1887

Abstract

The GenBank accession numbers for the 23S rRNA sequences determined in this study are AF192136–AF192150.

rRNA genes are thought unlikely to be laterally transferred, because rRNA must coevolve with a large number of cellular components to form the highly sophisticated translation apparatus and perform protein synthesis. In this paper, the authors first hypothesized that lateral gene transfer (LGT) might occur to rRNA genes via replacement of gene segments encoding individual domains of rRNA: the ‘simplified complexity hypothesis’. Comparative sequence analyses of the 16S and 23S rRNA genes from a large number of actinomycete species frequently identified rRNA genes containing short segments with an abnormally high number of non-random base variations. These variations were nearly always characterized by complementing covariations of several paired bases within the stem of a hairpin. The nature of these base variations is not consistent with random mutations but satisfies well the predictions of the ‘simplified complexity hypothesis’. The most parsimonious explanation for this phenomenon is the lateral transfer of rRNA gene segments between different bacterial species. This mode of LGT may create mosaic rRNA genes and occur repeatedly in different regions of a gene, gradually destroying the evolutionary history recorded in the nucleotide sequence.

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2000-11-01
2020-09-29
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References

  1. Asai T., Zaporojets D., Squires C., Squires C. L.. 1999; An Escherichia coli strain with all chromosomal rRNA operons inactivated: complete exchange of rRNA genes between bacteria. Proc Natl Acad Sci USA96:1971–1976[CrossRef]
    [Google Scholar]
  2. Brosius J., Palmer J. J., Kennedy J. P., Noller H. F.. 1978; Complete nucleotide sequence of a 16S ribosomal gene from Escherichia coli. Proc Natl Acad Sci USA75:4801–4805[CrossRef]
    [Google Scholar]
  3. Carranza S., Giribet G., Riberat C., Baguna J., Riutort M.. 1996; Evidence that two types of 18S rDNA coexist in the genome of Dugesia (Schmidtea) mediterranea (Platyhelminthes, Turbellaria, Tricladida). Mol Biol Evol13:824–832[CrossRef]
    [Google Scholar]
  4. Chun J., Goodfellow M.. 1995; A phylogenetic analysis of the genus Nocardia with 16S rRNA gene sequences. Int J Syst Bacteriol45:240–245[CrossRef]
    [Google Scholar]
  5. Doolittle W. F.. 1999; Phylogenetic classification and universal tree. Science284:2124–2128[CrossRef]
    [Google Scholar]
  6. Felsenstein J.. 1985; Confidence limits on phylogenies: an approach using the bootstrap. Evolution46:159–173
    [Google Scholar]
  7. Green R., Samaha R. R., Noller H. F.. 1997; Mutations at nucleotides G2251 and U2585 of 23S rRNA perturb the peptidyl transferase center of the ribosome. J Mol Biol266:40–50[CrossRef]
    [Google Scholar]
  8. Groisman E. A., Saier M. H. Jr, Ochman H.. 1992; Horizontal transfer of a phosphatase gene as evidence for mosaic structure of the Salmonella genome. EMBO J11:1309–1316
    [Google Scholar]
  9. Gunderson J. H., Sogin M. L., Wollet G., Hollingdale M., de la Cruz V. F., Waters A. P., McCutchan T. F.. 1987; Structurally distinct, stage-specific ribosomes occur in Plasmodium. Science238:933–937[CrossRef]
    [Google Scholar]
  10. Gutell R. G., Larsen N., Woese C. R.. 1994; Lessons from an evolving rRNA: 16S and 23S rRNA structures from a comparative perspective. Microbiol Rev58:10–26
    [Google Scholar]
  11. Higgins D. G., Bleasby A. J., Fuchs R.. 1992; clustal v: improved software for multiple sequence alignment. Comput Appl Biosci8:189–191
    [Google Scholar]
  12. Hillis D. M., Moritz C., Porter C. A., Baker R. J.. 1990; Evidence for biased gene conversion in concerted evolution of ribosomal DNA. Science251:308–310
    [Google Scholar]
  13. Jain R., Rivera M. C., Lake J. A.. 1999; Horizontal gene transfer among genomes: the complexity hypothesis. Proc Natl Acad Sci USA96:3801–3806[CrossRef]
    [Google Scholar]
  14. Koch C., Kroppenstedt R. M., Rainey F. A., Stackebrandt E.. 1996; 16S ribosomal DNA analysis of the genera Micromonospora, Actinoplanes, Catellatospora, Catenuloplanes, Couchioplanes, Dactylosporangium, and Pilimelia and emendation of the family Micromonosporaceae. Int J Syst Bacteriol46:765–768[CrossRef]
    [Google Scholar]
  15. Koonin E. V., Mushegian A. R., Galperin M. Y., Walker D. R.. 1999; Comparison of archaeal and bacterial genomes: computer analysis of protein sequences suggests a chimeric origin for the archaea. Mol Microbiol25:619–637
    [Google Scholar]
  16. Lawrence J. G., Ochman H.. 1997; Amelioration of bacterial genome: rates of change and exchange. J Mol Evol44:383–397[CrossRef]
    [Google Scholar]
  17. Mankin A. S.. 1997; Pactamycin resistance mutations in functional sites of 16S rRNA. J Mol Biol274:8–15[CrossRef]
    [Google Scholar]
  18. Mylvaganam S., Dennis P. P.. 1992; Sequence heterogeneity between the two genes encoding 16S rRNA from the halophilic archaebacterium Halobacterium marismortui. Genetics130:399–410
    [Google Scholar]
  19. Nelson K. E., Clayton R. A., Gill S. R..22 other authors 1999; Evidence for lateral gene transfer between Archaea and Bacteria from genome sequence of Thermotoga maritima. Nature399:323–329[CrossRef]
    [Google Scholar]
  20. Niebel H., Dorsch M., Stackebrandt E.. 1987; Cloning and expression in Escherichia coli of Proteus vulgaris genes for 16S ribosomal RNA. J Gen Microbiol133:2401–2409
    [Google Scholar]
  21. Rheims H., Schumann P., Rohde M., Stackebrandt E.. 1998; Verrucosispora gifhornensis gen. nov., sp. nov., a new member of the actinobacterial family Micromonosporaceae. Int J Syst Bacteriol48:1119–1127[CrossRef]
    [Google Scholar]
  22. Rivera M. C., Jain R., Moore J. E., Lake J. A.. 1998; Genomic evidence for two functionally distinct gene classes. Proc Natl Acad Sci USA95:6239–6244[CrossRef]
    [Google Scholar]
  23. Saitou N., Nei M.. 1987; The neighbour-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol4:406–425
    [Google Scholar]
  24. Sawyer S.. 1989; Statistical tests for detecting gene conversion. Mol Biol Evol6:526–538
    [Google Scholar]
  25. Smith J. M., Dowson C. G., Spratt B. G.. 1991; Localized sex in bacteria. Nature349:29–31[CrossRef]
    [Google Scholar]
  26. Swofford D. L., Begle D. P.. 1993; Phylogenetic Analysis Using Parsimony (Version 3.1), User’s Manual Champaign, IL: Smithsonian Institute Laboratory of Molecular Systematics;
    [Google Scholar]
  27. Syvanen M.. 1994; Horizontal gene transfer: evidence and possible consequences. Annu Rev Genet28:237–261[CrossRef]
    [Google Scholar]
  28. Ueda K., Seki T., Kudo T., Yoshida T., Kataoka M.. 1999; Two distinct mechanisms cause heterogeneity of 16S rRNA. J Bacteriol181:78–82
    [Google Scholar]
  29. Van de Peer Y., Chapelle S., Wachter R. D.. 1996; A quantitative map of nucleotide substitution rates in bacterial rRNA. Nucleic Acids Res24:3381–3391[CrossRef]
    [Google Scholar]
  30. Wang Y., Zhang Z. S., Ruan J. S.. 1996; A proposal to transfer Microbispora bispora (Lechevalier 1965) to a new genus, Thermobispora gen. nov., as Thermobispora bispora comb. nov. Int J Syst Bacteriol46:933–938[CrossRef]
    [Google Scholar]
  31. Wang Y., Zhang Z. S., Ramanan N.. 1997; The actinomycete Thermobispora bispora contains two distinct types of transcriptionally active 16S rRNA genes. J Bacteriol179:3270–3276
    [Google Scholar]
  32. Ward-Rainey N., Rainey F. A., Stackebrandt E.. 1996; The phylogenetic structure of the genus Streptosporangium. Syst Appl Microbiol19:50–55[CrossRef]
    [Google Scholar]
  33. Woese C. R.. 1987; Bacterial evolution. Microbial Rev51:221–271
    [Google Scholar]
  34. Woese C. R.. 1998; The universal ancestor. Proc Natl Acad Sci USA95:6854–6859[CrossRef]
    [Google Scholar]
  35. Woese C. R., Kandler O., Wheelis M. L.. 1990; Towards a natural system of organisms: proposal for the domains Archaea, Bacteria and Eucarya. Proc Natl Acad Sci USA87:4576–4579[CrossRef]
    [Google Scholar]
  36. Yap W. H., Wang Y.. 1999; Molecular cloning and comparative sequence analyses of rRNA operons in Streptomyces nodosus ATCC 14899. Gene232:77–85[CrossRef]
    [Google Scholar]
  37. Yap W. H., Zhang Z. S., Wang Y.. 1999; Distinct types of rRNA operons exist in the genome of the actinomycete Thermomonospora chromogena and evidence for horizontal transfer of an entire rRNA operon. J Bacteriol181:5201–5209
    [Google Scholar]
  38. Zhang Z. S., Wang Y., Ruan J. S.. 1998; Reclassification of Thermomonospora and Microtetraspora. Int J Syst Bacteriol48:411–422[CrossRef]
    [Google Scholar]
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