Mycological Progress

, Volume 1, Issue 1, pp 3–17 | Cite as

Chaunopycnis pustulata sp. nov., a new clavicipitalean anamorph producing metabolites that modulate potassium ion channels

  • Gerald F. Bills
  • Jon D. Polishook
  • Michael A. Goetz
  • Raymond F. Sullivan
  • James F. WhiteJr.
Article

Abstract

Two morphologically similar strains of hyphomycetous fungi, MF5785 and MF5638, produced potent indole diterpene antagonists of the calcium-gated potassium ion channel, Maxi-K, and a diterpene blocker (nalanthalide) of the voltage-gated potassium channel, Kv 1.3, respectively. The two strains were tentatively identified in the literature as Nalanthamala species. Analyses of their secondary metabolite profiles by HPLC and mass spectroscopy demonstrated that both produced a series of indole diterpenes, of which at least one was produced by both strains. Another strain, Chaunopycnis alba (MF6799), that produced the diterpene, nalanthalide, also produced indole diterpene metabolites. Morphological comparisons and phylogenetic studies based on 28S and ITS rDNA sequences indicated that MF5785 and MF5368, and another soil-derived strain GB6597, belonged to a monophyletic clade of the Clavicipitaceae that included the anamorph Chaunopycnis alba and several Cordyceps and Tolypocladium species. A new species of Chaunopycnis is therefore proposed to accommodate MF5785, MF5368, and GB6597. The possible synonymy of Albophoma yamanashiensis with C. alba also is discussed. Within the Clavicipitaceae, indole diterpenoid compounds have only been known from the graminicolous species (subfamily Clavicipitoideae); therefore delineation of a Chaunopycnis clade has revealed a previously unrecognized lineage of indole diterpene-producing fungi among the subfamily Cordycipitoideae.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Literature cited

  1. Anonymous (1999) Chapman & Hall Dictionary of Natural Products. Headfast/CD Software, Head Software International.Google Scholar
  2. Bills GF, Giacobbe RA, Lee SH, Peláez F, Tkacz JS (1992) Tremorgenic mycotoxins, paspalitrem A and C, from a tropical Phomopsis. — Mycological Research 96: 977–983.CrossRefGoogle Scholar
  3. Candia S, Garcia ML, Latorre R (1992) Mode of action of iberiotoxin, a potent blocker of the large conductance Ca(2+)-activated K+ channel. — Biophysical Journal 63: 583–590.PubMedCrossRefGoogle Scholar
  4. Curran J, Driver F, Ballard JWO, Milner RJ (1994) Phylogeny of Metarhizium: analysis of ribosomal DNA sequence data. — Mycological Research 98: 547–552.CrossRefGoogle Scholar
  5. DeFarias FP, Carvalho MF, Lee SH, Kaczorowski GJ, Suarez-Kurtz G (1996) Effects of the K+ channel blockers paspalitrem C and paxilline on mammalian smooth muscle. — European Journal of Pharmacology 314: 123–128.PubMedCrossRefGoogle Scholar
  6. Desai UJ, Pfaffle PK (1995) Single-step purification of a thermostable DNA polymerase expressed in Escherichia coli. — Biotechniques 19: 780–784.PubMedGoogle Scholar
  7. Felix JP, Buginanesi RM, Schmalhofer WA, Borris R, Goetz MA, Hensens OD, Bao JM, Kayser F, Parsons WH, Rupprecht K, Garcia ML, Kaczorowski GJ, Slaughter RS (1999) Identification and biochemical characterization of a novel nortriterpene inhibitor of the human lymphocyte voltage-gated potassium channel Kv 1.3. — Biochemistry 38: 4922–4930.PubMedCrossRefGoogle Scholar
  8. Galvez A, Gimenez-Gallego G, Reuben JP, Roy-Contancin L, Feigenbaum P, Kaczorowski GJ, Garcia ML (1990) Purification and characterization of a unique, potent, peptidyl probe for the high conductance calcium-activated potassium channel from venom of the scorpion Buthus tamulus. — Journal of Biological Chemistry 265: 11083–11090.PubMedGoogle Scholar
  9. Gams W (1975) Cephalosporium-like hyphomycetes: some tropical species. — Transactions of the British Mycological Society 64: 389–404.CrossRefGoogle Scholar
  10. Gams W (1980) Chaunopycnis alba, gen. et sp. nov., a soil fungus intermediate between Moniliales and Sphaeropsidales. — Persoonia 11: 75–79.Google Scholar
  11. Gams W (1997) Cephalosporium-like hyphomycetes. Extracted, translated, and supplemented from Cephalosporium-artige Schimmelplize (Hyphomycetes). G. Fischer-Verlag and W. Gams, Stuttgart and Baarn.Google Scholar
  12. Garcia ML, Giacobbe RA, Hensens OD, Lee SH, McManus OB, Zink DL (1996) Indole diterpene alkaloid compounds. U.S. Patent 5,541,208.Google Scholar
  13. Garcia-Calvo M, Leonard RJ, Novick J, Stevens SP, Schmalhofer W, Kaczorowski GJ, Garcia ML (1993) Purification, characterization, and biosynthesis of margatoxin, a component of Centruroides margaritatus venom that selectively inhibits voltage-dependent potassium channels. — Journal of Biological Chemistry 268: 18866–18874.PubMedGoogle Scholar
  14. Gimenez-Gallego G, Navia MA, Reuben JP, Katz GM, Kaczorowski GJ, Garcia ML (1988) Purification, sequence, and model structure of charybdotoxin, a potent selective inhibitor of calcium-activated potassium channels. — Proceedings of the National Academy of Sciences, USA 85: 3329–3333.CrossRefGoogle Scholar
  15. Goetz MA, Hensens OD, Zink DL, Borris RP, Morales F, Tamyo-Castillo G, Slaughter RS, Felix J Ball RG (1998) Potent nor-triterpenoid blockers of the voltage-gated potassium channel Kv1.3 from Spachea correae. — Tetrahedron Letters 39: 2895–2898.CrossRefGoogle Scholar
  16. Goetz MA, Zink DL, Dezeny G, Dombrowski A, Polishook J, Felix JP, Slaughter RS, Singh SB (2001) Diterpenoid pyrones, novel blockers of the voltage-gated potassium channel Kv1.3 from fungal fermentations. — Tetrahedron Letters 42: 1255–1257.CrossRefGoogle Scholar
  17. Hensens OD, Ondeyka JG, Dombrowski AW, Ostlind DA, Zink DL (1999) Isolation and structure of nodulisporic acid A1 and A2, novel insecticides from a Nodulisporium sp. — Tetrahedron Letters 40: 5455–5458.CrossRefGoogle Scholar
  18. Hopple JS, Vilgalys R (1999) Phylogenetic relationships in the mushroom genus Coprinus and dark-spored allies based on sequence data from the nuclear gene coding for the large ribosomal subunit RNA: Divergent domains, outgroups, and monophyly. — Molecular Phylogenetics and Evolution 13: 1–19.PubMedCrossRefGoogle Scholar
  19. Huang XH, Tomoda H, Nishida H, Masuma R, Omura S (1995) Terpendoles, novel ACAT inhibitors produced by Albophoma yamanashiensis. I. Production, isolation and biological properties. — Journal of Antibiotics 48: 1–4.PubMedCrossRefGoogle Scholar
  20. Joung C, McMillan L, Telfer E, Scott B (2001) Molecular cloning and genetic analysis of an indole-diterpene gene cluster from Penicillium paxilli. — Molecular Microbiology 39: 754–764.CrossRefGoogle Scholar
  21. Jukes TH, Cantor CR (1969) Evolution of protein molecules. In H. R. Munro (eds) Mammilian Protein Metabolism. pp. 21–132. Academic Press, New York, NY, USA.Google Scholar
  22. Kjer KM, Blahnik RJ, Holzenthal R (2001) Phylogeny of Trichoptera (Caddisflies). Zoologica Scripta, in press.Google Scholar
  23. Knaus H-G, McManus OB, Lee SH, Schmalhofer WA, Garcia-Calvo M, Helms LM, Sanchez M, Giangiacomo K, Reuben JP, Smith AB, Kaczorowski GJ, Garcia ML (1994) Tremorgenic indole alkaloids inhibit smooth muscle high-conductance calcium-activated potassium channels. — Biochemistry 33: 5819–5828.PubMedCrossRefGoogle Scholar
  24. Kobayashi T, Masuma R, Omura S, Watanabe K (1994) Materials for the fungus flora of Japan (47). — Mycoscience 35: 399–401.CrossRefGoogle Scholar
  25. Kobayasi Y (1983) Miscellaneous notes on fungi (3). — Journal of Japanese Botany 58: 221–223.Google Scholar
  26. Kornerup A, Wanscher JH (1978) Methuen handbook of colour. Eyre Methuen, London, United Kingdom.Google Scholar
  27. Möller C, Buehler T, Dreyfuss MM (1995) Intraspecific genetic diversity of Chaunopycnis alba detected by random amplified polymorphic DNA assay. — Mycological Research 99: 681–688.CrossRefGoogle Scholar
  28. Möller C, Gams W (1993) Two new hyphomycetes isolated from Antarctic lichens. — Mycotaxon 48: 441–450.Google Scholar
  29. Möller C, Weber G, Dreyfuss MM (1996) Intraspecific diversity in the fungal species Chaunopycnis alba: implications for microbial screening programs. — Journal of Industrial Microbiology 17: 359–372.CrossRefGoogle Scholar
  30. Moncalvo JM, Lutzoni FM, Rehner SA, Johnson J, Vilgalys R (2000) Phylogenetic relationships of agaric fungi based on nuclear large subunit ribosomal DNA sequences. Systematic Biology: 278–305.Google Scholar
  31. Munday-Finch SC, Wilkins AL, Miles CO, Tomoda H, Omura S (1997) Isolation and structure elucidation of lolilline, a possible biosynthetic precursor of the lolitrem family of tremorgenic mycotoxins. — Journal of Agricultural and Food Chemistry 45: 199–204.CrossRefGoogle Scholar
  32. Neuvéglise C, Brygoo Y, Vercambre B, Riba G (1994) Comparative analysis of molecular and biological characteristics of strains of Beauveria brongniartii isolated from insects. — Mycological Research 98: 322–328.CrossRefGoogle Scholar
  33. Nikoh N, Fukatsu T (2000) Interkingdom host jumping underground: phylogenetic analysis of entomoparasitic fungi of the genus Cordyceps. — Molecular and Biological Evolution 17: 629–638.CrossRefGoogle Scholar
  34. Omura S, Tomoda H, Masuma R (1994) FO-2546 substance, its production and its use as inhibitor of acyl-coA cholesterol acyl transferase. Patent Cooperation Treaty WO 94/09004.Google Scholar
  35. Ondeyka JG, Ball RG, Garcia ML, Dombrowski AW, Sabinis G, Kaczorowski GJ, Zink DL, Bills GF, Goetz MA, Schmalhofer WA, Singh SB (1995) A carotane sesquiterpene as a potent modulator of the maxi-K channel from Arthrinium phaeospermum. — Bioorganic and Medicinal Chemistry Letters 5: 733–744.CrossRefGoogle Scholar
  36. Ondeyka JG, Helms GL, Hensens OD, Goetz MA, Zink DL, Tsipouras A, Shoop W, Slayton L, Dombrowski AW, Polishook JD, Ostlind DA, Tsou NN, Ball RG, Singh SB (1997) Nodulisporic acid A, a novel and potent insecticide from a Nodulisporium sp., isolation, structure determination and chemical transformations. — Journal of the American Chemical Society 119: 8809–8816.CrossRefGoogle Scholar
  37. Posada D, Crandall KA (1988) Modeltest: testing the model of DNA substitution. — Bioinformatics 14: 817–818.CrossRefGoogle Scholar
  38. Ridgway R (1912) Color standards and nomenclature. Published by the author, Washington, D.C., USA.Google Scholar
  39. Rossman AY, McKemy JM, Pardo-Schultheiss RA, Schroers H-J (2001) Molecular studies of the Bionectriaceae using large subunit rDNA sequences. — Mycologia 93: 100–110.CrossRefGoogle Scholar
  40. Samson RA (1974) Paecilomyces and some allied hyphomycetes. — Studies in Mycology 6: 1–119.Google Scholar
  41. Samson RA, Evans HC, Latgé JP (1988) Atlas of entomopathogenic fungi. Springer-Verlag, Berlin, Germany.CrossRefGoogle Scholar
  42. Samson RA, Soares GC (1984) Entomopathogenic species of the hyphomycete genus Tolypocladium. — Journal of Invertebrate Pathology 43: 133–139.CrossRefGoogle Scholar
  43. Smith MM, Warren VA, Thomas BS, Brochu RM, Ertel EA, Rohrer S, Schaeffer J, Schmatz D, Petuch BR, Tang YS, Meinke PT, Kaczorowski GJ, Cohen CJ (2000) Nodulisporic acid opens insect glutamate-gated chloride channels: identification of a new high-affinity modulator. — Biochemistry 39: 5543–5554.PubMedCrossRefGoogle Scholar
  44. Subramanian CV (1956) Hyphomycetes II. — Journal of the Indian Botanical Society 35: 446–494.Google Scholar
  45. Sullivan R, Bergen MS, Patel R, Bills GF, Alderman SC, Spatafora JW, White J (2001) Neoclaviceps monostipa: features of an enigmatic clavicipitalean fungus and the phyletic status of the anamorphic genus Ephelis. — Mycologia 93: 90–99.CrossRefGoogle Scholar
  46. Swofford DL (1999) PAUP*. Phylogenetic Analysis Using Parsimony and Other Methods. Version 5. Sinauer Associates, Sunderland, MA.Google Scholar
  47. Swofford DL, Olsen GJ, Waddell PJ, Hillis DM (1996) Phylogenetic Inference. In D. M. Hillis, C. Moritz & B. K. Mable (eds) Molecular Systematics. pp. 407–514. Sinauer Associates, Sunderland, MA, USA.Google Scholar
  48. Taylor JW, Jacobson DJ, Kroken S, Kasuga T, Geiser DM, Hibbett DS, Fischer MC (2000) Phylogenetic species recognition and species concepts in fungi. Fungal Genetics and Biology 31: 21–32.PubMedCrossRefGoogle Scholar
  49. Tomada H, Tabata N, Yang D, Takayanagi H, Omura S (1995) Terpendoles, novel ACAT inhibitors produced by Albophoma yamanashiensis. III. Production, isolation and structure elucidation of new components. — Journal of Antibiotics 48: 793–804.CrossRefGoogle Scholar
  50. Turner WB, Aldridge DC (1983) Fungal Metabolites II. Academic Press, London, UK.Google Scholar
  51. Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. — Journal of Bacteriology 172: 4238–4246.PubMedGoogle Scholar
  52. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innis, D. H. Gelfand, J. J. Sninsky & T. J. White (eds) PCR protocols: a guide to methods and applications. pp. 315–322. Academic Press, San Diego, CA, USA.Google Scholar
  53. Yao Y, Peter AB, Baur R, Sigal E (1989) The tremorgen aflatrem is a positive allosteric modulator of the K-aminobutyric acid receptor channel in Xenopus oocytes. — Molecular Pharmacology 35: 319–323.PubMedGoogle Scholar

Copyright information

© DGfM 2002

Authors and Affiliations

  • Gerald F. Bills
    • 1
  • Jon D. Polishook
    • 2
  • Michael A. Goetz
    • 2
  • Raymond F. Sullivan
    • 3
  • James F. WhiteJr.
    • 3
  1. 1.Centro de Investigación BásicaMerck Sharp & Dohme de España S.A.MadridSpain
  2. 2.Merck Research LaboratoriesRahwayUSA
  3. 3.Department of Plant Pathology, Cook CollegeRutgers UniversityNew BrunswickUSA

Personalised recommendations