Five Iranian Trichoderma isolates from species T. viride, T. viridescens, T. asperellum, T. longibrachiatum and T. citrinoviride — selected from the Fungal Collection of the Bu Ali Sina University, Hamedan, Iran — were investigated for their peptaibol production. All examined isolates showed remarkable antibacterial activities during the screening of their extracts for peptaibol content with a Micrococcus luteus test culture. HPLC-ESI-IT MS was used for identification and elucidation of the amino acid sequences of peptaibols. The detected peptaibol compounds contain 20 or 18 amino acid residues and belong to the trichobrachin and trichotoxin groups of peptaibols, respectively. T. longibrachiatum and T. citrinoviride produced trichobrachins, while trichotoxins could be detected in T. viride, T. viridescens and T. asperellum. Out of 37 sequences detetermined, 26 proved to be new, yet undescribed compounds, while others were identified as previously reported trichotoxins (trichotoxin A-50s and T5D2) and trichobrachins (longibrachins AI, AII, AIII, BII and BIII). Compounds within the two groups of detected peptaibols differed from each other only by a single or just a few amino acid changes.
Biemann, K. (1990) Sequencing of peptides by tandem mass spectrometry and high-energy collisioninduced dissociation. Methods Enzymol. 193, 455–479.
Boheim, G., Irmscher, G., Jung, G. (1978) Trichotoxin A-40, a new membrane-exciting peptide. Part B. Voltage-dependent pore formation in bilayer lipid membranes and comparison with other alamethicin analogues. Biochim. Biophys. Acta –Biomem. 507, 485–506.
Brito, J. P., Ramada, M. H., De Magalhães, M. T., Silva, L. P., Ulhoa, C. J. (2014) Peptaibols from Trichoderma asperellum TR356 strain isolated from Brazilian soil. SpringerPlus 3, 600.
Brückner, H., König, W. A., Aydin, M, J. G. (1985) Trichotoxin A40. Purification by counter-current distribution and sequencing of isolated fragments. Biochim. Biophys. Acta 827, 51–62.
Brückner, H., Przybylski, M. (1984) Isolation and structural characterization of polypeptide antibiotics of the peptaibol class by high-performance liquid chromatography with field desorption and fast atom bombardment mass spectrometry. J. Chromatogr. 296, 263–275.
Chiang, Y. M., Lee, K. H., Sanchez, J. F., Keller, N. P., Wang, C. C. (2009) Unlocking fungal cryptic natural products. Nat. Prod. Commun. 4, 1505–1510.
Chugh, J. K., Wallace, B. A. (2001) Peptaibols: models for ion channels. Biochem. Soc. Trans. 29, 565.
Chutrakul, C., Alcocer, M., Bailey, K., Peberdy, J. F. (2008) The production and characterisation of trichotoxin peptaibols, by Trichoderma asperellum. Chem. Biodivers. 5, 1694–1706.
Degenkolb, T., Brückner, H. (2008) Peptaibiomics: towards a myriad of bioactive peptides containing C(alpha)-dialkylamino acids? Chem. Biodivers. 5, 1817–1843.
Grodnitskaya, I. D., Sorokin, N. D. (2006) Use of micromycetes Trichoderma for soil bioremediation in tree nurseries. Biol. Bull. 33, 400–403.
Ha, T. (2010) Using Trichoderma species for biological control of plant pathogens in Vietnam. ISSAAS J. 16, 17–21.
Harman, G. E., Howell, C. R., Viterbo, A., Chet, I., Lorito, M. (2004) Trichoderma species –opportunistic, avirulent plant symbionts. Nat. Rev. Microbiol. 2, 43–56.
Hatvani, L., Manczinger, L., Vágvölgyi, C., Kredics, L. (2013) Trichoderma as a human pathogen. In: Mukherjee, P. K., Horwitz, B. A., Singh, U. S., Mukherjee, M., Schmoll, M. (eds) Trichoderma –Biology and Applications. CAB International, Wallingford, UK. pp. 292–313.
Hou, C. T., Ciegler, A., Hesseltine, C. W. (1972) New mycotoxin, trichotoxin A, from Trichoderma viride isolated from southern leaf blight-infected corn. Appl. Microbiol. 23, 183–185.
Kredics, L., Antal, Z., Manczinger, L., Nagy, E. (2001) Breeding of mycoparasitic Trichoderma strains for heavy metal resistance. Lett. Appl. Microbiol. 33, 112–116.
Kredics, L., García Jimenez, L., Naeimi, S., Czifra, D., Urbán, P., Manczinger, L., Vágvölgyi, C., Hatvani, L. (2010) A challenge to mushroom growers: the green mould disease of cultivated champignons. In: Méndez-Vilas, A. (ed.) Current Research, Technology and Education Topics in Applied Microbiology and Microbial Biotechnology. Formatex Research Center, Badajoz, Spain. pp. 295–305.
Kredics, L., Hatvani, L., Naeimi, S., Körmöczi, P., Manczinger, L., Vágvölgyi, C., Druzhinina, I. (2014) Biodiversity of the genus Hypocrea/Trichoderma in different habitats. In: Gupta, V. K., Schmoll, M., Herrera-Estrella, A., Upadhyay, R. S., Druzhinina, I., Tuohy, M. (eds) Biotechnology and Biology of Trichoderma. Elsevier Science B. V., Amsterdam, The Netherlands. pp. 3–24.
Kubicek, C. P., Komon-Zelazowska, M., Sándor, E., Druzhinina, I. S. (2007) Facts and challenges in the understanding of the biosynthesis of peptaibols by Trichoderma. Chem. Biodivers. 4, 1068–1082.
Leclerc, G., Goulard, C., Prigent, Y., Bodo, B., Wróblewski, H., Rebuffat, S. (2001) Sequences and antimycoplasmic properties of longibrachins LGB II and LGB III, two novel 20-residue peptaibols from Trichoderma longibrachiatum. J. Nat. Prod. 64, 164–170.
Leitgeb, B., Szekeres, A., Manczinger, L., Vágvölgyi, C., Kredics, L. (2007) The history of alamethicin: a review of the most extensively studied peptaibol. Chem. Biodivers. 4, 1027–1051.
Lorito, M., Woo, S. L., Garcia, I., Colucci, G., Harman, G. E., Pintor-Toro, J. A., Scala, F. (1998) Genes from mycoparasitic fungi as a source for improving plant resistance to fungal pathogens. Proc. Natl Acad. Sci. USA 95, 7860–7865.
Marahiel, M. A., Stachelhaus T., Mootz, H. D. (1997) Modular peptide synthetases involved in nonribosomal peptide synthesis. Chem. Rev. 97, 2651–2674.
Marik, T., Szekeres, A., Druzhinina, I. S., Andersson, M. A., Salkinoja-Salonen, M., Tyagi, C., Leitgeb, B., Vágvölgyi, C., Kredics, L. (2016) Bioactive peptaibols of forest-derived Trichoderma isolates from section Longibrachiatum. In: Lukac, M., Grenni, P., Gamboni, M. (eds) Soil Biological Communities and Ecosystem Resilience, “Sustainability in Plant and Crop Protection”, Springer Int. Publ. AG, Cham (WWW), Switzerland (in press).
Marik, T., Szekeres, A., Várszegi, C., Czifra, D., Vágvölgyi, C., Kredics, L. (2013) Rapid bioactivitybased pre-screening method for the detection of peptaibiotic-producing Trichoderma strains. Acta Biol. Szeged 57, 1–7.
Marik, T., Várszegi, C., Kredics, L., Vágvölgyi, C., Szekeres, A. (2013) Mass spectrometric investigation of alamethicin. Acta Biol. Szeged. 57, 109–112.
Meyer, C. E., Reusser, F. (1967) A polypeptide antibacterial agent isolated from Trichoderma viride. Experientia 23, 85–86.
Mikkola, R., Andersson, M. A., Kredics, L., Grigoriev, P. A., Sundell, N., Salkinoja-Salonen, M. S. (2012) 20-Residue and 11-residue peptaibols from the fungus Trichoderma longibrachiatum are synergistic in forming Na+/K+-permeable channels and adverse action towards mammalian cells. FEBS J. 279, 4172–4190.
Mohamed-Benkada, M., Montagu, M., Biard, J. F., Mondeguer, F., Verite, P., Dalgalarrondo, M., Bissett, J., Pouchus, Y. F. (2006) New short peptaibols from a marine Trichoderma strain. Rapid Commun. Mass Spectrom. 20, 1176–1180.
Mueller, P., Rudin, D. O. (1968) Action potentials induced in biomolecular lipid membranes. Nature 217, 713–719.
Mukherjee, P. K., Wiest, A., Ruiz, N., Keightley, A., Moran-Diez, M. E., McCluskey, K., Pouchus, Y. F., Kenerley, C. M. (2010) Two classes of new peptaibols are synthesized by a single non-ribosomal peptide synthetase of Trichoderma virens. J. Biol. Chem. 286, 4544–4554.
Nelson, E. B. (2004) Biological control of Oomycetes and fungal pathogens. In: Goodman, R. M. (ed.) Encyclopedia of Plant and Crop Science. Marcell Dekker Inc., New York, USA. pp. 137–140.
Neumann, N. K. N., Stoppacher, N., Zeilinger, S., Degenkolb, T., Brückner, H., Schuhmacher, R. (2015) The peptaibiotics database –a comprehensive online resource. Chem. Biodivers. 12, 743–751.
Payne, J. W., Jakes, R., Hartley, B. S. (1970) The primary structure of alamethicin. Biochem. J. 117, 757–766.
Pócsfalvi, G., Ritieni, A., Ferranti, P., Randazzo, G., Vékey, K., Malorni, A. (1997) Microheterogeneity characterization of a paracelsin mixture from Trichoderma reesei using high-energy collision-induced dissociation tandem mass spectrometry. Rapid Commun. Mass Spectrom. 11, 922–930.
Roepstorff, P., Fohlman, J. (1984) Proposal for a common nomenclature for sequence ions in mass spectra of peptides. Biomed. Mass. Spectrom. 11, 601.
Ruiz, N., Petit, K., Vansteelandt, M., Kerzaon, I., Baudet, J., Amzil, Z., Biard, J.-F., Grovel, O., Pouchus, Y. F. (2010) Enhancement of domoic acid neurotoxicity on Diptera larvae bioassay by marine fungal metabolites. Toxicon 55, 805–810.
Schmoll, M., Schuster, A. (2010) Biology and biotechnology of Trichoderma. Appl. Microbiol. Biotechnol. 87, 787–799.
Shakeri, J., Foster, H. (2007) Proteolytic activity and antibiotic production by Trichoderma harzianum in relation to pathogenicity to insects. Enzyme Microb. Technol. 40, 961–968.
Stoppacher, N., Neumann, N. K., Burgstaller, L., Zeilinger, S., Degenkolb, T., Brückner, H., Schuhmacher, R. (2013) The comprehensive peptaibiotics database. Chem. Biodivers. 10, 734–743.
Strieker, M., Tanovic, A., Marahiel, M. A. (2010) Nonribosomal peptide synthetases: structures and dynamics. Curr. Opin. Struct. Biol. 20, 234–240.
Suwan, S., Isobe, M., Kanokmedhakul, S., Lourit, N., Kanokmedhakul, K., Soytong, K., Koga, K. (2000) Elucidation of high micro-heterogeneity of an acidic-neutral trichotoxin mixture from Trichoderma harzianum by electrospray ionization quadrupole time-of-flight mass spectrometry. J. Mass Spectrom. 35, 1438–1451.
Szabó, M., Csepregi, K., Gálber, M., Virányi, F., Fekete, C. (2012) Control plant-parasitic nematodes with Trichoderma species and nematode-trapping fungi: The role of chi18-5 and chi18-12 genes in nematode egg-parasitism. Biol. Control 63, 121–128.
Szekeres, A., Leitgeb, B., Kredics, L., Antal, Z, Hatvani, L., Manczinger, L., Vágvölgyi, C. (2005) Peptaibols and related peptaibiotics of Trichoderma –a review. Acta Microbiol. Immunol. Hung. 52, 137–168.
Verma, V. C., Gond, S. K., Kumar, A., Kharwar, R. N., Strobel, G. (2007) The endophytic mycoflora of bark, leaf, and stem tissues of Azadirachta indica A. Juss (neem) from Varanasi (India). Microb. Ecol. 54, 119–125.
Vinale, F., Sivasithamparam, K. E. A. (2012) Trichoderma secondary metabolites that affect plant metabolism. Nat. Prod. Commun. 7, 1545–1550.
Vinale, F., Sivasithamparam, K., Ghisalberti, E. L., Woo, S. L., Nigro, M., Marra, R., Lombardi, N., Pascale, A., Ruocco, M., Lanzuise, S., Manganiello, G., Lorito, M. (2014) Trichoderma secondary metabolites active on plants and fungal pathogens. Open Mycol. J. 8, 127–139.
Weindling, R. (1932) Trichoderma lignorum as a parasite of other soil fungi. Phytopathology 22, 837–845.
Whitmore, L., Chugh, J. K., Snook, C. F., Wallace, B. A. (2003) The peptaibol database: a sequence and structure resource. J. Pept. Sci. 9, 663–665.
Whitmore, L., Wallace, B. A. (2004) The peptaibol database: a database for sequences and structures of naturally occurring peptaibols. Nucl. Acids Res. 32, D593–D594.
Wiest, A., Grzegorski, D., Xu, B.-W., Goulard, C., Rebuffat, S., Ebbole, D. J., Bodo, B., Kenerley, C. (2002) Identification of peptaibols from Trichoderma virens and cloning of a peptaibol synthetase. J. Biol. Chem. 277, 20862–20868.