Advertisement

Applied Microbiology and Biotechnology

, Volume 103, Issue 1, pp 53–68 | Cite as

Roles of saprotrophic fungi in biodegradation or transformation of organic and inorganic pollutants in co-contaminated sites

  • Andrea Ceci
  • Flavia Pinzari
  • Fabiana Russo
  • Anna Maria PersianiEmail author
  • Geoffrey Michael Gadd
Mini-Review
  • 250 Downloads

Abstract

For decades, human activities, industrialization, and agriculture have contaminated soils and water with several compounds, including potentially toxic metals and organic persistent xenobiotics. The co-occurrence of those toxicants poses challenging environmental problems, as complicated chemical interactions and synergies can arise and lead to severe and toxic effects on organisms. The use of fungi, alone or with bacteria, for bioremediation purposes is a growing biotechnology with high potential in terms of cost-effectiveness, an environmental-friendly perspective and feasibility, and often representing a sustainable nature-based solution. This paper reviews different ecological, metabolic, and physiological aspects involved in fungal bioremediation of co-contaminated soils and water systems, not only addressing best methods and approaches to assess the simultaneous presence of metals and organic toxic compounds and their consequences on provided ecosystem services but also the interactions between fungi and bacteria, in order to suggest further study directions in this field.

Keywords

Co-contamination Organic pollutants Potentially toxic metals Soil saprotrophic fungi Xenobiotics Biodegradation Biotransformation 

Notes

Acknowledgements

Geomicrobiology Group (GMG) gratefully acknowledges financial support in his laboratory from the Natural Environment Research Council, UK.

Funding

Research support in the GMG is received from the Natural Environment Research Council, UK (NE/M010910/1 (TeaSe); NE/M011275/1 (COG3)).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical statement

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Alisi C, Musella R, Tasso F, Ubaldi C, Manzo S, Cremisini C, Sprocati AR (2009) Bioremediation of diesel oil in a co-contaminated soil by bioaugmentation with a microbial formula tailored with native strains selected for heavy metals resistance. Sci Total Environ 407:3024–3032.  https://doi.org/10.1016/j.scitotenv.2009.01.011 CrossRefPubMedGoogle Scholar
  2. Almeida R, Mucha AP, Teixeira C, Bordalo AA, Almeida CMR (2013) Biodegradation of petroleum hydrocarbons in estuarine sediments: metal influence. Biodegradation 24:111–123.  https://doi.org/10.1007/s10532-012-9562-9 CrossRefPubMedGoogle Scholar
  3. Alvarez A, Saez JM, Davila Costa JS, Colin VL, Fuentes MS, Cuozzo SA, Benimeli CS, Polti MA, Amoroso MJ (2017) Actinobacteria: current research and perspectives for bioremediation of pesticides and heavy metals. Chemosphere 166:41–62.  https://doi.org/10.1016/j.chemosphere.2016.09.070 CrossRefPubMedGoogle Scholar
  4. Arjoon A, Olaniran AO, Pillay B (2013) Co-contamination of water with chlorinated hydrocarbons and heavy metals: challenges and current bioremediation strategies. Int J Environ Sci Technol 10:395–412.  https://doi.org/10.1007/s13762-012-0122-y CrossRefGoogle Scholar
  5. Asif MB, Hai FI, Hou J, Price WE, Nghiem LD (2017) Impact of wastewater derived dissolved interfering compounds on growth, enzymatic activity and trace organic contaminant removal of white rot fungi—a critical review. J Environ Manag 201:89–109.  https://doi.org/10.1016/j.jenvman.2017.06.014 CrossRefGoogle Scholar
  6. Atagana HI (2009) Biodegradation of PAHs by fungi in contaminated-soil containing cadmium and nickel ions. Afr J Biotechnol 8:5780–5789.  https://doi.org/10.5897/AJB2009.000-9465 CrossRefGoogle Scholar
  7. Baldrian P (2003) Interactions of heavy metals with white-rot fungi. Enzym Microb Technol 32:78–91.  https://doi.org/10.1016/S0141-0229(02)00245-4 CrossRefGoogle Scholar
  8. Baldrian P, in Der Wiesche C, Gabriel J, Nerud F, Zadražil F (2000) Influence of cadmium and mercury on activities of ligninolytic enzymes and degradation of polycyclic aromatic hydrocarbons by Pleurotus ostreatus in soil. Appl Environ Microbiol 66:2471–2478.  https://doi.org/10.1128/AEM.66.6.2471-2478.2000 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Barker AV, Bryson GM (2002) Bioremediation of heavy metals and organic toxicants by composting. Sci World J 2:407–420.  https://doi.org/10.1100/tsw.2002.91 CrossRefGoogle Scholar
  10. Bhardwaj G (2013) Biosurfactants from fungi: a review. J Pet Environ Biotechnol 04:1–6.  https://doi.org/10.4172/2157-7463.1000160 CrossRefGoogle Scholar
  11. Bhattacharya S, Das A, Prashanthi K, Palaniswamy M, Angayarkanni J (2014) Mycoremediation of benzo[a]pyrene by Pleurotus ostreatus in the presence of heavy metals and mediators. 3 Biotech 4:205–211.  https://doi.org/10.1007/s13205-013-0148-y CrossRefPubMedGoogle Scholar
  12. Blasco C, Picó Y (2009) Prospects for combining chemical and biological methods for integrated environmental assessment. TrAC Trends Anal Chem 28:745–757.  https://doi.org/10.1016/j.trac.2009.04.010 CrossRefGoogle Scholar
  13. Blasi B, Poyntner C, Rudavsky T, Prenafeta-Boldú FX, de Hoog S, Tafer H, Sterflinger K (2016) Pathogenic yet environmentally friendly? Black fungal candidates for bioremediation of pollutants. Geomicrobiol J 33:308–317.  https://doi.org/10.1080/01490451.2015.1052118 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Boswell GP, Jacobs H, Davidson FA, Gadd GM, Ritz K (2002) Functional consequences of nutrient translocation in mycelial fungi. J Theor Biol 217:459–477.  https://doi.org/10.1006/jtbi.2002.3048 CrossRefPubMedGoogle Scholar
  15. Boswell GP, Jacobs H, Davidson FA, Gadd GM, Ritz K (2003) Growth and function of fungal mycelia in heterogeneous environments. Bull Math Biol 65:447–477.  https://doi.org/10.1016/S0092-8240(03)00003-X CrossRefPubMedGoogle Scholar
  16. Boswell GP, Jacobs H, Ritz K, Gadd GM, Davidson FA (2007) The development of fungal networks in complex environments. Bull Math Biol 69:605–634.  https://doi.org/10.1007/s11538-005-9056-6 CrossRefPubMedGoogle Scholar
  17. Bourceret A, Cébron A, Tisserant E, Poupin P, Bauda P, Beguiristain T, Leyval C (2016) The bacterial and fungal diversity of an aged PAH- and heavy metal-contaminated soil is affected by plant cover and edaphic parameters. Microb Ecol 71:711–724.  https://doi.org/10.1007/s00248-015-0682-8 CrossRefPubMedGoogle Scholar
  18. Brandl H, Bosshard R, Wegmann M (2001) Computer-munching microbes: metal leaching from electronic scrap by bacteria and fungi. Hydrometallurgy 59:319–326.  https://doi.org/10.1016/S0304-386X(00)00188-2 CrossRefGoogle Scholar
  19. Brijwani K, Rigdon A, Vadlani PV (2010) Fungal laccases: production, function, and applications in food processing. Enzyme Res 2010:149748–149710.  https://doi.org/10.4061/2010/149748 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Ceci A, Pierro L, Riccardi C, Pinzari F, Maggi O, Persiani AM, Gadd GM, Petrangeli Papini M (2015) Biotransformation of β-hexachlorocyclohexane by the saprotrophic soil fungus Penicillium griseofulvum. Chemosphere 137:101–107.  https://doi.org/10.1016/j.chemosphere.2015.05.074 CrossRefPubMedGoogle Scholar
  21. Ceci A, Pinzari F, Riccardi C, Maggi O, Pierro L, Petrangeli Papini M, Gadd GM, Persiani AM (2018) Metabolic synergies in the biotransformation of organic and metallic toxic compounds by a saprotrophic soil fungus. Appl Microbiol Biotechnol 102:1019–1033.  https://doi.org/10.1007/s00253-017-8614-9 CrossRefPubMedGoogle Scholar
  22. Chanda A, Gummadidala PM, Gomaa OM (2016) Mycoremediation with mycotoxin producers: a critical perspective. Appl Microbiol Biotechnol 100:17–29.  https://doi.org/10.1007/s00253-015-7032-0 CrossRefPubMedGoogle Scholar
  23. Chen M, Xu P, Zeng G, Yang C, Huang D, Zhang J (2015a) Bioremediation of soils contaminated with polycyclic aromatic hydrocarbons, petroleum, pesticides, chlorophenols and heavy metals by composting: applications, microbes and future research needs. Biotechnol Adv 33:745–755.  https://doi.org/10.1016/j.biotechadv.2015.05.003 CrossRefPubMedGoogle Scholar
  24. Chen R, Zhou Z, Liu Y, Jiang J, Li Q, Song H, Pei D, Xu H (2015b) Mycoremediation potential and tolerance responses of Oudemansiella radicata in cadmium–pyrene co-contaminated soil. J Soils Sediments 15:1083–1093.  https://doi.org/10.1007/s11368-015-1093-7 CrossRefGoogle Scholar
  25. Chirakkara RA, Cameselle C, Reddy KR (2016) Assessing the applicability of phytoremediation of soils with mixed organic and heavy metal contaminants. Rev Environ Sci Biotechnol 15:299–326.  https://doi.org/10.1007/s11157-016-9391-0 CrossRefGoogle Scholar
  26. Colpaert JV, Muller LAH, Lambaerts M, Adriaensen K, Vangronsveld J (2004) Evolutionary adaptation to Zn toxicity in populations of Suilloid fungi. New Phytol 162:549–559.  https://doi.org/10.1111/j.1469-8137.2004.01037.x CrossRefGoogle Scholar
  27. Coulibaly L, Gourene G, Agathos NS (2003) Utilization of fungi for biotreatment of raw wastewaters. Afr J Biotechnol 2:620–630CrossRefGoogle Scholar
  28. Crowther TW, Maynard DS, Crowther TR, Peccia J, Smith JR, Bradford MA (2014) Untangling the fungal niche: the trait-based approach. Front Microbiol 5:579.  https://doi.org/10.3389/fmicb.2014.00579 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Cui J, Zhang L (2008) Metallurgical recovery of metals from electronic waste: a review. J Hazard Mater 158:228–256.  https://doi.org/10.1016/j.jhazmat.2008.02.001 CrossRefPubMedGoogle Scholar
  30. Czaplicki LM, Cooper E, Ferguson PL, Stapleton HM, Vilgalys R, Gunsch CK (2016) A new perspective on sustainable soil remediation—case study suggests novel fungal genera could facilitate in situ biodegradation of hazardous contaminants. Remediat J 26:59–72.  https://doi.org/10.1002/rem.21458 CrossRefGoogle Scholar
  31. Deacon LJ, Janie Pryce-Miller E, Frankland JC, Bainbridge BW, Moore PD, Robinson CH (2006) Diversity and function of decomposer fungi from a grassland soil. Soil Biol Biochem 38:7–20.  https://doi.org/10.1016/j.soilbio.2005.04.013 CrossRefGoogle Scholar
  32. Del Carmen Vargas-García M, López MJ, Suárez-Estrella F, Moreno J (2012) Compost as a source of microbial isolates for the bioremediation of heavy metals: in vitro selection. Sci Total Environ 431:62–67.  https://doi.org/10.1016/j.scitotenv.2012.05.026 CrossRefGoogle Scholar
  33. Deshmukh R, Khardenavis AA, Purohit HJ (2016) Diverse metabolic capacities of fungi for bioremediation. Indian J Microbiol 56:247–264.  https://doi.org/10.1007/s12088-016-0584-6 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Dewey KA, Gaw SK, Northcott GL, Lauren DR, Hackenburg S (2012) The effects of copper on microbial activity and the degradation of atrazine and indoxacarb in a New Zealand soil. Soil Biol Biochem 52:64–74.  https://doi.org/10.1016/j.soilbio.2012.04.009 CrossRefGoogle Scholar
  35. Dhanarani S, Viswanathan E, Piruthiviraj P, Arivalagan P, Kaliannan T (2016) Comparative study on the biosorption of aluminum by free and immobilized cells of Bacillus safensis KTSMBNL 26 isolated from explosive contaminated soil. J Taiwan Inst Chem Eng 69:61–67.  https://doi.org/10.1016/j.jtice.2016.09.032 CrossRefGoogle Scholar
  36. Dighton J (2016) Fungi in ecosystem processes, Second edn. CRC Press/Taylor and Francis Group, New YorkCrossRefGoogle Scholar
  37. Fernández-Fueyo E, Ruiz-Dueñas FJ, Martínez AT (2014) Engineering a fungal peroxidase that degrades lignin at very acidic pH. Biotechnol Biofuels 7:114.  https://doi.org/10.1186/1754-6834-7-114 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Fester T, Giebler J, Wick LY, Schlosser D, Kästner M (2014) Plant–microbe interactions as drivers of ecosystem functions relevant for the biodegradation of organic contaminants. Curr Opin Biotechnol 27:168–175.  https://doi.org/10.1016/j.copbio.2014.01.017 CrossRefPubMedGoogle Scholar
  39. Fuentes A, Almonacid L, Ocampo JA, Arriagada C (2016) Synergistic interactions between a saprophytic fungal consortium and Rhizophagus irregularis alleviate oxidative stress in plants grown in heavy metal contaminated soil. Plant Soil 407:355–366.  https://doi.org/10.1007/s11104-016-2893-2 CrossRefGoogle Scholar
  40. Gadd GM (2001) Fungi in bioremediation. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  41. Gadd GM (2004) Mycotransformation of organic and inorganic substrates. Mycologist 18:60–70.  https://doi.org/10.1017/S0269-915X(04)00202-2 CrossRefGoogle Scholar
  42. Gadd GM (2007) Geomycology: biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation. Mycol Res 111:3–49.  https://doi.org/10.1016/j.mycres.2006.12.001 CrossRefPubMedGoogle Scholar
  43. Gadd GM (2009) Biosorption: critical review of scientific rationale, environmental importance and significance for pollution treatment. J Chem Technol Biotechnol 84:13–28.  https://doi.org/10.1002/jctb.1999 CrossRefGoogle Scholar
  44. Gadd GM (2010) Metals, minerals and microbes: geomicrobiology and bioremediation. Microbiology 156:609–643.  https://doi.org/10.1099/mic.0.037143-0 CrossRefPubMedGoogle Scholar
  45. Gadd GM (2016) Fungi and industrial pollutants. In: Kubicek CP, Druzhinina IS (eds) The Mycota, volume IV: environmental and microbial relationships. Springer, Heidelberg, pp 89–125Google Scholar
  46. Gadd GM (2017) Geomycology: geoactive fungal roles in the biosphere. In: Dighton J, White JF (eds) The fungal community: its organization and role in the ecosystem, Fourth edn. CRC Press/Taylor and Francis Group, New York, pp 459–469Google Scholar
  47. Gadd GM, Rhee YJ, Stephenson K, Wei Z (2012) Geomycology: metals, actinides and biominerals. Environ Microbiol Rep 4:270–296.  https://doi.org/10.1111/j.1758-2229.2011.00283.x CrossRefPubMedGoogle Scholar
  48. Gao J, Kim JS, Terziev N, Cuccui I, Daniel G (2018) Effect of thermal modification on the durability and decay patterns of hardwoods and softwoods exposed to soft rot fungi. Int Biodeterior Biodegrad 127:35–45.  https://doi.org/10.1016/j.ibiod.2017.11.009 CrossRefGoogle Scholar
  49. Gharieb MM (2002) Biosorption and solubilization of copper oxychloride fungicide by Aspergillus niger and the influence of calcium. Biodegradation 13:191–199.  https://doi.org/10.1023/A:1020839320157 CrossRefPubMedGoogle Scholar
  50. Gianfreda L, Rao MA (2008) Interactions between xenobiotics and microbial and enzymatic soil activity. Crit Rev Environ Sci Technol 38:269–310.  https://doi.org/10.1080/10643380701413526 CrossRefGoogle Scholar
  51. Giardina P, Faraco V, Pezzella C, Piscitelli A, Vanhulle S, Sannia G (2010) Laccases: a never-ending story. Cell Mol Life Sci 67:369–385.  https://doi.org/10.1007/s00018-009-0169-1 CrossRefPubMedGoogle Scholar
  52. Godoy P, Reina R, Calderón A, Wittich R-M, García-Romera I, Aranda E (2016) Exploring the potential of fungi isolated from PAH-polluted soil as a source of xenobiotics-degrading fungi. Environ Sci Pollut Res 23:20985–20996.  https://doi.org/10.1007/s11356-016-7257-1 CrossRefGoogle Scholar
  53. Gomaa OM, Momtaz OA (2015) Copper induction and differential expression of laccase in Aspergillus flavus. Braz J Microbiol 46:285–292.  https://doi.org/10.1590/S1517-838246120120118 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Gururajan K, Belur PD (2018) Screening and selection of indigenous metal tolerant fungal isolates for heavy metal removal. Environ Technol Innov 9:91–99.  https://doi.org/10.1016/j.eti.2017.11.001 CrossRefGoogle Scholar
  55. Guzik U, Hupert-Kocurek K, Wojcieszysk D (2013) Intradiol dioxygenases—the key enzymes in xenobiotics degradation. In: Chamy R (ed) Biodegradation of hazardous and special products. IntechOpen, pp. 129–153.  https://doi.org/10.5772/56205. Available from: https://www.intechopen.com/books/biodegradation-of-hazardous-and-special-products/intradiol-dioxygenases-the-key-enzymes-in-xenobiotics-degradation
  56. Harms H, Schlosser D, Wick LY (2011) Untapped potential: exploiting fungi in bioremediation of hazardous chemicals. Nat Rev Microbiol 9:177–192.  https://doi.org/10.1038/nrmicro2519 CrossRefPubMedGoogle Scholar
  57. Harms H, Wick L, Schlosser D (2017) The fungal community in organically polluted systems. In: Dighton J, White JF (eds) The fungal community: its organization and role in the ecosystem, Fourth edn. CRC Press/Taylor and Francis Group, New York, pp 459–469CrossRefGoogle Scholar
  58. Hong JW, Park JY, Gadd GM (2010) Pyrene degradation and copper and zinc uptake by Fusarium solani and Hypocrea lixii isolated from petrol station soil. J Appl Microbiol 108:2030–2040.  https://doi.org/10.1111/j.1365-2672.2009.04613.x CrossRefPubMedGoogle Scholar
  59. Hutchinson GE (1957) Concluding remarks. Cold Spring Harb Symp Quant Biol 22:415–427.  https://doi.org/10.1101/SQB.1957.022.01.039 CrossRefGoogle Scholar
  60. Ichinose H (2013) Cytochrome P450 of wood-rotting basidiomycetes and biotechnological applications. Biotechnol Appl Biochem 60:71–81.  https://doi.org/10.1002/bab.1061 CrossRefPubMedGoogle Scholar
  61. Iqbal M, Saeed A, Edyvean RGJ, O’Sullivan B, Styring P (2005) Production of fungal biomass immobilized loofa sponge (FBILS)-discs for the removal of heavy metal ions and chlorinated compounds from aqueous solution. Biotechnol Lett 27:1319–1323.  https://doi.org/10.1007/s10529-005-0477-y CrossRefPubMedGoogle Scholar
  62. Jacobs H, Boswell GP, Scrimgeour CM, Davidson FA, Gadd GM, Ritz K (2004) Translocation of carbon by Rhizoctonia solani in nutritionally-heterogeneous microcosms. Mycol Res 108:453–462.  https://doi.org/10.1017/S0953756204009840 CrossRefPubMedGoogle Scholar
  63. Jia Z, Deng J, Chen N, Shi W, Tang X, Xu H (2017) Bioremediation of cadmium–dichlorophen co-contaminated soil by spent Lentinus edodes substrate and its effects on microbial activity and biochemical properties of soil. J Soils Sediments 17:315–325.  https://doi.org/10.1007/s11368-016-1562-7 CrossRefGoogle Scholar
  64. Jiang J, Liu H, Li Q, Gao N, Yao Y, Xu H (2015) Combined remediation of Cd–phenanthrene co-contaminated soil by Pleurotus cornucopiae and Bacillus thuringiensis FQ1 and the antioxidant responses in Pleurotus cornucopiae. Ecotoxicol Environ Saf 120:386–393.  https://doi.org/10.1016/j.ecoenv.2015.06.028 CrossRefPubMedGoogle Scholar
  65. Keesstra S, Geissen V, Mosse K, Piiranen S, Scudiero E, Leistra M, van Schaik L (2012) Soil as a filter for groundwater quality. Curr Opin Environ Sustain 4:507–516.  https://doi.org/10.1016/j.cosust.2012.10.007 CrossRefGoogle Scholar
  66. Kirker GT, Bishell AB, Jusino MA, Palmer JM, Hickey WJ, Lindner DL (2017) Amplicon-based sequencing of soil fungi from wood preservative test sites. Front Microbiol 8:1997.  https://doi.org/10.3389/fmicb.2017.01997 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Liu F, Wu J, Ying G-G, Luo Z, Feng H (2012) Changes in functional diversity of soil microbial community with addition of antibiotics sulfamethoxazole and chlortetracycline. Appl Microbiol Biotechnol 95:1615–1623.  https://doi.org/10.1007/s00253-011-3831-0 CrossRefPubMedGoogle Scholar
  68. Liu S-H, Zeng G-M, Niu Q-Y, Liu Y, Zhou L, Jiang L-H, Tan X, Xu P, Zhang C, Cheng M (2017) Bioremediation mechanisms of combined pollution of PAHs and heavy metals by bacteria and fungi: a mini review. Bioresour Technol 224:25–33.  https://doi.org/10.1016/j.biortech.2016.11.095 CrossRefPubMedGoogle Scholar
  69. Loreau M (2000) Biodiversity and ecosystem functioning: recent theoretical advances. Oikos 91:3–17.  https://doi.org/10.1034/j.1600-0706.2000.910101.x CrossRefGoogle Scholar
  70. Lu M, Zhang Z-Z, Wu X-J, Xu Y-X, Su X-L, Zhang M, Wang J-X (2013) Biodegradation of decabromodiphenyl ether (BDE-209) by a metal resistant strain, Bacillus cereus JP12. Bioresour Technol 149:8–15.  https://doi.org/10.1016/j.biortech.2013.09.040 CrossRefPubMedGoogle Scholar
  71. Ma X, Ling Wu L, Fam H (2014) Heavy metal ions affecting the removal of polycyclic aromatic hydrocarbons by fungi with heavy-metal resistance. Appl Microbiol Biotechnol 98:9817–9827.  https://doi.org/10.1007/s00253-014-5905-2 CrossRefPubMedGoogle Scholar
  72. Ma XK, Li TT, Fam H, Charles Peterson E, Zhao WW, Guo W, Zhou B (2017) The influence of heavy metals on the bioremediation of polycyclic aromatic hydrocarbons in aquatic system by a bacterial–fungal consortium. Environ Technol 39:2128–2137.  https://doi.org/10.1080/09593330.2017.1351492 CrossRefPubMedGoogle Scholar
  73. Markowicz A, Cycoń M, Piotrowska-Seget Z (2016) Microbial community structure and diversity in long-term hydrocarbon and heavy metal contaminated soils. Int J Environ Res 10:321–332.  https://doi.org/10.22059/ijer.2016.57792 CrossRefGoogle Scholar
  74. Mougin C, Cheviron N, Pinheiro M, Lebrun JD, Boukcim H (2013) New insights into the use of filamentous fungi and their degradative enzymes as tools for assessing the ecotoxicity of contaminated soils during bioremediation processes. In: Goltapeh EM, Danesh YR, Varma A (eds) Fungi as bioremediators. Springer, Berlin, Heidelberg, pp 419–432.  https://doi.org/10.1007/978-3-642-33811-3_18 CrossRefGoogle Scholar
  75. Oladipo OG, Awotoye OO, Olayinka A, Bezuidenhout CC, Maboeta MS (2018) Heavy metal tolerance traits of filamentous fungi isolated from gold and gemstone mining sites. Braz J Microbiol 49:29–37.  https://doi.org/10.1016/j.bjm.2017.06.003 CrossRefPubMedGoogle Scholar
  76. Panagos P, Van Liedekerke M, Yigini Y, Montanarella L (2013) Contaminated sites in Europe: review of the current situation based on data collected through a European network. J Environ Public Health 4:1–11.  https://doi.org/10.1155/2013/158764 CrossRefGoogle Scholar
  77. Peay KG, Kennedy PG, Talbot JM (2016) Dimensions of biodiversity in the earth mycobiome. Nat Rev Microbiol 14:434–447.  https://doi.org/10.1038/nrmicro.2016.59 CrossRefPubMedGoogle Scholar
  78. Peng M, Zi X, Wang Q (2015) Bacterial community diversity of oil-contaminated soils assessed by high throughput sequencing of 16S rRNA genes. Int J Environ Res Public Health 12:12002–12015.  https://doi.org/10.3390/ijerph121012002 CrossRefPubMedPubMedCentralGoogle Scholar
  79. Persiani AM, Maggi O, Montalvo J, Casado MA, Pineda FD (2008) Mediterranean grassland soil fungi: patterns of biodiversity, functional redundancy and soil carbon storage. Plant Biosyst 142:111–119.  https://doi.org/10.1080/11263500701872713 CrossRefGoogle Scholar
  80. 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 435–436:402–410.  https://doi.org/10.1016/j.scitotenv.2012.07.027 CrossRefPubMedGoogle Scholar
  81. Polti MA, Aparicio JD, Benimeli CS, Amoroso MJ (2014) Simultaneous bioremediation of Cr(VI) and lindane in soil by actinobacteria. Int Biodeterior Biodegrad 88:48–55.  https://doi.org/10.1016/j.ibiod.2013.12.004 CrossRefGoogle Scholar
  82. Ponomarova O, Patil KR (2015) Metabolic interactions in microbial communities: untangling the Gordian knot. Curr Opin Microbiol 27:37–44.  https://doi.org/10.1016/j.mib.2015.06.014 CrossRefPubMedGoogle Scholar
  83. Prenafeta-Boldú FX, Kuhn A, Luykx DMAM, Anke H, van Groenestijn JW, de Bont JAM (2001) Isolation and characterisation of fungi growing on volatile aromatic hydrocarbons as their sole carbon and energy source. Mycol Res 105:477–484.  https://doi.org/10.1017/S0953756201003719 CrossRefGoogle Scholar
  84. Rao M, Scelza R, Scotti R, Gianfreda L (2010) Role of enzymes in the remediation of polluted environments. J Soil Sci Plant Nutr 10:333–353CrossRefGoogle Scholar
  85. Řezáčová V, Hršelová H, Gryndlerová H, Mikšík I, Gryndler M (2006) Modifications of degradation-resistant soil organic matter by soil saprobic microfungi. Soil Biol Biochem 38:2292–2299.  https://doi.org/10.1016/j.soilbio.2006.02.011 CrossRefGoogle Scholar
  86. Ruiz-Dueñas FJ, Guillén F, Camarero S, Pérez-Boada M, Martínez MJ, Martínez ÁT (1999) Regulation of peroxidase transcript levels in liquid cultures of the ligninolytic fungus Pleurotus eryngii. Appl Environ Microbiol 65:4458–4463PubMedPubMedCentralGoogle Scholar
  87. Sánchez C (2009) Lignocellulosic residues: biodegradation and bioconversion by fungi. Biotechnol Adv 27:185–194.  https://doi.org/10.1016/j.biotechadv.2008.11.001 CrossRefPubMedGoogle Scholar
  88. Sandrin TR, Hoffman DR (2007) Bioremediation of organic and metal co-contaminated environments: effects of metal toxicity, speciation, and bioavailability on biodegradation. In: Singh SN, Tripathi RD (eds) Environmental bioremediation technologies. Springer, Berlin, Heidelberg, pp 1–34Google Scholar
  89. Sandrin TR, Maier RM (2003) Impact of metals on the biodegradation of organic pollutants. Environ Health Perspect 111:1093–1101CrossRefGoogle Scholar
  90. Sandrin TR, Chech AM, Maier RM (2000) A rhamnolipid biosurfactant reduces cadmium toxicity during naphthalene biodegradation. Appl Environ Microbiol 66:4585–4588.  https://doi.org/10.1128/AEM.66.10.4585-4588.2000 CrossRefPubMedPubMedCentralGoogle Scholar
  91. Sharaf EF, Alharbi E (2013) Removal of heavy metals from waste water of tanning leather industry by fungal species isolated from polluted soil. Afr J Biotechnol 12:4351–4355CrossRefGoogle Scholar
  92. Sharma S, Malaviya P (2014) Bioremediation of tannery wastewater by chromium resistant fungal isolate Fusarium chlamydosporium SPFS2-g. Curr World Environ 9:721–727CrossRefGoogle Scholar
  93. Sharma S, Malaviya P (2016) Bioremediation of tannery wastewater by chromium resistant novel fungal consortium. Ecol Eng 91:419–425.  https://doi.org/10.1016/j.ecoleng.2016.03.005 CrossRefGoogle Scholar
  94. Singh AP, Singh T (2014) Biotechnological applications of wood-rotting fungi: a review. Biomass Bioenergy 62:198–206.  https://doi.org/10.1016/j.biombioe.2013.12.013 CrossRefGoogle Scholar
  95. Spina F, Cecchi G, Landinez-Torres A, Pecoraro L, Russo F, Wu B, Cai L, Liu XZ, Tosi S, Varese GC, Zotti M, Persiani AM (2018) Fungi as a toolbox for sustainable bioremediation of pesticides in soil and water. Plant Biosyst 152:474–488.  https://doi.org/10.1080/11263504.2018.1445130 CrossRefGoogle Scholar
  96. Srivastava S, Thakur IS (2006) Isolation and process parameter optimization of Aspergillus sp. for removal of chromium from tannery effluent. Bioresour Technol 97:1167–1173.  https://doi.org/10.1016/j.biortech.2005.05.012 CrossRefPubMedGoogle Scholar
  97. Stenuit BA, Agathos SN (2010) Microbial 2,4,6-trinitrotoluene degradation: could we learn from (bio)chemistry for bioremediation and vice versa? Appl Microbiol Biotechnol 88:1043–1064.  https://doi.org/10.1007/s00253-010-2830-x CrossRefPubMedGoogle Scholar
  98. Stolte J, Tesfai M, Øygarden L, Kværnø S, Keizer J, Verheijen F, Panagos P, Ballabio C, Hessel R (2016) Soil threats in Europe. EUR 27607 EN;  https://doi.org/10.2788/488054 (print);  https://doi.org/10.2788/828742 (online)
  99. Tan T, Cheng P (2003) Biosorption of metal ions with Penicillium chrysogenum. Appl Biochem Biotechnol 104:119–128CrossRefGoogle Scholar
  100. Tortella GR, Diez MC, Durán N (2005) Fungal diversity and use in decomposition of environmental pollutants. Crit Rev Microbiol 31:197–212.  https://doi.org/10.1080/10408410500304066 CrossRefPubMedGoogle Scholar
  101. Treseder KK, Maltz MR, Hawkins BA, Fierer N, Stajich JE, McGuire KL (2014) Evolutionary histories of soil fungi are reflected in their large-scale biogeography. Ecol Lett 17:1086–1093.  https://doi.org/10.1111/ele.12311 CrossRefPubMedGoogle Scholar
  102. Urík M, Gardošová K, Bujdoš M, Matúš P (2014) Sorption of humic acids onto fungal surfaces and its effect on heavy metal mobility. Water Air Soil Pollut 225:1839.  https://doi.org/10.1007/s11270-013-1839-z CrossRefGoogle Scholar
  103. Wang Y, Zhang B, Chen N, Wang C, Feng S, Xu H (2017) Combined bioremediation of soil co-contaminated with cadmium and endosulfan by Pleurotus eryngii and Coprinus comatus. J Soils Sediments 18:2136–2147.  https://doi.org/10.1007/s11368-017-1762-9 CrossRefGoogle Scholar
  104. Wu M, Xu Y, Ding W, Li Y, Xu H (2016) Mycoremediation of manganese and phenanthrene by Pleurotus eryngii mycelium enhanced by Tween 80 and saponin. Appl Microbiol Biotechnol 100:7249–7261.  https://doi.org/10.1007/s00253-016-7551-3 CrossRefPubMedGoogle Scholar
  105. Wuana RA, Okieimen RN, Vesuwe RN (2014) Mixed contaminant interactions in soil: implications for bioavailability, risk assessment and remediation. Afr J Environ Sci Technol 8:691–706.  https://doi.org/10.5897/AJEST2013.1624 CrossRefGoogle Scholar
  106. Xie Y, Fan J, Zhu W, Amombo E, Lou Y, Chen L, Fu J (2016) Effect of heavy metals pollution on soil microbial diversity and bermudagrass genetic variation. Front Plant Sci 7:1–12.  https://doi.org/10.3389/fpls.2016.00755 CrossRefGoogle Scholar
  107. Ye S, Zeng G, Wu H, Zhang C, Liang J, Dai J, Liu Z, Xiong W, Wan J, Xu P, Cheng M (2017) Co-occurrence and interactions of pollutants, and their impacts on soil remediation—a review. Crit Rev Environ Sci Technol 47:1528–1553.  https://doi.org/10.1080/10643389.2017.1386951 CrossRefGoogle Scholar
  108. Zeng G, Huang D, Huang G, Hu T, Jiang X, Feng C, Chen Y, Tang L, Liu H (2007) Composting of lead-contaminated solid waste with inocula of white-rot fungus. Bioresour Technol 98:320–326.  https://doi.org/10.1016/j.biortech.2006.01.001 CrossRefPubMedGoogle Scholar
  109. Zhai Z, Yang T, Zhang B, Zhang J (2015) Effects of metal ions on the catalytic degradation of dicofol by cellulase. J Environ Sci 33:163–168.  https://doi.org/10.1016/j.jes.2014.12.023 CrossRefGoogle Scholar
  110. Zhang M, Pereira e silva Mde C, Chaib De Mares M, van Elsas JD (2014) The mycosphere constitutes an arena for horizontal gene transfer with strong evolutionary implications for bacterial–fungal interactions. FEMS Microbiol Ecol 89:516–526.  https://doi.org/10.1111/1574-6941.12350 CrossRefPubMedGoogle Scholar
  111. Zhang S, Yao H, Lu Y, Yu X, Wang J, Sun S, Liu M, Li D, Li Y-F, Zhang D (2017) Uptake and translocation of polycyclic aromatic hydrocarbons (PAHs) and heavy metals by maize from soil irrigated with wastewater. Sci Rep 7:12165.  https://doi.org/10.1038/s41598-017-12437-w CrossRefPubMedPubMedCentralGoogle Scholar
  112. Zhou Z, Chen Y, Liu X, Zhang K, Xu H (2015) Interaction of copper and 2,4,5-trichlorophenol on bioremediation potential and biochemical properties in co-contaminated soil incubated with Clitocybe maxima. RSC Adv 5:42768–42776.  https://doi.org/10.1039/C5RA04861C CrossRefGoogle Scholar
  113. Zhu Z, Yang X, Wang K, Huang H, Zhang X, Fang H, Li T, Alva AK, He Z (2012) Bioremediation of Cd–DDT co-contaminated soil using the Cd-hyperaccumulator Sedum alfredii and DDT-degrading microbes. J Hazard Mater 235–236:144–151.  https://doi.org/10.1016/j.jhazmat.2012.07.033 CrossRefPubMedGoogle Scholar
  114. Zhu Y, Zhuang L, Goodell B, Cao J, Mahaney J (2016) Iron sequestration in brown-rot fungi by oxalate and the production of reactive oxygen species (ROS). Int Biodeterior Biodegrad 109:185–190.  https://doi.org/10.1016/j.ibiod.2016.01.023 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Laboratorio di Biodiversità dei Funghi, Dipartimento di Biologia AmbientaleSapienza Università di RomaRomeItaly
  2. 2.Centro di Ricerca Agricoltura e AmbienteConsiglio per la Ricerca in agricoltura e l’analisi dell’Economia Agraria (CREA-AA)RomeItaly
  3. 3.Department of Life SciencesNatural History MuseumLondonUK
  4. 4.Geomicrobiology Group, School of Life SciencesUniversity of DundeeDundeeScotland, UK

Personalised recommendations