Abstract
Up to 300,000 potentially unique mycotoxins were reported by the Council of Agricultural Science Technology in 2003. Nevertheless, little information is available on fungal biological control agents (FBCAs) that have been developed or are being developed. The knowledge on fungal secondary metabolites and their toxicological significance depends on what is already known in the published scientific literature or in few cases becomes apparent by chance from high throughput screening programmes during product development. The purpose of this chapter is to describe what data basis is most frequently used for a routine evaluation of fungal metabolites and their residues in FBCAs. A decision scheme is discussed, which should be used to assess metabolite toxicity in the context of a worst-case scenario testing. This risk assessment procedure will help to identify the low risk, if any, of old and newly developed microbial pest control agents, and give support to applicants to market their FBCAs.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Aly AH, Edrada-Ebel R, Wray V, Muller WEG, Kozytska S, Hentschel U, Proksch P, Ebel R (2008) Bioactive metabolites from the endophytic fungus Ampelomyces sp. isolated from the medicinal plant urospermum picroides. Phytochem 69:1716–1725
Aneja M, Gianfagna TJ, Hebbar PK (2005) Trichoderma harzianum produces nonanoic acid, an inhibitor of spore germination and mycelial growth of two cacao pathogens. Physiol Molecular Plant Pathol 67:304–307
Anitha R, Murugesan K (2005) Production of gliotoxin on natural substrates by Trichoderma virens. J Basic Microbiol 45:12–19
Baker DD, Chu M, Oza U, Rajgarhia V (2007) The value of natural products to future pharmaceutical discovery. Nat Prod Rep 24:1225–1244
Boss D, Maurhofer M, Schläpfer E, Défago G (2007) Elsinochrome A production by the bindweed biocontrol fungus Stagonospora convolvuli LA39 does not pose a risk to the environment or the consumer of treated crops. FEMS Microbiol Ecol 59:194–205
Bruckner H, Koza A (2003) Solution phase synthesis of the 14-residue peptaibol antibiotic trichovirin I. Amino Acids 24:311–323
Butt TM (2002) Use of entomogenous fungi for the control of insect pests. In: Kempken F (ed) The Mycota XI agricultural applications. Springer, Berlin, pp 111–134
Butt TM, Jackson C, Magan N (2001) Fungi as biocontrol agents: progress, problems and potential. CABI, Wallingford, CT
Butt TM, Skrobek A, Wang C, Shah FA, El Hadj NB (2004) RAFBCA Report P1 Final. EU RTD project (QLK1-2001-01391) Risk assessment of fungal biological control agents. University Swansea, Swansea
CAN (2007) Registration decision. Health Canada Pest Management Regulatory Agency. RD2007-06. http://www.pmra-arla.gc.ca/english/pdf/rdd/rd2007-06-e.pdf. Accessed 4 Jun 2007
Calvo AM, Wilson RA, Bok JW, Keller NP (2002) Relationship between secondary metabolism and fungal development. Microbiol Mol Biol Rev 66:447–459
Cheng YL, Mcnally DJ, Labbe C, Voyer N, Belzile F, Belanger RR (2003) Insertional mutagenesis of a fungal biocontrol agent led to discovery of a rare cellobiose lipid with antifungal activity. Appl Environ Microbiol 69:2595–2602
Chovanec P, Kalinak M, Liptaj T, Pronayova N, Jakubik T, Hudecova D, Varecka L (2005) Study of Trichoderma viride metabolism under conditions of the restriction of oxidative processes. Can J Microbiol 51:853–862
Cole RJ, Jarvis BB, Schweikert MA (2003) Handbook of secondary fungal metabolites, vol III. Academic, Amsterdam
Cole RJ, Schweikert MA (2003a) Handbook of secondary fungal metabolites, vol I. Academic, Amsterdam
Cole RJ, Schweikert MA (2003b) Handbook of secondary fungal metabolites, vol II. Academic, Amsterdam
EU (1991) EC Directive 91/414/EC. Off J Eur Union 1999 L 0414
EU (2001a) EC Directive 2001/36/EC. Off J Eur Union L 164/1
EU (2001b) EC Directive 2001/47/EC. Off J Eur Union L 175/21
EU (2003) EC Directive 2003/79/EC. Off J Eur Union 14.6.2003
EU (2004) EC Regulation 2229/2004. Off J Eur Union L 379/13
EU (2005a) EC Directive 2005/2/EC. Off J Eur Union L 20/15
EU (2005b) SANCO/10383/2004 – rev. 4. Off J Eur Union OJ No L 020
EU (2007a) EC Regulation 1097/2007. Off J Eur Union L 246/31
EU (2007b) EC Directive 2007/380/EC. Off J Eur Union 2.6.2007
EU (2008a) EC Directive 2008/113/EC. Off J Eur Union L 330/6
EU (2008b) EC Directive 2008/565/EC. Off J Eur Union L 181/49
EU (2008c) EC Directive 2008/44/EC. Off J Eur Union L 94/13
El-Hasan A, Walker F, Buchenauer H (2008) Trichoderma harzianum and its metabolite 6-pentyl-alpha-pyrone suppress fusaric acid produced by Fusarium moniliforme. J Phytopathol 156:79–87
Evidente A, Cabras A, Maddau L, Serra S, Andolfi A, Motta A (2003) Viridepyronone, a new antifungal 6-substituted 2 h-pyran-2-one produced by Trichoderma viride. J Agri Food Chem 51(24):6957–6960
Favilla M, Macchia L, Gallo A, Altomare C (2006) Toxicity assessment of metabolites of fungal biocontrol agents using two different (Artemia salina and Daphnia magna) invertebrate bioassays. Food Chem Toxicol 44:1922–1931
Femenia-Rios M, Garcia-Pajon CM, Hernandez-Galan R, Macias-Sanchez AJ, Collado IG (2006) Synthesis and free radical scavenging activity of a novel metabolite from the fungus Colletotrichum gloeosporioides. Bioorg Med Chem Let 16:5836–5839
Ganassi S, De Cristofaro A, Grazioso P, Altomare C, Logrieco A, Sabatini MA (2007) Detection of fungal metabolites of various Trichoderma species by the aphid Schizaphis graminum. Entomol Exper Applic 122(1):77–86
Goettel MS, Hajek AE, Siegel JP, Evans HC (2001) Safety of fungal biocontrol agents. In: Butt TM, Jackson C, Magan N (eds) Fungi as biocontrol agents: progress, problems and potential. CABI, Wallingford, CT, pp 347–375
Hoffmeister D, Keller NP (2007) Natural products of filamentous fungi: enzymes, genes, and their regulation. Nat Prod Rep 24:393–416
Holmes E, Tang HR, Wang YL, Seger C (2006) The Assessment of plant metabolite profiles by NMR-based methodologies. Planta Med 72:771–785
Inacio ML, Silva GH, Teles HL, Trevisan HC, Cavalheiro AJ, Bolzani VDS, Young MCM, Pfenning LH, Araujo AR (2006) Antifungal metabolites from Colletotrichum gloeosporioides, an endophytic fungus in Cryptocarya mandioccana Nees (Lauraceae). Biochem Syst Ecol 34:822–824
Kabaluk T, Gazdik K (2005) Directory of microbial pesticides for agricultural crops in OECD countries. http://www4.agr.gc.ca/resources/prod/doc/pmc/pdf/micro_e.pdf. Accessed 14 Feb 2008
Krasnoff SB, Keresztes I, Gillilan RE, Szebenyi DME, Donzelli BGG, Churchill ACL, Gibson DM (2007) Serinocyclins A and B, cyclic heptapeptides from Metarhizium anisopliae. J Nat Prod 70:1919–1924
Krasnoff SB, Sommers CH, Moon YS, Donzelli BGG, Vandenberg JD, Churchill ACL, Gibson DM (2006) Production of mutagenic metabolites by Metarhizium anisopliae. J Agri Food Chem 54:7083–7088
Krasnoff SB, Sommers CH, Moon YS, Donzelli BGG, Vandenberg JD, Churchill ACL, Gibson DM (2008) Production of mutagenic metabolites by Metarhizium anisopliae (Vol 54, Pg 7083, 2006). J Agri Food Chem 56:1158
Laengle T, Strasser H (2010) Developing a risk index to comparatively assess environmental risks posed by microbial and conventional pest control agents. Biocont Sci Technol 20(7):659–681
Lee SY, Kinoshita H, Ihara F, Igarashi Y, Nihira T (2008) Identification of novel derivative of helvolic acid from Metarhizium anisopliae grown in medium with insect component. J Biosci Bioeng 105:476–480
McQuilken MP, Gemmell J, Hill RA, Whipps JM (2003) Production of macrosphelide a by the mycoparasite Coniothyrium minitans. FEMS Microbiol Let 219:27–31
Moon YS, Donzelli BGG, Krasnoff SB, Mclane H, Griggs MH, Cooke P, Vandenberg JD, Gibson DM, Churchill ACL (2008) Agrobacterium-mediated disruption of a nonribosomal peptide synthetase gene in the invertebrate pathogen Metarhizium anisopliae reveals a peptide spore factor. Appl Environ Microbiol 74(14):4366–4380
Nielsen KF, Smedsgaard J (2003) Fungal metabolite screening: database of 474 mycotoxins and fungal metabolites for dereplication by standardised liquid chromatography-UV-mass spectrometry methodology. J Chrom A 1002:111–136
OECD (2004) Appendix 6b part 4. Dossier Guidance for Microbials, Series on Pesticides No. 23. http://www.oecd.org/dataoecd/26/57/27766483.pdf. Accessed 16 Sept 2008
OECD (2007) Biological pesticide registration. Environment Directorate. http://www.oecd.org/document/8/0,2340,en_2649_34383_31962760_1_1_1_1,00.html. Accessed 20 Jun 2007
Reino JL, Guerro RF, Hernández-Galán R, Collado IG (2008) Secondary metabolites from species of the biocontrol agent Trichoderma. Phytochem Rev 7:89–123
Rochon D, Belliveau B (2006) OECD Issue Paper – Discussion on microbial metabolite residues in treated food crops. http://www.rebeca-net.de/downloads/DRAFT%20OECD%20ISSUE%20PAPER%20CONTAMINATIONS.pdf. Accessed 7 Aug 2007
Seger C, Sturm S (2007) Analytical aspects of plant metabolite profiling platforms: current standings and future aims. J Proteome Res 6:480–497
Skrobek A, Boss D, Defago G, Butt TM, Maurhofer M (2006) Evaluation of different biological test systems to assess the toxicity of metabolites from fungal biocontrol agents. Toxicol Lett 161:43–52
Skrobek A, Butt TM (2005) Toxicity testing of destruxins and crude extracts from the insect-pathogenic fungus Metarhizium anisopliae. FEMS Microbiol Lett 251:23–28
Strasser H, Altomare C, Typas M, Butt TM (2008) REBECA proposal on the assessment of microbial metabolites. In: Ehlers RU, Enkerli J, Glazer I, Lopez-Ferber M, Thaczuk C (eds) Insect pathogens and Insect Nematodes. IOBC Bull 31:21–26
Strasser H, Typas M, Altomare C, Butt TM (2007) Annex 7: Position paper on microbial metabolite assessment. In: Strauch O, Strasser H, Ehlers RU, Hausschild R (eds) Deliverable 10: Proposals for improved regulatory procedures for microbial BCAs. http://www.rebeca-net.de/downloads/report/deliverable%2010.pdf. Accessed 28 Feb 2008
Strasser H, Vey A, Butt TM (2000) Are there any risks in using entomopathogenic fungi for pest control, with particular reference to the bioactive metabolites of Metarhizium, Tolypocladium and Beauveria species?. Biocont Sci Technol 10:717–735
Strobel G (2006) Muscodor albus and its biological promise. J Ind Microbiol Biotechnol 33:514–522
Thomson Reuters (2008) ISI Web of knowledge. http://isiwebofknowledge.com/. Accessed 16 Sept 2008
US EPA (1999a) Beauveria bassiana ATCC 74040 (128818) Fact sheet. http://www.epa.gov/oppbppd1/biopesticides/ingredients/factsheets/factsheet_128818.htm. Accessed 17 Jan 2011
US EPA (1999b) Paecilomyces fumosoroseus Apopka Strain 97 (115002) Fact sheet. http://www.epa.gov/pesticides/biopesticides/ingredients/factsheets/factsheet_115002.htm. Accessed 17 Jan 2011
US EPA (2000a) Beauveria bassiana strain GHA (128924) Fact sheet. http://www.epa.gov/oppbppd1/biopesticides/ingredients/tech_docs/tech_128924.htm. Accessed 17 Jan 2011
US EPA (2000b) Candida oleophila isolate I-182 (021008) Fact sheet. http://www.epa.gov/oppbppd1/biopesticides/ingredients/factsheets/factsheet_021008.htm. Accessed 17 Jan 2011
US EPA (2000c) Gliocladium virens GL-21 (129000) Fact sheet. http://www.epa.gov/oppbppd1/biopesticides/ingredients/factsheets/factsheet_129000.htm. Accessed 17 Jan 2011
US EPA (2000d) Trichoderma harzianum Rifai Strain T-39 (119200) Fact sheet. http://www.epa.gov/opp00001/biopesticides/ingredients/factsheets/factsheet_119200.htm. Accessed 17 Jan 2011
US EPA (2000e) Trichoderma polysporum ATCC 20475 (128902) Trichoderma harzianum ATCC 20476 (128903) Fact sheet. http://www.epa.gov/oppbppd1/biopesticides/ingredients/factsheets/factsheet_128902.htm. Accessed 17 Jan 2011
US EPA (2001a) Metarhizium anisopliae strain ESF1 (129056) Fact sheet. http://www.epa.gov/oppbppd1/biopesticides/ingredients/factsheets/factsheet_129056.htm. Accessed 17 Jan 2011
US EPA (2001b) Trichoderma harzianum Rifai Strain T-22 (ATCC # 20847) (119202) Fact sheet. http://www.epa.gov/pesticides/biopesticides/ingredients/factsheets/factsheet_119202.htm. Accessed 17 Jan 2011
US EPA (2001c). Coniothyrium minitans CON/M/91-08 (028836) Fact sheet. http://www.epa.gov/Â oppbppd1/biopesticides/ingredients/factsheets/factsheet_028836.htm. Accessed 17 Jan 2011
US EPA (2002a) Beauveria bassiana strain 447 (128815) Fact sheet. http://www.epa.gov/oppbppd1/biopesticides/ingredients/factsheets/factsheet_128815.htm. Accessed 17 Jan 2011
US EPA (2002b) Gliocladium catenulatum strain J1446 (021009) Fact sheet. http://www.epa.gov/oppbppd1/biopesticides/ingredients/factsheets/factsheet_021009.htm. Accessed 17 Jan 2011
US EPA (2002c) Pseudozyma flocculosa strain PF-A22 UL (119196) Fact http://www.epa.gov/oppbppd1/biopesticides/ingredients/factsheets/factsheet_119196.htm. Accessed 17 Jan 2011
US EPA (2002d) Puccinia thlaspeos strain woad (dyer’s woad rust) (006489) Fact sheet. http://www.epa.gov/pesticides/biopesticides/ingredients/factsheets/factsheet_006489.htm. Accessed 17 Jan 2011
US EPA (2003a) Aspergillus flavus strain AF36 (006456) Fact sheet. http://epa.gov/oppbppd1/biopesticides/ingredients/factsheets/factsheet_006456.htm. Accessed 17 Jan 2011
US EPA (2003b) Metarhizium anisopliae strain F52 (029056) Biopesticide fact sheet. http://www.epa.gov/pesticides/biopesticides/ingredients/factsheets/factsheet_029056.htm. Accessed 17 Jan 2011
US EPA (2004) Aspergillus flavus NRRL 21882 (006500) Fact sheet. http://www.epa.gov/oppbppd1/biopesticides/ingredients/factsheets/factsheet_006500.htm. Accessed 17 Jan 2011
US EPA (2005a) Alternaria destruens Strain 059 (028301) Fact sheet. http://www.epa.gov/oppbppd1/biopesticides/ingredients/factsheets/factsheet_028301.htm. Accessed 17 Jan 2011
US EPA (2005b) Biopesticide Registration Action Document Verticillium Isolate WCS850 (PC Code). http://epa.gov/pesticides/biopesticides/ingredients/tech_docs/brad_081305.pdf. Accessed 17 Jan 2011
US EPA (2005c) Chondrostereum purpureum strain HQ1 (081309) Fact sheet. http://www.epa.gov/oppbppd1/biopesticides/ingredients/factsheets/factsheet_081309.htm. Accessed 17 Jan 2011
US EPA (2005d) Muscodor albus QST 20799 (006503) Fact sheet. http://www.epa.gov/oppbppd1/biopesticides/ingredients/factsheets/factsheet_006503.htm Accessed 17 Jan 2011
US EPA (2005e) Paecilomyces lilacinus strain 251 (028826) Fact sheet. http://www.epa.gov/oppbppd1/biopesticides/ingredients/factsheets/factsheet_028826.htm. Accessed 17 Jan 2011
US EPA (2006a) Beauveria bassiana HF23 (090305) Fact sheet. http://www.epa.gov/oppbppd1/biopesticides/ingredients/factsheets/factsheet_090305.htm. Accessed 17 Jan 2011
US EPA (2006b) Biopesticide registration Document Beauveria bassiana HF23 (PC Code 090305). http://www.epa.gov/oppbppd1/biopesticides/ingredients/tech_docs/brad_090305.pdf. Acessed 17 Jan 2011
US EPA (2006c) Colletotrichum gleoesporiodes f.sp. aeschynomene (226300) Biopesticides registration action document. http://www.epa.gov/oppbppd1/biopesticides/ingredients/tech_docs/brad_226300.htm. Accessed 17 Jan 2011
US EPA (2007a) New Biopesticide Active Ingredients – 2007. http://www.epa.gov/oppbppd1/biopesticides/product_lists/new_ai_2007.htm. Accessed 24 Jan 2008
US EPA (2007b) Pythium oligandrum DV 74 (028816) Fact sheet. http://epa.gov/oppbppd1/biopesticides/ingredients/factsheets/factsheet_028816.htm. Accessed 17 Jan 2011
Vey A, Hoagland RE, Butt TM (2001) Toxic metabolites of fungal biocontrol agents. In: Butt TM, Jackson C, Magan N (eds) Fungi as biocontrol agents: progress, problems and potential. CABI, Wallingford, CT, pp 311–346
Vinale F, Marra R, Scala F, Ghisalberti EL, Lorito M, Sivasithamparam K (2006) Major secondary metabolites produced by two commercial Trichoderma strains active against different phytopathogens. Lett Appl Microbiol 43:143–148
Xu YQ, Zhan JX, Wijeratne EMK, Burns AM, Gunatilaka AAL, Molnar L (2007) Cytotoxic and antihaptotactic beauvericin analogues from precursor-directed biosynthesis with the insect pathogen Beauveria bassiana ATCC 7159. J Nat Prod 70:1467–1471
Zhang HY, Xie HH, Qiu SX, Xue JH, Wei XY (2008) Heteroatom-containing antibacterial phenolic metabolites from a terrestrial Ampelomyces fungus. Biosci Biotechnol Biochem 72:1746–1749
Acknowledgements
This work was supported by the European Commission, Specific Support Action SSPE-022709. The authors are indebted to the RAFBCA team (QLK1-CT2001-01391) to provide the actual reference list on metabolites. We also wish to thank Claudio Altomare (ISPA Bari), Rüdiger Hausschild (GAB Consulting, Lamstedt), and Olaf Strauch (University Kiel) for their helpful discussion and kindly reviewing the manuscript
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2011 Springer Netherlands
About this chapter
Cite this chapter
Strasser, H., Hutwimmer, S., Burgstaller, W. (2011). Metabolite Toxicology of Fungal Biocontrol Agents. In: Ehlers, RU. (eds) Regulation of Biological Control Agents. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-3664-3_9
Download citation
DOI: https://doi.org/10.1007/978-90-481-3664-3_9
Published:
Publisher Name: Springer, Dordrecht
Print ISBN: 978-90-481-3663-6
Online ISBN: 978-90-481-3664-3
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)