1887

Abstract

The planctomycetes, order , are a distinct phylum of domain . Genes encoding the RNA portion of ribonuclease P (RNase P) of some planctomycete members were sequenced and compared with existing database planctomycete sequences. gene sequences encoding RNase P RNA were generated by a conserved primer PCR strategy for , , , strain ATCC 35122, , one other strain, and three other strains of the group. These sequences were aligned against reference bacterial sequences and secondary structures of corresponding RNase P RNAs deduced by a comparative approach. P12 helices were found to be highly variable in length, as were helices P16.1 and P19, when present. RNase P RNA secondary structures of isolates were found to have unusual features relative to other planctomycetes, including a long P9 helix and an insert in the P13 helix not found in any other member of domain . These unique features are consistent with other unusual properties of this genus, distinguishing it from other bacteria. Phylogenetic analyses indicate that relationships between planctomycetes derived from RNase P RNA are consistent with 16S rRNA-based analyses.

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2004-07-01
2020-01-18
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References

  1. Altman, S. ( 1975; ). Biosynthesis of transfer RNA in Escherichia coli. Cell 4, 21–29.[CrossRef]
    [Google Scholar]
  2. Altman, S., Baer, M. F., Bartkiewicz, M., Gold, H., Guerrier-Takada, C., Kirsebom, L. A., Lumelsky, N. & Peck, K. ( 1989; ). Catalysis by the RNA subunit of RNase P – a minireview. Gene 82, 63–64.[CrossRef]
    [Google Scholar]
  3. Brochier, C. & Philippe, H. ( 2002; ). Phylogeny: a non-hyperthermophilic ancestor for Bacteria. Nature 417, 244.[CrossRef]
    [Google Scholar]
  4. Brown, J. W. ( 1999; ). The ribonuclease P database. Nucleic Acids Res 27, 314.[CrossRef]
    [Google Scholar]
  5. Brown, J. W. & Pace, N. R. ( 1991; ). Structure and evolution of ribonuclease P RNA. Biochimie 73, 689–697.[CrossRef]
    [Google Scholar]
  6. Brown, J. W., Nolan, J. M., Haas, E. S., Rubio, M. A. T., Major, F. & Pace, N. R. ( 1996; ). Comparative analysis of ribonuclease P RNA using gene sequences from natural microbial populations reveals tertiary structural elements. Proc Natl Acad Sci U S A 93, 3001–3006.[CrossRef]
    [Google Scholar]
  7. Butler, M. K., Wang, J., Webb, R. I. & Fuerst, J. A. ( 2002; ). Molecular and ultrastructural confirmation of classification of ATCC 35122 as a strain of Pirellula staleyi. Int J Syst Evol Microbiol 52, 1663–1667.[CrossRef]
    [Google Scholar]
  8. Christian, E. L., Kaye, N. M. & Harris, M. E. ( 2000; ). Helix P4 is a divalent metal ion binding site in the conserved core of the ribonuclease P ribozyme. RNA 6, 511–519.[CrossRef]
    [Google Scholar]
  9. Condon, C. & Putzer, H. ( 2002; ). The phylogenetic distribution of bacterial ribonucleases. Nucleic Acids Res 30, 5339–5346.[CrossRef]
    [Google Scholar]
  10. Derakshani, M., Lukow, T. & Liesack, W. ( 2001; ). Novel bacterial lineages at the (sub)division level as detected by signature nucleotide-targeted recovery of 16S rRNA genes from bulk soil and rice roots of flooded rice microcosms. Appl Environ Microbiol 67, 623–631.[CrossRef]
    [Google Scholar]
  11. Deutscher, M. P. ( 1984; ). Processing of tRNA in prokaryotes and eukaryotes. CRC Crit Rev Biochem 17, 45–71.[CrossRef]
    [Google Scholar]
  12. Di Giulio, M. ( 2003; ). The ancestor of the Bacteria domain was a hyperthermophile. J Theor Biol 224, 277–283.[CrossRef]
    [Google Scholar]
  13. Embley, T. M., Hirt, R. P. & Williams, D. M. ( 1994; ). Biodiversity at the molecular level: the domains, kingdoms and phyla of life. Philos Trans R Soc London B Biol Sci 345, 21–33.[CrossRef]
    [Google Scholar]
  14. Felsenstein, J. ( 1989; ). phylip – phylogeny inference package (version 3.2). Cladistics 5, 164–166.
    [Google Scholar]
  15. Frank, D. N. & Pace, N. R. ( 1998; ). Ribonuclease P: unity and diversity in a tRNA processing ribozyme. Annu Rev Biochem 67, 153–180.[CrossRef]
    [Google Scholar]
  16. Franzmann, P. D. & Skerman, V. B. D. ( 1984; ). Gemmata obscuriglobus, a new genus and species of the budding bacteria. Antonie van Leeuwenhoek 50, 261–268.[CrossRef]
    [Google Scholar]
  17. Fuerst, J. A. ( 1995; ). The planctomycetes: emerging models for microbial ecology, evolution and cell biology. Microbiology 141, 1493–1506.[CrossRef]
    [Google Scholar]
  18. Fuerst, J. A. & Webb, R. I. ( 1991; ). Membrane-bounded nucleoid in the eubacterium Gemmata obscuriglobus. Proc Natl Acad Sci U S A 88, 8184–8188.[CrossRef]
    [Google Scholar]
  19. Garrity, G. M., Winters, M. & Searles, D. B. ( 2001; ). Taxonomic outline of the procaryotic genera. In Bergey's Manual of Systematic Bacteriology, release 1.0, April 2001. New York: Springer. http://dx.doi.org/10.1007/bergeysoutline
  20. Giovannoni, S. J., Schabtach, E. & Castenholz, R. W. ( 1987; ). Isosphaera pallida, gen. and comb. nov., a gliding, budding eubacterium from hot springs. Arch Microbiol 147, 276–284.[CrossRef]
    [Google Scholar]
  21. Glöckner, F. O., Kube, M., Bauer, M. & 11 other authors ( 2003; ). Complete genome sequence of the marine planctomycete Pirellula sp. strain 1. Proc Natl Acad Sci U S A 100, 8298–8303.[CrossRef]
    [Google Scholar]
  22. Green, C. J., Rivera-León, R. & Vold, B. S. ( 1996; ). The catalytic core of RNase P. Nucleic Acids Res 24, 1497–1503.[CrossRef]
    [Google Scholar]
  23. Guerrier-Takada, C., Gardiner, K., Marsh, T., Pace, N. & Altman, S. ( 1983; ). The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme. Cell 35, 849–857.[CrossRef]
    [Google Scholar]
  24. Haas, E. S. & Brown, J. W. ( 1998; ). Evolutionary variation in bacterial RNase P RNAs. Nucleic Acids Res 26, 4093–4099.[CrossRef]
    [Google Scholar]
  25. Haas, E. S., Brown, J. W., Pitulle, C. & Pace, N. R. ( 1994; ). Further perspective on the catalytic core and secondary structure of ribonuclease P RNA. Proc Natl Acad Sci U S A 91, 2527–2531.[CrossRef]
    [Google Scholar]
  26. Haas, E. S., Banta, A. B., Harris, J. K., Pace, N. R. & Brown, J. W. ( 1996; ). Structure and evolution of ribonuclease P RNA in Gram-positive bacteria. Nucleic Acids Res 24, 4775–4782.[CrossRef]
    [Google Scholar]
  27. Hancock, J. M. & Vogler, A. P. ( 2000; ). How slippage-derived sequences are incorporated into rRNA variable-region secondary structure: implications for phylogeny reconstruction. Mol Phylogenet Evol 14, 336–374.
    [Google Scholar]
  28. Harris, M. E., Kazantsev, A. V., Chen, J.-L. & Pace, N. R. ( 1997; ). Analysis of the tertiary structure of the ribonuclease P ribozyme-substrate complex by site-specific photoaffinity crosslinking. RNA 3, 561–576.
    [Google Scholar]
  29. Harris, J. K., Haas, E. S., Williams, D., Frank, D. N. & Brown, J. W. ( 2001; ). New insight into RNase P RNA structure from comparative analysis of the archaeal RNA. RNA 7, 220–232.[CrossRef]
    [Google Scholar]
  30. Herrmann, B., Pettersson, B., Everett, K. D. E., Mikkelsen, N. E. & Kirsebom, L. A. ( 2000; ). Characterization of the rnpB gene and RNase P RNA in the order Chlamydiales. Int J Syst Evol Microbiol 50, 149–158.[CrossRef]
    [Google Scholar]
  31. Hugenholtz, P., Goebel, B. M. & Pace, N. R. ( 1998; ). Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol 180, 4765–4774.
    [Google Scholar]
  32. Jeffares, D. C., Poole, A. M. & Penny, D. ( 1998; ). Relics from the RNA world. J Mol Evol 46, 18–36.[CrossRef]
    [Google Scholar]
  33. Kirsebom, L. A. & Svärd, S. G. ( 1994; ). Base pairing between Escherichia coli RNase P RNA and its substrate. EMBO J 13, 4870–4876.
    [Google Scholar]
  34. Kuypers, M. M. M., Sliekers, A. O., Lavik, G., Schmid, M., Jørgensen, B. B., Kuenen, J. G., Sinninghe Damsté, J. S., Strous, M. & Jetten, M. S. M. ( 2003; ). Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature 422, 608–611.[CrossRef]
    [Google Scholar]
  35. Liesack, W. & Stackebrandt, E. ( 1992; ). Occurrence of novel groups of the domain Bacteria as revealed by analysis of genetic material isolated from an Australian terrestrial environment. J Bacteriol 174, 5072–5078.
    [Google Scholar]
  36. Liesack, W., Söller, R., Stewart, T., Haas, H., Giovannoni, S. & Stackebrandt, E. ( 1992; ). The influence of tachytelically (rapidly) evolving sequences on the topology of phylogenetic trees – intrafamily relationships and the phylogenetic position of Planctomycetaceae as revealed by comparative analysis of 16S ribosomal RNA sequences. Syst Appl Microbiol 15, 357–362.[CrossRef]
    [Google Scholar]
  37. Lindsay, M. R., Webb, R. I. & Fuerst, J. A. ( 1997; ). Pirellulosomes: a new type of membrane-bounded cell compartment in planctomycete bacteria of the genus Pirellula. Microbiology 143, 739–748.[CrossRef]
    [Google Scholar]
  38. Lindsay, M. R., Webb, R. I., Strous, M., Jetten, M. S. M., Butler, M. K., Forde, R. J. & Fuerst, J. A. ( 2001; ). Cell compartmentalisation in planctomycetes: novel types of structural organisation for the bacterial cell. Arch Microbiol 175, 413–429.[CrossRef]
    [Google Scholar]
  39. Maeda, T., Furushita, M., Hamamura, K. & Shiba, T. ( 2001; ). Structures of ribonuclease P RNAs of Vibrio core species. FEMS Microbiol Lett 198, 141–146.[CrossRef]
    [Google Scholar]
  40. Massire, C., Jaeger, L. & Westhof, E. ( 1997; ). Phylogenetic evidence for a new tertiary interaction in bacterial RNase P RNAs. RNA 3, 553–556.
    [Google Scholar]
  41. Massire, C., Jaeger, L. & Westhof, E. ( 1998; ). Derivation of the three-dimensional architecture of bacterial ribonuclease P RNAs from comparative sequence analysis. J Mol Biol 279, 773–793.[CrossRef]
    [Google Scholar]
  42. Nicholas, K. B. & Nicholas, H. B., Jr ( 1997; ). GeneDoc: a tool for editing and annotating multiple sequence alignments. Distributed by the authors: http://www.psc.edu/biomed/genedoc
  43. Oh, B.-K. & Pace, N. R. ( 1994; ). Interaction of the 3′-end of tRNA with ribonuclease P RNA. Nucleic Acids Res 22, 4087–4094.[CrossRef]
    [Google Scholar]
  44. Pace, N. R. & Brown, J. W. ( 1995; ). Evolutionary perspective on the structure and function of ribonuclease P, a ribozyme. J Bacteriol 177, 1919–1928.
    [Google Scholar]
  45. Pitulle, C., Strehse, C., Brown, J. W. & Breitschwerdt, E. B. ( 2002; ). Investigation of the phylogenetic relationships within the genus Bartonella based on comparative sequence analysis of the rnpB gene, 16S rDNA and 23S rDNA. Int J Syst Evol Microbiol 52, 2075–2080.[CrossRef]
    [Google Scholar]
  46. Schlesner, H. ( 1994; ). The development of media suitable for the microorganisms morphologically resembling Planctomyces spp., Pirellula spp., and other Planctomycetales from various aquatic habitats using dilute media. Syst Appl Microbiol 17, 135–145.[CrossRef]
    [Google Scholar]
  47. Schlesner, H. & Stackebrandt, E. ( 1986; ). Assignment of the genera Planctomyces and Pirella to a new family Planctomycetaceae fam. nov. and description of the order Planctomycetales ord. nov. Syst Appl Microbiol 8, 174–176.[CrossRef]
    [Google Scholar]
  48. Schlesner, H., Rendsmann, C., Tindall, B. J., Gade, D., Rabus, R., Pfeiffer, S. & Hirsch, P. ( 2004; ). Taxonomic heterogeneity within the Planctomycetales as derived by DNA–DNA hybridization, description of Rhodopirellula baltica gen. nov., sp. nov., transfer of Pirellula marina to the genus Blastopirellula gen. nov. as Blastopirellula marina comb. nov., and emended description of the genus Pirellula. Int J Syst Evol Microbiol Papers in press, http://dx.doi.org/10.1099/ijs.0.63113-0
    [Google Scholar]
  49. Schmid, M., Twachtmann, U., Klein, M., Strous, M., Juretschko, S., Jetten, M., Metzger, J. W., Schleifer, K.-H. & Wagner, M. ( 2000; ). Molecular evidence for genus level diversity of bacteria capable of catalyzing anaerobic ammonium oxidation. Syst Appl Microbiol 23, 93–106.[CrossRef]
    [Google Scholar]
  50. Schön, A., Fingerhut, C. & Hess, W. R. ( 2002; ). Conserved and variable domains within divergent RNase P RNA gene sequences of Prochlorococcus strains. Int J Syst Evol Microbiol 52, 1383–1389.[CrossRef]
    [Google Scholar]
  51. Sinninghe Damsté, J. S., Strous, M., Rijpstra, W. I. C., Hopmans, E. C., Geenevasen, J. A. J., van Duin, A. C. T., van Niftrik, L. A. & Jetten, M. S. M. ( 2002; ). Linearly concatenated cyclobutane lipids form a dense bacterial membrane. Nature 419, 708–712.[CrossRef]
    [Google Scholar]
  52. Strous, M., Fuerst, J. A., Kramer, E. H. M., Logemann, S., Muyzer, G., van de Pas-Schoonen, K. T., Webb, R., Kuenen, J. G. & Jetten, M. S. M. ( 1999; ). Missing lithotroph identified as new planctomycete. Nature 400, 446–449.[CrossRef]
    [Google Scholar]
  53. Vergin, K. L., Urbach, E., Stein, J. L., DeLong, E. F., Lanoil, B. D. & Giovannoni, S. J. ( 1998; ). Screening of a fosmid library of marine environmental genomic DNA fragments reveals four clones related to members of the order Planctomycetales. Appl Environ Microbiol 64, 3075–3078.
    [Google Scholar]
  54. Vioque, A. ( 1997; ). The RNase P RNA from cyanobacteria: short tandemly repeated repetitive (STRR) sequences are present within the RNase P RNA gene in heterocyst-forming cyanobacteria. Nucleic Acids Res 25, 3471–3477.[CrossRef]
    [Google Scholar]
  55. Walter, A. E., Turner, D. H., Kim, J., Lyttle, M. H., Müller, P., Matthews, D. H. & Zuker, M. ( 1994; ). Coaxial stacking of helixes enhances binding of oligoribonucleotides and improves predictions of RNA folding. Proc Natl Acad Sci U S A 91, 9218–9222.[CrossRef]
    [Google Scholar]
  56. Wang, J., Jenkins, C., Webb, R. I. & Fuerst, J. A. ( 2002; ). Isolation of Gemmata-like and Isosphaera-like planctomycete bacteria from soil and freshwater. Appl Environ Microbiol 68, 417–422.[CrossRef]
    [Google Scholar]
  57. Woese, C. R., Stackebrandt, E., Macke, T. J. & Fox, G. E. ( 1985; ). A phylogenetic definition of the major eubacterial taxa. Syst Appl Microbiol 6, 143–151.[CrossRef]
    [Google Scholar]
  58. Yoon, J.-H. & Park, Y.-H. ( 2000; ). Comparative sequence analyses of the ribonuclease P (RNase P) RNA genes from ll-2,6-diaminopimelic acid-containing actinomycetes. Int J Syst Evol Microbiol 50, 2021–2029.[CrossRef]
    [Google Scholar]
  59. Zahler, N. H., Christian, E. L. & Harris, M. E. ( 2003; ). Recognition of the 5′ leader of pre-tRNA substrates by the active site of ribonuclease P. RNA 9, 734–745.[CrossRef]
    [Google Scholar]
  60. Zuker, M. ( 2003; ). Mfold web server for nucleic acid folding and hybridisation prediction. Nucleic Acids Res 31, 3406–3415.[CrossRef]
    [Google Scholar]
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