Applied Microbiology and Biotechnology

, Volume 103, Issue 17, pp 7203–7215 | Cite as

Biodegradation of polycyclic aromatic hydrocarbons by native Ganoderma sp. strains: identification of metabolites and proposed degradation pathways

  • Giselle Torres-FarradáEmail author
  • Ana M. Manzano-León
  • François Rineau
  • Miguel Ramos Leal
  • Sofie Thijs
  • Inge Jambon
  • Jenny Put
  • Jan Czech
  • Gilda Guerra Rivera
  • Robert Carleer
  • Jaco Vangronsveld
Environmental biotechnology


Since polycyclic aromatic hydrocarbons (PAHs) are mutagenic, teratogenic, and carcinogenic, they are of considerable environmental concern. A biotechnological approach to remove such compounds from polluted ecosystems could be based on the use of white-rot fungi (WRF). The potential of well-adapted indigenous Ganoderma strains to degrade PAHs remains underexplored. Seven native Ganoderma sp. strains with capacity to produce high levels of laccase enzymes and to degrade synthetic dyes were investigated for their degradation potential of PAHs. The crude enzymatic extracts produced by Ganoderma strains differentially degraded the PAHs assayed (naphthalene 34—73%, phenanthrene 9—67%, fluorene 11—64%). Ganoderma sp. UH-M was the most promising strain for the degradation of PAHs without the addition of redox mediators. The PAH oxidation performed by the extracellular enzymes produced more polar and soluble metabolites such as benzoic acid, catechol, phthalic and protocatechuic acids, allowing us to propose degradation pathways of these PAHs. This is the first study in which breakdown intermediates and degradation pathways of PAHs by a native strain of Ganoderma genus were determined. The treatment of PAHs with the biomass of this fungal strain enhanced the degradation of the three PAHs. The laccase enzymes played an important role in the degradation of these compounds; however, the role of peroxidases cannot be excluded. Ganoderma sp. UH-M is a promising candidate for the bioremediation of ecosystems polluted with PAHs.


Polycyclic aromatic hydrocarbons Ganoderma sp. Laccase Intermediate metabolites Degradation pathways 



The authors are grateful to the financial support of the following grants: the BOF-BILA grant from Hasselt University for G. Torres-Farradá, the UHasselt Methusalem project 08M03VGRJ and to the International Foundation for Sciences (IFS, Sweden) (grant F/4442-2). The authors are also grateful to the technical support of Carine Put and Ann Wijgaerts.

Funding information

This work was supported by a BOF BILA grant from Hasselt University for G. Torres Farradá, by the UHasselt Methusalem project 08M03VGRJ, and by the International Foundation for Sciences (IFS, Sweden) (grant F/4442-2).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

No ethical approval is required since this article does not have studies with animals or humans.

Supplementary material

253_2019_9968_MOESM1_ESM.pdf (196 kb)
ESM 1 (PDF 196 kb)


  1. Acevedo F, Pizzulb L, Pilar Castillo M, Cuevas R, Diez MC (2011) Degradation of polycyclic aromatic hydrocarbons by the Chilean white-rot fungus Anthracophyllum discolor. J Hazard Mater 185:212–219CrossRefGoogle Scholar
  2. Agrawal N, Verma P, Shahi SK (2018) Degradation of polycyclic aromatic hydrocarbons (phenanthrene and pyrene) by the ligninolytic fungi Ganoderma lucidum isolated from the hardwood stump. Bioresour Bioprocess 5:11. CrossRefGoogle Scholar
  3. Almaguer M, Rojas-Flores T, Rodríguez-Rajo J, Aira MJ (2014) Airborne basidiospores of Coprinus and Ganoderma in a Caribbean region. Aerobiologia 30:197–204CrossRefGoogle Scholar
  4. Arun A, PraveenRaja P, Arthi R, Ananthi M, Sathish Kumar K, Eyini M (2008) Polycyclic aromatic hydrocarbons (PAHs) biodegradation by basidiomycetes fungi, Pseudomonas isolate, and their cocultures: comparative in vivo and in silico approach. Appl Biochem Biotechnol 151:132–142CrossRefGoogle Scholar
  5. Baldrian P (2006) Fungal laccases-occurrence and properties. FEMS Microbiol Rev 30(2):215–242CrossRefGoogle Scholar
  6. Berrin JG, Navarro D, Couturier M, Olivé C, Grisel S, Haon M, Taussac S, Lechat C, Courtecuisse R, Favel AP, Coutinho L, Lesage-Meessena A (2012) Exploring the natural fungal biodiversity of tropical and temperate forests toward improvement of biomass conversion. Appl Environ Microbiol 78(18):6483–6490CrossRefGoogle Scholar
  7. Bezalel L, Hadar Y, Cerniglia C (1996) Mineralization of polycyclic aromatic hydrocarbons by the white rot fungus Pleurotus ostreatus. Appl Environ Microbiol 62(1):292–295Google Scholar
  8. Bogan BW, Lahner LM, Sullivan WR, Paterek JR (2003) Degradation of straight-chain aliphatic and high-molecular-weight polycyclic aromatic hydrocarbons by a strains of Mycobacterium austroafricanum. J Appl Microbiol 94:230–239CrossRefGoogle Scholar
  9. Cabarroi M, Maldonado S, Castillo L (2008) Hongos del Jardín Botánico nacional de Cuba. Revista del Jardín Botánico Nacional 29:161–169Google Scholar
  10. Ceci A, Pinzari F, Russo F, Persiani AM, Gadd M (2018) Roles of saprotrophic fungi in biodegradation or transformation of organic and inorganic pollutants in co-contaminated sites. Appl Microbiol Biotechnol 103:53–68. CrossRefGoogle Scholar
  11. Chupungars K, Rerngsamran P, Thaniyavarn S (2009) Polycyclic aromatic hydrocarbons degradation by Agrocybe sp. CU-43 and its fluorene transformation. Int Biodeterior Biodegradation 63(1):93–99CrossRefGoogle Scholar
  12. Claiborne A, Fridovich I (1979) Purification of the o-dianisidine peroxidase from Escherichia coli. Physicochemical characterization and analysis of its dual catalatic and peroxidatic activities. J Biol Chem 254:4245–4252Google Scholar
  13. Fadzil M, Mohd T, Mohd W, Darul KN (2008) Concentration and distribution of polycyclic aromatic hydrocarbons (PAHs) in the town of Kota Bharu. Malay J Anal Sci 12(3):609–618Google Scholar
  14. Field JA, Jong E, Feijoo Costa G, Bont JA (1992 Jul) Biodegradation of polycyclic aromatic hydrocarbons by new isolates of white rot fungi. Appl Environ Microbiol 58(7):2219–2226Google Scholar
  15. Hadibarata T, Tachibana S (2009) Identification of phenanthrene metabolites produced by Polyporus sp. S133. Interdisciplinary studies on environmental chemistry—environmental research in Asia. In: Obayashi Y, Isobe T, Subramanian A, Suzuki S, Tanabe S, pp 293–299Google Scholar
  16. Hadibarata T, Yusoff ARM, Aris A, Kristanti RA (2012) Identification of naphthalene metabolism by white rot fungus Armillaria sp. Folia Microbiol 58(5):385–391. CrossRefGoogle Scholar
  17. Hadibarata T, Fikri M, Zubir A, Rubiyatno L, Chuang T, Mohd A, Razman M, Salim Mohammad A (2013) Degradation and transformation of anthracene by white-rot fungus Armillaria sp. F022. Folia Microbiol 58:385–391. CrossRefGoogle Scholar
  18. Hammel KE, Gai WZ, Green B, Moen MA (1992) Oxidative degradation of phenanthrene by the ligninolytic fungus Phanerochaete chrysosporium. Appl Environ Microbiol 58:1832–1818Google Scholar
  19. Haritash AK, Kaushik CP (2009) Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review. J Hazard Mater 169:1–15CrossRefGoogle Scholar
  20. Husain Q (2006) Potential Applications of the oxidoreductive enzymes in the decolorization and detoxification of textile and other synthetic dyes from polluted water: a review. Crit Rev Biotechnol 26(4):201–221CrossRefGoogle Scholar
  21. Kanaly RA, Harayama S (2000) Biodegradation of high molecular weight polycyclic aromatic hydrocarbons by bacteria. J Bacteriol 182:2059–2067CrossRefGoogle Scholar
  22. Khammuang S, Sarnthima R (2009) Laccase activity from fresh fruiting bodies of Ganoderma sp. MK05: purification and remazol brilliant blue R decolorization. J Biol Sci 9(1):83–87CrossRefGoogle Scholar
  23. Levin L, Melignani E, Ramos A (2010) Effect of nitrogen sources and vitamins on ligninolytic enzyme production by some white-rot fungi. Dye decolorization by selected culture filtrates. Bioresour Technol 101:4554–4563CrossRefGoogle Scholar
  24. Lin C, Gan S, Kiat H (2011) Fenton based remediation of polycyclic aromatic hydrocarbons-contaminated soils. Chemosphere 83:1414–1430CrossRefGoogle Scholar
  25. Majeau JA, Brar SK, Tyagi R (2010) Laccases for removal of recalcitrant and emerging pollutants. Bioresour Technol 101:2331–2350CrossRefGoogle Scholar
  26. Malarczyk E, Kochmanska-Rdest J, Jarosz-Wilkolazka A (2009) Influence of very low doses of mediators on fungal laccase activity-nonlinearity beyond imagination. Nonlinear Biomed Phys 3:10. CrossRefGoogle Scholar
  27. Manavalan T, Manavalan A, Kalaichelvan P, Thangavelua P, Heesed K (2013) Characterization of optimized production, purification and application of laccase from Ganoderma lucidum. Biochem Eng J 70:106–114CrossRefGoogle Scholar
  28. Manoli E, Kouras A, Karagkiozidou O, Argyropoulos G, Voutsa D, Samara C (2016) Polycyclic aromatic hydrocarbons (PAHs) at traffic and urban background sites of northern Greece: source apportionment of ambient PAH levels and PAH-induced lung cancer risk. Environ Sci Pollut Res 23:3556–3568CrossRefGoogle Scholar
  29. Manzano AM, Torres G, González A, Banguela A, Ramos-G onzález PL, Valiente PA, Sánchez MI, Lamar A, Rochefort D, Mclean MD, Ramos-Leal M, Guerra G (2013) Role of laccase isozymes in textile dye decolorization and diversity of laccase genes from Ganoderma weberianum B-18. J Appl Sci Environ Sanit 8:237–242 (ISSN 0126-2807)Google Scholar
  30. Marco-Urrea E, Gabarrell X, Caminal G, Vincent T, Reddy CA (2008) Aerobic degradation by white-rot fungi of trichloroethylene (TCE) and mixtures of TCE and perchloroethylene (PCE). J Chem Technol Biotechnol 83(9):1190–1196CrossRefGoogle Scholar
  31. Minter et al.2001Minter, D. W., Rodríguez, M., and Mena J. (2001). Fungi of the Caribbean. An Annotated Checklist. London: PDMS Publishing.Google Scholar
  32. Mirza R, Faghiri I, Abedi E (2012) Contamination of polycyclic aromatic hydrocarbons in surface sediments of Khure-Musa Estuarine, Persian Gulf. World J Fish Mar Sci 4(2):136–141. Google Scholar
  33. Murugesan, K, In-Hyun, N, Kim, Y, and Chang, Y (2007) Decolorizationof reactive dyes by a thermostable laccase produced by Ganoderma lucidum in solid state culture. Enzyme Microb. Tech. 4, 1662–1672. doi: 10.1016/j.enzmictec.2006.08.028
  34. Novotný Č, Erbanová P, Cajthaml T, Rothschild N, Dosoretz C, Šašek V (2000) Irpex lacteus, a white rot fungus applicable to water and soil bioremediation. Appl Microbiol Biotechnol 54(6):850–853CrossRefGoogle Scholar
  35. Novotný Č, Svobodova K, Erbanova P, Cajthaml T, Kasinatha A, Lang E (2004) Lignolytic fungi in bioremediation: extracellular enzyme production and degradation rate. Soil Biol Biochem 36:1545–1551CrossRefGoogle Scholar
  36. Pointing SB, Bucher VVC, Vrijmoed LLP (2000) Dye decolorization by subtropical basidiomycetous fungi and the effect of metals on dye degradation. World J Microbiol Biotechnol 16:199–205CrossRefGoogle Scholar
  37. Pozdnyakova NN, Chernyshovaa MP, Grineva VS, Landesmanb EO, Turkovskayaa V (2016) Degradation of fluorene and fluoranthene by the basidiomycete Pleurotu sostreatus. Appl Biochem Microbiol 52(6):621–628Google Scholar
  38. Revankar MS, Lele S (2007) Synthetic dye decolourization by White Rot Fungus, Ganoderma sp. WR-I. Bioresour Technol 98:775–780CrossRefGoogle Scholar
  39. Rodríguez-Couto S (2007) Decolouration of industrial azo dyes by crude laccase from Trametes hirsuta. J Hazard Mater 148:768–770CrossRefGoogle Scholar
  40. Rodríguez-Couto S, Rosales E, Sanromán MA (2006) Decolourization of synthetic dyes by Trametes hirsuta in expanded-bed reactors. Chemosphere 62:1558–1563.
  41. Samanta S, Singh OM, JainT R (2011) Polycyclic aromatic hydrocarbons: environmental pollution and bioremediation. Trends Biotechnol 20(6):243–248Google Scholar
  42. Shrestha P, Joshi B, Malla R, Sreerama L (2016) Isolation and physicochemical characterization of laccase from Ganoderma lucidum-CDBT1 isolated from its native habitat in Nepal. Biomed Res Int 2016:1–10. Google Scholar
  43. Srinivasan C, D’Souza TM, Boominathan K, Reddy CA (1995) Demonstration of laccase in the white rot basidiomycete Phanerochaete chrysosporium BKM F1767. Appl Environ Microbiol 61:4274–4277Google Scholar
  44. Teerapatsakul C, Abe N, Bucke C, Chitradon L (2007) Novel laccases of Ganoderma sp. KU-Alk4, regulated by different glucose concentration in alkaline media. World J Microbiol Biotechnol 23:1559–1567CrossRefGoogle Scholar
  45. Ting WTE, Yuan SY, Wu SD, Chang BV (2011) Biodegradation of phenanthrene and pyrene by Ganoderma lucidum. Int Biodeterior Biodegradation 65:238–242CrossRefGoogle Scholar
  46. Torres-Farradá G, Manzano AM, Rineau F, Ledo LL, Sánchez- López MI, Thijs S, Colpaert J, Ramos-Leal M, Guerra G, Vangronsveld J (2017) Diversity of ligninolytic enzymes and their genes in strains of the genus Ganoderma: applicable for biodegradation of xenobiotic compounds? Front Microbiol 8:898. CrossRefGoogle Scholar
  47. Torres-Farradá G, Manzano AM, Ramos-Leal M, Domínguez O, Sánchez MI, Jaco Vangronsveld J, Guerra G (2018) Biodegradation and detoxification of dyes and industrial effluents by Ganoderma weberianum B-18 immobilized in a lab-scale packed-bed bioreactor. Bioremediat J 22(4):1–8. Google Scholar
  48. Torres–Torres MG, Guzmán–Dávalos L (2005) Variación morfológica de Ganoderma curtisii en México. Rev Mex Micol 21:39–47Google Scholar
  49. Wesenberg D, Kyriakides I, Agathos S (2003) White-rot fungi and their enzymes for the treatment of industrial dye effluents. Biotechnol Adv 22:161–187CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Giselle Torres-Farradá
    • 1
    Email author
  • Ana M. Manzano-León
    • 2
  • François Rineau
    • 3
  • Miguel Ramos Leal
    • 2
  • Sofie Thijs
    • 3
  • Inge Jambon
    • 3
  • Jenny Put
    • 4
  • Jan Czech
    • 4
  • Gilda Guerra Rivera
    • 1
  • Robert Carleer
    • 4
  • Jaco Vangronsveld
    • 3
  1. 1.Department of Microbiology and Virology, Faculty of BiologyUniversity of HavanaHavanaCuba
  2. 2.Department of Plant PhytopathologyResearch Institute for Tropical Fruit Trees (IIFT)HavanaCuba
  3. 3.Centre for Environmental SciencesHasselt UniversityHasseltBelgium
  4. 4.Institute for Materials ResearchHasselt UniversityHasseltBelgium

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