Peptaibol Profiles of Iranian Trichoderma Isolates

Abstract

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.

References

  1. 1.

    Biemann, K. (1990) Sequencing of peptides by tandem mass spectrometry and high-energy collisioninduced dissociation. Methods Enzymol. 193, 455–479.

    Article  CAS  PubMed  Google Scholar 

  2. 2.

    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.

    Article  CAS  Google Scholar 

  3. 3.

    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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. 4.

    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.

    Article  PubMed  Google Scholar 

  5. 5.

    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.

    Article  Google Scholar 

  6. 6.

    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.

    CAS  PubMed  PubMed Central  Google Scholar 

  7. 7.

    Chugh, J. K., Wallace, B. A. (2001) Peptaibols: models for ion channels. Biochem. Soc. Trans. 29, 565.

    Article  CAS  PubMed  Google Scholar 

  8. 8.

    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.

    Article  CAS  PubMed  Google Scholar 

  9. 9.

    Degenkolb, T., Brückner, H. (2008) Peptaibiomics: towards a myriad of bioactive peptides containing C(alpha)-dialkylamino acids? Chem. Biodivers. 5, 1817–1843.

    Article  CAS  PubMed  Google Scholar 

  10. 10.

    Grodnitskaya, I. D., Sorokin, N. D. (2006) Use of micromycetes Trichoderma for soil bioremediation in tree nurseries. Biol. Bull. 33, 400–403.

    Article  CAS  Google Scholar 

  11. 11.

    Ha, T. (2010) Using Trichoderma species for biological control of plant pathogens in Vietnam. ISSAAS J. 16, 17–21.

    Google Scholar 

  12. 12.

    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.

    Article  CAS  PubMed  Google Scholar 

  13. 13.

    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.

    Google Scholar 

  14. 14.

    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.

    CAS  PubMed  PubMed Central  Google Scholar 

  15. 15.

    Kredics, L., Antal, Z., Manczinger, L., Nagy, E. (2001) Breeding of mycoparasitic Trichoderma strains for heavy metal resistance. Lett. Appl. Microbiol. 33, 112–116.

    Article  CAS  PubMed  Google Scholar 

  16. 16.

    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.

    Google Scholar 

  17. 17.

    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.

    Google Scholar 

  18. 18.

    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.

    Article  CAS  PubMed  Google Scholar 

  19. 19.

    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.

    Article  CAS  PubMed  Google Scholar 

  20. 20.

    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.

    Article  CAS  PubMed  Google Scholar 

  21. 21.

    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.

    Article  CAS  PubMed  Google Scholar 

  22. 22.

    Marahiel, M. A., Stachelhaus T., Mootz, H. D. (1997) Modular peptide synthetases involved in nonribosomal peptide synthesis. Chem. Rev. 97, 2651–2674.

    Article  CAS  PubMed  Google Scholar 

  23. 23.

    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).

    Google Scholar 

  24. 24.

    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.

    Google Scholar 

  25. 25.

    Marik, T., Várszegi, C., Kredics, L., Vágvölgyi, C., Szekeres, A. (2013) Mass spectrometric investigation of alamethicin. Acta Biol. Szeged. 57, 109–112.

    Google Scholar 

  26. 26.

    Meyer, C. E., Reusser, F. (1967) A polypeptide antibacterial agent isolated from Trichoderma viride. Experientia 23, 85–86.

    Article  CAS  PubMed  Google Scholar 

  27. 27.

    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.

    Article  CAS  PubMed  Google Scholar 

  28. 28.

    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.

    Article  CAS  PubMed  Google Scholar 

  29. 29.

    Mueller, P., Rudin, D. O. (1968) Action potentials induced in biomolecular lipid membranes. Nature 217, 713–719.

    Article  CAS  PubMed  Google Scholar 

  30. 30.

    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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. 31.

    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.

    Google Scholar 

  32. 32.

    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.

    Article  CAS  PubMed  Google Scholar 

  33. 33.

    Payne, J. W., Jakes, R., Hartley, B. S. (1970) The primary structure of alamethicin. Biochem. J. 117, 757–766.

    CAS  PubMed  PubMed Central  Google Scholar 

  34. 34.

    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.

    Article  PubMed  Google Scholar 

  35. 35.

    Roepstorff, P., Fohlman, J. (1984) Proposal for a common nomenclature for sequence ions in mass spectra of peptides. Biomed. Mass. Spectrom. 11, 601.

    Article  CAS  PubMed  Google Scholar 

  36. 36.

    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.

    Article  CAS  PubMed  Google Scholar 

  37. 37.

    Schmoll, M., Schuster, A. (2010) Biology and biotechnology of Trichoderma. Appl. Microbiol. Biotechnol. 87, 787–799.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. 38.

    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.

    Article  CAS  Google Scholar 

  39. 39.

    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.

    Article  CAS  PubMed  Google Scholar 

  40. 40.

    Strieker, M., Tanović, A., Marahiel, M. A. (2010) Nonribosomal peptide synthetases: structures and dynamics. Curr. Opin. Struct. Biol. 20, 234–240.

    Article  CAS  PubMed  Google Scholar 

  41. 41.

    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.

    Article  CAS  PubMed  Google Scholar 

  42. 42.

    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.

    Article  Google Scholar 

  43. 43.

    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.

    Article  CAS  PubMed  Google Scholar 

  44. 44.

    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.

    Article  CAS  PubMed  Google Scholar 

  45. 45.

    Vinale, F., Sivasithamparam, K. E. A. (2012) Trichoderma secondary metabolites that affect plant metabolism. Nat. Prod. Commun. 7, 1545–1550.

    CAS  PubMed  Google Scholar 

  46. 46.

    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.

    Article  Google Scholar 

  47. 47.

    Weindling, R. (1932) Trichoderma lignorum as a parasite of other soil fungi. Phytopathology 22, 837–845.

    Google Scholar 

  48. 48.

    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.

    Article  CAS  PubMed  Google Scholar 

  49. 49.

    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.

  50. 50.

    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.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding authors

Correspondence to Doustmorad Zafari or László Kredics.

Rights and permissions

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Tamandegani, P.R., Zafari, D., Marik, T. et al. Peptaibol Profiles of Iranian Trichoderma Isolates. BIOLOGIA FUTURA 67, 431–441 (2016). https://doi.org/10.1556/018.67.2016.4.9

Download citation

Keywords

  • Trichoderma
  • peptaibol
  • antimicrobial activity
  • high performance liquid chromatography
  • electrospray ionization mass spectrometry