1887

Abstract

Submerged cultures of four Streptomyces species accumulated triacylglycerol (TAG), ranging from 50 to 150 mg (I medium), during the post-exponential phase of growth. also produced glycogen (80 mg I). Identity of TAG species was confirmed after TLC, by mass spectroscopy and by quantitative IR spectroscopy and reaction of the hydroxamate derivatives with ferric chloride. This is the first substantive report showing the storage of TAG in bacteria. Distribution of diacylglycerol acyltransferase (TAG synthase) activity from and during incubation on different media paralleled the formation of TAG. Accumulation of TAG may be necessary to maintain cell integrity after glucose becomes exhausted from the medium, and also to provide the C units needed for subsequent biosynthesis of acetate-derived antibiotics in appropriate species. Actinorhodin was formed by when grown on YEME medium only after exhaustion of glucose; the carbon source may therefore originate from TAG. All the organisms examined in this study formed isoprenoid-derived hydrocarbons (up to 3 mg I) which were identified as squalene plus hydrogenated derivatives.

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1994-04-01
2024-04-20
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References

  1. Augustyn J.M., Elliott W.B. A modified hydroxamate assay of phospholipase A activity. Anal biochem 1969; 31:246–250
    [Google Scholar]
  2. Ballio A., Barcellona S., Boniforti L. The component fatty acids of lipids from some Streptomyces species. Biocbem J 1965; 94:11c–13c
    [Google Scholar]
  3. Bell R.M., Coleman R.A. Enzymes of triacylglycerol formation in mammals. In The Enumes 1983 Edited by Boyer P.D. London & New York: Academic Press; 16 pp 87–111
    [Google Scholar]
  4. Benyon J.H. Mass Spectrometry and its Applications to Organic Chemistry 1960 Edited by Amsterdam: Elsevier; pp 379–386
    [Google Scholar]
  5. Berdy J. Recent developments of antibiotic research and classification of antibiotics according to chemical structure. Adv Appl Microbiol 1974; 18:309–406
    [Google Scholar]
  6. Brafia A.F., Manzanal M.B., Hardisson C. Characterization of intracellular polysaccharides of Streptomyces. Can J Microbiol 1982; 28:1320–1323
    [Google Scholar]
  7. Brafia A.F., Méndez C., Diaz L.A., Manzanal M.B., Hardisson C. Glycogen and trehalose accumulation during colony development in Streptomyces antibioticus. J Gen Microbiol 1986; 132:1319–1326
    [Google Scholar]
  8. Bushell M.E. Growth, product formation and fermentation technology. In Actinomycetes in biotechnology 1988 Edited by Goodfellow M., Williams S.T., Mordarski M. London: Academic Press; pp 185–217
    [Google Scholar]
  9. Chater K.F., Merrick M.J. Streptomycetes. In Developmental biology of Prokaryotes 1979 Edited by Parish J.H. Berkeley & Los Angeles: University of California Press; pp 93–114
    [Google Scholar]
  10. Coleman R., Bell R.M. Triacylglycerol synthesis in isolated fat cells: studies on the microsomal diacylglycerol acyltransferase activity using ethanol dispersed diacylglycerols. J biol Chem 1976; 251:4537–4543
    [Google Scholar]
  11. Dawes E.A. Starvation, survival and energy reserves. In bacteria in their Natural Environments (SGM Special Publication no. 16) 1985 Edited by Fletcher M., Floodgate G.D. London: Academic Press; pp 43–79
    [Google Scholar]
  12. Dawes E.A., Senior P.J. The role and regulation of energy reserve polymers in microorganisms. Adv Microb Physiol 1973; 10:135–266
    [Google Scholar]
  13. Daza A., Martin J.F., Dominguez A., Gil J.A. Sporulation of several species of Streptomyces in submerged cultures after nutritional downshift. J Gen Microbiol 1989; 135:2483–2491
    [Google Scholar]
  14. Dubowski K.M. An o-toluidine method for body-fluid glucose determination. Clin Chem 1962; 8:215–235
    [Google Scholar]
  15. Folch J., Lees M., Sloane-Stanley G.H. A simple method for the isolation and purification of total lipid from animal tissues. J Biol Chem 1957; 226:497–509
    [Google Scholar]
  16. Goldfine H. Comparative aspects of bacterial lipids. Adv Microb Physiol 1972; 8:1–58
    [Google Scholar]
  17. Goldfine H. Lipids of prokaryotes structure and distribution. Curr Top Membr Transp 1982; 17:1–43
    [Google Scholar]
  18. Goldman P., Vagelos P.R. The specificity of triglyceride synthesis from diglycerides in chicken adipose tissue. J Biol Chem 1961; 236:2620–2623
    [Google Scholar]
  19. Hanahan D.J., Vercamer R. The action of lecithinase D on lecithin The enzymatic preparation of D-1,2-dipalmitolein and D-1,2-dipalmitin. J Am Chem Soc 1954; 76:1804–1806
    [Google Scholar]
  20. Harwood J.L., Russell N.J. Lipids in Plants and Microbes 1984 London: George Allen & Unwin.;
    [Google Scholar]
  21. Hobbs G., Frazer C.M., Gardner D.C.J., Flett F., Oliver S.G. Pigmented antibiotic production by Streptomyces coelicolor A3(2): kinetics and the influence of nutrients. J Gen Microbiol 1990; 136:2291–2296
    [Google Scholar]
  22. Holdsworth J.E., Ratledge C. Lipid turnover in oleaginous yeasts. J Gen Microbiol 1988; 134:339–346
    [Google Scholar]
  23. Hopwood D.A. Genetic analysis and genome structure in Streptomyces coelicolor. Bacteriol Rev 1967; 31:371–405
    [Google Scholar]
  24. Hopwood D.A., Khosla C. Genes for polyketide secondary metabolic pathways in microorganisms and plants. Ciba Symp 1992; 171:88–112
    [Google Scholar]
  25. Hopwood D.A., Bibb M.J., Chater K.F., Kieser T., Bruton C.J., Kieser H.M., Lydiate D.J., Smith C.P., Ward J.M., Schrempf H. Genetic Manipulation of Streptomyces 1985 A Laboratory Manual. Norwich: John Innes Foundation.;
    [Google Scholar]
  26. Horinouchi S., Beppu T. Production in large quantities of actinorhodin and undecylprodigiosin induced by afsB in Streptomyces lividans. Agric Biol Chem 1984; 48:2131–2133
    [Google Scholar]
  27. Jackson L.L., Biomqvist G.J. Insect waxes. In Chemistry and Biochemistry of Natural Waxes 1976 Edited by Kollatukudy P.E. Oxford & New York: Elsevier; pp 201–233
    [Google Scholar]
  28. Kannan L.V., Rehacek Z. Formation of poly-β-hydroxybutyrate by actinomycetes. Indian J Biochem 1970; 7:126–129
    [Google Scholar]
  29. Kates M. Bacterial lipids. Adv Lipid Res 1964; 2:17–84
    [Google Scholar]
  30. Kates M. Techniques of Lipidology: Isolation, Analysis and Identification of Lipids 1988 Amsterdam: Elsevier; pp 100–110
    [Google Scholar]
  31. Kollatukudy P.E. Cutin, suberin and waxes. In The Biochemistry of Plants 1980 Edited by Stumpf P.K. New York & London: Academic Press; 4 pp 571–645
    [Google Scholar]
  32. Law J.H., Slepecky R.A. Assay of polyhydroxybutyric acid. J Bacteriol 1961; 82:33–36
    [Google Scholar]
  33. Lennarz W.J. Lipid metabolism in the bacteria. Adv Lipid Res 1966; 4:175–225
    [Google Scholar]
  34. Marshall M.O., Knusden J. Factors influencing the in vitro activity of diacylglycerol acyltransferase from bovine mammary gland and liver towards butyryl-CoA and palmitoyl-CoA. Biochim Biophys Acta 1980; 617:393–397
    [Google Scholar]
  35. Martin J.F., Demain A.L. Control of antibiotic synthesis. Microbiol Rev 1980; 44:230–251
    [Google Scholar]
  36. Metcalfe L.D., Schmitz A.A. The rapid preparation of fatty acid methyl esters for gas chromatographic analysis. Anal Chem 1961; 33:363–364
    [Google Scholar]
  37. Murphy D.J., Hills M.J., Bowra S., Fairbairn D., Richards D., Ross J.H., Slocombe S.P., Taylor R.D., Whitfield H.V. Oilseed biochemistry and molecular biology: enzymes and genes of fatty acid modification and triacylgylcerol biosynthesis. In John Innes Institute Annual Report 1991 Norwich: John Innes Foundation; pp 9–11
    [Google Scholar]
  38. Okanishi M., Suzuki K., Umezawa H. Formation and reversion of Streptomycete protoplasts: cultural conditions and morphological study. J Gen Microbiol 1974; 80:389–400
    [Google Scholar]
  39. Olukoshi E.R., Packter N.M. Isolation of triacylglycerol synthase activity from Streptomyces lividans. Biochem Soc Trans 1992; 20:99S
    [Google Scholar]
  40. Packter N.M. Biosynthesis of acetate-derived phenols (polyketides). In The Biochemistry of Plants 1980 Edited by Stumpf P.K. New York & London: Academic Press; 4 pp 535–570
    [Google Scholar]
  41. Packter N.M., Collins J.S. Effect of inhibitors of protein synthesis on the formation of phenols derived from acetate and shikimic acid in Aspergillus fumigatus. Eur J Biochem 1974; 42:291–302
    [Google Scholar]
  42. Packter N.M., Flatman S., Lucock A.J. Formation of storage lipids and actinorhodin, a phenolic antibiotic in Streptomyces coelicolor. Biochem Soc Trans 1985; 13:251–252
    [Google Scholar]
  43. Paznokas J.L., Kaplan A. Purification and properties of a triacylglycerol lipase from Mycobacterium phlei. Biochim Biophys Acta 1977; 487:405–421
    [Google Scholar]
  44. Pieringer R.A. Formation of bacterial glycerolipids. In The Enzymes 1983 Edited by Boyer P.D. New York & London: Academic Press; 16 pp 255–306
    [Google Scholar]
  45. Pieringer R.A., Bonner H. Jr, Kunnes R.S. Biosynthesis of phosphatidic acid, diglyceride and triglyceride by fatty acyltransferase pathways in Escherichia coli. J Biol Chem 1967; 242:2719–2724
    [Google Scholar]
  46. Preiss J., Romeo T. Physiology, biochemistry and genetics of bacterial glycogen synthesis. Adv Microb Physiol 1989; 30:183–238
    [Google Scholar]
  47. Raetz C.R.H., Newman K.F. Diglyceride kinase mutants of Escherichia coli: inner membrane association of 1,2-diglyceride and its relation to synthesis of membrane-derived oligosaccharides. J Bacteriol 1979; 137:860–868
    [Google Scholar]
  48. Ratledge C. The physiology of the mycobacteria. Adv Microb Physiol 1976; 13:115–244
    [Google Scholar]
  49. Rudd B.A.M., Hopwood D.A. A pigmented mycelial antibiotic in Streptomyces coelicolor: control by a chromosomal gene cluster. J Gen Microbiol 1980; 119:333–340
    [Google Scholar]
  50. Ryhage R., Stenhagen E. Mass spectrometry of long-chain esters. In Mass Spectrometry of Organic Ions 1963 Edited by McLafferty F.W. New York: Academic Press; pp 399–452
    [Google Scholar]
  51. Sarzala M.G., Van Golde L.M.G., Dekruff B., Van Deenen L.L.M. The intramitochondrial distribution of some enzymes involved in the biosynthesis of rat liver phospholipids. Biochim Biophys Acta 1970; 202:106–119
    [Google Scholar]
  52. Shaw N. Lipid composition as a guide to the classification of bacteria. Adv Appl Microbiol 1974; 17:63–108
    [Google Scholar]
  53. Sigal N., Cattaneo J., Segel I.H. Glycogen accumulation by wild-type and uridine diphosphate glucose pyrophosphorylase-negative strains of Escherichia coli. Arch Biochem Biophys 1964; 108:440–451
    [Google Scholar]
  54. Tornabene T.G., Kates M., Gelpi E., Oro J. Occurrence of squalene, di-and tetrahydrosqualenes, and vitamin MK8 in an extremely halophilic bacterium, Halobacterium cutirubrum. J Lipid Res 1969; 10:294–303
    [Google Scholar]
  55. Van Golde L.M.G., Fleischer B., Fleischer S. Some studies on the metabolism of phospholipids in Golgi complex from bovine and rat liver in comparison to other subcellular fractions. Biochim Biophys Acta 1971; 249:318–330
    [Google Scholar]
  56. Verma J.N., Khuller G.K. Metabolism of neutral lipids and acvlated sugars in Streptomyces griseus. FEMS Microbiol Lett 1980; 9:73–75
    [Google Scholar]
  57. Verma J.N., Khuller G.K. Lipids of actinomycetes. Adv Lipid Res 1983; 20:257–307
    [Google Scholar]
  58. Vining L.C., Doull J.L. Catabolite repression of secondary metabolism in actinomycetes. In Biology of Actinomycetes 1988 Tokyo: Japan Scientific Press; pp 406–411
    [Google Scholar]
  59. Ward A.C., Packter N.M. Relationship between fatty acid and phenol synthesis in Aspergillus fumigatus. Eur J Biochem 1974; 46:323–333
    [Google Scholar]
  60. Weete J.D. Lipid Biochemistry of Fungi and Other Organisms 1980 New York & London: Plenum Press;
    [Google Scholar]
  61. Weiss S.B., Kennedy E.P., Kiyasu J.Y. The enzymatic synthesis of triglycerides. J Biol Chem 1960; 235:40–44
    [Google Scholar]
  62. White P.J., Nairn J., Price N.C., Nimmo H.G., Coggins J.R., Hunter I.S. Phosphoglycerate mutase from Streptomyces coelicolor A3(2): purification and characterization of the enzyme and cloning and sequence analysis of the gene. J Bacteriol 1992; 174:434–440
    [Google Scholar]
  63. Wright L.F., Hopwood D.A. Actinorhodin is a chromosomally-determined antibiotic in Streptomyces coelicolor A3(2). J Gen Microbiol 1976; 96:289–297
    [Google Scholar]
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