1887

Abstract

In many prokaryotic species, 16S rRNA genes are present in multiple copies, and their sequences in general do not differ significantly owing to concerted evolution. At the time of writing, the genus of the family comprises nine species with validly published names, all of which possess two to four highly heterogeneous 16S rRNA genes. Existence of multiple heterogeneous 16S rRNA genes makes it difficult to reconstruct a biological phylogenetic tree using their sequence data. If the orthologous gene is able to be discriminated from paralogous genes, a tree reconstructed from orthologous genes will reflect a simple biological phylogenetic relationship. At present, however, we have no means to distinguish the orthologous rRNA operon from paralogous ones in the members of the family . In this study, we found that the dihydroorotate oxidase gene, , was present in the immediate upstream of one 16S rRNA gene in each of ten strains of the family whose genome sequences have been determined, and the direction of the gene was opposite to that of the 16S rRNA genes. In two other strains whose genome sequences have been determined, the gene was present in far separated positions. We designed PCR primer sets to amplify DNA fragments encompassing a region from the conserved region of the gene to a conserved region of the tRNA-Ala gene or the 23S rRNA gene to determine the 16S rRNA gene sequences preceded by the gene, and to see if the gene is conserved in the immediate upstream of rRNA operon(s) in the type strains of the type species of 28 genera of the family . Seventeen type strains, including the ten strains mentioned above, gave amplified DNA fragments of approximately 4000 bp, while eleven type strains, including the two strains mentioned above, did not give any PCR products. These eleven strains are members of the Clade I haloarchaea, originally defined by Walsh (2004) and expanded by Minegishi (2010). Analysis of contig sequences of three strains belonging to the Clade I haloarchaea also revealed the absence of the gene in the immediate upstream of any 16S rRNA genes. It may be scientifically sound to hypothesize that during the evolution of members of the family , a gene transposition event happened in one group and this was followed by subsequent speciation processes in each group, yielding species/genera of the Clade I group and ‘the rest’ of the present family .

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2012-01-01
2019-12-09
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References

  1. Anderson I. , Ulrich L. E. , Lupa B. , Susanti D. , Porat I. , Hooper S. D. , Lykidis A. , Sieprawska-Lupa M. , Dharmarajan L. . & other authors ( 2009; ). Genomic characterization of methanomicrobiales reveals three classes of methanogens. . PLoS ONE 4:, e5797. [CrossRef] [PubMed]
    [Google Scholar]
  2. 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. (Erratum: Genome Res 14, 2510). [CrossRef] [PubMed]
    [Google Scholar]
  3. Bapteste É. , Brochier C. , Boucher Y. . ( 2005; ). Higher-level classification of the Archaea: evolution of methanogenesis and methanogens. . Archaea 1:, 353–363. [CrossRef] [PubMed]
    [Google Scholar]
  4. Belda E. , Moya A. , Silva F. J. . ( 2005; ). Genome rearrangement distances and gene order phylogeny in γ-Proteobacteria . . Mol Biol Evol 22:, 1456–1467. [CrossRef] [PubMed]
    [Google Scholar]
  5. Bolhuis H. , Palm P. , Wende A. , Falb M. , Rampp M. , Rodriguez-Valera F. , Pfeiffer F. , Oesterhelt D. . ( 2006; ). The genome of the square archaeon Haloquadratum walsbyi: life at the limits of water activity. . BMC Genomics 7:, 169. [CrossRef] [PubMed]
    [Google Scholar]
  6. Boucher Y. , Douady C. J. , Sharma A. K. , Kamekura M. , Doolittle W. F. . ( 2004; ). Intragenomic heterogeneity and intergenomic recombination among haloarchaeal rRNA genes. . J Bacteriol 186:, 3980–3990. [CrossRef] [PubMed]
    [Google Scholar]
  7. Brochier C. , Forterre P. , Gribaldo S. . ( 2005; ). An emerging phylogenetic core of Archaea: phylogenies of transcription and translation machineries converge following addition of new genome sequences. . BMC Evol Biol 5:, 36. [CrossRef] [PubMed]
    [Google Scholar]
  8. Chartier F. , Laine B. , Belaïche D. , Touzel J. P. , Sautière P. . ( 1989; ). Primary structure of the chromosomal protein MC1 from the archaebacterium Methanosarcina sp. CHTI 55. . Biochim Biophys Acta 1008:, 309–314.[PubMed] [CrossRef]
    [Google Scholar]
  9. Cui H. L. , Zhou P. J. , Oren A. , Liu S. J. . ( 2009; ). Intraspecific polymorphism of 16S rRNA genes in two halophilic archaeal genera, Haloarcula and Halomicrobium . . Extremophiles 13:, 31–37. [CrossRef] [PubMed]
    [Google Scholar]
  10. Dennis P. P. , Ziesche S. , Mylvaganam S. . ( 1998; ). Transcription analysis of two disparate rRNA operons in the halophilic archaeon Haloarcula marismortui . . J Bacteriol 180:, 4804–4813.[PubMed]
    [Google Scholar]
  11. Eickbush T. H. , Eickbush D. G. . ( 2007; ). Finely orchestrated movements: evolution of the ribosomal RNA genes. . Genetics 175:, 477–485. [CrossRef] [PubMed]
    [Google Scholar]
  12. Enache M. , Itoh T. , Fukushima T. , Usami R. , Dumitru L. , Kamekura M. . ( 2007; ). Phylogenetic relationships within the family Halobacteriaceae inferred from rpoB′ gene and protein sequences. . Int J Syst Evol Microbiol 57:, 2289–2295. [CrossRef] [PubMed]
    [Google Scholar]
  13. Hartman A. L. , Norais C. , Badger J. H. , Delmas S. , Haldenby S. , Madupu R. , Robinson J. , Khouri H. , Ren Q. . & other authors ( 2010; ). The complete genome sequence of Haloferax volcanii DS2, a model archaeon. . PLoS ONE 5:, e9605. [CrossRef] [PubMed]
    [Google Scholar]
  14. Iino T. , Mori K. , Suzuki K. . ( 2010; ). Methanospirillum lacunae sp. nov., a methane-producing archaeon isolated from a puddly soil, and emended descriptions of the genus Methanospirillum and Methanospirillum hungatei . . Int J Syst Evol Microbiol 60:, 2563–2566. [CrossRef] [PubMed]
    [Google Scholar]
  15. Jacquet M. , Kalekine M. , Boy-Marcotte E. . ( 1985; ). Sequence analysis of a Dictyostelium discoideum gene coding for an active dihydroorotate dehydrogenase in yeast. . Biochimie 67:, 583–588. [CrossRef] [PubMed]
    [Google Scholar]
  16. Kanehisa M. , Goto S. . ( 2000; ). KEGG: Kyoto encyclopedia of genes and genomes. . Nucleic Acids Res 28:, 27–30. [CrossRef] [PubMed]
    [Google Scholar]
  17. Kanehisa M. , Goto S. , Hattori M. , Aoki-Kinoshita K. F. , Itoh M. , Kawashima S. , Katayama T. , Araki M. , Hirakawa M. . ( 2006; ). From genomics to chemical genomics: new developments in KEGG. . Nucleic Acids Res 34: (Database issue), D354–D357. [CrossRef] [PubMed]
    [Google Scholar]
  18. Koonin E. V. . ( 2005; ). Orthologs, paralogs, and evolutionary genomics. . Annu Rev Genet 39:, 309–338. [CrossRef] [PubMed]
    [Google Scholar]
  19. Laine B. , Culard F. , Maurizot J. C. , Sautière P. . ( 1991; ). The chromosomal protein MC1 from the archaebacterium Methanosarcina sp. CHTI 55 induces DNA bending and supercoiling. . Nucleic Acids Res 19:, 3041–3045. [CrossRef] [PubMed]
    [Google Scholar]
  20. Larsen J. N. , Jensen K. F. . ( 1985; ). Nucleotide sequence of the pyrD gene of Escherichia coli and characterization of the flavoprotein dihydroorotate dehydrogenase. . Eur J Biochem 151:, 59–65. [CrossRef] [PubMed]
    [Google Scholar]
  21. Liao D. . ( 2000; ). Gene conversion drives within genic sequences: concerted evolution of ribosomal RNA genes in bacteria and archaea. . J Mol Evol 51:, 305–317.[PubMed]
    [Google Scholar]
  22. Luo H. , Sun Z. , Arndt W. , Shi J. , Friedman R. , Tang J. . ( 2009; ). Gene order phylogeny and the evolution of methanogens. . PLoS ONE 4:, e6069. [CrossRef] [PubMed]
    [Google Scholar]
  23. Minegishi H. , Kamekura M. , Itoh T. , Echigo A. , Usami R. , Hashimoto T. . ( 2010; ). Further refinement of the phylogeny of the Halobacteriaceae based on the full-length RNA polymerase subunit B′ (rpoB′) gene. . Int J Syst Evol Microbiol 60:, 2398–2408. [CrossRef] [PubMed]
    [Google Scholar]
  24. 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.[PubMed]
    [Google Scholar]
  25. Nei M. , Rooney A. P. . ( 2005; ). Concerted and birth-and-death evolution of multigene families. . Annu Rev Genet 39:, 121–152. [CrossRef] [PubMed]
    [Google Scholar]
  26. Savage K. N. , Krumholz L. R. , Oren A. , Elshahed M. S. . ( 2007; ). Haladaptatus paucihalophilus gen. nov., sp. nov., a halophilic archaeon isolated from a low-salt, sulfide-rich spring. . Int J Syst Evol Microbiol 57:, 19–24. [CrossRef] [PubMed]
    [Google Scholar]
  27. Shimane Y. , Hatada Y. , Minegishi H. , Mizuki T. , Echigo A. , Miyazaki M. , Ohta Y. , Usami R. , Grant W. D. , Horikoshi K. . ( 2010; ). Natronoarchaeum mannanilyticum gen. nov., sp. nov., an aerobic, extremely halophilic archaeon isolated from commercial salt. . Int J Syst Evol Microbiol 60:, 2529–2534. [CrossRef] [PubMed]
    [Google Scholar]
  28. Vreeland R. H. , Straight S. , Krammes J. , Dougherty K. , Rosenzweig W. D. , Kamekura M. . ( 2002; ). Halosimplex carlsbadense gen. nov., sp. nov., a unique halophilic archaeon, with three 16S rRNA genes, that grows only in defined medium with glycerol and acetate or pyruvate. . Extremophiles 6:, 445–452. [CrossRef] [PubMed]
    [Google Scholar]
  29. Walsh D. A. , Bapteste E. , Kamekura M. , Doolittle W. F. . ( 2004; ). Evolution of the RNA polymerase B′ subunit gene (rpoB′) in Halobacteriales: a complementary molecular marker to the SSU rRNA gene. . Mol Biol Evol 21:, 2340–2351. [CrossRef] [PubMed]
    [Google Scholar]
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