Skip to main content
SpringerLink
Log in

Spectinomycin operon ofMicrococcus luteus: Evolutionary implications of organization and novel codon usage

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Summary

The complete DNA sequence of theMicrococcus luteus spectinomycin (spc) operon and its adjacent regions has been determined. The sequence has revealed the presence of genes that are homologous to those of theEscherichia coli ribosomal and related proteins, L14, L24, L5, S8, L6, L18, S5, L30, L15, and secretion protein Y (secY), and the gene for adenylate kinase (adk). The gene arrangement in the spc operon is essentially the same as that ofE. coli except for the absence in theM. luteus spc operon of the genes for S14 and X protein that exist in theE. coli spc operon.SecY andadk seem to be composed of another operon (adk operon) with at least an open reading frame. The deduced amino acid sequences for these ribosomal proteins are well conserved among the two species (40–65% identity). Reflecting the high genomic guanine and cytosine (GC) content ofM. luteus (74%), the codon usage of the genes is extremely biased toward use of G and C, about 94% of the codon third positions being G or C. Seven codons, AUA, AAA, AGA, UUA, GUA, CUA, and CAA, all of which have A at the codon third positions, are completely absent in theM. luteus genes examined. Out of 11 genes in theM. luteus spc and adk operons, 5 (10) use GUG (UGA) and 6 (1) use AUG (UAA) as an initiation (termination) codon.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Andachi Y, Muto A, Yamao F, Osawa S (1987) Novel codonanticodon recognition patterns inMycoplasma capricolum. Proc Jpn Acad Ser (B) 63:353–356

    CAS  Google Scholar 

  • Arikan K, Kulkarni MS, Thomas DC, Sancar A (1986) Sequences of theE. coli uvrB gene and protein. Nucleic Acids Res 14:2637–2650

    Article  PubMed  CAS  Google Scholar 

  • Brune M, Schumann R, Wittinghofer F (1985) Cloning and sequencing of the adenylate kinase gene (adk) ofEscherichia coli. Nucleic Acids Res 13:7139–7151

    Article  PubMed  CAS  Google Scholar 

  • Cerretti DP, Dean D, Davis GR, Bedwell DM, Nomura M (1983) Thespc ribosomal protein operon ofEscherichia coli: sequence and cotranscription of the ribosomal protein genes and a protein export gene. Nucleic Acids Res 11:2599–2616

    Article  PubMed  CAS  Google Scholar 

  • Chen EY, Seeburg PH (1985) Supercoil sequencing: a fast and simple method for sequencing plasmid DNA. DNA 4:165–170

    PubMed  CAS  Google Scholar 

  • Godson HP, Soll D, Khorana HG (1973) A simple method of preparing large amounts ofox 174 RSI supercoiled DNA. Biochim Biophys Acta 299:516–520

    PubMed  CAS  Google Scholar 

  • Hara-Yokoyama M, Yokoyama S, Watanabe T, Watanabe K, Kitazume Y, Miyazawa T (1986) Characteristic anticodon sequences of major tRNA species from an extreme thermophile,Thermus thermophilus HB8. FEBS Lett 202:149–152

    Article  CAS  Google Scholar 

  • Holmes DS, Quigley M (1981) A rapid boiling method for the preparation of bacterial plasmids. Anal Biochem 114:193–197

    Article  PubMed  CAS  Google Scholar 

  • Hori H, Osawa S (1986) Evolutionary change in 5S rRNA secondary structure and phylogenic tre of 352 5S rRNA species. BioSystems 19:163–172

    Article  PubMed  CAS  Google Scholar 

  • Husain I, Houten B, Thomas DC, Sancar A (1986) Sequences ofEscherichia coli uvrA gene and protein reveal two potential ATP binding sites. J Biol Chem 261:4895–4901

    PubMed  CAS  Google Scholar 

  • Ikemura T (1981) The correlation between the abundance ofEscherichia coli tRNA and the occurrence of the respective codons in its protein genes. J Mol Biol 146:1–21

    Article  PubMed  CAS  Google Scholar 

  • Jukes TH, Bhushan V (1986) Silent nucleotide substitutions and G+C content of some mitochondrial and bacterial genes. J Mol Evol 24:39–44

    Article  PubMed  CAS  Google Scholar 

  • Kloos WE (1969) Factors affecting transformation ofMicrococcus lysodeikticus. J Bacteriol 98:1397–1399

    PubMed  CAS  Google Scholar 

  • Korneluk RG, Quan F, Gravel RA (1985) Rapid and reliable sequencing of double-stranded DNA. Gene 40:317–323

    Article  PubMed  CAS  Google Scholar 

  • Lindahl L, Zengel JM (1986) Ribosomal genes inEscherichia coli. Annu Rev Genet 20:297–326

    Article  PubMed  CAS  Google Scholar 

  • Mizusawa S, Nishimura S, Seela F (1986) Improvement of the dideoxy chain termination method of DNA sequencing by uses of deoxy-7-deazaguanosine triphosphate in place of dGTP. Nucleic Acids Res 14:1319–1324

    Article  PubMed  CAS  Google Scholar 

  • Muramatsu T, Miyazawa T, Nishikawa K, Nemote F, Kuchino Y, Nishimura S, Yokoyama S (1988) A novel lysine-substituted nucleoside in the first position of the anticodon of minor isoleucine tRNA fromEscherichia coli. J Biol Chem 263:9261–9267

    PubMed  CAS  Google Scholar 

  • Muto A, Osawa S (1987) The guanine and cytosine content of genomic DNA and bacterial evolution. Proc Natl Acad Sci USA 84:166–169

    Article  PubMed  CAS  Google Scholar 

  • Muto A, Yamao Y, Osawa S (1987) The genome ofMycoplasma capricolum. Prog Nucleic Acid Res Mol Biol 34:29–58

    Article  PubMed  CAS  Google Scholar 

  • Nomura M, Gours R, Baughman G (1984) Regulation of the synthesis of ribosomes and ribosomal components. Annu Rev Biochem 53:75–118

    Article  PubMed  CAS  Google Scholar 

  • Ohama T, Yamao F, Muto A, Osawa S (1987) Organization and codon usage of the streptomycin operon inMicrococcus luteus, a bacterium with a high genomic G+C content. J Bacteriol 169:4770–4777

    PubMed  CAS  Google Scholar 

  • Ohkubo S, Muto A, Kawauchi Y, Yamao F, Osawa S (1987) The ribosomal protein gene cluster ofMycoplasma capricolum. Mol Gen Genet 210:314–322

    Article  PubMed  CAS  Google Scholar 

  • Osawa S, Jukes TH, Muto A, Yamao F, Ohama T, Andachi Y (1987) Role of directional mutation pressure in the evolution of the eubacterial genetic code. Cold Spring Harbor Symp Quant Biol 52:777–789

    PubMed  CAS  Google Scholar 

  • Osawa S, Ohama T, Yamao F, Muto A, Jukes TH, Ozeki H, Umesono K (1988) Directional mutation pressure and transfer RNA in choice of the third nucleotide of synonymous two-codon sets. Proc Natl Acad Sci USA 85:1124–1128

    Article  PubMed  CAS  Google Scholar 

  • Piggot PT, Hoch JA (1985) Revised genetic linkage map ofBacillus subtilis. Microbiol Rev 49:158–179

    PubMed  CAS  Google Scholar 

  • Post LE, Nomura M (1980) DNA sequence from thestr operon ofEscherichia coli. J Biol Chem 255:4660–4666

    PubMed  CAS  Google Scholar 

  • Putney SD, Benkovic SJ, Schimmel PR (1981) A DNA fragment with an alpha-phosphorothioate nucleotide at one end is asymmetrically blocked from digestion by exonuclease III and can be replicatedin vivo. Proc Natl Acad Sci USA 78:7350–7354

    Article  PubMed  CAS  Google Scholar 

  • Sancar A, Clarke ND, Griswold J, Kennedy WJ, Rupp WD (1981) Identification of theuvrB gene product. J Mol Biol 148:63–76

    Article  PubMed  CAS  Google Scholar 

  • Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467

    Article  PubMed  CAS  Google Scholar 

  • Shiba K, Ito K, Yura T, Cerretti DP (1984) A defined mutation in the protein export gene within thespc ribosomal operon ofEscherichia coli. EMBO J 3:631–635

    PubMed  CAS  Google Scholar 

  • Shiota S, Nakayama Y (1988) Evidence for aMicrococcus luteus gene homologous touvrB ofEscherichia coli. Mol Gen Genet 213:21–29

    Article  PubMed  CAS  Google Scholar 

  • Shultz J, Silhavy TJ, Berman ML, Fiil N, Emr SD (1982) A previously unidentified gene in thespc operon ofEscherichia coli K12 specifies a component of the protein export machinery. Cell 31:227–235

    Article  PubMed  CAS  Google Scholar 

  • Sueoka N (1961) Correlation between base composition of deoxyribonucleic acid and amino acid composition of protein. Proc Natl Acad Sci USA 47:1141–1149

    Article  PubMed  CAS  Google Scholar 

  • Sueoka N (1962) On the genetic basis of variation and heterogeneity of DNA base composition. Proc Natl Acad Sci USA 48:582–592

    Article  PubMed  CAS  Google Scholar 

  • Sueoka N (1988) directional mutation pressure and neutral molecular evolution. Proc Natl Acad Sci USA 85:2653–2657

    Article  PubMed  CAS  Google Scholar 

  • Yamao F, Muto A, Kawauchi Y, Iwami M, Iwagami S, Azumi Y, Osawa S (1985) UGA is read as tryptophan inMycoplasma capricolum. Proc Natl Acad Sci USA 82:2306–2309

    Article  PubMed  CAS  Google Scholar 

  • Yanish-Perron C, Vieira J, Messing J (1985) Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. DNA 4:165–170

    Article  Google Scholar 

  • Yanofsky C (1981) Attenuation in the control of expression of bacterial operons. Nature 289:751–758

    Article  PubMed  CAS  Google Scholar 

  • Yokota T, Sugisaki M, Takanami M, Kaziro K (1980) The nucleotide sequence of the clonedtufA gene ofEscherichia coli. Gene 12:25–31

    Article  PubMed  CAS  Google Scholar 

  • Yokoyama S, Watanabe T, Murano K, Ishikura H, Yamaizumi Z, Nishimura S, Miyazawa T (1985) Molecular mechanism of codon recognition by tRNA species with modified uridine in the first position of the anticodon. Proc Natl Acad Sci USA 82:4905–4909

    Article  PubMed  CAS  Google Scholar 

  • Zengel JM, Arch RH, Lindahl L (1984) The nucleotide sequence ofEscherichia coli fus gene, coding for elongation factor G. Nucleic Acids Res 12:2181–2191

    Article  PubMed  CAS  Google Scholar 

  • Zurawski G, Zurawski SM (1985) Studies of theEscherichia coli S10 ribosomal protein operon. Nucleic Acids Res 13:4521–4526

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory of Molecular Genetics, Department of Biology, Faculty of Science, Nagoya University, Chikusa-ku, 464, Nagoya, Japan

    Takeshi Ohama, Akira Muto & Syozo Osawa

Authors
  1. Takeshi Ohama
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Akira Muto
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Syozo Osawa
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ohama, T., Muto, A. & Osawa, S. Spectinomycin operon ofMicrococcus luteus: Evolutionary implications of organization and novel codon usage. J Mol Evol 29, 381–395 (1989). https://doi.org/10.1007/BF02602908

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02602908

Key words

Search

Navigation