1887

Abstract

Informational genes such as those encoding rRNAs are related to transcription and translation, and are thus considered to be rarely subject to lateral gene transfer (LGT) between different organisms, compared to operational genes having metabolic functions. However, several lines of evidence have suggested or confirmed the occurrence of LGT of DNA segments encoding evolutionarily variable regions of rRNA genes between different organisms. In the present paper, we show, for the first time to our knowledge, that variable regions of the 18S rRNA gene are segmentally replaced by multiple copies of different sequences in a single strain of the green microalga , resulting in at least 17 genotypes, nine of which were actually transcribed. Recombination between different 18S rRNA genes occurred in seven out of eight variable regions (V1–V5 and V7–V9) of eukaryotic small subunit (SSU) rRNAs. While no recombination was observed in V1, one to three different recombination loci were demonstrated for the other regions. Such segmental replacement was also implicated for helix H37, which is defined as V6 of prokaryotic SSU rRNAs. Our observations provide direct evidence for redundant recombination of an informational gene, which encodes a component of mature ribosomes, in a single strain of one organism.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2007/009365-0
2007-11-01
2019-10-18
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/11/3879.html?itemId=/content/journal/micro/10.1099/mic.0.2007/009365-0&mimeType=html&fmt=ahah

References

  1. Alverson, A. J. & Kolnick, L. ( 2005; ). Intragenomic nucleotide polymorphism among small subunit (18S) rDNA paralogs in the diatom genus Skeletonema (Bacillariophyta). J Phycol 41, 1248–1257.[CrossRef]
    [Google Scholar]
  2. 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 U S A 96, 1971–1976.[CrossRef]
    [Google Scholar]
  3. Baliga, N. S., Bonneau, R., Facciotti, M. T., Pan, M., Glusman, G., Deutsch, E. W., Shannon, P., Chiu, Y., Weng, R. S. & other authors ( 2004; ). Genome sequence of Haloarcula marismortui: a halophilic archaeon from the Dead Sea. Genome Res 14, 2221–2234.[CrossRef]
    [Google Scholar]
  4. Boucher, Y., Douady, C. J., Sharma, A. K., Kameoka, M. & Doolittle, W. F. ( 2004; ). Intragenomic heterogeneity and intergenomic recombination among haloarchaeal rRNA genes. J Bacteriol 186, 3980–3990.[CrossRef]
    [Google Scholar]
  5. Bradley, R. D. & Hillis, D. M. ( 1997; ). Recombinant DNA sequences generated by PCR amplification. Mol Biol Evol 14, 592–593.[CrossRef]
    [Google Scholar]
  6. Buckler, E. S., IV, Ippolito, A. & Holtsford, T. P. ( 1997; ). The evolution of ribosomal DNA: divergent paralogues and phylogenetic implications. Genetics 145, 821–832.
    [Google Scholar]
  7. Carranza, S., Giribet, G., Ribera, C., Baguña, J. & Riutort, M. ( 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]
    [Google Scholar]
  8. Cubero, O. F., Bridge, P. D. & Crespo, A. ( 2000; ). Terminal-sequence conservation identifies spliceosomal introns in ascomycete 18S rRNA genes. Mol Biol Evol 17, 751–756.[CrossRef]
    [Google Scholar]
  9. Dávila-Aponte, J. A., Huss, V. A. R., Sogin, M. L. & Cech, T. R. ( 1991; ). A self-splicing group I intron in the nuclear pre-rRNA of the green alga, Ankistrodesmus stipitatus. Nucleic Acids Res 19, 4429–4436.[CrossRef]
    [Google Scholar]
  10. Dewhirst, F. E., Shen, Z., Scimeca, M. S., Stokes, L. N., Boumenna, T., Chen, T., Paster, B. J. & Fox, J. G. ( 2005; ). Discordant 16S and 23S rRNA gene phylogenies for the genus Helicobacter: implications for phylogenetic inference and systematics. J Bacteriol 187, 6106–6118.[CrossRef]
    [Google Scholar]
  11. Farris, J. S., Källersjö, M., Kluge, A. G. & Bult, C. ( 1994; ). Testing significance of incongruence. Cladistics 10, 315–319.[CrossRef]
    [Google Scholar]
  12. Felsenstein, J. ( 1985; ). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.[CrossRef]
    [Google Scholar]
  13. Felsenstein, J. ( 1988; ). Phylogenies from molecular sequences: inference and reliability. Annu Rev Genet 22, 521–565.[CrossRef]
    [Google Scholar]
  14. Gogarten, J. P., Doolittle, W. F. & Lawrence, J. G. ( 2002; ). Prokaryotic evolution in light of gene transfer. Mol Biol Evol 19, 2226–2238.[CrossRef]
    [Google Scholar]
  15. Gunderson, J. H., Sogin, M. L., Wollett, G., Hollingdale, M., De La Cruz, V. F., Waters, A. P. & McCutchan, T. F. ( 1987; ). Structurally distinct, stage-specific ribosomes occur in Plasmodium. Science 238, 933–937.[CrossRef]
    [Google Scholar]
  16. Hillis, D. M., Moritz, C., Porter, C. A. & Baker, R. J. ( 1991; ). Evidence for biased gene conservation in concerted evolution of ribosomal DNA. Science 251, 308–310.[CrossRef]
    [Google Scholar]
  17. Huelsenbeck, J. P. & Ronquist, F. ( 2001; ). mrbayes: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.[CrossRef]
    [Google Scholar]
  18. Jackson, S. A., Cannone, J. J., Lee, J. C., Gutell, R. R. & Woodson, S. A. ( 2002; ). Distribution of rRNA introns in the three-dimensional structure of the ribosome. J Mol Biol 323, 35–52.[CrossRef]
    [Google Scholar]
  19. Jain, R., Rivera, M. C. & Lake, J. A. ( 1999; ). Horizontal gene transfer among genomes: the complexity hypothesis. Proc Natl Acad Sci U S A 96, 3801–3806.[CrossRef]
    [Google Scholar]
  20. Jeeninga, R. E., Van Delft, Y., de Graaff-Vincent, M., Dirks-Mulder, A., Venema, J. & Raue, H. A. ( 1997; ). Variable regions V13 and V3 of Saccharomyces cerevisiae contain structural features essential for normal biogenesis and stability of 5.8S and 25S rRNA. RNA 3, 476–488.
    [Google Scholar]
  21. King, T. C., Sirdeskmukh, R. & Schlessinger, D. ( 1986; ). Nucleolytic processing of ribonucleic acid transcripts in prokaryotes. Microbiol Rev 50, 428–451.
    [Google Scholar]
  22. Krieger, J. & Fuerst, P. A. ( 2002; ). Evidence of multiple alleles of the nuclear 18S ribosomal RNA gene in sturgeon (Family: Acipenseridae). J Appl Ichthyol 18, 290–297.[CrossRef]
    [Google Scholar]
  23. Krieger, J. & Fuerst, P. A. ( 2004; ). Characterization of nuclear 18S rRNA gene sequence diversity and expression in an individual lake sturgeon (Acipenser fulvescens). J Appl Ichthyol 20, 433–439.[CrossRef]
    [Google Scholar]
  24. Krieger, J., Hett, A. K., Fuerst, P. A., Birstein, V. J. & Ludwig, A. ( 2006; ). Unusual intraindividual variation of the nuclear 18S rRNA gene is widespread within the Acipenseridae. J Hered 97, 218–225.[CrossRef]
    [Google Scholar]
  25. Long, E. O. & Dawid, I. B. ( 1980; ). Repeated genes in eukaryotes. Annu Rev Biochem 49, 727–764.[CrossRef]
    [Google Scholar]
  26. Marin, B., Palm, A., Klingberg, M. & Melkonian, M. ( 2003; ). Phylogeny and taxonomic revision of plastid-containing euglenophytes based on SSU rDNA sequence comparisons and synapomorphic signatures in the SSU rRNA secondary structure. Protist 154, 99–145.[CrossRef]
    [Google Scholar]
  27. Mashkova, T. D., Serenkova, T. L., Mazo, A. M., Avdonina, T. A., Timofeyeva, Y. & Kisselev, L. L. ( 1981; ). The primary structure of oocyte and somatic 5S rRNAs from the loach Misgurnus fossilis. Nucleic Acids Res 9, 2141–2151.[CrossRef]
    [Google Scholar]
  28. McVean, G., Awadalla, P. & Fearnhead, P. ( 2002; ). A coalescent-based method for detecting and estimating recombination rates from gene sequences. Genetics 160, 1231–1241.
    [Google Scholar]
  29. McVean, G. A. T., Myers, S., Hunt, S., Deloukas, P., Bentley, D. & Donnelly, P. ( 2004; ). The fine-scale structure of recombination rate variation in the human genome. Science 304, 581–584.[CrossRef]
    [Google Scholar]
  30. Miller, S. R., Augustine, S., Olson, T. L., Blankenship, R. E., Selker, J. & Wood, A. M. ( 2005; ). Discovery of a free-living chlorophyll d-producing cyanobacterium with a hybrid proteobacterial/cyanobacterial small-subunit rRNA gene. Proc Natl Acad Sci U S A 102, 850–855.[CrossRef]
    [Google Scholar]
  31. Mylvaganam, S. & Dennis, P. P. ( 1992; ). Sequence heterogeneity between the two genes encoding 16S rRNA from the halophilic archaebacterium Haloarcula marismortui. Genetics 130, 399–410.
    [Google Scholar]
  32. Nomura, M., Traub, P. & Bechmann, H. ( 1968; ). Hybrid 30S ribosomal particles reconstituted from components of different bacterial origins. Nature 219, 793–799.
    [Google Scholar]
  33. Pore, R. S. ( 1998; ). Prototheca, a yeastlike alga. In The Yeasts, a Taxonomic Study, pp. 881–887. Edited by C. P. Kurtzman & J. W. Fell. Amsterdam: Elsevier.
  34. Shimodaira, H. & Hasegawa, M. ( 1999; ). Multiple comparisons of log-likelihoods with application to phylogenetic inference. Mol Biol Evol 16, 1114–1116.[CrossRef]
    [Google Scholar]
  35. Sweeney, R., Chen, L. & Yao, M. C. ( 1994; ). An rRNA variable region has an evolutionarily conserved essential role despite sequence divergence. Mol Cell Biol 14, 4203–4215.
    [Google Scholar]
  36. Sweeney, R., Fan, Q. & Yao, M. C. ( 1996; ). Antisense ribosomes: rRNA as a vehicle for antisense RNAs. Proc Natl Acad Sci U S A 93, 8518–8523.[CrossRef]
    [Google Scholar]
  37. Swofford, D. L. ( 2002; ). paup* - Phylogenetic Analysis Using Parsimony (*and other methods), version 4.0b10. Sunderland, MA: Sinauer Associates.
  38. Ueda, K., Seki, T., Kudo, T., Yoshida, T. & Kataoka, M. ( 1999; ). Two distinct mechanisms cause heterogeneity of 16S rRNA. J Bacteriol 181, 78–82.
    [Google Scholar]
  39. Ueno, R., Hanagata, N., Urano, N. & Suzuki, M. ( 2005; ). Molecular phylogeny and phenotypic variation in the heterotrophic green algal genus Prototheca (Trebouxiophyceae, Chlorophyta). J Phycol 41, 1268–1280.[CrossRef]
    [Google Scholar]
  40. Wang, Y. & Zhang, Z. ( 2000; ). Comparative sequence analyses reveal frequent occurrence of short segments containing an abnormally high number of non-random base variations in bacterial rRNA genes. Microbiology 146, 2845–2854.
    [Google Scholar]
  41. Wang, Y., Zhang, Z. & Ramanan, N. ( 1997; ). The actinomycete Thermobispora bispora contains two distinct types of transcriptionally active 16S rRNA genes. J Bacteriol 179, 3270–3276.
    [Google Scholar]
  42. Wuyts, J., De Rijk, P., Van de Peer, Y., Pison, G., Rousseeuw, P. & De Wachter, R. ( 2000; ). Comparative analysis of more than 3000 sequences reveals the existence of two pseudoknots in area V4 of eukaryotic small subunit ribosomal RNA. Nucleic Acids Res 28, 4698–4708.[CrossRef]
    [Google Scholar]
  43. Yap, W. H., Zhang, Z. & 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 Bacteriol 181, 5201–5209.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2007/009365-0
Loading
/content/journal/micro/10.1099/mic.0.2007/009365-0
Loading

Data & Media loading...

Supplements

Supplementary figure legends [PDF file](9 KB)

PDF

Supplementary Fig. S1 [PDF file](25 KB)

PDF

Supplementary Fig. S2(a) [PDF file](441 KB)

PDF

Supplementary Fig. S2(b) [PDF file](417 KB)

PDF

Supplementary Fig. S2(c) [PDF file](426 KB)

PDF
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