Skip to main content
Log in

Potency of Phlebia species of white rot fungi for the aerobic degradation, transformation and mineralization of lindane

  • Microbial Ecology and Environmental Microbiology
  • Published:
Journal of Microbiology Aims and scope Submit manuscript

Abstract

The widespread use of the organochlorine insecticide lindane in the world has caused serious environmental problems. The main purpose of this paper is to investigate the potency of several Phlebia species of white rot fungi to degrade, transform and mineralize lindane, and to provide the feasibility of using white rot fungi for bioremediation at contaminated sites. Based on tolerance experiment results, Phlebia brevispora and Phlebia lindtneri had the highest tolerance to lindane and were screened by degradation tests. After 25 days of incubation, P. brevispora and P. lindtneri degraded 87.2 and 73.3% of lindane in low nitrogen medium and 75.8 and 64.9% of lindane in high nitrogen medium, respectively. Several unreported hydroxylation metabolites, including monohydroxylated, dehydroxylated, and trihydroxylated products, were detected and identified by GC/MS as metabolites of lindane. More than 10% of [14C] lindane was mineralized to 14CO2 by two fungi after 60 days of incubation, and the mineralization was slightly promoted by the addition of glucose. Additionally, the degradation of lindane and the formation of metabolites were efficiently inhibited by piperonyl butoxide, demonstrating that cytochrome P450 enzymes are involved in the fungal transformation of lindane. The present study showed that P. brevispora and P. lindtneri were efficient degraders of lindane; hence, they can be applied in the bioremediation process of lindane-contaminated sites.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Arisoy, M. 1998. Biodegradation of chlorinated organic compounds by white-rot fungi. Bull. Environ. Contam. Toxicol.60, 872–876.

    Article  CAS  PubMed  Google Scholar 

  • Asif, M.B., Hai, F.I., Singh, L., Price, W.E., and Nghiem, L.D. 2017. Degradation of pharmaceuticals and personal care products by white-rot fungi–a critical review. Curr. Pollut. Rep.3, 88–103.

    Article  CAS  Google Scholar 

  • Bumpus, J.A., Tien, M., Wright, D., and Aust, S.D. 1985. Oxidation of persistent environmental pollutants by a white rot fungus. Science228, 1434–1436.

    Article  CAS  PubMed  Google Scholar 

  • Dritsa, V. and Rigas, F. 2013. The ligninolytic and biodegradation potential on lindane of Pleurotus ostreatus spp. J. Mining World Express2, 23–30.

    Google Scholar 

  • Gao, J., Liu, L., Liu, X., Lu, J., Zhou, H., Huang, S., Wang, Z., and Spear, P.A. 2008. Occurrence and distribution of organochlorine pesticides-lindane, p,p´-DDT, and heptachlor epoxide-in surface water of China. Environ. Int.34, 1097–1103.

    Article  CAS  PubMed  Google Scholar 

  • Girish, K. and Kunhi, M. 2013. Microbial degradation of gammahexachlorocyclohexane (lindane). Afr. J. Microbiol. Res.7, 1635–1643.

    Article  CAS  Google Scholar 

  • Hadibarata, T. and Kristanti, R.A. 2012. Fate and cometabolic degradation of benzo[a]pyrene by white-rot fungus Armillaria sp. F022. Bioresour. Technol.107, 314–318.

    Article  CAS  PubMed  Google Scholar 

  • Kamei, I. and Kondo, R. 2005. Biotransformation of dichloro-, trichloro-, and tetrachloro- dibenzo-p-dioxin by the white-rot fungus Phlebia lindtneri. Appl. Microbiol. Biotechnol.68, 560–566.

    Article  CAS  PubMed  Google Scholar 

  • Kamei, I., Sonoki, S., Haraguchi, K., and Kondo, R. 2006. Fungal bioconversion of toxic polychlorinated biphenyls by white-rot fungus, Phlebia brevispora. Appl. Microbiol. Biotechnol.73, 932–940.

    Article  CAS  PubMed  Google Scholar 

  • Kamei, I., Takagi, K., and Kondo, R. 2010. Bioconversion of dieldrin by wood-rotting fungi and metabolite detection. Pest Manag. Sci.66, 888–891.

    CAS  PubMed  Google Scholar 

  • Kaur, H., Kapoor, S., and Kaur, G. 2016. Application of ligninolytic potentials of a white-rot fungus Ganoderma lucidum for degradation of lindane. Environ. Monit. Assess.188, 588.

    Article  PubMed  CAS  Google Scholar 

  • Kennedy, D.W., Aust, S.D., and Bumpus, J.A. 1990. Comparative biodegradation of alkyl halide insecticides by the white rot fungus, Phanerochaete chrysosporium (BKM-F-1767). Appl. Environ. Microbiol.56, 2347–2353.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar, M., Chaudhaey, P., Dwivedi, M., Kumar, R., Paul, D., Jain, R.K., Garg, S.K., and Kumar, A. 2005. Enhanced biodegradation of β- and δ-hexachlorocyclohexane in the presence of α- and γ-isomers in contaminated soils. Environ. Sci. Technol.39, 4005–4011.

    Article  CAS  PubMed  Google Scholar 

  • Kumar, K. and Pannu, R. 2018. Perspectives of lindane (γ-hexachlorocyclohexane) biodegradation from the environment: a review. Bioresour. Bioprocess.5, 29.

    Article  CAS  Google Scholar 

  • Lal, R. and Saxena, D.M. 1982. Accumulation, metabolism and effects of organochlorine insecticides on microorganisms. Microbiol. Rev.40, 95–127.

    Article  Google Scholar 

  • Madaj, R., Sobiecka, E., and Kalnowska, H. 2018. Lindane, kepone and pentachlorobenzene: chloropesticides banned by Stockholm convention. Int. J. Environ. Sci. Technol.15, 471–480.

    Article  CAS  Google Scholar 

  • Mohapatra, S. and Pandey, M. 2015. Biodegradation of hexachlorocyclohexane (HCH) isomers by white rot fungus, Pleurotus florida. J. Bioremed. Biodeg.6, 280.

  • Mohapatra, S., Veena, S.S., Pandey, M., and Deepa, M. 2012. Biodegradation of gamma-hexachlorocyclohexane by various Pleurotus species. Pestic. Res. J.24, 212–216.

    CAS  Google Scholar 

  • Mori, T., Kitano, S., and Kondo, R. 2003. Biodegradation of chloronaphthalenes and polycyclic aromatic hydrocarbons by the whiterot fungus Phlebia lindtneri. Appl. Microbiol. Biotechnol.61, 380–383.

    Article  CAS  PubMed  Google Scholar 

  • Mori, T. and Kondo, R. 2002. Oxidation of chlorinated dibenzo-pdioxin and dibenzofuran by white-rot fungus, Phlebia lindtneri. FEMS Microbiol. Lett.216, 223–227.

    Article  CAS  PubMed  Google Scholar 

  • Mori, T., Nakamura, K., and Kondo, R. 2009. Fungal hydroxylation of polychlorinated naphthalenes with chlorine migration by wood rotting fungi. Chemosphere77, 1230–1235.

    Article  CAS  PubMed  Google Scholar 

  • Mougin, C., Pericaud, C., Dubroca, J., and Asther, M. 1997. Enhanced mineralization of lindane in soils supplemented with the white rot basidiomycete Phanerochaete chrysosporium. Soil Biol. Biochem.29, 1321–1324.

    Article  Google Scholar 

  • Mougin, C., Pericaud, C., Malosse, C., Laugero, C., and Asther, M. 1996. Biotransformation of the insecticide lindane by the white rot basidiomycete Phanerochaete chrysosporium. Pestic. Sci.47, 51–59.

    Article  CAS  Google Scholar 

  • Nagata, Y., Prokop, Z., Sato, Y., Jerabek, P., Kumar, A., Ohtsubo, Y., Tsuda, M., and Damborsky, J. 2005. Degradation of β-hexachlorocyclohexane by haloalkane dehalogenase LinB from Sphingomonas paucimobilis UT26. Appl. Environ. Microbiol.71, 2183–2185.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakamura, R., Kondo, R., Shen, M.H., Ochiai, H., Hisamatsu, S., and Sonoki, S. 2012. Identification of cytochrome P450 monooxygenase genes from the white-rot fungus Phlebia brevispora. AMB Express2, 8.

  • Papadopoulou, K., Rigas, F., and Doulia, D. 2006. Lindane degradation in soil by Pleurotus ostreatus. WSEAS Trans. Environ. Dev.2, 489–496.

    CAS  Google Scholar 

  • Phillips, T.M., Seech, A.G., Lee, H., and Trevors, J.T. 2005. Biodegradation of hexachlorocyclohexane (HCH) by microorganisms. Biodegradation16, 362–392.

    Article  CAS  Google Scholar 

  • Quintero, J.C., Lu-Chau, T.A., Moreira, M.T., Feijoo, G., and Lema, J.M. 2007. Bioremediation of HCH present in soil by the whiterot fungus Bjerkandera adusta in a slurry batch bioreactor. Int. Biodeter. Biodegr.60, 319–326.

    Article  CAS  Google Scholar 

  • Quintero, J.C., Moreira, M.T., Feijoo, G., and Lema, J.M. 2008. Screening of white rot fungal species for their capacity to degrade lindane and other isomers of hexachlorocyclohexane (HCH). Cien. Inv. Agr.35, 159–167.

    Article  Google Scholar 

  • Raina, V., Hauser, A., Buser, H.R., Rentsch, D., Sharma, P., Lal, R., Holliger, C., Poiger, T., Muller, M.D., and Kohler, H.E. 2007. Hydroxylated metabolites of β- and δ-hexachlorocyclohexane: bacterial formation, stereochemical configuration, and occurrence in groundwater at a former production. Environ. Sci. Technol.41, 4292–4298.

    Article  CAS  PubMed  Google Scholar 

  • Raina, V., Rentsch, D., Geiger, T., Sharma, P., Buser, H.R., Holliger, C., Lal, R., and Kohler, H.E. 2008. New metabolites in the degradation of α- and γ-hexachlorocyclohexane (HCH): pentachlorocyclohexenes are hydroxylated to cyclohexenols and cyclohexenediols by the haloalkane dehalogenase LinB from Sphingobium indicum B90A. J. Agric. Food Chem.56, 6594–6603.

    Article  CAS  PubMed  Google Scholar 

  • Rigas, F., Dritsa, V., Marchant, R., Papadopoulou, K., Avramides, E.J., and Hatzianestis, I. 2005. Biodegradation of lindane by Pleurotus ostreatus via central composite design. Environ. Int.31, 191–196.

    Article  CAS  PubMed  Google Scholar 

  • Rigas, F., Papadopoulou, K., Dritsa, V., and Doulia, D. 2007. Bioremediation of a soil contaminated by lindane utilizing the fungus Ganoderma australe via response surface methodology. J. Hazard. Mater.140, 325–332.

    Article  CAS  PubMed  Google Scholar 

  • Rigas, F., Papadopoulou, K., Philippoussis, A., Papadopoulou, J., and Chatzipavlidis, J. 2009. Bioremediation of lindane contaminated soil by Pleurotus ostreatus in non sterile conditions using multilevel factorial design. Water Air Soil Pollut.197, 121–129.

    Article  CAS  Google Scholar 

  • Sadiq, S., Haq, M.I., Ahmad, I., Ahad, K., Rashid, A., and Rafiq, N. 2015. Bioremediation potential of white rot fungi, Pleurotus spp against organochlorines. J. Bioremediat. Biodegrad.6, 308.

    Google Scholar 

  • Sadiq, S., Mahmood-ul-Hassan, M., Ahad, K., and Nazir, S. 2018. Bioremediation of hexachlorocyclohexane (HCH) in soil using spent mushroom compost of Pleurotus ostreatus. Bioremediat. J.22, 126–135.

    Article  CAS  Google Scholar 

  • Saez, J.M., Bigliardo, A.L., Raimondo, E.E., Briceno, G.E., Polti, M.A., and Benimeli, C.S. 2018. Lindane dissipation in a biomixture: effect of soil properties and bioaugmentation. Ecotoxicol. Environ. Saf.156, 97–105.

    Article  CAS  PubMed  Google Scholar 

  • Sari, A.A., Hanifah, U., and Iton, K. 2017. Potency of Trametes versicolor U97 for degrading lindane in liquid medium. J. Lignocellulose Tech.2, 55–65.

    Google Scholar 

  • Sharma, P., Raina, V., Kumari, R., Malhotra, S., Dogra, C., Kumari, H., Kohler, H.E., Buser, H., Holliger, C., and Lal, R. 2006. Haloalkane dehalogenase LinB is responsible for β- and δ-hexachlorocyclohexane transformation in Sphingobium indicum B90A. Appl. Environ. Microbiol.72, 5720–5727.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh, B.K. and Kuhad, R.C. 1999. Biodegradation of lindane (γ-hexachlorocyclohexane) by the white-rot fungus Trametes hirsutus. Lett. Appl. Microbiol.28, 238–241.

    Article  CAS  PubMed  Google Scholar 

  • Singh, B.K. and Kuhad, R.C. 2000. Degradation of insecticide lindane (γ-HCH) by white-rot fungi Cyathus bulleri and Phanerochaete sordida. Pest Manag. Sci.56, 142–146.

    Article  CAS  Google Scholar 

  • Singh, B.K., Kuhad, R.C., Singh, A., Tripathi, K.K., and Ghosh, P.K. 2000. Microbial degradation of the pesticide lindane (γ-hexachlorocyclohexane). Adv. Appl. Microbiol.47, 269–298.

    Article  CAS  PubMed  Google Scholar 

  • Suhara, H., Sakai, K., Kondo, R., Maekawa, N., and Kubayashi, T. 2002. Identification of the basidiomycetous fungus isolated from butt rot of the Japanese cypress. Mycoscience43, 477–481.

    Article  Google Scholar 

  • Tien, M. and Kirk, T.K. 1988. Lignin peroxidase of Phanerochaete chrysosporium. Methods Enzymol.161, 238–249.

    Article  CAS  Google Scholar 

  • Ulčnik, A., Kralj Cigić, I., and Pohleven, F. 2013. Degradation of lindane and endosulfan by fungi, fungal and bacterial laccases. World J. Microbiol. Biotechnol.29, 2239–2247.

    Article  PubMed  CAS  Google Scholar 

  • Ulčnik, A., Kralj Cigić, I., Zupančič-Kralj, L., Tavzes, Č., and Pohleven, F. 2012. Bioremediation of lindane by wood-decaying fungi. Drvna Ind.63, 271–276.

    Article  Google Scholar 

  • Waite, D.T., Gurprasad, N.P., Sproull, J.F., Quiring, D.V., and Kotylak, M.W. 2001. Atmospheric movements of lindane (γ-hexachlorocyclohexane) from canola fields planted with treated seed. J. Environ. Qual.30, 768–775.

    Article  CAS  PubMed  Google Scholar 

  • Xiao, P. and Kondo, R. 2019. Biodegradation and bioconversion of endrin by white rot fungi, Phlebia acanthocystis and Phlebia brevispora. Mycoscience60, 255–261.

    Article  Google Scholar 

  • Xiao, P., Mori, T., Kamei, I., and Kondo, R. 2011.. Metabolism of organochlorine pesticide heptachlor and its metabolite heptachlor epoxide by white rot fungi, belonging to genus Phlebia. FEMS Microbiol. Lett.314, 140–146.

    Article  CAS  PubMed  Google Scholar 

  • Xiao, P., Mori, T., Kamei, I., and Kondo, R. 2011.. A novel metabolic pathway for biodegradation of DDT by the white rot fungi, Phlebia lindtneri and Phlebia brevispora. Biodegradation22, 859–867.

    Article  CAS  PubMed  Google Scholar 

  • Xiao, P., Mori, T., and Kondo, R. 2011.. Biotransformation of the organochlorine pesticide trans-chlordane by wood-rot fungi. N. Biotechnol.29, 107–115.

    Article  CAS  PubMed  Google Scholar 

  • Xu, G. and Wang, J. 2014. Biodegradation of decabromodiphenyl ether (BDE-209) by white-rot fungus Phlebia lindtneri. Chemosphere110, 70–77.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the Fundamental Research Funds for the Central Universities (2572017CA08); the Heilongjiang Provincial Natural Science Foundation (LH2019- D002); and the National Natural Science Foundation of China (41201307).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Pengfei Xiao.

Additional information

Conflict of Interest

The authors declare no competing financial interests to this work.

Supplemental material for this article may be found at http://www.springerlink.com/content/120956

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xiao, P., Kondo, R. Potency of Phlebia species of white rot fungi for the aerobic degradation, transformation and mineralization of lindane. J Microbiol. 58, 395–404 (2020). https://doi.org/10.1007/s12275-020-9492-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-020-9492-x

Keywords

Navigation