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The Trichoderma brevicompactum clade: a separate lineage with new species, new peptaibiotics, and mycotoxins

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Abstract

The Brevicompactum clade is recognized as a separate lineage in Trichoderma/Hypocrea. This includes T. brevicompactum and the new species T. arundinaceum, T. turrialbense, T. protrudens and Hypocrea rodmanii. The closest relative of the Brevicompactum clade is the Lutea clade. With the exception of H. rodmanii, all members of this clade produce the simple trichothecene-type toxins harzianum A or trichodermin. All members of the clade produce peptaibiotics, including alamethicins. Strains previously reported as T. harzianum (ATCC 90237), T. viride (NRRL 3199) or Hypocrea sp. (F000527, CBS 113214) to produce trichothecenes are reidentified as T. arundinaceum. The Brevicompactum clade is not closely related to species that have biological application.

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References

  • Adams PM, Hanson JR (1972) Sesquiterpenoid metabolites of Trichoderma polysporum and T. sporulosum. Phytochemistry 11:423

    Article  CAS  Google Scholar 

  • Auvin-Guette C, Rebuffat S, Prigent Y, Bodo B (1992) Trichogin A IV, an 11-residue lipopeptaibol from Trichoderma longibrachiatum. J Am Chem Soc 114:2170–2174

    Article  CAS  Google Scholar 

  • Auvin-Guette C, Rebuffat S, Vuidepot I, Massias M, Bodo B (1993) Structural elucidation of trichokoningins KA and KB, peptaibols from Trichoderma koningii. J Chem Soc Perkin Trans I:249–255

    Google Scholar 

  • Bamburg JR, Strong FM (1969) Mycotoxins of the trichothecane family produced by Fusarium tricinctum and Trichoderma lignorum. Phytochemistry 8:2405–2410

    Article  CAS  Google Scholar 

  • Bissett J (1991) A revision of the genus Trichoderma. III. Section Pachybasium. Can J Bot 69:2373–2417

    Article  Google Scholar 

  • Brückner H, Jung G (1980) Identification of N-acetyl-α-aminobutryic acid after selective trifluoroacetolysis of alamethicin and related peptide antibiotics. Chromatographia 13:170–174

    Article  Google Scholar 

  • Carbone I, Kohn LM (1999) A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91:553–556

    Article  CAS  Google Scholar 

  • Chaverri P, Samuels GJ (2003) Hypocrea/Trichoderma (Ascomycota, Hypocreales, Hypocreaceae): species with green ascospores. Stud Mycol 48:1–116

    Google Scholar 

  • Chaverri P, Bischoff JF, Hodge KT (2005) A new species of Hypocrella, H. macrostroma, and its relationship to other species with large stromata. Mycol Res 109:1268–1275

    Article  PubMed  Google Scholar 

  • Coats JH, Meyer CE, Reusser F (1974) Alamethicin and production therefor. Patent U.S.3833723 A61k 21/00 (424–118):1–8

  • Corley DG, Miller-Wideman M, Durley RC (1994) Isolation and structure of harzianum A: a new trichothecene from Trichoderma harzianum. J Nat Prod 57:442–425

    Google Scholar 

  • Cvetnić Z, Pepelnjak S (1997) Distribution and mycotoxin-producing ability of some fungal isolates from the air. Atmos Environ 31:491–495

    Article  Google Scholar 

  • Degenkolb T, Berg A, Gams W, Schlegel B, Gräfe U (2003) The occurrence of peptaibols and structurally related peptaibiotics and their mass spectrometric identification via diagnostic fragment ions. J Pept Sci 9:666–678

    Article  PubMed  CAS  Google Scholar 

  • Degenkolb T, Gräfenhan T, Nirenberg HI, Gams W, Brückner H (2006a) Trichoderma brevicompactum Complex: Rich source of novel and recurrent plant-protective polypeptide antibiotics. J Agric Food Chem 54:7047–7061

    Article  PubMed  CAS  Google Scholar 

  • Degenkolb T, Gräfenhan T, Berg A, Nirenberg HI, Gams W, Brückner H (2006b) Peptaibiomics: Screening for polypeptide antibiotics (Peptaibiotics) from plant-protective Trichoderma species. Chem Biodivers 3:593–610

    Article  PubMed  CAS  Google Scholar 

  • Degenkolb T, Kirschbaum J, Brückner H (2007) New sequences, constituents, and producers of peptaibiotics: an updated review. Chem Biodivers 4:1052–1067

    Article  CAS  Google Scholar 

  • Degenkolb T, von Döhren H, Nielsen KF, Samuels GJ, Brückner H (2008a) Recent advances and future prospects in peptaibiotics and mycotoxin research and their importance for chemotaxonomy of Trichoderma and Hypocrea. Chem Biodivers 5:671–680 doi:10.1002/cbdv.200890064 (May 20)

  • Degenkolb T, Gams W, Brückner H (2008b) Natural cyclo-peptaibiotics and related cyclo-tetrapeptides: structural diversity and future prospects. Chem Biodivers 5:693–706 doi:10.1002/cbdv.200890066

    Google Scholar 

  • Dettman JR, Jacobson DJ, Taylor JW (2003) A multilocus genealogical approach to phylogenetic species recognition in the model eukaryote Neurospora. Evolution 57:2703–2720

    PubMed  Google Scholar 

  • Dodd S, Lieckfeldt E, Chaverri P, Overton BE, Samuels GJ (2002) Taxonomy and phylogenetic relationships of two species of Hypocrea with Trichoderma anamorphs. Mycol Prog 1:409–428

    Article  Google Scholar 

  • Domsch KH, Gams W, Anderson T-H (2007) Compendium of soil fungi, 2nd taxonomically revised edition by W. Gams. IHW, Eching

  • Don RH, Cox PT, Wainwright BJ, Baker K, Mattick JS (1991) Touchdown PCR to circumvent spurious priming during gene amplification. Nucleic Acids Res 19:4008

    Article  PubMed  CAS  Google Scholar 

  • Evans HC, Holmes KA, Thomas SE (2003) Endophytes and mycoparasites associated with an indigenous forest tree, Theobroma gileri, in Equador and a preliminary assessment of their potential as biological control agents of cocoa diseases. Mycol Prog 2:149-160

    Article  Google Scholar 

  • Favilla M, Macchia L, Gallo A, Altomare C (2006) Toxicity assessment of fungal biocontrol agents using two different (Artemia salina and Daphnia magna) invertebrate bioassays. Food Chem Toxicol 44:1922–1931

    Article  PubMed  CAS  Google Scholar 

  • Fujita T, Wada S-I, Iida A, Nishimura T, Kanai M, Toyoma N (1994) Fungal metabolites. XIII. Isolation and structure elucidation of new peptaibols, trichodecenins-I and -II from Trichoderma viride. Chem Pharm Bull 42:489-494

    PubMed  CAS  Google Scholar 

  • Gilly M, Benson NR, Pellegrini M (1985) Affinity labeling the ribosome with eukaryotic-specific antibiotics - (bromoacetyl)trichodermin. Biochemistry 24:5787–5792

    Article  PubMed  CAS  Google Scholar 

  • Godtfredsen WO, Vangedal S (1964) Trichodermin, a new antibiotic related to trichothecin. Proc Chem Soc 1964:188–189

    Google Scholar 

  • Godtfredsen WO, Vangedal S (1965) Trichodermin, a new sesquiterpene antiobiotic. Acta Chem Scand 19:1088–1102

    Article  PubMed  CAS  Google Scholar 

  • Gräfenhan T (2006) Epidemiology and biological control of latent grapevine trunk diseases. PhD Thesis. Faculty of Agriculture and Horticulture, Humboldt-University Berlin, Germany. 138 pp

  • Hanada RE, de Souza JT, Pomella AWV, Hebbar KP, Pereira JO, Ismaiel A, Samuels GJ (2008) Trichoderma martiale sp. nov., a new endophyte from sapwood of Theobroma cacao with a potential for biological control. Mycol Res (In press)

  • Hawksworth DL (2001) The magnitude of fungal diversity, the 1.5 million estimate revisited. Mycol Res 105:1422–1432

    Article  Google Scholar 

  • Huang Q, Tezuka Y, Kikuchi T, Nishi A, Tubaki K, Tanaka K (1995) Studies on metabolites of mycoparasitic fungi. II. Metabolites of Trichoderma koningii. Chem Pharm Bull 43:223-229

    PubMed  CAS  Google Scholar 

  • Huelsenbeck JP (2000) MrBayes: Bayesian inferences of phylogeny (software). University of Rochester, New York

    Google Scholar 

  • Huelsenbeck JP, Ronquist F, Nielsen ES, Bollback JP (2001) Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294:2310–2314

    Article  PubMed  CAS  Google Scholar 

  • Jaklitsch WM, Samuels GJ, Dodd SL, Lu B-S, Druzhinina IS (2006) Hypocrea rufa/Trichoderma viride: a reassessment, and description of five closely related species with and without warted conidia. Stud Mycol 56:135-177

    Article  PubMed  Google Scholar 

  • Jin H-Z, Lee J-H, Zhang W-D, Lee H-B, Hong Y-S, Kim Y-H, Lee J-J (2007) Harzianums A and B produced by a fungal strain, Hypocrea sp. F000527, and their cytotoxicity against tumor cell lines. J Asian Nat Prod Res 9:203–207

    Article  PubMed  CAS  Google Scholar 

  • Kindermann J, El-Ayouti Y, Samuels GJ, Kubicek CP (1998) Phylogeny of the genus Trichoderma based on sequence analysis of the internal transcript spacer 1 of the rDNA cluster. Fungal Genet Biol 24:298-309

    Article  PubMed  CAS  Google Scholar 

  • Kirschbaum J, Krause C, Winzheimer RK, Brückner H (2003) Alamethicin sequences reconsidered and reconciled. J Pept Sci 9:799-809

    Article  PubMed  CAS  Google Scholar 

  • Kornerup A, Wanscher JH (1978) Methuen handbook of colour, 3rd edn. Eyre Methuen, London

    Google Scholar 

  • Kraus GF, Druzhinina I, Gams W, Bissett J, Zafari D, Szakacs G, Koptchinski A, Prillinger H, Zare R, Kubicek CP (2004) Trichoderma brevicompactum sp. nov. Mycologia 96:1059-1073

    Article  Google Scholar 

  • Krause C, Kirschbaum J, Brückner H (2006) Peptaibiomics: an advanced, rapid and selective analysis of peptaibiotics/peptaibols by SPE/LC-ES-MS. Amino Acids 30:435-443

    Article  PubMed  CAS  Google Scholar 

  • Kubicek CP, Baker S, Gamauf C, Kennerley CM, Druzhinina IS (2008) Purifying selection and birth-and-death evolution in the class II hydrophobin gene families of the ascomycete Trichoderma/Hypocrea. BMC Evol Biol 8:4 doi:10.1186/1471-2148-8-4

  • Küsters E, Portmann A (1994) Enantiomeric separation of amino alcohols by gas chromatography on a chiral stationary phase; influence of the perfluoroacetylating reagent on the separation. J High Resolut Chromatogr 17:639-642

    Article  Google Scholar 

  • Laatsch H (2007) AntiBase 2007. The natural compound identifier. Wiley, Weinheim, Germany

    Google Scholar 

  • Landreau A, Pouchus YF, Sallenave-Namont C, Biard J-F, Boumard M-C, Robiou Du Pont T, Mondeguer F, Goulard C, Verbist J-F (2002) Combined use of LC/MS and a biological test for rapid identification of marine mycotoxins produced by Trichoderma koningii. J Microbiol Methods 48:181-194

    Article  PubMed  CAS  Google Scholar 

  • Lee HB, Kim Y, Jin HZ, Lee JJ, Kim C-J, Park JY, Jung HS (2005) A new Hypocrea strain producing harzianum A cytotoxic to tumour cell lines. Lett Appl Microbiol 40:497-503

    Article  PubMed  CAS  Google Scholar 

  • Leitgeb B, Szekeres A, Manczinger A, Vágvölgyi C, Kredics L (2007) The history of alamethicin: a review of the most extensively studied peptaibol. Chem Biodivers 4:1027-1051

    Article  PubMed  CAS  Google Scholar 

  • Liao LL, Grollman AP, Horwitz SB (1976) Mechanism of action of 12,13-epoxytrichothecene, anguidine, an inhibitor of protein-synthesis. Biochim Biophys Acta 454:273–284

    PubMed  CAS  Google Scholar 

  • Linder MB, Szilvay GR, Nakari-Setälä T, Penttilä ME (2005) Hydrophobins: the protein-amphiphiles of filamentous fungi. FEMS Microbiol Rev 29:877-896

    Article  PubMed  CAS  Google Scholar 

  • Liu YJ, Whelen S, Hall BD (1999) Phylogenetic relationships among Ascomycetes: Evidence from an RNA polymerase II subunit. Mol Biol Evol 16:1799-1808

    PubMed  CAS  Google Scholar 

  • Lorito M, Farkas V, Rebuffat S, Bodo B, Kubicek CP (1996) Cell wall synthesis is a major target of mycoparasitic antagonism by Trichoderma harzianum. J Bacteriol 178:6382–6385

    PubMed  CAS  Google Scholar 

  • Maddison DR, Maddison WM (2005) MacClade 4 Analysis of phylogeny and character evolution (version 4.06). Sinauer Associates, Sunderland Mass. http://macclade.org/index.html

  • Mason-Gamer RJ, Kellogg EA (1996) Testing for phylogenetic conflict among molecular data sets in the tribe Triticeae (Gramineae). Syst Biol 45:524–545

    Article  Google Scholar 

  • Mau B, Newton M, Larget B (1999) Bayesian phylogenetic inference via Markov chain Monte Carlo methods. Biometrics 55:1–12

    Article  PubMed  CAS  Google Scholar 

  • Mohamed-Benkada M, Montagu M, Biard JF, Modeguer F, Vérité P, Dalgalarrondo M, Bissett J, Pouchus YF (2006) New short peptaibols from a marine Trichoderma strain. Rapid Comm Mass Spectrometry 20:1176–1180

    Article  CAS  Google Scholar 

  • Neuhof T, Dieckmann R, Druzhinina IS, Kubicek CP, von Döhren H (2007a) Intact-cell MALDI-TOF mass spectrometry analysis of peptaibol formation by the genus Trichoderma/Hypocrea: can molecular phylogeny of species predict peptaibol structures? Microbiology 153:3417-3437

    Article  PubMed  CAS  Google Scholar 

  • Neuhof T, Dieckmann R, Druzhinina IS, Kubicek CP, Nakari-Setälä T, Penttilä M, von Döhren H (2007b) Direct identification of hydrophobins and their processing in Trichoderma using Intact-Cell MALDI-TOF mass spectrometry. FEBS J 274:841-852

    Article  PubMed  CAS  Google Scholar 

  • New AP, Eckers C, Haskins NJ, Neville WA, Elson S, Hueso-Rodriguez JA, Rivera-Sagredo A (1996) Structures of polysporins A-D, four new peptaibols isolated from Trichoderma polysporum. Tetrahedron Lett 37:3039-3042

    Article  CAS  Google Scholar 

  • Nielsen KF, Gräfenhan T, Zafari D, Thrane U (2005) Trichothecene production by Trichoderma brevicompactum. J Agric Food Chem 53:8190-8196

    Article  PubMed  CAS  Google Scholar 

  • Nirenberg H (1976) Untersuchungen über die morphologische und biologische Differenzierung in der Fusarium-Sektion Liseola. Mitt Biol Bundesanst Land- Forstwirtsch Berlin-Dahlem 169:1-117

    Google Scholar 

  • Oh S-U, Yun B-S, Kim J-H, Yoo I-D (2002) Atroviridins A-C and neoatroviridins A-D, novel peptaibol antibiotics produced by Trichoderma atroviride F80317. J Antibiot 55:557-564

    PubMed  CAS  Google Scholar 

  • Poirier L, Quiniou F, Ruiz N, Montagu M, Amiard J-C, Pouchus YF (2007) Toxicity assessment of peptaibols and contaminated sediments on Crassostrea gigas embryos. Aquat Toxicol 83:254–262

    Article  PubMed  CAS  Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:917-918

    Article  Google Scholar 

  • Psurek A, Neusüss C, Degenkolb T, Brückner H, Balaguer E, Imhof D, Scriba GKE (2006) Detection of new amino acid sequences of alamethicins F30 by nonaqueous capillary electrophoresis-mass spectrometry. J Pept Sci 12:279–290

    Article  PubMed  CAS  Google Scholar 

  • Rambaut A, Drummond A (2004) TRACER v 1.2.1. http://evolve.zoo.ox.ac.uk/software.html?id5tracer

  • Rannala B, Yang Z (1996) Probability distribution of molecular evolutionary trees: a new method of phylogenetic interference. J Mol Evol 43:304–311

    Article  PubMed  CAS  Google Scholar 

  • Rebuffat S, Goulard C, Bodo B (1995) Antibiotic peptides from Trichoderma harzianum: harzianins HC, proline-rich 14-residue peptaibols. J Chem Soc Perkin Trans I:1849-1855

  • Reeb V, Lutzoni F, Roux C (2004) Contribution of RPB2 to multilocus phylogenetic studies of the Euascomycetes (Pezizomycotina, Fungi) with special emphasis on lichen-forming Acarosporaceae and evolution of polyspory. Mol Phylogenet Evol 32:1036–1060

    Article  PubMed  CAS  Google Scholar 

  • Ruiz N, Wielgoz-Collin G, Poirier L, Grovel O, Petit KE, Mohamed-Benkada M, Robiou Du Pont T, Bissett J, Vérité P, Barnathan G, Pouchus YF (2007) New trichobrachins, 11-residue peptaibols from a marine strain of Trichoderma longibrachiatum. Peptides 28:1351–1358

    Article  PubMed  CAS  Google Scholar 

  • Saikawa Y, Okamoto H, Inui T, Makabe M, Okuno T, Suda T, Hashimoto K, Nakata M (2001) Toxic principles of a poisonous mushroom Podostroma cornu-damae. Tetrahedron 57:8277–8281

    Article  CAS  Google Scholar 

  • Sallenave C, Pouchus YF, Bardouil M, Lassus P, Roquebert F, Verbist J-F (1999) Bioaccumulation of mycotoxins by shellfish: contamination of mussels by metabolites of a Trichoderma koningii strain isolated in the marine environment. Toxicon 37:77–83

    Article  PubMed  CAS  Google Scholar 

  • Samuels GJ (2006) Trichoderma: systematics, the sexual state and ecology. Phytopathology 96:195–206

    Article  CAS  Google Scholar 

  • Samuels GJ, Dodd SL, Gams W, Castlebury LA, Petrini O (2002) Trichoderma species associated with the green mold epidemic of commercially grown Agaricus bisporus. Mycologia 94:146–170

    Article  Google Scholar 

  • Samuels GJ, Dodd S, Lu B-S, Petrini O, Schroers H-J, Druzhinina IS (2006) The Trichoderma koningii aggregate species. Stud Mycol 56:67–133

    Article  PubMed  Google Scholar 

  • Sivasithamparam K, Ghisalberti EL (1998) Secondary metabolism in Trichoderma and Gliocladium. In: Kubicek CP, Harman GE (eds) Trichoderma and Gliocladium. Volume 1. Basic biology, taxonomy, and genetics. Francis & Taylor, London, pp 139–191

    Google Scholar 

  • Swofford DL (2002) PAUP*: Phylogenetic analysis using parsimony (*and other methods). Version 4.06b10. Sinauer Associates, Sunderland, Mass.

    Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface; flexible strategies for multiple sequence alignmjent aided by quality analysis tools. Nucleic Acids Res 24:4876–4882

    Article  Google Scholar 

  • Viterbo A, Chet I (2006) TasHyd1, a new hydrophobin gene from the biocontrol agent Trichoderma asperellum, is involved in plant root colonization. Mol Plant Pathol 7:249-258

    Article  CAS  Google Scholar 

  • Watts R, Dahiya J, Chaudhary K, Tauro P (1988) Isolation and characterization of a new antifungal metabolite of Trichoderma reesei. Plant Soil 107:81–84

    Article  CAS  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: aguide to methods and applications. Academic Press, San Diego, pp 315–322

    Google Scholar 

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Acknowledgments

Dr. James L. Swezey, USDA-ARS, NCAUR, provided culture NRRL 3199. Dr. Harry Evans and CABI-BioScience provided endophytic cultures. CBS and BBA provided additional cultures; we especially acknowledge Ms. Trix Merckx (CBS) for her assistance in receiving and dispatching cultures. Latin descriptions were kindly corrected by Prof. Dr. Ferdinand R. Prostmeier (Justus Liebig Universität, Gießen, Germany). Financial support by the Studienstiftung Mykologie (Cologne, Germany), the Erwin-Stein-Stiftung (Gießen, Germany), the Danish Research Council for Technology and Production Sciences (26-04-0050) and the Centre for Advanced Food Studies (LMC) (Copenhagen, Denmark) is gratefully acknowledged.

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Correspondence to Gary J. Samuels.

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Hypocrea rodmanii Samuels & Chaverri, Trichoderma arundinaceum Zafari, Gräfenhan & Samuels, Trichoderma protrudens Samuels & Chaverri, Trichoderma turrialbense Samuels, Degenkolb, K.F. Nielsen & Gräfenhan.

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Degenkolb, T., Dieckmann, R., Nielsen, K.F. et al. The Trichoderma brevicompactum clade: a separate lineage with new species, new peptaibiotics, and mycotoxins. Mycol Progress 7, 177–219 (2008). https://doi.org/10.1007/s11557-008-0563-3

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