     Document Type: Article

References (60)

1. Abadjieva, A., J. Patel, M. Webb, V. Zinkevich, and K. Firman. 1993. A deletion mutant of the type IC restriction endonuclease EcoR1241 expressing a novel DNA specificity. Nucleic Acids Res. 21:4435-4443.
2. Adamczyk-Poplawska, M., A. Kondrzycka, K. Urbanek, and A. Piekarowicz. 2003. Tetra-amino-acid tandem repeats are involved in HsdS complementation in type IC restriction-modification systems. Microbiology 149:3311-3319.
3. Alm, R. A., L. S. Ling, D. T. Moir et al. (26 co-authors). 1999. Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 397:176-180.
4. Baba, T., F. Takeuchi, M. Kuroda et al. (17 co-authors). 2002. Genome and virulence determinants of high virulence community-acquired MRSA. Lancet 359:1819-1827.
5. Baba, T., F. Takeuchi, M. Kuroda, H. Yuzawa, T. Ito, and K. Hiramatsu. 2004. The genome of Staphylococcus aureus. Pp. 66-153 in D. A. A. Ala'Aladeen and K. Hiramatsu, eds. The Staphylococcus aureus: molecular and clinical aspects. Horwood, Chichester, United Kingdom.
6. Brussow, H., C. Canchaya, and W. D. Hardt. 2004. Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol. Mol. Biol. Rev. 68:560-602.
7. Chedin, F., E. Dervyn, R. Dervyn, S. D. Ehrlich, and P. Noirot. 1994. Frequency of deletion formation decreases exponentially with distance between short direct repeats. Mol. Microbiol. 12:561-569.
8. Chin, V., V. Valinluck, S. Magaki, and J. Ryu. 2004. KpnBI is the prototype of a new family (IE) of bacterial type I restriction-modification system. Nucleic Acids Res. 32:e138.
9. Datta, A., M. Hendrix, M. Lipsitch, and S. Jinks-Robertson. 1997. Dual roles for DNA sequence identity and the mismatch repair system in the regulation of mitotic crossing-over in yeast. Proc. Natl. Acad. Sci. USA 94:9757-9762.
10. Fitzgerald, J. R., S. D. Reid, E. Ruotsalainen, T. J. Tripp, M. Liu, R. Cole, P. Kuusela, P. M. Schlievert, A. Jarvinen, and J. M. Musser. 2003. Genome diversification in Staphylococcus aureus: molecular evolution of a highly variable chromosomal region encoding the staphylococcal exotoxin-like family of proteins. Infect. Immun. 71:2827-2838.
11. Forsman, P., A. Tilsala-Timisjarvi, and T. Alatossava. 1997. Identification of staphylococcal and streptococcal causes of bovine mastitis using 16S-23S rRNA spacer regions. Microbiology 143:3491-3500.
12. Foster, T. J., and M. Hook. 1998. Surface protein adhesins of Staphylococcus aureus. Trends Microbiol. 6:484-488.
13. Fujitani, Y., and I. Kobayashi. 1999. Effect of DNA sequence divergence on homologous recombination as analyzed by a random-walk model. Genetics 153:1973-1988.
14. Fujitani, Y., K. Yamamoto, and I. Kobayashi. 1995. Dependence of frequency of homologous recombination on the homology length. Genetics 140:797-809.
15. Fuller-Pace, F. V., L. R. Bullas, H. Delius, and N. E. Murray. 1984. Genetic recombination can generate altered restriction specificity. Proc. Natl. Acad. Sci. USA 81:6095-6099.
16. Gann, A. A., A. J. Campbell, J. F. Collins, A. F. Coulson, and N. E. Murray. 1987. Reassortment of DNA recognition domains and the evolution of new specificities. Mol. Microbiol. 1:13-22.
17. Giannino, V., G. Rappazzo, A. Scuto, O. Di Marco, A. Privitera, M. Santagati, and S. Stefani. 2001. rrn operons in Haemophilus parainfluenzae and mosaicism of conserved and species-specific sequences in the 16S-23S rDNA long spacer. Res. Microbiol. 152:461-468.
18. Gill, S. R., D. E. Fouts, G. L. Archer et al. (32 co-authors). 2005. Insights on evolution of virulence and resistance from the complete genome analysis of an early methicillin-resistant Staphylococcus aureus strain and a biofilm-producing methicillin-resistant Staphylococcus epidermidis strain. J. Bacteriol. 187:2426-2438.
19. Gubler, M., D. Braguglia, J. Meyer, A. Piekarowicz, and T. A. Bickle. 1992. Recombination of constant and variable modules alters DNA sequence recognition by type IC restriction-mod-ification enzymes. Embo J. 11:233-240.
20. Gurtler, V. 1999. The role of recombination and mutation in 16S-23S rDNA spacer rearrangements. Gene 238:241-252.
21. Gurtler, V., and H. D. Barrie. 1995. Typing of Staphylococcus aureus strains by PCR-amplification of variable-length 16S-23S rDNA spacer regions: characterization of spacer sequences. Microbiology 141:1255-1265.
22. Gurtler, V., and B. C. Mayall. 2001. Genetic transfer and genome evolution in MRSA. Microbiology 147:3195-3197.
23. Gurtler, V., and V. A. Stanisich. 1996. New approaches to typing and identification of bacteria using the 16S-23S rDNA spacer region. Microbiology 142:3-16.
24. Harvey, S., C. W. Hill, C. Squires, and C. L. Squires. 1988. Loss of the spacer loop sequence from the rrnB operon in the Escherichia coli K-12 subline that bears the relA1 mutation. J. Bacteriol. 170:1235-1238.
25. Hill, C. W. 1999. Large genomic sequence repetitions in bacteria: lessons from rRNA operons and Rhs elements. Res. Microbiol. 150:665-674.
26. Hiramatsu, K., L. Cui, M. Kuroda, and T. Ito. 2001. The emergence and evolution of methicillin-resistant Staphylococcus aureus. Trends Microbiol. 9:486-493.
27. Holden, M. T., E. J. Feil, J. A. Lindsay et al. (48 co-authors). 2004. Complete genomes of two clinical Staphylococcus aureus strains: evidence for the rapid evolution of virulence and drug resistance. Proc. Natl. Acad. Sci. USA 101:9786-9791.
28. Katayama, Y., T. Ito, and K. Hiramatsu. 2000. A new class of genetic element, Staphylococcus cassette chromosome mec, encodes methicillin resistance in Staphylococcus aureus. Antimicrob. Agents Chemother. 44:1549-1555.
29. Khasanov, F. K., D. J. Zvingila, A. A. Zainullin, A. A. Prozorov, and V. I. Bashkirov. 1992. Homologous recombination between plasmid and chromosomal DNA in Bacillus subtilis requires approximately 70 bp of homology. Mol. Gen. Genet. 234:494-497.
30. Kim, J. S., A. DeGiovanni, J. Jancarik, P. D. Adams, H. Yokota, R. Kim, and S. H. Kim. 2005. Crystal structure of DNA sequence specificity subunit of a type I restriction-modification enzyme and its functional implications. Proc. Natl. Acad. Sci. USA 102:3248-3253.
31. Kobayashi, I. 2004. Restriction-modification systems as minimal forms of life. Pp. 19-62 in A. Pingoud, ed. Restriction endonucleases. Springer-Verlag, Berlin, Germany.
32. Kuroda, M., T. Ohta, I. Uchiyama et al. (37 co-authors). 2001. Whole genome sequencing of meticillin-resistant Staphylococcus aureus. Lancet 357:1225-1240.
33. Lan, R., and P. R. Reeves. 1998. Recombination between rRNA operons created most of the ribotype variation observed in the seventh pandemic clone of Vibrio cholerae. Microbiology 144:1213-1221.
34. Liao, D. 2000. Gene conversion drives within genic sequences: concerted evolution of ribosomal RNA genes in bacteria and archaea. J. Mol. Evol. 51:305-317.
35. Lina, G., G. A. Bohach, S. P. Nair, K. Hiramatsu, E. Jouvin-Marche, and R. Mariuzza. 2004. Standard nomenclature for the superantigens expressed by Staphylococcus. J. Infect. Dis. 189:2334-2336.
36. Lindsay, J. A., and M. T. Holden. 2004. Staphylococcus aureus: superbug, super genome? Trends Microbiol. 12:378-385.
37. Lovett, S. T. 2004. Encoded errors: mutations and rearrangements mediated by misalignment at repetitive DNA sequences. Mol. Microbiol. 52:1243-1253.
38. Lovett, S. T., T. J. Gluckman, P. J. Simon, V. A. Sutera Jr, and P. T. Drapkin. 1994. Recombination between repeats in Escherichia coli by a recA-independent, proximity-sensitive mechanism. Mol. Gen. Genet. 245:294-300.
39. MacWilliams, M. P., and T. A. Bickle. 1996. Generation of new DNA binding specificity by truncation of the type IC EcoDXXI hsdS gene. Embo J. 15:4775-4783.
40. McDevitt, D., and T. J. Foster. 1995. Variation in the size of the repeat region of the fibrinogen receptor (clumping factor) of Staphylococcus aureus strains. Microbiology 141:937-943.
41. Michel, B. 1999. Illegitimate recombination in bacteria. Pp. 129-150 in R. L. Charlebois, ed. Organization of the prokaryotic genome. ASM Press, Washington, D. C.
42. Murray, N. E. 2000. Type I restriction systems: sophisticated molecular machines (a legacy of Bertani and Weigle). Microbiol. Mol. Biol. Rev. 64:412-434.
43. Naito, T., K. Kusano, and I. Kobayashi. 1995. Selfish behavior of restriction-modification systems. Science 267:897-899.
44. Nei, M., and S. Kumar. 2001. Molecular evolution and phylogenetics. Oxford University Press, New York.
45. Nobusato, A., I. Uchiyama, S. Ohashi, and I. Kobayashi. 2000. Insertion with long target duplication: a mechanism for gene mobility suggested from comparison of two related bacterial genomes. Gene 259:99-108.
46. Ohta, T., H. Hirakawa, K. Morikawa et al. (12 co-authors). 2004. Nucleotide substitutions in Staphylococcus aureus strains, Mu50, Mu3, and N315. DNA Res. 11:51-56.
47. Privitera, A., G. Rappazzo, P. Sangari, V. Giannino, L. Licciardello, and S. Stefani. 1998. Cloning and sequencing of a 16S/23S ribosomal spacer from Haemophilus parainfluenzae reveals an invariant, mosaic-like organisation of sequence blocks. FEMS Microbiol. Lett. 164:289-294.
48. Read, T. D., S. L. Salzberg, M. Pop et al. (13 co-authors). 2002. Comparative genome sequencing for discovery of novel polymorphisms in Bacillus anthracis. Science 296:2028-2033.
49. Reed, S. B., C. A. Wesson, L. E. Liou, W. R. Trumble, P. M. Schlievert, G. A. Bohach, and K. W. Bayles. 2001. Molecular characterization of a novel Staphylococcus aureus serine protease operon. Infect. Immun. 69:1521-1527.
50. Robinson, D. A., and M. C. Enright. 2004. Evolution of Staphylococcus aureus by large chromosomal replacements. J. Bacteriol. 186:1060-1064.
51. Rocha, E. P. 2004. Order and disorder in bacterial genomes. Curr. Opin. Microbiol. 7:519-527.
52. Rocha, E. P., and A. Blanchard. 2002. Genomic repeats, genome plasticity and the dynamics of Mycoplasma evolution. Nucleic Acids Res. 30:2031-2042.
53. Ruzin, A., J. Lindsay, and R. P. Novick. 2001. Molecular genetics of SaPI1 - a mobile pathogenicity island in Staphylococcus aureus. Mol. Microbiol. 41:365-377.
54. Schouler, C., M. Gautier, S. D. Ehrlich, and M. C. Chopin. 1998. Combinational variation of restriction modification specificities in Lactococcus lactis. Mol. Microbiol. 28:169-178.
55. Titheradge, A. J., J. King, J. Ryu, and N. E. Murray. 2001. Families of restriction enzymes: an analysis prompted by molecular and genetic data for type ID restriction and modification systems. Nucleic Acids Res. 29:4195-4205.
56. Uchiyama, I., T. Higuchi, and I. Kobayashi. 2000. CGAT: comparative genome analysis tool for closely related microbial genomes. Genome Informatics 11:341-342.
57. van der Woude, M. W., and A. J. Baumler. 2004. Phase and antigenic variation in bacteria. Clin. Microbiol. Rev. 17:581-611.
58. Vulic, M., F. Dionisio, F. Taddei, and M. Radman. 1997. Molecular keys to speciation: DNA polymorphism and the control of genetic exchange in enterobacteria. Proc. Natl. Acad. Sci. USA 94:9763-9767.
59. Williams, R. J., J. M. Ward, B. Henderson, S. Poole, B. P. O'Hara, M. Wilson, and S. P. Nair. 2000. Identification of a novel gene cluster encoding staphylococcal exotoxin-like proteins: characterization of the prototypic gene and its protein product, SET1. Infect. Immun. 68:4407-4415.
60. Yamaguchi, T., K. Nishifuji, M. Sasaki, Y. Fudaba, M. Aepfelbacher, T. Takata, M. Ohara, H. Komatsuzawa, M. Amagai, and M. Sugai. 2002. Identification of the Staphylococcus aureus etd pathogenicity island which encodes a novel exfoliative toxin, ETD, and EDIN-B. Infect. Immun. 70:5835-5845.