Advertisement

Environmental Science and Pollution Research

, Volume 22, Issue 15, pp 11781–11791 | Cite as

Biodegradation of pesticides using fungi species found in the aquatic environment

  • B. R. Oliveira
  • A. Penetra
  • V. V. Cardoso
  • M. J. Benoliel
  • M. T. Barreto Crespo
  • R. A. Samson
  • V. J. Pereira
Research Article

Abstract

Relatively limited attention has been given to the presence of fungi in the aquatic environment compared to their occurrence in other matrices. Taking advantage and recognizing the biodegradable capabilities of fungi is important, since these organisms may produce many potent enzymes capable of degrading toxic pollutants. Therefore, the aim of this study was to evaluate the potential ability of some species of filamentous fungi that occur in the aquatic environment to degrade pesticides in untreated surface water. Several laboratory-scale experiments were performed using the natural microbial population present in the aquatic environment as well as spiked fungi isolates that were found to occur in different water matrices, to test the ability of fungi to degrade several pesticides of current concern (atrazine, diuron, isoproturon and chlorfenvinphos). The results obtained in this study showed that, when spiked in sterile natural water, fungi were able to degrade chlorfenvinphos to levels below detection and unable to degrade atrazine, diuron and isoproturon. Penicillium citrinum, Aspergillus fumigatus, Aspergillus terreus and Trichoderma harzianum were found to be able to resist and degrade chlorfenvinphos. These fungi are therefore expected to play an important role in the degradation of this and other pollutants present in the aquatic environment.

Keywords

Fungi Biodegradation Pesticides Surface water 

Notes

Acknowledgments

Financial support from Fundação para a Ciência e a Tecnologia—through the project PTDC/AAC-AMB/108303/2008, the grant PEst-OE/EQB/LA0004/2011 and the fellowship BPD/26990/2006—is gratefully acknowledged.

We also thank EPAL as participant institution of the project PTDC/AAC-AMB/108303/2008 for supplying the untreated real water matrices used and for the analysis of the breakdown products.

Vanessa J. Pereira thanks the Department of Geography and Environmental Engineering at Johns Hopkins University for hosting her as a Visiting Scholar during the academic year 2012/2013.

Supplementary material

11356_2015_4472_MOESM1_ESM.docx (20 kb)
ESM 1 (DOCX 20 kb)

References

  1. Al-gabr HM, Zheng T, Yu X (2014) Occurrence and quantification of fungi and detection of mycotoxigenic fungi in drinking water in Xiamen City, China. Sci Total Environ 466–467:1103–1111CrossRefGoogle Scholar
  2. Badali H, Gueidan C, Najafzadeh MJ, Bonifaz A, Gerritsvan den Ende AHG, Hoog GS (2005) Biodiversity of the genus Cladophialophora. Stud Mycol 61:175–191CrossRefGoogle Scholar
  3. Bhalerao TS, Puranik PR (2009) Microbial degradation of monocrotophos by Aspergillus oryzae. Int Biodeterior Biodegrad 63:503–508CrossRefGoogle Scholar
  4. Bordjiba O, Steiman R, Kadri M, Semadi A, Guiraud P (2001) Removal of herbicides from liquid media by fungi isolated from a contaminated soil. J Environ Qual 30:418–426CrossRefGoogle Scholar
  5. Bouchiat R, Veignie E, Grizard D, Soebert C, Vigier M, Rafin C (2015) Ability of filamentous fungi to degrade four emergent water priority pollutants. Desalin Water Treat. doi: 10.1080/19443994.2015.1013508
  6. Boyandin AN, Prudnikova SV, Karpov VA, Ivonin VN, Đỗ NL, Nguyễn TH, Lê TMH, Filichev NL, Levin AL, Filipenko ML, Volova TG, Gitelson II (2013) Microbial degradation of polyhydroxyalkanoates in tropical soils. Int Biodeterior Biodegrad 83:77–84CrossRefGoogle Scholar
  7. Castillo LE, Cruz EL, Ruepert C (1997) Ecotoxicology and pesticides in tropical aquatic ecosystems of Central America. Environ Toxicol Chem 16:41–51CrossRefGoogle Scholar
  8. Donald DB, Cessna AJ, Sverko E, Glozier NE (2007) Pesticides in surface drinking-water supplies of the Northern Great plains. Environ Health Perspect 115:1183–1191CrossRefGoogle Scholar
  9. Ellegaard-Jensen L, Knudsen BE, Johansen A, Albers CN, Aamand J, Rosendahl S (2014) Fungal–bacterial consortia increase diuron degradation in water-unsaturated systems. Sci Total Environ 466–467:699–705CrossRefGoogle Scholar
  10. Evans CS, Hedger JN (2001) Degradation of plant cell wall polymers. In: Gadd GM (ed) Fungi in bioremediation. Cambridge University Press, Cambridge, p 26Google Scholar
  11. Gao D, Du L, Yang J, Wu W, Liang H (2010) A critical review of the application of white rot fungus to environmental pollution control. Crit Rev Biotechnol 30:70–77CrossRefGoogle Scholar
  12. Gao Y, Chen S, Hu M, Hu Q, Luo J, Li Y (2012) Purification and characterization of a novel chlorpyrifos hydrolase from Cladosporium cladosporioides Hu-01. PLoS ONE 7:1–8CrossRefGoogle Scholar
  13. Glass NL, Donaldson GC (1994) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microbiol 61:1323–1330Google Scholar
  14. Graymore M, Stagnitti F, Allinson G (2001) Impacts of atrazine in aquatic ecosystems. Environ Int 26:483–495CrossRefGoogle Scholar
  15. Hageskal G, Gaustad P, Heier BT, Skaar I (2006) Occurrence of moulds in drinking water. J Appl Microbiol 102:774–780CrossRefGoogle Scholar
  16. Hageskal G, Lima N, Skaar I (2009) The study of fungi in drinking water. Mycol Res 133:165–172CrossRefGoogle Scholar
  17. Hincapié M, Maldonado MI, Oller I, Gernjak W, Sánchez-Pérez JA, Ballesteros MM, Malato S (2005) Solar photocatalytic degradation and detoxification of EU priority substances. Catal Today 101:203–210CrossRefGoogle Scholar
  18. Hong S-B, Go S-J, Shin H-D, Frisvad JC, Samson RA (2005) Polyphasic taxonomy of Aspergillus fumigatus and related species. Mycologia 97:1316–1329CrossRefGoogle Scholar
  19. Jiao N, Herndl GJ, Hansell DA, Benner R, Kattner G, Wilhelm SW, Kirchman DL, Weinbauer MG, Luo T, Chen F, Azam F (2010) Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean. Nat Rev Microbiol 8:593–599CrossRefGoogle Scholar
  20. Jin HM, Kim JM, Lee HJ, Madsen EL, Jeon CO (2012) Alteromonas as a key agent of polycyclic aromatic hydrocarbon biodegradation in crude oil-contaminated coastal sediment. Environ Sci Technol 46:7731–7740CrossRefGoogle Scholar
  21. Kanzler D, Buzina W, Paulitsch A, Haas D, Platzer S, Marth E, Mascher F (2007) Occurrence and hygienic relevance of fungi in drinking water. Mycoses 51:165–169CrossRefGoogle Scholar
  22. Katayama A, Matsumura F (1993) Degradation of organochlorine pesticides, particularly endosulfan, by Trichoderma harzianum. Environ Toxicol Chem 12:1059–1065CrossRefGoogle Scholar
  23. Lade HS, Waghmode TR, Kadam AA, Govindwar SP (2012) Enhanced biodegradation and detoxification of disperse azo dye Rubine GFL and textile industry effluent by defined fungal-bacterial consortium. Int Biodeterior Biodegrad 72:94–107CrossRefGoogle Scholar
  24. Lee DG, Zhao F, Rezenom YH, Russell DH, Chu K-H (2012) Biodegradation of triclosan by a wastewater microorganism. Water Res 46:4226–4234CrossRefGoogle Scholar
  25. Lew S, Lew M, Biedunkiewicz A, Szarek J (2013) Impact of pesticide contamination on aquatic microorganism populations in the littoral zone. Arch Environ Contam Toxicol 64:399–409CrossRefGoogle Scholar
  26. Lo C-C (2010) Effect of pesticides on soil microbial community. J Environ Sci Health, Part B 45:348–359CrossRefGoogle Scholar
  27. Madigan MT, Martinko JM, Dunlap PV, Clark DP (2012) Brock biology of microorganisms. Pearson Prentice Hall, Upper Saddle, p 992Google Scholar
  28. Maiti S, Ray D, Mitra D, Mukhopadhyay A (2013) Isolation and characterisation of starch/polyvinyl alcohol degrading fungi from aerobic compost environment. Int Biodeterior Biodegrad 82:9–12CrossRefGoogle Scholar
  29. Malmstrøm J, Christophersen C, Frisvad JC (2000) Secondary metabolites characteristic of Penicillium citrinum, Penicillium steckii and related species. Phytochemistry 54:301–309CrossRefGoogle Scholar
  30. Matson PA, Parton WJ, Power AG, Swift MJ (1997) Agricultural intensification and ecosystem properties. Science 227:504–509CrossRefGoogle Scholar
  31. 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. Enzym Microb Technol 39:1365–1372CrossRefGoogle Scholar
  32. Mitchell R, Gu J-D (2010) Environmental microbiology. Wiley Blackwell, Hoboken, pp 410Google Scholar
  33. Mollea C, Bosco F, Ruggeri B (2005) Fungal biodegradation of naphthalene: microcosms studies. Chemosphere 60:636–643CrossRefGoogle Scholar
  34. O’Donnell K, Sarver BAJ, Brandt M, Chang DC, Noble-Wang J, Park BJ, Sutton DA, Benjamin L, Lindsley M, Padhye A, Geiser DM, Ward TJ (2007) Phylogenetic diversity and microsphere array-based genotyping of human pathogenic Fusaria, including isolates from the multistate contact lens-associated U.S. keratitis outbreaks of 2005 and 2006. J Clin Microbiol 45:2235–2248CrossRefGoogle Scholar
  35. Oliveira BR, Barreto Crespo MT, San Romão MV, Benoliel MJ, Samson RA, Pereira VJ (2013) New insights concerning the occurrence of fungi in water sources and their potential pathogenicity. Water Res 47:6338–6347CrossRefGoogle Scholar
  36. Pereira VJ, Basílio MC, Fernandes D, Domingues M, Paiva JM, Benoliel MJ, Crespo MT, San Romão MV (2009) Occurrence of filamentous fungi and yeasts in three different drinking water sources. Water Res 43:3813–3819CrossRefGoogle Scholar
  37. Pinto AP, Serrano C, Pires T, Mestrinho E, Dias L, Teixeira DM, Caldeira AT (2012) Degradation of terbuthylazine, difenoconazole and pendimethalin pesticides by selected fungi cultures. Sci Total Environ 435–436:402–410CrossRefGoogle Scholar
  38. Polman JK, Stoner D, Delezene-Briggs K (1994) Bioconversion of coal, lignin, and dimethoxybenzyl alcohol by Penicillium citrinum. J Ind Microbiol 13:292–299CrossRefGoogle Scholar
  39. Pothuluri JV, Evans FE, Doerge DR, Churchwell MI, Cerniglia CE (1996) Metabolism of metolachlor by the fungus Cunninghamella elegans. Arch Environ Contam Toxicol 32:117–125CrossRefGoogle Scholar
  40. Purnomo AS, Mori T, Putra SR, Kondo R (2013) Biotransformation of heptachlor and heptachlor epoxide by white-rot fungus Pleurotus ostreatus. Int Biodeterior Biodegrad 82:40–44CrossRefGoogle Scholar
  41. Relyea RA (2009) A cocktail of contaminants: how mixtures of pesticides at low concentrations affect aquatic communities. Oecologia 159:363–376CrossRefGoogle Scholar
  42. Rodriguez-Mozaz S, López de Alda MJ, Barceló D (2004) Monitoring of estrogens, pesticides and bisphenol A in natural waters and drinking water treatment plants by solid-phase extraction–liquid chromatography–mass spectrometry. J Chromatogr A 1045:85–92CrossRefGoogle Scholar
  43. Rouchaud J, Roucourt P, Van de Steene F, Pelerents C, Gillet J, Benoit F, Ceustermans N (1988) Fate of the insecticide chlorfenvinphos in the soil of cauliflower field crops. Bull Environ Contam Toxicol 40:47–53CrossRefGoogle Scholar
  44. Rouchaud J, Metsue M, Van de Steene F, Pelerents C, Gillet J, Benoit F, Ceustermans N, Vanparys L (1989) Influence of continuous monoculture and insecticide treatments on the rate of chlorfenvinphos soil biodegradation in cabbage crops. Bull Environ Contam Toxicol 42:409–416CrossRefGoogle Scholar
  45. Samson RA, Seifert KA, Kuijpers AFA, Houbraken JAMP, Frisvad JC (2004) Phylogenetic analysis of Penicillium subgenus Penicillium using partial β-tubulin sequences. Stud Mycol 49:175–200Google Scholar
  46. Sanches S, Penetra A, Rodrigues A, Cardoso VV, Ferreira E, Benoliel MJ, Barreto Crespo MT, Crespo JG, Pereira VJ (2013) Removal of pesticides from water combining low pressure UV photolysis with nanofiltration. Sep Purif Technol 115:73–82CrossRefGoogle Scholar
  47. Saravanan R, Sivakumar T (2013) Biodiversity and biodegradation potentials of fungi isolated from marine systems of East Coast of Tamil Nadu, India. Int J Curr Microbiol Appl Sci 2:192–201Google Scholar
  48. Schiavano GF, Parlani L, Sisti M, Sebastianelli G, Brandi G (2014) Occurrence of fungi in dialysis water and dialysate from eight haemodialysis units in central Italy. J Hosp Infect 86:194–200CrossRefGoogle Scholar
  49. Silambarasan S, Abraham J (2012) Ecofriendly method for bioremediation of chlorpyrifos from agricultural soil by novel fungus Aspergillus terreus JAS1. Water Air Soil Pollut 224:1–11Google Scholar
  50. Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S (2002) Agricultural sustainability and intensive production practices. Nature 418:671–677CrossRefGoogle Scholar
  51. Tripathi P, Singh PC, Mishra A, Chauhan PS, Dwivedi S, Bais RT, Tripathi RD (2013) Trichoderma: a potential bioremediator for environmental clean up. Clean Techn Environ Policy 15:541–550CrossRefGoogle Scholar
  52. Uhnáková B, Ludwig R, Pěknicová J, Homolka L, Lisá L, Šulc M, Petříčková A, Elzeinová F, Pelantová H, Monti D, Křen V, Haltrich D, Martínková L (2011) Biodegradation of tetrabromobisphenol A by oxidases in basidiomycetous fungi and estrogenic activity of the biotransformation products. Bioresour Technol 102:9409–9415CrossRefGoogle Scholar
  53. Ye J-S, Yin H, Qiang J, Peng H, Qin H-M, Zhang N, He B-Y (2011) Biodegradation of anthracene by Aspergillus fumigatus. J Hazard Mater 185:174–181CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • B. R. Oliveira
    • 1
  • A. Penetra
    • 2
  • V. V. Cardoso
    • 2
  • M. J. Benoliel
    • 2
  • M. T. Barreto Crespo
    • 1
    • 3
  • R. A. Samson
    • 4
  • V. J. Pereira
    • 1
    • 3
  1. 1.IBETOeirasPortugal
  2. 2.Empresa Portuguesa das Águas Livres, S.A.LisbonPortugal
  3. 3.Instituto de Tecnologia Química e BiológicaUniversidade Nova de LisboaOeirasPortugal
  4. 4.CBS-KNAW Fungal Biodiversity CentreUtrechtThe Netherlands

Personalised recommendations