Comparative sequence analyses reveal frequent occurrence of short segments containing an abnormally high number of non-random base variations in bacterial rRNA genes
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.
AsaiT., ZaporojetsD., SquiresC., SquiresC. L.1999; An Escherichia coli strain with all chromosomal rRNA operons inactivated: complete exchange of rRNA genes between bacteria. Proc Natl Acad Sci USA 96:1971–1976[CrossRef]
CarranzaS., GiribetG., RiberatC., BagunaJ., RiutortM.1996; Evidence that two types of 18S rDNA coexist in the genome of Dugesia (Schmidtea) mediterranea (Platyhelminthes, Turbellaria, Tricladida). Mol Biol Evol 13:824–832[CrossRef]
GreenR., SamahaR. R., NollerH. F.1997; Mutations at nucleotides G2251 and U2585 of 23S rRNA perturb the peptidyl transferase center of the ribosome. J Mol Biol 266:40–50[CrossRef]
GroismanE. A., SaierM. H.Jr, OchmanH.1992; Horizontal transfer of a phosphatase gene as evidence for mosaic structure of the Salmonella genome. EMBO J 11:1309–1316
GutellR. G., LarsenN., WoeseC. R.1994; Lessons from an evolving rRNA: 16S and 23S rRNA structures from a comparative perspective. Microbiol Rev 58:10–26
KochC., KroppenstedtR. M., RaineyF. A., StackebrandtE.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 Bacteriol 46:765–768[CrossRef]
KooninE. V., MushegianA. R., GalperinM. Y., WalkerD. R.1999; Comparison of archaeal and bacterial genomes: computer analysis of protein sequences suggests a chimeric origin for the archaea. Mol Microbiol 25:619–637
MylvaganamS., DennisP. P.1992; Sequence heterogeneity between the two genes encoding 16S rRNA from the halophilic archaebacterium Halobacterium marismortui. Genetics 130:399–410
NelsonK. E., ClaytonR. A., GillS. R.22 other authors1999; Evidence for lateral gene transfer between Archaea and Bacteria from genome sequence of Thermotoga maritima. Nature 399:323–329[CrossRef]
NiebelH., DorschM., StackebrandtE.1987; Cloning and expression in Escherichia coli of Proteus vulgaris genes for 16S ribosomal RNA. J Gen Microbiol 133:2401–2409
RheimsH., SchumannP., RohdeM., StackebrandtE.1998; Verrucosispora gifhornensis gen. nov., sp. nov., a new member of the actinobacterial family Micromonosporaceae. Int J Syst Bacteriol 48:1119–1127[CrossRef]
Van de PeerY., ChapelleS., WachterR. D.1996; A quantitative map of nucleotide substitution rates in bacterial rRNA. Nucleic Acids Res 24:3381–3391[CrossRef]
WangY., ZhangZ. S., RuanJ. 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 Bacteriol 46:933–938[CrossRef]
WoeseC. R., KandlerO., WheelisM. L.1990; Towards a natural system of organisms: proposal for the domains Archaea, Bacteria and Eucarya. Proc Natl Acad Sci USA 87:4576–4579[CrossRef]
YapW. H., ZhangZ. S., WangY.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 Bacteriol 181:5201–5209
Comparative sequence analyses reveal frequent occurrence of short segments containing an abnormally high number of non-random base variations in bacterial rRNA genes