1887

Abstract

-Inositol (SI) is a stereoisomer of inositol whose catabolism has not been characterized in bacteria. We found that 168 was able to grow using SI as its sole carbon source and that this growth was dependent on a functional operon for catabolism of -inositol (MI; another inositol isomer, which is abundant in nature). Previous studies elucidated the MI catabolic pathway in as comprising multiple stepwise reactions catalysed by a series of Iol enzymes. The first step of the pathway converts MI to -inosose (SIS) and involves the MI dehydrogenase IolG. Since IolG does not act on SI, we suspected that there could be another enzyme converting SI into SIS, namely an SI dehydrogenase. Within the whole genome, seven genes paralogous to have been identified and two of these, and (formerly known as and , respectively), were selected as candidate genes for the putative SI dehydrogenase since they were both prominently expressed when was grown on medium containing SI. and were cloned in and both were shown to encode a functional enzyme, revealing the two distinct SI dehydrogenases in . Since inactivation of impaired growth with SI as the carbon source, IolX was identified as a catabolic enzyme required for SI catabolism and it was shown to be NAD dependent. The physiological role of IolW remains unclear, but it may be capable of producing SI from SIS with NADPH oxidation.

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2010-05-01
2020-11-26
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References

  1. Berman T., Magasanik B. 1966; The pathway of myo-inositol degradation in Aerobacter aerogenes. J Biol Chem 241:800–806
    [Google Scholar]
  2. Candy D. J. 1967; Occurrence and metabolism of scyllo inositol in the locust. Biochem J 103:666–671
    [Google Scholar]
  3. Fujita Y., Freese E. 1981; Isolation and properties of a Bacillus subtilis mutant unable to produce fructose-bisphosphatase. J Bacteriol 145:760–767
    [Google Scholar]
  4. 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]
  5. Galbraith M. P., Feng S. F., Borneman J., Triplett E. W., de Bruijn F. J., Rossbach S. 1998; A functional myo-inositol catabolism pathway is essential for rhizopine utilization by Sinorhizobium meliloti. Microbiology 144:2915–2924
    [Google Scholar]
  6. Hipps P. P., Eveland M. R., Laird M. H., Sherman W. R. 1976; The identification of myo-inositol : NAD(P)+ oxidoreductase in mammalian brain. Biochem Biophys Res Commun 68:1133–1138
    [Google Scholar]
  7. Horner W. H., Thaker I. H. 1968; The metabolism of scyllo-inositol in Steptomyces griseus. Biochim Biophys Acta 165:306–308
    [Google Scholar]
  8. Ichimura K., Kohata K., Yamaguchi Y., Douzono M., Ikeda H., Koketsu M. 2000; Identification of l-inositol and scyllitol and their distribution in various organs in chrysanthemum. Biosci Biotechnol Biochem 64:865–868
    [Google Scholar]
  9. Inaoka T., Takahashi K., Yada H., Yoshida M., Ochi K. 2004; RNA polymerase mutation activates the production of a dormant antibiotic 3,3′-neotrehalosadiamine via an autoinduction mechanism in Bacillus subtilis. J Biol Chem 279:3885–3892
    [Google Scholar]
  10. Jiang G., Krishnan A. H., Kim Y. M., Wacek T. J., Krishnan H. B. 2001; A functional myo-inositol dehydrogenase gene is required for efficient nitrogen fixation and competitiveness of Sinorhizobium fredii USDA191 to nodulate soybean ( Glycine max [L.] Merr.). J Bacteriol 183:2595–2604
    [Google Scholar]
  11. Kaempfer R. O., Magasanik B. 1967; Effect of infection with T-even phage on the inducible synthesis of beta-galactosidase in Escherichia coli. J Mol Biol 27:453–468
    [Google Scholar]
  12. Kinnard R. L., Narasimhan B., Pliska-Matyshak G., Murthy P. P. 1995; Characterization of scyllo-inositol-containing phosphatidylinositol in plant cells. Biochem Biophys Res Commun 210:549–555
    [Google Scholar]
  13. Krings E., Krumbach K., Bathe B., Kelle R., Wendisch V. F., Sahm H., Eggeling L. 2006; Characterization of myo-inositol utilization by Corynebacterium glutamicum: the stimulon, identification of transporters, and influence on l-lysine formation. J Bacteriol 188:8054–8061
    [Google Scholar]
  14. McLaurin J., Golomb R., Jurewicz A., Antel J. P., Fraser P. E. 2000; Inositol stereoisomers stabilize an oligomeric aggregate of Alzheimer amyloid beta peptide and inhibit abeta-induced toxicity. J Biol Chem 275:18495–18502
    [Google Scholar]
  15. Morinaga T., Yamaguchi M., Makino Y., Nanamiya H., Takahashi K., Yoshikawa H., Kawamura F., Ashida H., Yoshida K. 2006; Functional myo-inositol catabolic genes of Bacillus subtilis Natto are involved in depletion of pinitol in natto (fermented soybean. Biosci Biotechnol Biochem 70:1913–1920
    [Google Scholar]
  16. Ogura M., Yamaguchi H., Yoshida K., Fujita Y., Tanaka T. 2001; DNA microarray analysis of Bacillus subtilis DegU, ComA and PhoP regulons: an approach to comprehensive analysis of B. subtilis two-component regulatory systems. Nucleic Acids Res 29:3804–3813
    [Google Scholar]
  17. Poole P. S., Blyth A., Reid C. J., Walters K. 1994; myo-Inositol catabolism and catabolite regulation in Rhizobium leguminosarum bv. viciae. Microbiology 140:2787–2795
    [Google Scholar]
  18. Ramaley R., Fujita Y., Freese E. 1979; Purification and properties of Bacillus subtilis inositol dehydrogenase. J Biol Chem 254:7684–7690
    [Google Scholar]
  19. Riggs B. M., Lansley T. A., Ryals P. E. 2007; Phosphatidylinositol synthase of Tetrahymena: inositol isomers as substrates in phosphatidylinositol biosynthesis and headgroup exchange reactions. J Eukaryot Microbiol 54:119–124
    [Google Scholar]
  20. Rosenberg N. K., Lee R. W., Yancey P. H. 2006; High contents of hypotaurine and thiotaurine in hydrothermal-vent gastropods without thiotrophic endosymbionts. J Exp Zool A Comp Exp Biol 305:655–662
    [Google Scholar]
  21. Sambrook J., Russell D. W. 2001 Molecular Cloning: a Laboratory Manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
  22. Sherman W. R., Stewart M. A., Simpson P. C., Goodwin S. L. 1968; The identification of myo-inosose-2 and scyllo-inositol in mammalian tissues. Biochemistry 7:819–824
    [Google Scholar]
  23. Stines-Chaumeil C., Talfournier F., Branlant G. 2006; Mechanistic characterization of the MSDH (methylmalonate semialdehyde dehydrogenase) from Bacillus subtilis. Biochem J 395:107–115
    [Google Scholar]
  24. Sun Y., Zhang G., Hawkes C. A., Shaw J. E., McLaurin J., Nitz M. 2008; Synthesis of scyllo-inositol derivatives and their effects on amyloid beta peptide aggregation. Bioorg Med Chem 16:7177–7184
    [Google Scholar]
  25. Townsend M., Cleary J. P., Mehta T., Hofmeister J., Lesne S., O'Hare E., Walsh D. M., Selkoe D. J. 2006; Orally available compound prevents deficits in memory caused by the Alzheimer amyloid-beta oligomers. Ann Neurol 60:668–676
    [Google Scholar]
  26. Vidal-Leiria M., van Uden N. 1973; Inositol dehydrogenase from the yeast Cryptococcus melibiosum. Biochim Biophys Acta 293:295–303
    [Google Scholar]
  27. Yebra M. J., Zuniga M., Beaufils S., Perez-Martinez G., Deutscher J., Monedero V. 2007; Identification of a gene cluster enabling Lactobacillus casei BL23 to utilize myo-inositol. Appl Environ Microbiol 73:3850–3858
    [Google Scholar]
  28. 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]
  29. Yoshida K. I., Shibayama T., Aoyama D., Fujita Y. 1999a; Interaction of a repressor and its binding sites for regulation of the Bacillus subtilis iol divergon. J Mol Biol 285:917–929
    [Google Scholar]
  30. Yoshida K., Fujita Y., Ehrlich S. D. 1999b; Three asparagine synthetase genes of Bacillus subtilis. J Bacteriol 181:6081–6091
    [Google Scholar]
  31. Yoshida K., Yamamoto Y., Omae K., Yamamoto M., Fujita Y. 2002; Identification of two myo-inositol transporter genes of Bacillus subtilis. J Bacteriol 184:983–991
    [Google Scholar]
  32. Yoshida K., Yamaguchi M., Ikeda H., Omae K., Tsurusaki K., Fujita Y. 2004; The fifth gene of the iol operon of Bacillus subtilis, iolE, encodes 2-keto- myo-inositol dehydratase. Microbiology 150:571–580
    [Google Scholar]
  33. Yoshida K., Yamaguchi M., Morinaga T., Ikeuchi M., Kinehara M., Ashida H. 2006; Genetic modification of Bacillus subtilis for production of d- chiro-inositol, an investigational drug candidate for treatment of type 2 diabetes and polycystic ovary syndrome. Appl Environ Microbiol 72:1310–1315
    [Google Scholar]
  34. Yoshida K., Yamaguchi M., Morinaga T., Kinehara M., Ikeuchi M., Ashida H., Fujita Y. 2008; myo-Inositol catabolism in Bacillus subtilis. J Biol Chem 283:10415–10424
    [Google Scholar]
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