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The biosynthesis of oxylipins of linoleic and arachidonic acids by the sewage fungus Leptomitus lacteus, including the identification of 8R-hydroxy-9Z,12Z-octadecadienoic acid

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Lipids

Abstract

When the sewage fungus Leptomitus lacteus was grown in liquid culture aerobically and then transferred to medium containing long-chain fatty acids, it produced a number of oxygenated fatty acids. From linoleic acid (18∶2n−6), the major metabolite produced was R-8-hydroxy-9Z,12Z-octadecadienoic acid (8R-HODE), with additional quantities of 8,11-di-HODE, 11,16-di-HODE, and 11,17-di-HODE. Other fatty acid derivatives identified included 7-HODE, 10-HODE, and 13-hydroxy-octadecamonoenoic acid. Arachidonic acid (20∶4n−6) was metabolized primarily to 18- and and 19-hydroxy-eicosatetraenoic acids (18- and 19-HETE) also as R enantiomers, along with smaller quantities of 17-HETE, 9-HETE, 14,15-dihydroxyeicosatrienoic acid and 11,12,19-trihydroxy-eicosatrienoic acid. The oxygenated products of long-chain fatty acids, in particular the biosynthesis of 8R-HODE, a compound classified as a precocious sporulation inducer, were similar to those produced by an unrelated fungal species in the Ascomycota, the take-all fungus Gaeumannomyces graminis. As in G. graminis, the biotransformation of linoleate to 8R-HODE was not significantly inhibited by exposure of the organism to CO. This indicated that the enzyme responsible for 8R-HODE biosynthesis in Leptomitus could be similar to that of G. graminis; yet we did not detect 7,8-di-HODE as a product of 18∶2n−6 metabolism as in G. graminis. CO did inhibit the biosynthesis of 14,15-di-HETE, 18-HETE, and 19-HETE in L. lacteus, which suggested the involvement of a cytochrome P450-type monooxygenase. The biosynthesis of 8R-HODE from 18∶2n−6 was found to occur in certain cell lysates, specifically in low speed (15,000×g) supernatant, following cell disruption.

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Abbreviations

16∶0:

palmitic acid

18∶1n−6:

9Z-oleic acid

18∶2n−6:

9Z,12Z-linoleic acid

20∶4n−6:

5Z,8Z,11Z,14Z-eicosatetraenoic acid

EI:

electron impact

GC-MS:

gas chromatography-mass spectrometry

9-HETE:

9-hydroxy-5Z,8Z,11Z,14Z-eicosatetraenoic acid

17-HETE:

18-hydroxy-5Z,8Z,11Z,14Z-eicosatetraenoic acid

18-HETE:

18-hydroxy-5Z,8Z,11Z,14Z-eicosatetraenoic acid

19-HETE:

19-hydroxy-5Z,8Z,11Z,14Z-eicosatetraenoic acid

14,15-HETriE:

14,15-dihydroxy-5Z,8Z,11Z-eicosatrienoic acid

11,12,19-HETriE:

11,12,19-trihydroxy-5Z,8Z,14Z-eicosatrienoic acid

7-HODE:

7-hydroxy-9Z,12Z-octadecadienoic acid

8-HODE:

8-hydroxy-9Z,12Z-octadecadienoic acid

10-HODE:

10-hydroxy-8Z,12Z-octadecadienoic acid

16-HODE:

16-hydroxy-9Z,12Z-octadecadienoic acid

8,11-di-HODE:

8,11-dihydroxy-9Z,12Z-octadecadienoic acid

11,16-di-HODE:

11,16-dihydroxy-9Z,12Z-octadecadienoic acid

11,17-di-HODE:

11,17-di-hydroxy-9Z,12Z-octadecadienoic acid

13-HOME:

13-hydroxy-9Z-octadecamonoenoic acid

9,10-di-HOME:

9,10-dihydroxy-12Z-octadecamonoenoic acid

12,13-di-HOME:

12,13-dihydroxy-9Z-octadecamonoenoic acid

HPLC:

high-performance liquid chromatography

LDS:

linoleate diol synthase

MS:

mass spectrometry

NDGA:

nordihydroguaiaretic acid

sp. act.:

specific activity

TLC:

thin-layer chromatography

TMSO:

trimethyl silyl ester

References

  1. Herman, R.P., and Luchini, M.M. (1989) Lipoxygenase Activity in Oomycete Saprolegnia Is Dependent on Environmental Cues and Reproductive Competence, Exp. Mycol. 13, 372–379.

    Article  CAS  Google Scholar 

  2. Brodowsky, I.D., and Oliw, E.H. (1992) Metabolism of 18−2n−6, 18−3n−3, 20−4n−6 and 20−5n−3 by the Fungus Gaeumannomyces graminis—Identification of Metabolites formed by 8-Hydroxylation and by ω2 and ω3 Oxygenation, Biochim. Biophys. Acta 1124, 59–65.

    PubMed  CAS  Google Scholar 

  3. Mazur, P., Meyers, H.V., Nakanishi, K., ElZayat, A.A.E., and Champe, S.P. (1990) Structural Elucidation of Sporogenic Fatty-Acid Metabolites from Aspergillus nidulans, Tetrahedron Lett. 31, 3837–3840.

    Article  CAS  Google Scholar 

  4. Bowers, W.S., Hoch, H.C., Evans, P.H., and Katayama M. (1986) Thallophytic Allelopathy—Isolation and Identification of Laetisaric Acid, Science 232, 105–106.

    Article  CAS  PubMed  Google Scholar 

  5. Needleman, P., Turk, J., Jakschik, B.A., Morrison, A.R., and Lefkowith, J.B. (1986) Arachidonic Acid Metabolism, Annu. Rev. Biochem. 55, 69–102.

    Article  PubMed  CAS  Google Scholar 

  6. Hamberg, M. (1986) Isolation and Structures of Lipoxygenase Products from Saprolegnia Parasitica, Biochim. Biophys. Acta 876, 688–692.

    CAS  Google Scholar 

  7. Herman, R.P., and Herman, C.A. (1985) Prostaglandins or Prostaglandin-Like Substances Are Implicated in Normal Growth and Development in Oomycetes, Prostaglandins 29, 819–830.

    Article  PubMed  CAS  Google Scholar 

  8. Schade, A.L. (1940) The Nutrition of Leptomitus, Am. J. Bot. 27, 376–384.

    Article  CAS  Google Scholar 

  9. Willoughby, L.G., and Roberts, R.J. (1991) Occurrence of the Sewage Fungus Leptomitus-lacteus, a Necrotroph on Perch (Perca-fluviatilis), in Windermere, Mycol. Res. 95, 755–768.

    Article  Google Scholar 

  10. Luthria, D.L., Baykousheva, S.P., and Sprecher, H. (1995) Double Bond Removal from Odd-Numbered Carbons During Peroxisomal β-Oxidation of Arachidonic Acid, J. Biol. Chem. 270, 13771–13778.

    Article  PubMed  CAS  Google Scholar 

  11. MacLouf, J., and Rigaud, M. (1982) Open Tubular glass Capillary Gas Chromatography for Separating Eicosanoids, Methods Enzymol. 86, 612–631.

    Article  PubMed  CAS  Google Scholar 

  12. Hamberg, M. (1971) Steric Analysis of Hydroperoxides Formed by Lipoxygenase Oxygenation of Linoleic Acid, Anal. Biochem. 43, 515–526.

    Article  PubMed  CAS  Google Scholar 

  13. Oliw, E.H., Fahlstadius, P., and Hamberg, M. (1986) Isolation and Biosynthesis of 20-Hydroxy Prostaglandins-E1 and 20-Hydroxy Prostaglandin-E2 in Ram Seminal Fluid, J. Biol. Chem. 261, 9216–9221.

    PubMed  CAS  Google Scholar 

  14. Hawkins, D.J., Kuhn, H., Petty, E.H., and Brash, A.R. (1988) Resolution of Enantiomers of Hydroxyeicosatetraenoate Derivatives by Chiral Phase High-Pressure Liquid Chromatography, Anal. Biochem. 173, 456–462.

    Article  PubMed  CAS  Google Scholar 

  15. Fox, S.R., Friend, J., and Ratledge, C. (1997) Optimisation of 3-Hydroxyeicosanoid Biosynthesis by the Yeast Dipodascopsis uninucleata, Biotechnol. Lett. 19, 155–158.

    Article  CAS  Google Scholar 

  16. Butcher, R.W. (1932) Contribution to Our Knowledge of the Ecology of Sewage Fungus, Transactions Brit. Mycolog. Soc., 17, 12–124.

    Google Scholar 

  17. Su, C., and Oliw, E.H. (1998) Managanese Lipoxygenase: Purification and Characterization, J. Biol. Chem. 273, 13072–13079.

    Article  PubMed  CAS  Google Scholar 

  18. Brodowsky, I.D., Hamberg, M., and Oliw, E.H. (1992) A Linoleic Acid (8R)-Dioxygenase and Hydroperoxide Isomerase of the Fungus Gaeumannomyces graminis, J. Biol. Chem. 267, 14738–14745.

    PubMed  CAS  Google Scholar 

  19. Smith, W.L., and Lands, W.E.M. (1971) Stimulation and Blockade of Prostaglandin Biosynthesis, J. Biol. Chem. 246, 6700–6702.

    PubMed  CAS  Google Scholar 

  20. Hamasaki, Y., and Tai, H.H. (1985) Gossypol, a Potent Inhibitor of Arachidonate 5-Lipoxygenase and 12-Lipoxygenase, Biochim. Biophys. Acta 834, 37–41.

    PubMed  CAS  Google Scholar 

  21. Agarwal, R., Wang, Z.Y., and Mukhtar, H. (1991) Nordihydroguaiaretic Acid, an Inhibitor of Lipoxygenase, Also Inhibits Cytochrome-P450-Mediated Monooxygenase Activity in Rat Epidermal and Hepatic Microsomes, Drug Metab. Dispos. 19, 620–624.

    PubMed  CAS  Google Scholar 

  22. Su, C., and Oliw, E.H. (1996) Purification and Characterization of Linoleate 8-Dioxygenase from the Fungus Gaeumannomyces graminis as a Novel Hemoprotein, J. Biol. Chem. 271, 14112–14118.

    Article  PubMed  CAS  Google Scholar 

  23. Su, C., Brodowsky, I.D., and Oliw, E.H. (1995) Studies on Linoleic Acid 8R-Dioxygenase and Hydroperoxide Isomerase of the Fungus Gaeumannomyces graminis, Lipids 30, 43–50.

    PubMed  CAS  Google Scholar 

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Author notes

  1. Asmita A. Prabhune

    Present address: Department of Biotechnology, The National Chemical Laboratory, 4110088, Pune, India

Authors and Affiliations

  1. Department of Biological Sciences, University of Hull, HU6 7RX, Hull, UK

    Simon R. Fox, Arzu Akpinar, Asmita A. Prabhune, John Friend & Colin Ratledge

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  1. Simon R. Fox
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  2. Arzu Akpinar
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  3. Asmita A. Prabhune
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Correspondence to Simon R. Fox.

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Fox, S.R., Akpinar, A., Prabhune, A.A. et al. The biosynthesis of oxylipins of linoleic and arachidonic acids by the sewage fungus Leptomitus lacteus, including the identification of 8R-hydroxy-9Z,12Z-octadecadienoic acid. Lipids 35, 23–30 (2000). https://doi.org/10.1007/s11745-000-0490-5

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  • DOI: https://doi.org/10.1007/s11745-000-0490-5

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