The role of recombination and mutation in 16S-23S rDNA spacer rearrangements

Gene

Volumn 238, Issue 1, 1999, Pages 241-252

  Gurtler V ^a  

^a AUSTIN HEALTH   (Australia)

Author keywords

Concerted evolution; Homologous recombination; Maximum likelihood; Phylogenomic analysis; rrn operon

Indexed keywords

RIBOSOME DNA;

ARTICLE; BACTERIAL MUTATION; CONTROLLED STUDY; DNA RECOMBINATION; GENE MUTATION; GENE REARRANGEMENT; GENETIC PROCEDURES; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; PHYLOGENY; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; SEQUENCE HOMOLOGY;

BACTERIA; BASE SEQUENCE; DNA, RIBOSOMAL; GENETIC HETEROGENEITY; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEIC ACID CONFORMATION; OPERON; PHYLOGENY; RECOMBINATION, GENETIC; RNA, RIBOSOMAL, 16S; RNA, RIBOSOMAL, 23S; SEQUENCE HOMOLOGY, NUCLEIC ACID;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECIUM; ESCHERICHIA COLI; HAEMOPHILUS INFLUENZAE; STAPHYLOCOCCUS AUREUS; VIBRIO CHOLERAE;

EID: 0344172783     PISSN: 03781119     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0378-1119(99)00224-3     Document Type: Article

References (62)

1. Antón A.I., Martínez-Murcia A.J., Rodríguez-Valera F. Sequence diversity in the 16S-23S intergenic spacer region (ISR) of the rRNA operons in representatives of the Escherichia coli ECOR collection. J. Mol. Evol. 47:1998;62-72.
2. Asai T., Zaporojets D., Squires C., Squires C.L. An Escherichia coli strain with all chromosomal rRNA operons inactivated: complete exchange of rRNA genes between bacteria. Proc. Natl. Acad. Sci. USA. 96:1999;1971-1976.
3. Blattner F.R., Plunkett G. 3rd, Bloch C.A., Perna N.T., Burland V., Riley M., Collado-Vides J., Glasner J.D., Rode C.K., Mayhew G.F., Gregor J., Davis N.W., Kirkpatrick H.A., Goeden M.A., Rose D.J., Mau B., Shao Y. The complete genome sequence of Escherichia coli K-12. Science. 277:1997;1453-1474.
4. Brosius J., Dull T.J., Sleeter D.D., Noller H.F. Gene organization and primary structure of a ribosomal RNA operon from Escherichia coli. J. Mol. Biol. 148:1981;107-127.
5. Bult C.J., White O., Olsen G.J., Zhou L., Fleischmann R.D., Sutton G.G., Blake J.A., FitzGerald L.M., Clayton R.A., Gocayne J.D., Kerlavage A.R., Dougherty B.A., Tomb J.F., Adams M.D., Reich C.I., Overbeek R., Kirkness E.F., Weinstock K.G., Merrick J.M., Glodek A., Scott J.L., Geoghagen N.S.M., Venter J.C. Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii. Science. 273:1996;1058-1073.
6. Cartwright C.P., Stock F., Beekmann S.E., Williams E.C., Gill V.J. PCR amplification of rRNA intergenic spacer regions as a method for epidemiologic typing of Clostridium difficile. J. Clin. Microbiol. 33:1995;184-187.
7. Chiaruttini C., Milet M. Gene organization, primary structure and RNA processing analysis of a ribosomal RNA operon in Lactococcus lactis. J. Mol. Biol. 230:1993;57-76.
8. Chun J., Huq A., Colwell R.R. Analysis of 16S-23S rRNA intergenic spacer regions of Vibrio cholerae and Vibrio mimicus. Appl. Environ. Microbiol. 65:1999;2202-2208.
9. Cilia V., Lafay B., Christen R. Sequence heterogeneities among 16S ribosomal RNA sequences, and their effect on phylogenetic analyses at the species level. Mol. Biol. Evol. 13:1996;451-461.
10. Clark C.G. On the evolution of ribosomal RNA. J. Mol. Evol. 25:1987;343-350.
11. Cole S.T., Brosch R., Parkhill J., Garnier T., Churcher C., Harris D., Gordon S.V., Eiglmeier K., Gas S., Barry C.E. 3rd, Tekaia F., Badcock K., Basham D., Brown D., Chillingworth T., Connor R., Davies R., Devlin K., Feltwell T., Gentles S., Hamlin N., Holroyd S., Hornsby T., Jagels K., Barrell B.G. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature. 393:1998;537-544.
12. Eisen J.A. Phylogenomics: improving functional predictions for uncharacterized genes by evolutionary analysis. Genome Res. 8:1998;163-167.
13. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J. Mol. Evol. 17:1981;368-376.
14. Felsenstein J. PHYLIP (Phylogeny Inference Package) Version 3.5c. 1993;University of Washington, Seattle, WA.
15. Fleischmann R.D., Adams M.D., White O., Clayton R.A., Kirkness E.F., Kerlavage A.R., Bult C.J., Tomb J.F., Dougherty B.A., Merrick J.M., et al. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science. 269:1995;496-512.
16. Forsman P., Tilsala-Timisjarvi A., Alatossava T. Identification of staphylococcal and streptococcal causes of bovine mastitis using 16S-23S rRNA spacer regions. Microbiology. 143:1997;3491-3500.
17. Fraser C.M., Gocayne J.D., White O., Adams M.D., Clayton R.A., Fleischmann R.D., Bult C.J., Kerlavage A.R., Sutton G., Kelley J.M., et al. The minimal gene complement of Mycoplasma genitalium. Science. 270:1995;397-403.
18. Fraser C.M., Casjens S., Huang W.M., Sutton G.G., Clayton R., Lathigra R., White O., Ketchum K.A., Dodson R., Hickey E.K., Gwinn M., Dougherty B., Tomb J.F., Fleischmann R.D., Richardson D., Peterson J., Kerlavage A.R., Quackenbush J., Salzberg S., Hanson M., van Vugt R., Palmer N., Adams M.D., Gocayne J., Venter J.C., et al. Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature. 390:1997;580-586.
19. Fraser C.M., Norris S.J., Weinstock G.M., White O., Sutton G.G., Dodson R., Gwinn M., Hickey E.K., Clayton R., Ketchum K.A., Sodergren E., Hardham J.M., McLeod M.P., Salzberg S., Peterson J., Khalak H., Richardson D., Howell J.K., Chidambaram M., Utterback T., McDonald L., Artiach P., Bowman C., Cotton M.D., Venter J.C., et al. Complete genome sequence of Treponema pallidum, the syphilis spirochete. Science. 281:1998;375-388.
20. Grassly N.C., Holmes E.C. A likelihood method for the detection of selection and recombination using nucleotide sequences. Mol. Biol. Evol. 14:1997;239-247.
21. Gürtler V., Wilson V.A., Mayall B.C. Classification of medically important clostridia using restriction endonuclease site differences of PCR-amplified 16S rDNA. J. Gen. Microbiol. 137:1991;2673-2679.
22. Gürtler V. Typing of Clostridium difficile strains by PCR-amplification of variable length 16S-23S rDNA spacer regions. J. Gen. Microbiol. 139:1993;3089-3097.
23. Gürtler V., Barrie H.D. Typing of Staphylococcus aureus strains by PCR-amplification of variable-length 16S-23S rDNA spacer regions: characterization of spacer sequences. Microbiology. 141:1995;1255-1265.
24. Gürtler V., Stanisich V.A. New approaches to typing and identification of bacteria using the 16S-23S rDNA spacer region. Microbiology. 142:1996;3-16.
25. Gürtler V., Rao Y., Pearson S.R., Bates S.M., Mayall B. DNA sequence heterogeneity in the three copies of the long 16S-23S rDNA spacer of Enterococcus faecalis isolates. Microbiology. 145:1999;1785-1796.
26. Hall L. Are point mutations or DNA rearrangements responsible for the restriction fragment length polymorphisms that are used to type bacteria? Microbiology. 140:1994;197-204.
27. Hancock J.M., Dover G.A. 'Compensatory slippage' in the evolution of ribosomal RNA genes. Nucleic Acids Res. 18:1990;5949-5954.
28. Hancock J.M., Vogler A.P. Modelling the secondary structures of slippage-prone hypervariable RNA regions: the example of the tiger beetle 18S rRNA variable region V4. Nucleic Acids Res. 26:1998;1689-1699.
29. Harvey S., Hill C.W., Squires C., Squires C.L. Loss of the spacer loop sequence from the rrnB operon in the Escherichia coli K-12 subline that bears the relA1 mutation. J. Bacteriol. 170:1988;1235-1238.
30. Himmelreich R., Hilbert H., Plagens H., Pirkl E., Li B.C., Herrmann R. Complete sequence analysis of the genome of the bacterium Mycoplasma pneumoniae. Nucleic Acids Res. 24:1996;4420-4449.
31. Ikemura T., Nomura M. Expression of spacer tRNA genes in ribosomal RNA transcription units carried by hybrid Col E1 plasmids in E. coli. Cell. 11:1977;779-793.
32. Jensen M.A., Webster J.A., Straus N. Rapid identification of bacteria on the basis of polymerase chain reaction-amplified ribosomal DNA spacer polymorphisms. Appl. Environ. Microbiol. 59:1993;945-952.
33. Kaneko T., Sato S., Kotani H., Tanaka A., Asamizu E., Nakamura Y., Miyajima N., Hirosawa M., Sugiura M., Sasamoto S., Kimura T., Hosouchi T., Matsuno A., Muraki A., Nakazaki N., Naruo K., Okumura S., Shimpo S., Takeuchi C., Wada T., Watanabe A., Yamada M., Yasuda M., Tabata S. Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. Supplement DNA Res. 3:1996;185-209.
34. Klenk H.P., Clayton R.A., Tomb J.F., White O., Nelson K.E., Ketchum K.A., Dodson R.J., Gwinn M., Hickey E.K., Peterson J.D., Richardson D.L., Kerlavage A.R., Graham D.E., Kyrpides N.C., Fleischmann R.D., Quackenbush J., Lee N.H., Sutton G.G., Gill S., Kirkness E.F., Dougherty B.A., McKenney K., Adams M.D., Loftus B., Venter J.C., et al. The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus. Nature. 390:1997;364-370.
35. Kunst F., Ogasawara N., Moszer I., Albertini A.M., Alloni G., Azevedo V., Bertero M.G., Bessieres P., Bolotin A., Borchert S., Borriss R., Boursier L., Brans A., Braun M., Brignell S.C., Bron S., Brouillet S., Bruschi C.V., Caldwell B., Capuano V., Carter N.M., Choi S.K., Codani J.J., Connerton I.F., Danchin A., et al. The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature. 390:1997;249-256.
36. Lan R., Reeves P.R. Recombination between rRNA operons created most of the ribotype variation observed in the seventh pandemic clone of Vibrio cholerae. Microbiology. 144:1998;1213-1221.
37. Levinson G., Gutman G.A. Slipped-strand mispairing: a major mechanism for DNA sequence evolution. Mol. Biol. Evol. 4:1987;203-221.
38. Liu S.L., Sanderson K.E. Homologous recombination between rrn operons rearranges the chromosome in host-specialized species of Salmonella. FEMS Microbiol. Lett. 164:1998;275-281.
39. Loughney K., Lund E., Dahlberg J.E. tRNA genes are found between 16S and 23S rRNA genes in Bacillus subtilis. Nucleic Acids Res. 10:1982;1607-1624.
40. Lund E., Dahlberg J.E., Lindahl L., Jaskunas S.R., Dennis P.P., Nomura M. Transfer RNA genes between 16S and 23S rRNA genes in rRNA transcription units of E. coli. Cell. 7:1976;165-177.
41. Maddison W.P., Maddison D.R. MacClade: Analysis of Phylogeny and Character Evolution. 1992;Sinauer Associates, Sunderland, MA.
42. Morgan E.A., Ikemura T., Nomura M. Identification of spacer tRNA genes in individual ribosomal RNA transcription units of Escherichia coli. Proc. Natl. Acad. Sci. USA. 74:1977;2710-2714.
43. Mylvaganam S., Dennis P.P. Sequence heterogeneity between the two genes encoding 16S rRNA from the halophilic archaebacterium Haloarcula marismortui. Genetics. 130:1992;399-410.
44. Naïmi A., Beck G., Branlant C. Primary and secondary structures of rRNA spacer regions in enterococci. Microbiology. 143:1997;823-834.
45. Ninet B., Monod M., Emler S., Pawlowski J., Metral C., Rohner P., Auckenthaler R., Hirschel B. Two different 16S rRNA genes in a mycobacterial strain. J. Clin. Microbiol. 34:1996;2531-2536.
46. Nomura M. Engineering of bacterial ribosomes: replacement of all seven Escherichia coli rRNA operons by a single plasmid-encoded operon. Proc. Natl. Acad. Sci. USA. 96:1999;1820-1822.
47. Nour M. Studies on the large subunit rRNA genes and their flanking regions of Leuconostocs. Can. J. Microbiol. 44:1998;807-818.
48. Ojaimi C., Davidson B.E., Saint Girons I., Old I.G. Conservation of gene arrangement and an unusual organization of rRNA genes in the linear chromosomes of the Lyme disease spirochaetes Borrelia burgdorferi, B. garinii and B. afzelii. Microbiology. 140:1994;2931-2940.
49. Privitera A., Rappazzo G., Sangari P., Giannino V., Licciardello L., Stefani S. Cloning and sequencing of a 16S/23S ribosomal spacer from Haemophilus parainfluenzae reveals an invariant, mosaic-like organisation of sequence blocks. FEMS Microbiol. Lett. 164:1998;289-294.
50. Reischl U., Feldmann K., Naumann L., Gaugler B.J., Ninet B., Hirschel B., Emler S. 16S rRNA sequence diversity in Mycobacterium celatum strains caused by presence of two different copies of 16S rRNA gene. J. Clin. Microbiol. 36:1998;1761-1764.
51. Sander P., Prammananan T., Bottger E.C. Introducing mutations into a chromosomal rRNA gene using a genetically modified eubacterial host with a single rRNA operon. Mol. Microbiol. 22:1996;841-848.
52. Sawada M., Osawa S., Kobayashi H., Hori H., Muto A. The number of ribosomal RNA genes in Mycoplasma capricolum. Mol. Gen. Genet. 182:1981;502-504.
53. Smith D.R., et al. Complete genome sequence of Methanobacterium thermoautotrophicum deltaH: functional analysis and comparative genomics. J. Bacteriol. 179:1997;7135-7155.
54. Sneath P.H. Evidence from Aeromonas for genetic crossing-over in ribosomal sequences. Int. J. Syst. Bacteriol. 43:1993;626-629.
55. Stephens R.S., Kalman S., Lammel C., Fan J., Marathe R., Aravind L., Mitchell W., Olinger L., Tatusov R.L., Zhao Q., Koonin E.V., Davis R.W. Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science. 282:1998;754-759.
56. Tautz D., Trick M., Dover G.A. Cryptic simplicity in DNA is a major source of genetic variation. Nature. 322:1986;652-656.
57. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:1997;4876-4882.
58. Tomb J.F., White O., Kerlavage A.R., Clayton R.A., Sutton G.G., Fleischmann R.D., Ketchum K.A., Klenk H.P., Gill S., Dougherty B.A., Nelson K., Quackenbush J., Zhou L., Kirkness E.F., Peterson S., Loftus B., Richardson D., Dodson R., Khalak H.G., Glodek A., McKenney K., Fitzegerald L.M., Lee N., Adams M.D., Venter J.C., et al. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature. 388:1997;539-547.
59. Wang Y., Zhang Z., Ramanan N. The actinomycete Thermobispora bispora contains two distinct types of transcriptionally active 16S rRNA genes. J. Bacteriol. 179:1997;3270-3276.
60. Woese C.R. Bacterial evolution. Microbiol. Rev. 51:1987;221-271.
61. Wu M., Davidson N. Use of gene 32 protein staining of single-strand polynucleotides for gene mapping by electron microscopy: application to the phi80d3ilvsu+7 system. Proc. Natl. Acad. Sci. USA. 72:1975;4506-4510.
62. Young R.A., Macklis R., Steitz J.A. Sequence of the 16S-23S spacer region in two ribosomal RNA operons of Escherichia coli. J. Biol. Chem. 254:1979;3264-3271.