Mycological Progress

, Volume 16, Issue 7, pp 713–728 | Cite as

Biodiversity and chemotaxonomy of Preussia isolates from the Iberian Peninsula

  • Víctor Gonzalez-MenendezEmail author
  • Jesus Martin
  • Jose A. Siles
  • M. Reyes Gonzalez-Tejero
  • Fernando Reyes
  • Gonzalo Platas
  • Jose R. Tormo
  • Olga Genilloud
Original Article


This work documents 32 new Preussia isolates from the Iberian Peninsula, including endophytic and saprobic strains. The morphological study of the teleomorphs and anamorphs was combined with a molecular phylogenetic analysis based on sequences of the ribosomal rDNA gene cluster and chemotaxonomic studies based on liquid chromatography coupled to electrospray mass spectrometry. Sixteen natural compounds were identified. On the basis of combined analyses, 11 chemotypes are inferred.


Preussia Chemotypes Mass spectrometry Secondary metabolites 



This work was carried out as part of the PhD Program “New Therapeutic Targets: Discovery and Development of New Antibiotics” from the School of Masters Degrees of the University of Granada. HRMS equipment used in this work was acquired with a grant for scientific infrastructures from the Local Government, Junta de Andalucía (BOJA-11-Nov-2007). Part of this work was also supported by the Andalusian Government grant RNM-7987 “Sustainable use of plants and their fungal parasites from arid regions of Andalucía for new molecules useful for antifungals and neuroprotectors”. We want to express our gratitude to Dr. Josep Guarro (Rovira i Virgili University, Reus, Spain) for the strains (WQ-056, WQ-023, WQ-124, WO-009, WQ-140, and WQ-064) and Dr. Gerald F. Bills for his comments and support.

Supplementary material

11557_2017_1305_MOESM1_ESM.pptx (47 kb)
ESM 1 (PPTX 47 kb)


  1. Andersen B, Dongo A, Pryor BM (2008) Secondary metabolite profiling of Alternaria dauci, A. porri, A. solani, and A. tomatophila. Mycol Res 112:241–250CrossRefPubMedGoogle Scholar
  2. Arenal F, Platas G, Peláez F (2004) Variability of spore length in some species of the genus Preussia (Sporormiella). Mycotaxon 89:137–151Google Scholar
  3. Arenal F, Platas G, Peláez F (2005) Two new Preussia species defined based on morphological and molecular evidence. Fungal Divers 20:1–15Google Scholar
  4. Arenal F, Platas G, Peláez F (2007) A new endophytic species of Preussia (Sporormiaceae) inferred from morphological observations and molecular phylogenetic analysis. Fungal Divers 25:1–17Google Scholar
  5. Arnold AE (2007) Understanding the diversity of foliar endophytic fungi: progress, challenges, and frontiers. Fungal Biol Rev 21:51–66CrossRefGoogle Scholar
  6. Asgari B, Zare R (2010) Two new species of Preussia from Iran. Nova Hedwigia 90:533–548CrossRefGoogle Scholar
  7. Barr ME (2000) Notes on coprophilous bitunicate ascomycetes. Mycotaxon 76:105–112Google Scholar
  8. Barrasa JM (1985) Estudio de los Ascomycetes coprófilas en España. Thesis, University of Alcalá de HenaresGoogle Scholar
  9. Barrasa JM, Checa J (1989) Dothidelaes coprófilas del Parque Natural de Monfragüe (Cáceres). VIII Simposios Ciencias CriptográmicasGoogle Scholar
  10. Barrasa JM, Moreno G (1980) Contribución al estudio de los hongos que viven sobre materias fecales (2a aportación). Acta Bot Malacitana Málaga 6:111–148Google Scholar
  11. Bergstrom JD, Dufresne C, Bills GF, Nallin-Omstead M, Byrne K (1995) Discovery, biosynthesis, and mechanism of action of the zaragozic acids: potent inhibitors of squalene synthase. Ann Rev Microbiol 49:607–639CrossRefGoogle Scholar
  12. Bills GF, Christensen M, Powell M, Thorn G (2004) Saprobic soil fungi. In: Mueller GM, Bills GF, Foster MS (eds) Biodiversity of fungi: inventory and monitoring methods. Elsevier Academic Press, Oxford, pp 271–302CrossRefGoogle Scholar
  13. Bills GF, González-Menéndez V, Platas G (2012) Kabatiella bupleuri sp. nov. (Dothideales), a pleomorphic epiphyte and endophyte of the Mediterranean plant Bupleurum gibraltarium (Apiaceae). Mycologia 104:962–973CrossRefPubMedGoogle Scholar
  14. Bills GF, Gloer JB, An Z (2013) Coprophilous fungi: antibiotic discovery and functions in an underexplored arena of microbial defensive mutualism. Curr Opin Microbiol 16(5):549–565CrossRefPubMedGoogle Scholar
  15. Boerema GH, de Gruyter J, Noordeloos ME, Hamers MEC (2004) A Phoma sect. Phoma. In: Boerema GH, de Gruyter J, Noordeloos ME, Hamers MEC (eds) Phoma identification manual. Differentiation of specific and infra-specific taxa in culture. CAB International, Wallingford, pp 32–118Google Scholar
  16. Cain RF (1961) Studies of coprophilous ascomycetes VII. Preussia. Can J Bot 39:1633–1666CrossRefGoogle Scholar
  17. Chen X, Shi Q, Lin G, Guo S, Yang J (2009) Spirobisnaphthalene analogues from the endophytic fungus Preussia sp. J Nat Prod 72:1712–1725CrossRefPubMedGoogle Scholar
  18. Clapp-Shapiro WH, Burgess BW, Giacobbe RA, Harris GH, Mandala S, Polishook J, Rattray M, Thornton RA, Zink DL, Cabello A, Diez MT, Martin I, Pelaez F (1998) Antifungal agent from Sporomiella minimoides. US patent US5801172AGoogle Scholar
  19. Cole RJ, Jarvis BB, Schweikert MA (2003) Handbook of secondary fungal metabolites. Academic Press, New YorkGoogle Scholar
  20. Collado J, González A, Platas G, Stchigel AM, Guarro J, Peláez F (2002) Monosporascus ibericus sp. nov., an endophytic ascomycete from plants on saline soils, with observations on the position of the genus based on sequence analysis of the 18S rDNA. Mycol Res 106:118–127CrossRefGoogle Scholar
  21. de Gruyter J, Woudenberg JH, Aveskamp MM, Verkley GJ, Groenewald JZ, Crous PW (2013) Redisposition of phoma-like anamorphs in Pleosporales. Stud Mycol 75:1–36CrossRefPubMedGoogle Scholar
  22. de la Cruz M, Martín J, González-Menéndez V, Pérez-Victoria I, Moreno C, Tormo JR, El Aouad N, Guarro J, Vicente F, Reyes F, Bills GF (2012) Chemical and physical modulation of antibiotic activity in Emericella species. Chem Biodivers 9:1095–1113CrossRefPubMedGoogle Scholar
  23. de la Torre M (1974) Estudio sistemático, ecológico y corológico de Ascomycetes españoles. Thesis doctoral (ined), Facultad de Farmacia, Universidad Complutense de Madrid, 264 ppGoogle Scholar
  24. Devarajan PT, Suryanarayanan TS (2006) Evidence for the role of phytophagous insects in dispersal of non-grass fungal endophytes. Fungal Divers 23:111–119Google Scholar
  25. Doveri F, Sarrocco S (2013) Sporormiella octomegaspora, a new hairy species with eight-celled ascospores from Spain. Mycotaxon 123:129–140CrossRefGoogle Scholar
  26. Du L, Robles AJ, King JB, Mooberry SL, Cichewicz RH (2014) Cytotoxic dimeric epipolythiodiketopiperazines from the ascomycetous fungus Preussia typharum. J Nat Prod 77:1459–1466CrossRefPubMedPubMedCentralGoogle Scholar
  27. Ellis JB, Everhart BM (eds) (1892) The North American Pyrenomycetes. A contribution to mycologic biology. Ellis & Everhart, Newfield, NJ, 793 ppGoogle Scholar
  28. Frisvad JC, Andersen B, Thrane U (2008) The use of secondary metabolite profiling in chemotaxonomy of filamentous fungi. Mycol Res 112:231–240CrossRefPubMedGoogle Scholar
  29. Fuckel L (1866) Fungi Rhenani Exsiccati Cent. XVI–XVIII 17–18:1601–1800Google Scholar
  30. González-Menéndez V, Asensio F, Moreno C, de Pedro N, Monteiro MC, de la Cruz M, Vicente F, Bills GF, Reyes F, Genilloud O, Tormo JR (2014) Assessing the effects of adsorptive polymeric resin additions on fungal secondary metabolite chemical diversity. Mycology 5:179–191CrossRefPubMedPubMedCentralGoogle Scholar
  31. González-Menéndez V, Pérez-Bonilla M, Pérez-Victoria I, Martín J, Muñoz F, Reyes F, Tormo JR, Genilloud O (2016) Multicomponent analysis of the differential induction of secondary metabolite profiles in fungal endophytes. Molecules 21:234–250CrossRefGoogle Scholar
  32. Guarro Artigas J (1983) Hongos coprófilos aislados en Cataluña. Ascomycetes. Anales Jard Bot Madrid 39:229–245Google Scholar
  33. Guarro J, Calvo MA, Ramirez C (1981) Soil ascomycetes from Catalunya (Spain). Nova Hedw 34:285–299Google Scholar
  34. Harris JP, Mantle PG (2001) Biosynthesis of ochratoxins by Aspergillus ochraceus. Phytochemistry 58:709–716CrossRefPubMedGoogle Scholar
  35. Hatori H, Shibata T, Nishikawa M, Ueda H, Hino M, Fujii T (2004) FR171456, a novel cholesterol synthesis inhibitor produced by Sporormiella minima no. 15604: II. Biological activities. J Antibiot 57:260–263CrossRefPubMedGoogle Scholar
  36. Hensens OD, Helms GL, Jones ETT, Harris GH (1995) Structure elucidation of australifungin, a potent inhibitor of sphinganine N-acyltransferase in sphingolipid biosynthesis from Sporormiella australis. J Org Chem 60:1772–1776CrossRefGoogle Scholar
  37. Höller U, König GM, Wright AD (1999) Three new metabolites from marine-derived fungi of the genera Coniothyrium and Microsphaeropsis. J Nat Prod 62:114–118CrossRefPubMedGoogle Scholar
  38. Johnson JH, Phillipson DW, Kahle AD (1989) The relative and absolute stereochemistry of the antifungal agent preussin. J Antibiot 42:1184–1185CrossRefPubMedGoogle Scholar
  39. Kim W, Peever TL, Park JJ, Park CM, Gang DR, Xian M, Davidson JA, Infantino A, Kaiser WJ, Chen W (2016) Use of metabolomics for the chemotaxonomy of legume-associated Ascochyta and allied genera. Sci Rep 6:20192CrossRefPubMedPubMedCentralGoogle Scholar
  40. Kinoshita K, Sasaki T, Awata M, Takada M, Yaginuma S (1997) Structure of sporostatin (M5032), an inhibitor of cyclic adenosine 3′,5′-monophosphate phosphodiesterase. J Antibiot 50:961–964CrossRefPubMedGoogle Scholar
  41. Kruys Å, Wedin M (2009) Phylogenetic relationships and an assessment of traditionally used taxonomic characters in the Sporormiaceae (Pleosporales, Dothideomycetes, Ascomycota), utilising multi-gene phylogenies. Syst Biodivers 7:465–478CrossRefGoogle Scholar
  42. Leyte-Lugo M, Figueroa M, del Carmen González M, Glenn AE, González-Andrade M, Mata R (2013) Metabolites from the entophytic fungus Sporormiella minimoides isolated from Hintonia latiflora. Phytochemistry 96:273–278Google Scholar
  43. Lundqvist NI (1960) Coprophilous ascomycetes from northern Spain. Svensk Bot Tidskr 54:523–529Google Scholar
  44. Mandala SM, Thornton RA, Frommer BR, Curotto JE, Rozdilsky W, Kurtz MB, Giacobbe RA, Bills GF, Cabello MA, Martín I, Peláez F, Harris GH (1995) The discovery of australifungin, a novel inhibitor of sphinganine N-acyltransferase from Sporormiella australis. Producing organism, fermentation, isolation, and biological activity. J Antibiot 48:349–356CrossRefPubMedGoogle Scholar
  45. Mapperson RR, Kotiw M, Davis RA, Dearnaley JD (2014) The diversity and antimicrobial activity of Preussia sp. endophytes isolated from Australian dry rainforests. Curr Microbiol 68:30–37CrossRefPubMedGoogle Scholar
  46. Massimo NC, Nandi Devan MM, Arendt KR, Wilch MH, Riddle JM, Furr SH, Steen C, U’Ren JM, Sandberg DC, Arnold AE (2015) Fungal endophytes in aboveground tissues of desert plants: infrequent in culture, but highly diverse and distinctive symbionts. Microb Ecol 70:61–76CrossRefPubMedPubMedCentralGoogle Scholar
  47. McGahren WJ and Mitscher LA (1968) Dihydroisocoumarins from a Sporormia fungus. J Org Chem 33:1577–1580 Google Scholar
  48. McGahren WJ, van den Hende JH, Mitscher LA (1969) Chlorinated cyclopentenone fungitoxic metabolites from the fungus, Sporormia affinis. J Am Chem Soc 91:157–162CrossRefPubMedGoogle Scholar
  49. Moreno-Arroyo B (2004) Inventario Micológico Básico de Andalucía. Consejería de Medio Ambiente, Junta de Andalucía, CórdobaGoogle Scholar
  50. Mudur SV, Gloer JB, Wicklow DT (2006) Sporminarins A and B: antifungal metabolites from a fungicolous isolate of Sporormiella minimoides. J Antibiot 59:500–506CrossRefPubMedGoogle Scholar
  51. Newcombe G, Campbell J, Griffith D, Baynes M, Launchbaugh K, Pendleton R (2016) Revisiting the life cycle of dung fungi, including Sordaria fimicola. PLoS One 11:e0147425CrossRefPubMedPubMedCentralGoogle Scholar
  52. Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274. doi: 10.1093/molbev/msu300 CrossRefPubMedGoogle Scholar
  53. Nirenberg HI (1976) Untersuchungen uber die morphologische und biologische Differenzierung in der Fusarium-Sektion Liseola. Mitt Biol Bundesanst Land-u Forstwirtsch (Berlin-Dahlem) 169:1–117Google Scholar
  54. Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala UniversityGoogle Scholar
  55. O’Donnell K (1993) Fusarium and its near relatives. In: Reynolds DR, Taylor JW (eds) The fungal holomorph: mitotic, meiotic and pleomorphic speciation in fungal systematics. CAB International, Wallingford, pp 225–233Google Scholar
  56. Oberwinkler F, Kirschner R, Arenal F, Villarreal M, Rubio V, Begerow D, Bauer R (2006) Two new pycnidial members of the Atractiellales: Basidiopycnis hyalina and Proceropycnis pinicola. Mycologia 98:637–649CrossRefPubMedGoogle Scholar
  57. Pérez-Victoria I, Martín J, Reyes F (2016) Combined LC/UV/MS and NMR strategies for the dereplication of marine natural products. Planta Med 82:857–871CrossRefPubMedGoogle Scholar
  58. Phukhamsakda C, Ariyawansa HA, Phillips AJL, Wanasinghe DN, Bhat DJ, McKenzie EHC, Singtripop C, Camporesi E, Hyde KD (2016) Additions to Sporormiaceae: introducing two novel genera, Sparticola and Forliomyces, from Spartium. Cryptogamie Mycol 37:75–97CrossRefGoogle Scholar
  59. Poch GK, Gloer JB (1991) Auranticins A and B: two new depsidones from a mangrove isolate of the fungus Preussia aurantiaca. J Nat Prod 54:213–217CrossRefPubMedGoogle Scholar
  60. Porras-Alfaro A, Herrera J, Sinsabaugh RL, Odenbach KJ, Lowrey T, Natvig DO (2008) Novel root fungal consortium associated with a dominant desert grass. Appl Environ Microbiol 74:2805–2813CrossRefPubMedPubMedCentralGoogle Scholar
  61. Robinson GW, O’Sullivan J, Meyers E, Wells JS, Del Mar JH (1988) Culpin. US patent US4914245AGoogle Scholar
  62. Rodriguez RJ, White JF Jr, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330CrossRefPubMedGoogle Scholar
  63. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574CrossRefPubMedGoogle Scholar
  64. Rukachaisirikul V, Buadam S, Sukpondma Y, Phongpaichit S, Sakayaroj J, Hutadilok-Towatana N (2013) Indanone and mellein derivatives from the Garcinia-derived fungus Xylaria sp. PSU-G12. Phytochem Lett 6:135–138CrossRefGoogle Scholar
  65. Sánchez-Márquez S, Bills GF, Herrero N, Zabalgogeazcoa Í (2012) Non-systemic fungal endophytes of grasses. Fungal Ecol 5:289–297CrossRefGoogle Scholar
  66. Sarrocco S (2016) Dung-inhabiting fungi: a potential reservoir of novel secondary metabolites for the control of plant pathogens. Pest Manag Sci 72:643–652CrossRefPubMedGoogle Scholar
  67. Sato T, Hanada T, Arioka M, Ando K, Sugiyama J, Uramoto M, Yamasaki M, Kitamoto K (1998) S19159, a modulator of neurite outgrowth produced by the ascomycete Preussia aemulans. I. Producing strain, fermentation, isolation and biological activity. J Antibiot (Tokyo) 51:897–901Google Scholar
  68. Schoch CL, Crous PW, Groenewald JZ, Boehm EW, Burgess TI, de Gruyter J (2009) A class-wide phylogenetic assessment of Dothideomycetes. Stud Mycol 64:1–15CrossRefPubMedPubMedCentralGoogle Scholar
  69. Schwartz RE, Liesch J, Hensens O, Zitano L, Honeycutt S, Garrity G, Fromtling RA, Onishi J, Monaghan R (1988) L-657,398, a novel antifungal agent: fermentation, isolation, structural elucidation and biological properties. J Antibiot 41:1774–1779CrossRefPubMedGoogle Scholar
  70. Sierra López D (1987) Aportación al conocimiento de los ascomicetes (Ascomycotina) de Cataluña. Societat Catalana de Micologia vol I, 481 ppGoogle Scholar
  71. Soláns MJ (1985) Tres especies del genero Preussia Fuckel (Sporormiella Ell. & Ev.). Novedades para el catalogo micológico español. Bol Soc Micol Castellana 9:29–36Google Scholar
  72. Soman AG, Gloer JB, Koster B, Malloch D (1999) Sporovexins A–C and a new preussomerin analog: antibacterial and antifungal metabolites from the coprophilous fungus Sporormiella vexans. J Nat Prod 62:659–661CrossRefPubMedGoogle Scholar
  73. Stadler M (2011) Importance of secondary metabolites in the Xylariaceae as parameters for assessment of their taxonomy, phylogeny, and functional biodiversity. Curr Res Environ Appl Mycol 1:75–133CrossRefGoogle Scholar
  74. Stadler M, Læssøe T, Fournier J, Decock C, Schmieschek B, Tichy H-V, Peršoh D (2014) A polyphasic taxonomy of Daldinia (Xylariaceae). Stud Mycol 77:1–143CrossRefPubMedPubMedCentralGoogle Scholar
  75. Talontsi FM, Lamshöft M, Douanla-Meli C, Kouam SF, Spiteller M (2014) Antiplasmodial and cytotoxic dibenzofurans from Preussia sp. harboured in Enantia chlorantha Oliv. Fitoterapia 93:233–238CrossRefPubMedGoogle Scholar
  76. Unamuno PLM (1941) Enumeración y distribución geográfica de los ascomicetos de la Península Ibérica y de las Islas Baleares. Men R Acad Madr, Ser Cienc Nat 8:1–403Google Scholar
  77. Urries MJ (1932) Datos sobre macromicetos de la provincia de Huesca. Bol Soc Esp His Nat 32:213–229Google Scholar
  78. Valldosera M, Guarro J (1990) Estudios sobre hongos coprófilos aislados en España. XV. El género Preussia (Sporormiella). Boletín de la Sociedad Micológica de Madrid 14:81–94Google Scholar
  79. von Arx JA (1973) Ostiolate and nonostiolate pyrenomycetes. Proc Kon Ned Akad Wet Ser C 76:289–296Google Scholar
  80. von Arx JA, Van der Aa HA (1987) Spororminula tenerifae gen. et sp. nov. Trans Br Mycol Soc 89:117–120CrossRefGoogle Scholar
  81. Wang Y, Gloer JB, Scott JA, Malloch D (1995) Terezines A–D: new amino acid-derived bioactive metabolites from the coprophilous fungus Sporormiella teretispora. J Nat Prod 58:93–99CrossRefPubMedGoogle Scholar
  82. Wang CY, Wang BG, Brauers G, Guan HS, Proksch P, Ebel R (2002) Microsphaerones A and B, two novel gamma-pyrone derivatives from the sponge-derived fungus Microsphaeropsis sp. J Nat Prod 65:772–775CrossRefPubMedGoogle Scholar
  83. Weber HA, Gloer JB (1988) Interference competition among natural fungal competitors: an antifungal metabolite from the coprophilous fungus Preussia fleischhakii. J Nat Prod 51:879–883CrossRefPubMedGoogle Scholar
  84. Weber HA, Gloer JB (1991) The preussomerins: novel antifungal metabolites from the coprophilous fungus Preussia isomera Cain. J Org Chem 56:4355–4360CrossRefGoogle Scholar
  85. Weber HA, Baenziger NC, Gloer JB (1990) Structure of preussomerin a: an unusual new antifungal metabolite from the coprophilous fungus Preussia isomera. J Am Chem Soc 112:6718–6719CrossRefGoogle Scholar
  86. Weber HA, Swenson DC, Gloer JB, Malloch D (1992) Similins A and B: new antifungal metabolites from the coprophilous fungus Sporormiella similis. Tetrahedron Lett 33:1157–1160CrossRefGoogle Scholar
  87. Xiong H, Xiao GK, Chen GD, Chen HR, Hu D, Li XX, Zhong SW, Guo LD, Yao XS, Gao H (2014) Sporormiellin A, the first tetrahydrofuran-fused furochromone with an unprecedented tetracyclic skeleton from Sporormiella minima. RSC Adv 46:24295–24299CrossRefGoogle Scholar
  88. Zaferanloo B, Bhattacharjee S, Ghorbani MM, Mahon PJ, Palombo EA (2014) Amylase production by Preussia minima, a fungus of endophytic origin: optimization of fermentation conditions and analysis of fungal secretome by LC-MS. BMC Microbiol 14:55CrossRefPubMedPubMedCentralGoogle Scholar
  89. Zhang F, Li L, Niu S, Si Y, Guo L, Jiang X, Che Y (2012) A thiopyranchromenone and other chromone derivatives from an endolichenic fungus, Preussia africana. J Nat Prod 75:230–237CrossRefPubMedGoogle Scholar

Copyright information

© German Mycological Society and Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Víctor Gonzalez-Menendez
    • 1
    Email author
  • Jesus Martin
    • 1
  • Jose A. Siles
    • 2
  • M. Reyes Gonzalez-Tejero
    • 3
  • Fernando Reyes
    • 1
  • Gonzalo Platas
    • 1
  • Jose R. Tormo
    • 1
  • Olga Genilloud
    • 1
  1. 1.Fundación MEDINA, Centro de Excelencia en Investigación de Medicamentos Innovadores en Andalucía, Parque Tecnológico de Ciencias de la Salud (PTS)GranadaSpain
  2. 2.Consejo Superior de Investigaciones Científicas, Estación Experimental del ZaidínGranadaSpain
  3. 3.Departamento de Botánica, Facultad de FarmaciaUniversidad de GranadaGranadaSpain

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