1887

Abstract

SUMMARY: Rhizopine (~-3-O-methyl-scy//o-inosamine) is a symbiosis-specif ic compound found in alfalfa nodules induced by specific Sinorhilobium meliloti strains. It has been postulated that rhizobial strains able to synthesize and catabolize rhizopine gain a competitive advantage in the rhizosphere. The pathway of rhizopine degradation is analysed here. Since rhizopine is an inositol derivative, it was tested whether inositol catabolism is involved in rhizopine utilization. A genetic locus required for the catabolism of inositol as sole carbon source was cloned from S. meliloti. This locus was delimited by transposon Tn5 mutagenesis and its DNA sequence was determined. Based on DNA similarity studies and enzyme assays, this genetic region was shown to encode an S, meliloti myo-inositol dehydrogenase. Strains that harboured a mutation in the myo-inositol dehydrogenase gene (idhA) did not display myo-inositol dehydrogenase activity, were unable to utilize myo-inositol as sole carbodenergy source, and were unable to catabolize rhizopine. Thus, myo-inositol dehydrogenase activity is essential for rhizopine utilization in s. meliloti.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-144-10-2915
1998-10-01
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/micro/144/10/mic-144-10-2915.html?itemId=/content/journal/micro/10.1099/00221287-144-10-2915&mimeType=html&fmt=ahah

References

  1. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.i. 1990; Basic local alignment search tool.. J Mol Biol 215:403–410
    [Google Scholar]
  2. Anderson W.A., Magasanik B. 1971a; The pathway of myoinositol degradation in Aerobacter aerogenes - identification of the intermediate 2-deoxy-5-keto-D-gluconic acid.. J Biol Chem 246:5653–5661
    [Google Scholar]
  3. Anderson W.A., Magasanik B. 1971b; The pathway of myoinositol degradation in Aerobacter aerogenes - conversion of 2- deoxy-5-keto-d-gluconic acid to glycolytic intermediates.. J Biol Chem 246:5662–5675
    [Google Scholar]
  4. Ausubel F.M., Brent R., Kingston R.E., Moore D.D., Seidman J.G., Smith J.A., Struhl K. 1992 Short Protocols in Molecular Biology New York: Wiley;
    [Google Scholar]
  5. Beringer J.E. 1974; R factor transfer in Rhizobium leguminosarum. . J Gen Microbiol 84:188–198
    [Google Scholar]
  6. Berman T., Magasanik B. 1966a; The pathway of myoinositol degradation in Aerobacter aerogenes - dehydrogenation and dehydration.. J Biol Chem 241:800–806
    [Google Scholar]
  7. Berman T., Magasanik B. 1966b; The pathway of myoinositol degradation in Aerobacter aerogenes - ring scission.. J Biol Chem 241:807–812
    [Google Scholar]
  8. Bosworth A.H., Williams M.K., Albrecht K.A. 7 other authors 1994; Alfalfa yield response to inoculation with recombinant strains of Rhizobium meliloti with an extra copy of dctABC and/or modified ttifA expression.. Appl Environ Microbiol 60:3815–3832
    [Google Scholar]
  9. de Bruijn F.J., Rossbach S. 1994; Transposon mutagenesis.. In Methods for General and Molecular Bacteriology pp. 387–405 Edited by Gerhardt P., Murray R. G. E., Wood W. A., Krieg N. R. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  10. de Bruijn F.J., Rossbach S., Schneider M., Ratet P., Messmer S., Szeto W., Ausubel F.M., Schell J. 1989; Rhizobium meliloti 1021 has three differentially regulated loci involved in glutamine biosynthesis, none of which is essential for symbiotic nitrogen fixation.. J Bacteriol 171:1673–1682
    [Google Scholar]
  11. Ditta G., Stanfield S., Corbin D., Helinski D.R. 1980; Broad host range DNA cloning system for Gram-negative bacteria: construction of a gene bank of Rhizobium meliloti. . Proc Natl Acad Sci USA 77:7347–7351
    [Google Scholar]
  12. Egelhoff T.T., Long S.R. 1985; Rhizobium meliloti nodulation genes: identification of nodDABC gene products, purification of nodA protein and expression of nodA in Rhizobium meliloti. . J Bacteriol 164:591–599
    [Google Scholar]
  13. Friedman A.M., Long S.R., Brown S.E., Buikema W.J., Ausubel F.M. 1982; Construction of a broad host range cloning vector and its use in the genetic analysis of Rhizobium mutants.. Gene 18:289–296
    [Google Scholar]
  14. Fujita Y., Shindo K., Miwa Y., Yoshida K. 1991; Bacillus subtilis inositol dehydrogenase-encoding gene (idh): sequence and expression in Escherichia coli. . Gene 108:121–125
    [Google Scholar]
  15. Gordon D.M., Ryder M.H., Heinrich K.H., Murphy P.J. 1996; An experimental test of the rhizopine concept in Rhi-zobium meliloti. . Appl Environ Microbiol 62:3991–3996
    [Google Scholar]
  16. Holt J.G. 1993 Bergey’s Manual of Determinative Bacteriology Baltimore, MD: Williams & Wilkins;
    [Google Scholar]
  17. Kiss G.B., Vincze E., Kalman Z., Forrai T., Kondorosi A. 1979; Genetic and biochemical analysis of mutants affected in nitrate reduction in Rhizobium meliloti. . J Gen Microbiol 113:105–118
    [Google Scholar]
  18. Kowalski M. 1970; Transducing phages of Rhizobium meliloti. . Acta Microbiol Pol Ser A 19:109–114
    [Google Scholar]
  19. Kunst F., Ogasawaka N., Mozer I. 148 others 1997; The complete genome sequence of the Gram-positive bacterium Bacillus subtilis. . Nature 390:249–256
    [Google Scholar]
  20. Loewus F.A. 1990; Structure and occurrence of inositols in plants.. In Inositol Metabolism in Plants pp. 1–11 Edited by Morre D. J., Boss W. F., Loewus F. A. New York: Wiley-Liss;
    [Google Scholar]
  21. Loewus F.A., Everard J.D., Young K.A. 1990; Inositol metabolism: precursor role and breakdown.. In Inositol Metab-olism in Plants pp. 21–45 Edited by Morre D. J., Boss W. F., Loewus F. A. New York: Wiley-Liss;
    [Google Scholar]
  22. Mansouri K., Piepersberg W. 1991; Genetics of streptomycin production in Streptomyces griseus: nucleotide sequence of five genes, strFGHIK, including a phosphatase gene.. Mol Gen Genet 228:459–469
    [Google Scholar]
  23. Meade H.M., Long S.R., Ruvkun G.B., Brown S.E., Ausubel F.M. 1982; Physical and genetic characterization of symbiotic and auxotrophic mutants of Rhizobium meliloti induced by transposon Tn5 mutagenesis.. J Bacteriol 149:114–122
    [Google Scholar]
  24. Miller J.H. 1992 A Short Course in Bacterial Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  25. Murphy P.J., Saint C.P. 1992; Rhizopines in the legume-Rhizobium symbiosis.. In Molecular Signals in Plant- Microbe Communication pp. 377–390 Edited by Verma D. P. S. Boca Raton, FL: CRC Press;
    [Google Scholar]
  26. Murphy P.J., Heycke N., Banfalvi Z., Tate M.E., de Bruijn F.J., Kondorosi A., Tempé J., Schell J. 1987; Genes for the catabolism and synthesis of an opine-like compound in Rhizobium meliloti are closely linked and on the Sym plasmid.. Proc Natl Acad Sci USA 84:493–497
    [Google Scholar]
  27. Murphy P.J., Heycke N., Trenz S.P., Ratet P., de Bruijn F.J., Schell J. 1988; Synthesis of an opine-like compound, a rhizopine, in alfalfa nodules is symbiotically regulated.. Proc Natl Acad Sci USA 85:9133–9137
    [Google Scholar]
  28. Murphy P.J., Trenz S.P., Grzemski W., de Bruijn F.J., Schell J. 1993; The Rhizobium meliloti rhizopine mos locus is a mosaic structure facilitating its symbiotic regulation.. J Bacteriol 175:5193–5204
    [Google Scholar]
  29. Poole P.S., Blyth A., Reid C.J., Walters K. 1994; myoinositol catabolism and catabolite regulation in Rhizobium leguminosarum bv. viciae.. Microbiology 140:2787–2795
    [Google Scholar]
  30. Ramaley R., Fujita Y., Freese E. 1979; Purification and properties of Bacillus subtilis inositol dehydrogenase.. J Biol Chem 254:7684–7690
    [Google Scholar]
  31. Rossbach S., Kulpa D.A., Rossbach U., de Bruijn F.J. 1994a; Molecular and genetic characterization of the rhizopine catabolism (mocABCR) genes of Rhizobium meliloti L5-30.. Mol Gen Genet 245:11–24
    [Google Scholar]
  32. Rossbach S., McSpadden B., Kulpa D., de Bruijn F.J. 1994b; Rhizopine synthesis and catabolism genes for the creation of ‘ biased rhizospheres ’ and a marker system to detect (genetically modified) microorganisms in the soil.. In Biotechnology Risk Assessment pp. 223–244 Edited by Levin M., Grim C., Angle J. S. College Park, MD: University of Maryland Biotechnology Institute;
    [Google Scholar]
  33. Rossbach S., McSpadden B., Ganoff M., de Bruijn F.J. 1995a; Rhizobium meliloti rhizopine catabolism genes: distribution, role in competition and potential as marker gene to track microbes.. In Biotechnology Risk Assessment pp. 180–188 Edited by Levin M., Grim C. , Angle J.S. College Park, MD: University of Maryland Biotechnology Institute;
    [Google Scholar]
  34. Rossbach S., Rasul G., Schneider M., Eardly B., de Bruijn F.J. 1995b; Structural and functional conservation of the rhizopine catabolism (moc) locus is limited to selected Rhizobium meliloti strains and unrelated to their geographical origin.. Mol Plant- Microbe Interact 8:549–559
    [Google Scholar]
  35. Sambrook J., Fritsch E.F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual, 2nd edn.. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  36. Scot L., Egsgaard H. 1984; Identification of ononitol and O- methyl-scyllo-inositol in pea nodules.. Planta 161:32–36
    [Google Scholar]
  37. Scupham A.J., Bosworth A.H., Ellis W.R., Wacek T.J., Albrecht K.A., Triplett E.W. 1996; Inoculation with Sinorhizobium meliloti RMBPC-2 increases alfalfa yield compared with inoculation with a nonengineered wild-type strain.. Appl Environ Microbiol 62:4260–4262
    [Google Scholar]
  38. Streeter J.G. 1987; Carbohydrate, organic acid, and amino acid composition of bacteroids and cytosol from soybean nodules.. Plant Physiol 85:768–773
    [Google Scholar]
  39. Tempe J., Petit A., Bannerot H. 1982; Presence de substances semblables a des opines dans des nodosites de luzerne.. C R Acad Sci Paris Ser III 295:413–426
    [Google Scholar]
  40. Thompson J., Donkersloot J.A. 1992; N-(carboxyalkyl) amino acids: occurrence, synthesis, and functions.. Annu Rev Biochem 61:517–557
    [Google Scholar]
  41. Wexler M., Gordon D.M., Murphy P.J. 1995; The distribution of inositol rhizopine genes in Rhizobium populations.. Soil Biol Biochem 27:531–537
    [Google Scholar]
  42. Williams M.K., Cannon F., McLean P., Beynon J. 1988; Vector for the integration of genes into a defined site in the Rhizobium meliloti genome.. In Molecular Genetics of Plant- Microbe Interactions pp. 198–199 Edited by Palacios R., Verma D. P. S. St Paul, MN: American Phytopathological Society;
    [Google Scholar]
  43. Yoshida K., Sano H., Miwa Y., Ogasawara N., Fujita Y. 1994; Cloning and nucleotide sequencing of a 15 kb region of the Bacillus subtilis genome containing the iol operon.. Microbiology 140:2289–2298
    [Google Scholar]
  44. Yoshida K.I., Aoyama D., Ishio I., Shibayama T., Fujita Y. 1997; Organization and transcription of the myo-inositol operon, iol, of Bacillus subtilis. . J Bacteriol 179:4591–4598
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-144-10-2915
Loading
/content/journal/micro/10.1099/00221287-144-10-2915
Loading

Data & Media loading...

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