Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter September 4, 2018

Two new usnic acid derivatives from the endophytic fungus Mycosphaerella sp.

  • Djalma M. de Oliveira , Cristiane B. Pereira , Graziele Mendes , Jochen Junker , Markus Kolloff , Luiz H. Rosa , Carlos A. Rosa , Tânia M.A. Alves , Carlos L. Zani , Susana Johann and Betania B. Cota ORCID logo EMAIL logo

Abstract

The endophytic fungus Mycosphaerella sp. (UFMGCB2032) was isolated from the healthy leaves of Eugenia bimarginata, a plant from the Brazilian savanna. Two novel usnic acid derivatives, mycousfuranine (1) and mycousnicdiol (2), were isolated from the ethyl acetate extract, and their structure was elucidated by NMR and MS analyses. Compounds 1 and 2 exhibited moderate antifungal activities against Cryptococcus neoformans and Cryptococcus gattii, each with minimum inhibitory concentration values of 50.0 μg/mL and 250.0 μg/mL, respectively.

Acknowledgments

We would like to thank the “Conselho Nacional de Desenvolvimento Cientifico e Tecnológico” (CNPq) for their financial support and scholarship award. This work was also supported in part by a grant from “Fundação de Amparo à Pesquisa do Estado de Minas Gerais” (FAPEMIG). The authors would also like to thank the staff (Charles da Silva Amaral and ElianeGonçalvesCarvalho) of the Program of Technological Development in Tools for Health PDTIS-FIOCRUZ, RPT13A platform for allowing us the use of its facilities.

References

1. Aptroot A. Mycosphaerella and its anamorphs: 2. Conspectus of Mycosphaerella, Vol. 5. Utrecht, The Netherlands: CBS Biodiversity Series, 2006:231.Search in Google Scholar

2. Farr DF, Bills GF, Chamuris GP, Rossman AY. Fungi on plants and plant products in the United States. St Paul, Minnesota: APS Press, 1995:1252.Search in Google Scholar

3. Crous PW, Braun U. Mycosphaerella and its anamorphs. 1. Names published in Cercospora and Passalora, Vol. 1. Utrecht, The Netherlands: CBS Biodiversity Series, 2003:571.Search in Google Scholar

4. Crous PW. Taxonomy and phylogeny of the genus Mycosphaerella and its anamorphs. Fungal Divers 2009;38:1–24.Search in Google Scholar

5. Assante G, Camarda L, Merlini L, Nasini G. Mycochromone and mycoxanthone: two new metabolites from Mycosphaerella rosigena. Phytochemistry 1979;18:311–3.10.1016/0031-9422(79)80077-1Search in Google Scholar

6. Assante G, Camarda L, Nasini G, Vaghi G. Isolation and characterization of new dothistromins from Mycosphaerella laricina Hart. Phytopathol Mediterr 1985;24:271–3.Search in Google Scholar

7. Albinati A, Brückner S, Camarda L, Nasini G. Rosigenin, an unusual metabolite from Mycosphaerella rosigena. Tetrahedron 1980;36:117–21.10.1016/0040-4020(80)85033-2Search in Google Scholar

8. Assante G, Camarda L, Merlini L, Nasini G. Secondary metabolites from Mycosphaerella ligulicola. Phytochemistry 1981;20:1955–7.10.1016/0031-9422(81)84043-5Search in Google Scholar

9. Arnone A, Camarda L, Nasini G, Assante G. Secondary mould metabolites. Part 15. Structure elucidation of rubellins A and B, two novel anthraquinone metabolites from Mycosphaerella rubella. J Chem Soc Perk T 1 1986;1:255–60.10.1039/p19860000255Search in Google Scholar

10. Arnone A, Nasini G, Pava OV. A reinvestigation of the structure of biruloquinone, a 9,1-phenanthrenequinone isolated from Mycosphaerella rubella. Phytochemistry 1991;30:2729–31.10.1016/0031-9422(91)85132-JSearch in Google Scholar

11. Arnone A, Nasini G, Pava OV. A hydroxytetradecatrienoic acid from Mycosphaerella rubella. Phytochemistry 1998;48: 507–10.10.1016/S0031-9422(98)00027-2Search in Google Scholar PubMed

12. Sassa T, Igarashi M, Nukina M. (−)-Mycousunine and (+)-isomycousunine, new phytotoxic usunic acid derivatives from the phytopathogenic fungus, Mycosphaerella nawae. Agric Biol Chem 1989;53:1743–4.10.1271/bbb1961.53.1743Search in Google Scholar

13. Sassa T, Igarashi M. Structures of (−)-Mycousnine, (−)-isomycousnine and (−)-oxymycousnine, new usnic acid derivatives from phytopathogenic Mycosphaerella nawae. Agric Biol Chem 1990;54:2231–7.10.1271/bbb1961.54.2231Search in Google Scholar

14. Arnone A, Assante G, Montorsi M, Nasini G. Asteromine, a bioactive secondary metabolite from a strain of Mycosphaerella asteroma. Phytochemistry 1995;38:595–7.10.1016/0031-9422(94)00620-9Search in Google Scholar

15. Moreno E, Varughese T, Spadafora C, Arnold AE, Coley PD, Kursar TA, et al. Chemical constituents of the new endophytic fungus Mycosphaerella sp. nov. and their anti-parasitic activity. Nat Prod Commun 2011;6:835–40.10.1177/1934578X1100600620Search in Google Scholar PubMed

16. Pereira CB, de Oliveira DM, Hughes AF, Kohlhoff M, Vieira ML, Martins Vaz AB, et al. Endophytic fungal compounds active against Cryptococcus neoformans and C. gattii. J Antibiot 2015;68:436–44.10.1038/ja.2015.11Search in Google Scholar PubMed

17. CLSI. Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts; Approved Standard, 3rd ed. CLSI document M27-A3. Wayne, PA: Clinical and Laboratory Standards Institute, 2008.Search in Google Scholar

18. Mycousfuranine: [α]D25=27.5 (c 0.2, MeOH); UV (MeOH) λmax (log ε) 225 (3.98), 250 (3.76), 286 (3.82), 334 (3.32); NMR data (DMSO-d6), see Table 1; HRESIMS [M−H] at m/z 319.0823 (Calcd for C16H15O7), [M+H]+ at m/z 321.0975 (Calcd for C16H17O7).Search in Google Scholar

19. König GM, Wright AW. 1H and 13C-NMR and biological activity investigations of four lichen-derived compounds. Phytochem Anal 1999;10:279–84.10.1002/(SICI)1099-1565(199909/10)10:5<279::AID-PCA464>3.0.CO;2-3Search in Google Scholar

20. Sammes MP, Maini PN. 13C NMR chemical shift assignments for some 2-substituted cyclic 1,3-diketones. Magn Reson Chem 1987;25:372–4.10.1002/mrc.1260250422Search in Google Scholar

21. Cremlyn RJ, Osborne AG, Warmsley JF. NMR spectral studies of dimedone-aldehyde adducts. Part 1. 1H-and 13C NMR spectral studies of dimedone. Spectrochim Acta A 1996;52:1423–32.10.1016/0584-8539(96)01695-9Search in Google Scholar

22. Huneck S. Struktur der (-)-placodiolsäure. Tetrahedron 1972;28:4011–7.10.1016/S0040-4020(01)93847-5Search in Google Scholar

23. Huneck S, Weinberg GD. The absolute configurations of (+)-usnic and (+)-isousnic acid. X-ray analyses of the (−)-α-phenylethylamine derivative of (+)-usnic acid and of (−)-pseudoplacodiolic acid, a new dibenzofuran, from the lichen Rhizoplaca chrysoleuca. Tetrahedron Lett 1981;22:351–2.10.1016/0040-4039(81)80095-0Search in Google Scholar

24. Connolly JD, Freer AA, Huneck S. Crystal structure of (−)-placodiolic acid, a dibenzofuran derivative from the lichen Rhizoplaca chrysoleuca. Phytochemistry 1984;23:702.10.1016/S0031-9422(00)80419-7Search in Google Scholar

25. Mycousnicdiol: [α]D25=144.4,, c 0.18, CHCl3); UV (MeOH) λmax (log ε) 220 (3.82), 251 (3.66), 281 (3.78), 334 (3.16); NMR data (DMSO-d6), see Table 1; HRESIMS [M+H]+ m/z 367.1025 (Calcd for C17H18O9).Search in Google Scholar

26. Foo YL. Amariin, a di-dehydrohexahydroxydiphenoyl hydrolysable tannin from Phyllanthus amarus. Phytochemistry 1993;33:487–91.10.1016/0031-9422(93)85545-3Search in Google Scholar

27. Nonaka G, Matsumoto Y, Nishioka I. Trapain, a new hydrolyzable tannin from Trapa japonica Flerov. Chem Pharm Bull 1981;4:1184–7.10.1248/cpb.29.1184Search in Google Scholar

28. Hoffman AM, Mayer SG, Strobel GA, Hess WM, Sovocool GW, Grange AH, et al. Purification, identification and activity of phomodione, a furandione from an endophytic Phoma species Phytochemistry 2008;69:1049–56.10.1016/j.phytochem.2007.10.031Search in Google Scholar

29. Imashiro F, Maeda S, Takegoshi K, Terao T, Saika A. Intermolecular hydrogen-bonding effects on 13C NMR shielding for enol forms of diketones in the solid state. Chem Phys Lett 1982;92:642–5.10.1016/0009-2614(82)83665-8Search in Google Scholar


Supplementary Material

The online version of this article offers supplementary material (https://doi.org/10.1515/znc-2017-0162).


Received: 2017-09-06
Revised: 2018-05-16
Accepted: 2018-08-04
Published Online: 2018-09-04
Published in Print: 2018-11-27

©2018 Walter de Gruyter GmbH, Berlin/Boston

Downloaded on 11.5.2024 from https://www.degruyter.com/document/doi/10.1515/znc-2017-0162/html
Scroll to top button