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Biodegradation of polycyclic aromatic hydrocarbons by Trichoderma species: a mini review

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Abstract

Fungi belonging to Trichoderma genus are ascomycetes found in soils worldwide. Trichoderma has been studied in relation to diverse biotechnological applications and are known as successful colonizers of their common habitats. Members of this genus have been well described as effective biocontrol organisms through the production of secondary metabolites with potential applications as new antibiotics. Even though members of Trichoderma are commonly used for the commercial production of lytic enzymes, as a biological control agent, and also in the food industry, their use in xenobiotic biodegradation is limited. Trichoderma stands out as a genus with a great range of substrate utilization, a high production of antimicrobial compounds, and its ability for environmental opportunism. In this review, we focused on the recent advances in the research of Trichoderma species as potent and efficient aromatic hydrocarbon-degrading organisms, as well as aimed to provide insight into its potential role in the bioremediation of soils contaminated with heavy hydrocarbons. Several Trichoderma species are associated with the ability to metabolize a variety of both high and low molecular weight polycyclic aromatic hydrocarbons (PAHs) such as naphthalene, phenanthrene, chrysene, pyrene, and benzo[a]pyrene. PAH-degrading species include Trichoderma hamatum, Trichoderma harzianum, Trichoderma reesei, Trichoderma koningii, Trichoderma viride, Trichoderma virens, and Trichoderma asperellum using alternate enzyme systems commonly seen in other organisms, such as multicooper laccases, peroxidases, and ring-cleavage dioxygenases. Within these species, T. asperellum stands out as a versatile organism with remarkable degrading abilities, high tolerance, and a remarkable potential to be used as a remediation agent in polluted soils.

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References

  • Acevedo F, Pizzul L, Castillo M del P, Cuevas R, Diez MC (2011) Degradation of polycyclic aromatic hydrocarbons by the Chilean white-rot fungus Anthracophyllum discolor. J Hazard Matter 185:212–219

  • Argumedo-Delira R, Alarcon A, Ferrera-Cerrato R, Almaraz JJ, Pena-Cabriales JJ (2012) Tolerance and growth of 11 Trichoderma strains to crude oil, naphthalene, phenanthrene and benzo[a]pyrene. J Environ Manag 95(Suppl):S291–S299

    Article  CAS  Google Scholar 

  • Atagana HI (2009) Biodegradation of PAHs by fungi in contaminated-soil containing cadmium and nickel ions. Afr J Biotechnol 8:5780–5789

    Google Scholar 

  • Balba MT (1993) Microorganisms and detoxification of industrial waste. In: Jones DG (ed) Exploitation of microorganisms. Springer, Netherlands, pp 371–410

    Chapter  Google Scholar 

  • Cazares-Garcia SV, Vazquez-Garciduenas MS, Vazquez-Marrufo G (2013) Structural and phylogenetic analysis of laccases from Trichoderma: a bioinformatic approach. PLoS One 8:e55295

    Article  CAS  Google Scholar 

  • Cerniglia CE, Sutherland GR (2010) Degradation of polycyclic aromatic hydrocarbons by fungi. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin, pp 2079–2110

    Chapter  Google Scholar 

  • Cobas M, Ferreira L, Tavares T, Sanroman MA, Pazos M (2013) Development of permeable reactive biobarrier for the removal of PAHs by Trichoderma longibrachiatum. Chemosphere 91:711–716

    Article  CAS  Google Scholar 

  • Cortes-Espinosa DV, Fernandez-Perrino FJ, Arana-Cuenca A, Esparza-Garcia F, Loera O, Rodriguez-Vazquez R (2006) Selection and identification of fungi isolated from sugarcane bagasse and their application for phenanthrene removal from soil. J Environ Sci Health A Tox Hazard Subst Environ Eng 41:475–486

    Article  CAS  Google Scholar 

  • Cristica M, Manoliu A, Barbaneagra T, Ciornea E (2010) Compared analysis of catalase and peroxidase activity in cellulolytic fungus Trichoderma reesei grown on medium with different concentrations of grinded wheat and barley straws. Stiint Univ Al I Cuza Iasi Sect II A Genet Biol Molec 12:89–93

  • Cunliffe M, Kertesz MA (2006) Effect of Sphingobium yanoikuyae B1 inoculation on bacterial community dynamics and polycyclic aromatic hydrocarbon degradation in aged and freshly PAH-contaminated soils. Environ Pollut 144:228–237

    Article  CAS  Google Scholar 

  • Chaineau CH, Morel J, Dupont J, Bury E, Oudot J (1999) Comparison of the fuel oil biodegradation potential of hydrocarbon-assimilating microorganisms isolated from a temperate agricultural soil. Sci Total Environ 227:237–247

    Article  CAS  Google Scholar 

  • Chutrakul C, Alcocer M, Bailey K, Peberdy JF (2008) The production and characterisation of trichotoxin peptaibols, by Trichoderma asperellum. Chem Biodivers 5:1694–1706

    Article  CAS  Google Scholar 

  • da Silva M, Cerniglia C, Pothuluri J, Canhos V, Esposito E (2003) Screening filamentous fungi isolated from estuarine sediments for the ability to oxidize polycyclic aromatic hydrocarbons. World J Microbiol Biotechnol 19:399–405

    Article  Google Scholar 

  • de los Santos-Villalobos S, Guzmán-Ortiz DA, Gómez-Lim MA, Gómez-Lim MA, Délano-Frier JP, de Folter S, Sánchez-García P, Peña-Cabriales JJ (2013) Potential use of Trichoderma asperellum (Samuels, Liechfeldt et Nirenberg) T8a as a biological control agent against anthracnose in mango (Mangifera indica L.). Biol Control 64:37–44

    Article  Google Scholar 

  • Ding G, Chen AJ, Lan J, Zhang HW, Chen XD, Liu XZ, Zou ZM (2012) Sesquiterpenes and cyclopeptides from the endophytic fungus Trichoderma asperellum Samuels, Lieckf & Nirenberg. Chem Biodivers 9:1205–1212

    Article  CAS  Google Scholar 

  • Druzhinina IS, Kopchinskiy AG, Kubicek CP (2006) The first 100 Trichoderma species characterized by molecular data. Mycoscience 47:55–64

    Article  CAS  Google Scholar 

  • Druzhinina IS, Seidl-Seiboth V, Herrera-Estrella A, Horwitz BA, Kenerley CM, Monte E, Mukherjee PK, Zeilinger S, Grigoriev IV, Kubicek CP (2011) Trichoderma: the genomics of opportunistic success. Nat Rev Microbiol 9:749–759

    Article  CAS  Google Scholar 

  • Field JA, Baten H, Boelsma F, Rulkens WH (1996) Biological elimination of polycyclic aromatic hydrocarbons in solvent extracts of polluted soil by the white rot fungus, Bjerkandera sp. Strain BOS55. Environ Technol 17:317–323

  • Hadibarata T, Tachibana S, Itoh K (2007) Biodegradation of phenanthrene by fungi screened from nature. Pak J Biol Sci 10:2535–2543

    Article  CAS  Google Scholar 

  • Hamzah D, Zain MA, Omar O, Senafi S (2012) Optimal physical and nutrient parameters for growth of Trichoderma virens UKMP-1M for heavy crude oil degradation. Sains Malays 41:71–79

    CAS  Google Scholar 

  • Harman GE, Lorito M, Lynch JM (2004) Uses of Trichoderma spp. to alleviate or remediate soil and water pollution. Adv Appl Microbiol 56:313–330

  • Hinga KR, Batchellor A (2005) Waste processing and detoxification. In: Hassan RM, Scholes R, Ash N (eds) Ecosystems and human well-being: current state and trends: findings of the condition and trends working group of the millennium ecosystem assessment. Island Press, Washington, pp 271–295

  • Hölker U, Dohse J, Höfer M (2002) Extracellular laccases in ascomycetes Trichoderma atroviride and Trichoderma harzianum. Folia Microbiol 47:423–427

    Article  Google Scholar 

  • Hughes KA, Bridge P, Clark MS (2007) Tolerance of Antarctic soil fungi to hydrocarbons. Sci Total Environ 372:539–548

    Article  CAS  Google Scholar 

  • Husaini A (2014) Bioremediation of crude oil by different fungal genera. Asian J Plant Biol 2:11–18

    Google Scholar 

  • Jaklitsch WM (2009) European species of Hypocrea part I. The green-spored species. Stud Mycol 63:1–91

    Article  Google Scholar 

  • Johnsen AR, Wick LY, Harms H (2005) Principles of microbial PAH-degradation in soil. Environ Pollut 133:71–84

    Article  CAS  Google Scholar 

  • Juhasz AL, Naidu R (2000) Bioremediation of high molecular weight polycyclic aromatic hydrocarbons: a review of the microbial degradation of benzo[a]pyrene. Int Biodeterior Biodegr 45:57–88

    Article  CAS  Google Scholar 

  • Kanaly RA, Harayama S (2000) Biodegradation of high-molecular-weight polycyclic aromatic hydrocarbons by bacteria. J Bacteriol 182:2059–2067

    Article  CAS  Google Scholar 

  • Lee H, Choi YS, Kim MJ, Huh NY, Kim GH, Lim YW, Kang SM, Cho ST, Kim JJ (2010) Degrading ability of oligocyclic aromates by Phanerochaete sordida selected via screening of white rot fungi. Folia Microbiol 55:447–453

    Article  CAS  Google Scholar 

  • Lee H, Jang Y, Choi Y, Kim M, Lee J, Lee H, Hong J, Lee YM, Kim G, Kim J (2014) Biotechnological procedures to select white rot fungi for the degradation of PAHs. J Microbiol Methods 97:56–62

    Article  CAS  Google Scholar 

  • Lee H, Jang Y, Yeong S, Jang S, Kim G, Kim J (2015) Bioremediation of polycyclic aromatic hydrocarbons in creosote-contaminated soil by Peniophora incarnata KUC8836. Biorem J 19:1–8

    Article  Google Scholar 

  • Matsubara M, Lynch JM, De Leij FAAM (2006) A simple screening procedure for selecting fungi with potential for use in the bioremediation of contaminated land. Enzyme Microb Technol 39:1365–1372

    Article  CAS  Google Scholar 

  • Mishra A, Nautiyal C (2009) Functional diversity of the microbial community in the rhizosphere of chickpea grown in diesel fuel-spiked soil amended with Trichoderma ressei using sole-carbon-source utilization profiles. World J Microbiol Biotechnol 25:1175–1180

    Article  CAS  Google Scholar 

  • Montgomery MT, Boyd TJ, Osburn CL, Smith DC (2010) PAH mineralization and bacterial organotolerance in surface sediments of the Charleston harbor estuary. Biodegradation 21:257–266

    Article  CAS  Google Scholar 

  • Ravelet C, Krivobok S, Sage L, Steiman R (2000) Biodegradation of pyrene by sediment fungi. Chemosphere 40:557–563

    Article  CAS  Google Scholar 

  • Reyes-Cesar A, Absalon AE, Fernandez FJ, Gonzalez JM, Cortes-Espinosa DV (2014) Biodegradation of a mixture of PAHs by non-ligninolytic fungal strains isolated from crude oil-contaminated soil. World J Microbiol Biotechnol 30:999–1009

    Article  CAS  Google Scholar 

  • Romero MC, Salvioli ML, Cazau MC, Arambarri AM (2002) Pyrene degradation by yeasts and filamentous fungi. Environ Pollut 117:159–163

    Article  CAS  Google Scholar 

  • Rosales E, Pérez-Paz A, Vázquez X, Pazos M, Sanromán MA (2012) Isolation of novel benzo[a]anthracene-degrading microorganisms and continuous bioremediation in an expanded-bed bioreactor. Bioprocess Biosyst Eng 35:851–855

    Article  CAS  Google Scholar 

  • Saraswathy A, Hallberg R (2002) Degradation of pyrene by indigenous fungi from a former gasworks site. FEMS Microbiol Lett 210:227–232

    Article  CAS  Google Scholar 

  • Sharon E, Chet I, Viterbo A, Bar-Eyal M, Nagan H, Samuels G, Spiegel Y (2007) Parasitism of Trichoderma on Meloidogyne javanica and role of the gelatinous matrix. Eur J Plant Pathol 118:247–258

    Article  Google Scholar 

  • Singh H (2006) Fungal metabolism of polycyclic aromatic hydrocarbons. In: Mycoremediation: fungal bioremediation. John Wiley & Sons, Inc., New Jersey, pp 283–356

  • Sivasithamparam K (1998) Root cortex—the final frontier for the biocontrol of root-rot with fungal antagonists: a case study on a sterile red fungus. Annu Rev Phytopathol 36:439–452

    Article  CAS  Google Scholar 

  • Slusarski C, Pietr SJ (2009) Combined application of dazomet and Trichoderma asperellum as an efficient alternative to methyl bromide in controlling the soil-borne disease complex of bell pepper. Crop Prot 28:668–674

    Article  CAS  Google Scholar 

  • Su SM, Zeng XB, Bai LY, Li LF, Duan R (2011) Arsenic biotransformation by arsenic-resistant fungi Trichoderma asperellum SM-12F1, Penicillium janthinellum SM-12F4, and Fusarium oxysporum CZ-8F1. Sci Total Environ 409:5057–5062

    Article  CAS  Google Scholar 

  • Thongkreda P, Lotrakula P, Prasongsuka S, Imaib T, Punnapayaka H (2011) Oxidation of polycyclic aromatic hydrocarbons by a tropical isolate of Pycnoporus coccineus and its laccase. ScienceAsia 37:225–233

    Article  Google Scholar 

  • Tondje PR, Roberts DP, Bon MC, Widmer T, Samuels GJ, Ismaiel A, Begoude AD, Tchana T, Nyemb-Tshomb E, Ndoumbe-Nkeng M, Bateman R, Fontem D, Hebbar KP (2007) Isolation and identification of mycoparasitic isolates of Trichoderma asperellum with potential for suppression of black pod disease of cacao in Cameroon. Biol Control 43:202–212

    Article  Google Scholar 

  • Van Gestel K, Mergaert J, Swings J, Coosemans J, Ryckeboer J (2003) Bioremediation of diesel oil-contaminated soil by composting with biowaste. Environ Pollut 125:361–368

    Article  Google Scholar 

  • Verdin A, Sahraoui AL, Durand R (2004) Degradation of benzo[a]pyrene by mitosporic fungi and extracellular oxidative enzymes. Int Biodeterior Biodegrad 53:65–70

    Article  CAS  Google Scholar 

  • Xu F, Deussen H-JW, Lopez B, Lam L, Li K (2001) Enzymatic and electrochemical oxidation of N-hydroxy compounds. Eur J Biochem 268:4169–4176

    Article  CAS  Google Scholar 

  • Zafra G, Absalón AE, Cuevas MC, Cortés-Espinosa DV (2014) Isolation and selection of a highly tolerant microbial consortium with potential for PAH biodegradation from heavy crude oil-contaminated soils. Water Air Soil Pollut 225:1826

    Article  Google Scholar 

  • Zafra G, Moreno-Montano A, Absalon AE, Cortes-Espinosa DV (2015a) Degradation of polycyclic aromatic hydrocarbons in soil by a tolerant strain of Trichoderma asperellum. Environ Sci Pollut Res 22:1034–1042

    Article  CAS  Google Scholar 

  • Zafra G, Absalon AE, Cortés-Espinosa DV (2015b) Morphological changes and growth of filamentous fungi in presence of high concentrations of PAHs. Braz J Microbiol 46:937–941

    Article  Google Scholar 

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Acknowledgments

This work was supported by the Consejo Nacional de Ciencia y Tecnología (CONACYT) project CB2008-105643, Instituto Politécnico Nacional projects SIP20131157, SIP20144071, and SIP20152025, and CONACYT grant 269828.

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  1. Instituto Politécnico Nacional, Centro de Investigación en Biotecnología Aplicada, Ex-Hacienda San Juan Molino, Carretera Estatal Tecuexcomac-Tepetitla Km 1.5, Tepetitla, 70900, Tlaxcala, México

    German Zafra & Diana V. Cortés-Espinosa

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  1. German Zafra
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  2. Diana V. Cortés-Espinosa
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Correspondence to German Zafra.

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Responsible editor: Robert Duran

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Zafra, G., Cortés-Espinosa, D.V. Biodegradation of polycyclic aromatic hydrocarbons by Trichoderma species: a mini review. Environ Sci Pollut Res 22, 19426–19433 (2015). https://doi.org/10.1007/s11356-015-5602-4

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  • DOI: https://doi.org/10.1007/s11356-015-5602-4

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