White rot fungi and advanced combined biotechnology with nanomaterials: promising tools for endocrine-disrupting compounds biotransformation

Critical Reviews in Biotechnology

Volumn 38, Issue 5, 2018, Pages 671-689

  Huang, Danlian ^a   Guo, Xueying ^a   Peng, Zhiwei ^a   Zeng, Guangming ^a   Xu, Piao ^a   Gong, Xiaomin ^a   Deng, Rui ^a   Xue, Wenjing ^a   Wang, Rongzhong ^a   Yi, Huan ^a   Liu, Caihong ^a  

^a HUNAN UNIVERSITY   (China)

Author keywords

biotransformation; combined biotechnology; endocrine disrupting compounds; metabolic pathways; nanomaterials; White rot fungi

Indexed keywords

ANTIBIOTICS; BIOCONVERSION; BIODIVERSITY; BIOTECHNOLOGY; ENDOCRINE DISRUPTERS; FUNGI; HEAVY METALS; METABOLISM; NANOSTRUCTURED MATERIALS; POLLUTION; SULFUR COMPOUNDS;

ADVANCED APPLICATIONS; BIOTRANSFORMATION; ENDOCRINE DISRUPTING COMPOUND; INTRACELLULAR METABOLISM; METABOLIC MECHANISM; METABOLIC PATHWAYS; SULFONAMIDE ANTIBIOTICS; WHITE ROT FUNGI;

CHEMICAL CONTAMINATION;

ENDOCRINE DISRUPTOR; HEAVY METAL; NANOMATERIAL; NONYLPHENOL; POLYCHLORINATED BIPHENYL; SULFONAMIDE;

ADSORPTION; BIOCATALYSIS; BIODEGRADATION; BIOTECHNOLOGY; BIOTRANSFORMATION; CELL METABOLISM; HEAVY METAL REMOVAL; MINERALIZATION; NONHUMAN; POLLUTION CONTROL; PRIORITY JOURNAL; REVIEW; WHITE ROT FUNGUS; BIOREMEDIATION; CHEMISTRY; ISOLATION AND PURIFICATION; METABOLISM; PHANEROCHAETE; PHYSIOLOGY;

BIODEGRADATION, ENVIRONMENTAL; BIOTECHNOLOGY; BIOTRANSFORMATION; ENDOCRINE DISRUPTORS; METALS, HEAVY; NANOSTRUCTURES; PHANEROCHAETE;

EID: 85032664375     PISSN: 07388551     EISSN: 15497801     Source Type: Journal    
DOI: 10.1080/07388551.2017.1386613     Document Type: Review

References (151)

1. Garcia-Garcia JD, Sanchez-Thomas R, Moreno-Sanchez R., Bio-recovery of non-essential heavy metals by intra- and extracellular mechanisms in free-living microorganisms. Biotechnol Adv. 2016;34:859–873.
2. Kulkarni M, Chaudhari A., Microbial remediation of nitro-aromatic compounds: an overview. J Environ Manage. 2007;85:496–512.
3. Gore AC, Chappell VA, Fenton SE, et al. Executive summary to EDC-2: the endocrine society's second scientific statement on endocrine-disrupting chemicals. Endocr Rev. 2015;36:593–602.
4. Schug TT, Blawas AM, Gray K, et al. Elucidating the links between endocrine disruptors and neurodevelopment. Endocrinology. 2015;156:1941–1951.
5. Henson MC, Chedrese PJ., Endocrine disruption by cadmium, a common environmental toxicant with paradoxical effects on reproduction. Exp Biol Med (Maywood). 2004;229:383–392.
6. Baulieu E-E, Schumacher M., Progesterone as a neuroactive neurosteroid, with special reference to the effect of progesterone on myelination. Steroids. 2000;65:605–612.
7. Higuchi T., Lignin biochemistry: biosynthesis and biodegradation. Wood Scitechnol. 1990;24:23–63.
8. Barr DP, Aust SD., Mechanisms white rot fungi use to degrade pollutants. Environ Sci Technol. 1994;28:78–87.
9. Tuomela M, Steffen KT, Kerko E, et al. Influence of Pb contamination in boreal forest soil on the growth and ligninolytic activity of litter-decomposing fungi. FEMS Microbiol Ecol. 2005;53:179–186.
10. Yang S, Hai FI, Nghiem LD, et al. Understanding the factors controlling the removal of trace organic contaminants by white-rot fungi and their lignin modifying enzymes: a critical review. Bioresour Technol. 2013;141:97–108.
11. Hofrichter M., Review: lignin conversion by manganese peroxidase (MnP). Enzyme Microb Technol. 2002;30:454–466.
12. Rodríguez-Rodríguez CE, Castro-Gutiérrez V, Chin-Pampillo JS, et al. On-farm biopurification systems: role of white rot fungi in depuration of pesticide-containing wastewaters. FEMS Microbiol Lett. 2013;345:1–12.
13. Xu P, Liu L, Zeng GM, et al. Heavy metal-induced glutathione accumulation and its role in heavy metal detoxification in Phanerochaete chrysosporium. Appl Microbiol Biotechnol. 2014;98:6409–6418.
14. Syed K, Porollo A, Lam YW, et al. A fungal P450 (CYP5136A3) capable of oxidizing polycyclic aromatic hydrocarbons and endocrine disrupting alkylphenols: role of Trp(129) and Leu(324). PLoS One. 2011;6:e28286.
15. 2-requiring oxygenase. P Natl. Acad Sci. 1984;81:2280–2284.
16. Huang DL, Zeng GM, Feng CL, et al. Degradation of lead-contaminated lignocellulosic waste by Phanerochaete chrysosporium and the reduction of lead toxicity. Environ Sci Technol. 2008;42:4946–4951.
17. Martinez D, Larrondo LF, Putnam N, et al. Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78. Nat Biotechnol. 2004;22:695–700.
18. Yang Z, Jia S, Zhang T, et al. How heavy metals impact on flocculation of combined pollution of heavy metals-antibiotics: a comparative study. Sep Purif Technol. 2015;149:398–406.
19. Tang WW, Zeng GM, Gong JL, et al. Impact of humic/fulvic acid on the removal of heavy metals from aqueous solutions using nanomaterials: a review. Sci Total Environ. 2014; 468–469:1014–1027.
20. Tang WW, Zeng GM, Gong JL, et al. Simultaneous adsorption of atrazine and Cu (II) from wastewater by magnetic multi-walled carbon nanotube. Chem Eng J. 2012;211–212:470–478.
21. Pan B, Qiu M, Wu M, et al. The opposite impacts of Cu and Mg cations on dissolved organic matter-ofloxacin interaction. Environ Pollut. 2012;161:76–82.
22. Berg J, Thorsen MK, Holm PE, et al. Cu exposure under field conditions coselects for antibiotic resistance as determined by a novel cultivation-independent bacterial community tolerance assay. Environ Sci Technol. 2010;44:8724–8728.
23. Huang BB, Wang T, Yang Z, et al. Iron-based bimetallic nanocatalysts for highly selective hydrogenation of acetylene in N,N-dimethylformamide at room temperature. ACS Sustain Chem Eng. 2017;5:5049–5058.
24. Tang WW, Peter K, Di H, et al. Fluoride and nitrate removal from brackish groundwaters by batch-mode capacitive deionization. Water Res. 2015;84:342–349.
25. Kato H., In vitro assays: tracking nanoparticles inside cells. Nat Nanotechnol. 2011;6:139–140.
26. Seiwert B, Golan-Rozen N, Weidauer C, et al. Electrochemistry combined with LC-HRMS: elucidating transformation products of the recalcitrant pharmaceutical compound carbamazepine generated by the white-rot fungus Pleurotus ostreatus. Environ Sci Technol. 2015;49:12342–12350.
27. Cao H, Chen X, Jassbi AR, et al. Microbial biotransformation of bioactive flavonoids. Biotechnol Adv. 2015;33:214–223.
28. Kracher D, Scheiblbrandner S, Felice AK, et al. Extracellular electron transfer systems fuel cellulose oxidative degradation. Science. 2016;352:1098–1101.
29. El Majidi N, Bouchard M, Carrier G., Systematic analysis of the relationship between standardized prenatal exposure to polychlorinated biphenyls and mental and motor development during follow-up of nine children cohorts. Regul Toxicol Pharmacol. 2013;66:130–146.
30. Eisenreich SJ, Looney BB, Thornton JD., Airborne organic contaminants in the Great Lakes ecosystem. Environ Sci Technol. 1981;15:30–38.
31. Jan J, Tratnik M., Polychlorinated biphenyls in residents around the River Krupa, Slovenia, Yugoslavia. Bull Environ Contam Toxicol. 1988;41:809–814.
32. Aoki Y. Polychlorinated biphenyls, polychlorinated dibenzo-p-dioxins, and polychlorinated dibenzofurans as endocrine disrupters-what we have learned from Yusho disease. Environ Res. 2001;86:2–11.
33. Newton I, Wyllie I, Asher A., Long-term trends in organochlorine and mercury residues in some predatory birds in Britain. Environ Pollut. 1993;79:143–151.
34. Covaci A, Voorspoels S, Roosens L, et al. Polybrominated diphenyl ethers (PBDEs) and polychlorinated biphenyls (PCBs) in human liver and adipose tissue samples from Belgium. Chemosphere. 2008;73:170–175.
35. Turrio-Baldassarri L, Abate V, Battistelli CL, et al. PCDD/F and PCB in human serum of differently exposed population groups of an Italian city. Chemosphere. 2008;73:228–234.
36. De SPM, Kuch B., Heavy metals, PCDD/F and PCB in sewage sludge samples from two wastewater treatment facilities in Rio de Janeiro State, Brazil. Chemosphere. 2005;60:844–853.
37. Li Q, Wang Y, Luo C, et al. Characteristics and potential sources of polychlorinated biphenyl pollution in a suburban area of Guangzhou, southern China. Atmos Environ. 2017;156:70–76.
38. Eaton DC., Mineralization of polychlorinated biphenyls by Phanerochaete chrysosporium: a ligninolytic fungus. Enzyme Microb Technol. 1985;7:194–196.
39. Thomas DR, Carswell KS, Georgiou G., Mineralization of biphenyl and PCBs by the white rot fungus Phanerochaete chrysosporium. Biotechnol Bioeng. 1992;40:1395–1402.
40. Kamei I, Kogura R, Kondo R. Metabolism of 4,4'-dichlorobiphenyl by white-rot fungi Phanerochaete chrysosporium and Phanerochaete sp. MZ142. Appl Microbiol Biotechnol. 2006;72:566–575.
41. Cajthaml T., Biodegradation of endocrine‐disrupting compounds by ligninolytic fungi: mechanisms involved in the degradation. Environ Microbiol. 2015;17:4822–4834.
42. Yadav J, Quensen J, Tiedje JM, et al. Degradation of polychlorinated biphenyl mixtures (Aroclors 1242, 1254, and 1260) by the white rot fungus Phanerochaete chrysosporium as evidenced by congener-specific analysis. Appl Environ Microbiol. 1995;61:2560–2565.
43. Cameron MD, Aust SD., Degradation of chemicals by reactive radicals produced by cellobiose dehydrogenase from Phanerochaete chrysosporium. Arch Biochem Biophys. 1999;367:1151–1121.
44. Subramanian V, Yadav JS., Regulation and heterologous expression of P450 enzyme system components of the white rot fungus Phanerochaete chrysosporium. Enzyme Microb Technol. 2008;43:205–213.
45. Fujihiro S, Higuchi R, Hisamatsu S, et al. Metabolism of hydroxylated PCB congeners by cloned laccase isoforms. Appl Microbiol Biotechnol. 2009;82:853–860.
46. Cvancarova M, Kresinova Z, Filipova A, et al. Biodegradation of PCBs by ligninolytic fungi and characterization of the degradation products. Chemosphere. 2012;88:1317–1323.
47. Babaei AA, Mahvi AH, Nabizadeh R, et al. Occurrence of nonylphenol an endocrine disrupter in Karun River, Khuzestan Province, Iran. Int J Environ Sci Technol. 2013;11:477–482.
48. Chen HW, Liang CH, Wu ZM, et al. Occurrence and assessment of treatment efficiency of nonylphenol, octylphenol and bisphenol-A in drinking water in Taiwan. Sci Total Environ. 2013;449:20–28.
49. White R, Jobling S, Hoare SA, et al. Environmentally persistent alkylphenolic compounds are estrogenic. Endocrinology. 1994;135:175–182.
50. Chen ML, Chang CC, Shen YJ, et al. Quantification of prenatal exposure and maternal-fetal transfer of nonylphenol. Chemosphere. 2008;73:239–245.
51. Huang DL, Hu CJ, Zeng GM, et al. Combination of Fenton processes and biotreatment for wastewater treatment and soil remediation. Sci Total Environ. 2017;574:1599–1610.
52. Maletz S, Floehr T, Beier S, et al. In vitro characterization of the effectiveness of enhanced sewage treatment processes to eliminate endocrine activity of hospital effluents. Water Res. 2013;47:1545–1557.
53. Kim J, Korshin GV, Velichenko AB., Comparative study of electrochemical degradation and ozonation of nonylphenol. Water Res. 2005;39:2527–2534.
54. Subramanian V, Yadav JS., Role of P450 monooxygenases in the degradation of the endocrine-disrupting chemical nonylphenol by the white rot fungus Phanerochaete chrysosporium. Appl Environ Microbiol. 2009;75:5570–5580.
55. Ting WTE, Yuan SY, Wu SD, et al. Biodegradation of phenanthrene and pyrene by Ganoderma lucidum. Int Biodeterior Biodegradation. 2011;65:238–242.
56. Garcia-Morales R, Rodriguez-Delgado M, Gomez-Mariscal K, et al. Biotransformation of endocrine-disrupting compounds in groundwater: bisphenol A, nonylphenol, ethynylestradiol and triclosan by a laccase cocktail from Pycnoporus sanguineus CS43. Water Air Soil Pollut. 2015;226:251.
57. Mendez-Hernandez JE, Eibes G, Arca-Ramos A, et al. Continuous removal of nonylphenol by versatile peroxidase in a two-stage membrane bioreactor. Appl Biochem Biotechnol. 2015;175:3038–3047.
58. Huang DL, Qin XM, Xu P, et al. Composting of 4-nonylphenol-contaminated river sediment with inocula of Phanerochaete chrysosporium. Bioresour Technol. 2016;221:47–54.
59. Wang J, Majima N, Hirai H, et al. Effective removal of endocrine-disrupting compounds by lignin peroxidase from the white-rot fungus Phanerochaete sordida YK-624. Curr Microbiol. 2012;64:300–303.
60. Syed K, Porollo A, Lam YW, et al. CYP63A2, a catalytically versatile fungal P450 monooxygenase capable of oxidizing higher-molecular-weight polycyclic aromatic hydrocarbons, alkylphenols, and alkanes. Appl Environ Microbiol. 2013;79:2692–2702.
61. Krupiński M, Szewczyk R, Długoński J., Detoxification and elimination of xenoestrogen nonylphenol by the filamentous fungus Aspergillus versicolor. Int Biodeterior Biodegradation. 2013;82:59–66.
62. Syed K, Yadav JS., P450 monooxygenases (P450ome) of the model white rot fungus Phanerochaete chrysosporium. Crit Rev Microbiol. 2012;38:339–363.
63. Travis J., Reviving the antibiotic miracle. Science. 1994;264:360–362.
64. Wise R., Antimicrobial resistance: priorities for action. J Antimicrob Chemother. 2002;49:585–586.
65. Pei R, Kim S-C, Carlson KH, et al. Effect of river landscape on the sediment concentrations of antibiotics and corresponding antibiotic resistance genes (ARG). Water Res. 2006;40:2427–2435.
66. Sarmah AK, Meyer MT, Boxall AB., A global perspective on the use, sales, exposure pathways, occurrence, fate and effects of veterinary antibiotics (VAs) in the environment. Chemosphere. 2006;65:725–759.
67. 4 magnetic nanoparticles as heterogeneous activator of persulfate. J Hazard Mater. 2011;186:1398–1404.
68. Lai HT, Wang TS, Chou CC., Implication of light sources and microbial activities on degradation of sulfonamides in water and sediment from a marine shrimp pond. Bioresour Technol. 2011;102:5017–5023.
69. Huang DL, Wang Y, Zhang C, et al. Influence of morphological and chemical features of biochar on hydrogen peroxide activation: implications on sulfamethazine degradation. Rsc Adv. 2016;6:73186–73196.
70. Barber LB, Keefe SH, LeBlanc DR, et al. Fate of sulfamethoxazole, 4-nonylphenol, and 17β-estradiol in groundwater contaminated by wastewater treatment plant effluent. Environ Sci Technol. 2009;43:4843–4850.
71. Nieto A, Borrull F, Pocurull E, et al. Occurrence of pharmaceuticals and hormones in sewage sludge. Environ Toxicol Chem. 2010;29:1484–1489.
72. Rodríguez-Rodríguez CE, García-Galán MJ, Blánquez P, et al. Continuous degradation of a mixture of sulfonamides by Trametes versicolor and identification of metabolites from sulfapyridine and sulfathiazole. J Hazard Mater. 2012;213:347–354.
73. Reis PJ, Reis AC, Ricken B, et al. Biodegradation of sulfamethoxazole and other sulfonamides by Achromobacter denitrificans PR1. J Hazard Mater. 2014;280:741–749.
74. Gonçalves AG, Órfão JJ, Pereira MFR., Catalytic ozonation of sulphamethoxazole in the presence of carbon materials: catalytic performance and reaction pathways. J Hazard Mater. 2012;239:167–174.
75. Huang DL, Wang RZ, Liu YG, et al. Application of molecularly imprinted polymers in wastewater treatment: a review. Environ Sci Pollut Res Int. 2015;22:963–977.
76. Li X, Xu QM, Cheng JS, et al. Improving the bioremoval of sulfamethoxazole and alleviating cytotoxicity of its biotransformation by laccase producing system under coculture of Pycnoporus sanguineus and Alcaligenes faecalis. Bioresour Technol. 2016;220:333–340.
77. Kim YH., Discovery and characterization of new O-methyltransferase from the genome of the lignin-degrading fungus Phanerochaete chrysosporium for enhanced lignin degradation. Enzyme Microb Technol. 2016;82:66–73.
78. Cañas AI, Camarero S., Laccases and their natural mediators: biotechnological tools for sustainable eco-friendly processes. Biotechnol Adv. 2010;28:694–705.
79. Prieto A, Möder M, Rodil R, et al. Degradation of the antibiotics norfloxacin and ciprofloxacin by a white-rot fungus and identification of degradation products. Bioresour Technol. 2011;102:10987–10995.
80. Suda T, Hata T, Kawai S, et al. Treatment of tetracycline antibiotics by laccase in the presence of 1-hydroxybenzotriazole. Bioresour Technol. 2012;103:498–501.
81. Weng SS, Liu SM, Lai HT., Application parameters of laccase-mediator systems for treatment of sulfonamide antibiotics. Bioresour Technol. 2013;141:152–159.
82. Hasegawa T, Matsuoka Y., Implication of light sources and microbial activities on degradation of sulfonamides in water and sediment from a marine shrimp pond. Bioresour Technol. 2011;102:5017–5023.
83. Majeau JA, Brar SK, Tyagi RD., Laccases for removal of recalcitrant and emerging pollutants. Bioresour Technol. 2010;101:2331–2350.
84. Weng SS, Ku KL, Lai HT., The implication of mediators for enhancement of laccase oxidation of sulfonamide antibiotics. Bioresour Technol. 2012;113:259–264.
85. Winter HR, Unadkat JD., Identification of cytochrome P450 and arylamine N-acetyltransferase isoforms involved in sulfadiazine metabolism. Drug Metab Dispos. 2005;33:969–976.
86. Guo Xl, Zhu Zw, Li Hl. Biodegradation of sulfamethoxazole by Phanerochaete chrysosporium. J Mol Liq. 2014;198:169–172.
87. Valko M, Morris H, Cronin M., Metals, toxicity and oxidative stress. Curr Med Chem. 2005;12:1161–1208.
88. Huang DL, Liu L, Zeng GM, et al. The effects of rice straw biochar on indigenous microbial community and enzymes activity in heavy metal-contaminated sediment. Chemosphere. 2017;174:545–55.
89. Guyot E, Solovyova Y, Tomkiewicz C, et al. Determination of heavy metal concentrations in normal and pathological human endometrial biopsies and in vitro regulation of gene expression by metals in the Ishikawa and Hec-1b endometrial cell line. PLoS One. 2015;10:e0142590.
90. Huang DL, Xue WJ, Zeng GM, et al. Immobilization of Cd in river sediments by sodium alginate modified nanoscale zero-valent iron: impact on enzyme activities and microbial community diversity. Water Res. 2016;106:15–25.
91. Xu P, Zeng GM, Huang DL, et al. Cadmium induced hydrogen peroxide accumulation and responses of enzymatic antioxidants in Phanerochaete chrysosporium. Ecol Eng. 2015;75:110–115.
92. Flora S, Mittal M, Mehta A., Heavy metal induced oxidative stress & its possible reversal by chelation therapy. Indian J Med Res. 2008;128:501–523.
93. Colborn T, vom Saal FS, Soto AM., Developmental effects of endocrine-disrupting chemicals in wildlife and humans. Environ Health Perspect. 1993;101:378–384.
94. Choe SY, Kim SJ, Kim HG, et al. Evaluation of estrogenicity of major heavy metals. Sci Total Environ. 2003;312:15–21.
95. García-García JD, Olin-Sandoval V, Saavedra E, et al. Sulfate uptake in photosynthetic Euglena gracilis. Mechanisms of regulation and contribution to cysteine homeostasis. BBA-Gen Subjects. 2012;1820:1567–1575.
96. Pompella A, Visvikis A, Paolicchi A, et al. The changing faces of glutathione, a cellular protagonist. Biochem Pharmacol. 2003;66:1499–1503.
97. Sun Q, Ye ZH, Wang XR, et al. Cadmium hyperaccumulation leads to an increase of glutathione rather than phytochelatins in the cadmium hyperaccumulator Sedum alfredii. J Plant Physiol. 2007;164:1489–1498.
98. Delalande O, Desvaux H, Godat E, et al. Cadmium-glutathione solution structures provide new insights into heavy metal detoxification. FEBS J. 2010;277:5086–5096.
99. Kristanti RA., Bioremediation of crude oil by white rot fungi Polyporus sp. S133. J Microbiol Biotechnol. 2011;21:995–1000.
100. Grill E, Löffler S, Winnacker E-L, et al. Phytochelatins, the heavy-metal-binding peptides of plants, are synthesized from glutathione by a specific γ-glutamylcysteine dipeptidyl transpeptidase (phytochelatin synthase). Proc Natl Acad Sci. 1989;86:6838–6842.
101. Wünschmann J, Beck A, Meyer L, et al. Phytochelatins are synthesized by two vacuolar serine carboxypeptidases in Saccharomyces cerevisiae. FEBS Lett. 2007;581:1681–1687.
102. Schneider T, Schellenberg M, Meyer S, et al. Quantitative detection of changes in the leaf‐mesophyll tonoplast proteome in dependency of a cadmium exposure of barley (Hordeum vulgare L.) plants. Proteomics. 2009;9:2668–2677.
103. Mendoza-Cózatl DG, Zhai Z, Jobe TO, et al. Tonoplast-localized Abc2 transporter mediates phytochelatin accumulation in vacuoles and confers cadmium tolerance. J Biol Chem. 2010;285:40416–40426.
104. Dorčák V, Krężel A., Correlation of acid-base chemistry of phytochelatin PC2 with its coordination properties towards the toxic metal ion Cd (II). Dalton T. 2003;11:2253–2259.
105. Huang Y, Liao B, Xiao L., Relieving of Cd toxicity to glycine max seedlings by spraying NAA and added Zn. Ecol Environ. 2008;1:240–244.
106. Wang W, Xu W, Zhou K, et al. Research progressing of present contamination of Cd in soil and restoration method. Wuhan Univ J Nat Sci. 2015;20:430–444.
107. Zhou J, Yang Y, Zhang CY., Toward biocompatible semiconductor quantum dots: from biosynthesis and bioconjugation to biomedical application. Chem Rev. 2015;115:11669–11717.
108. Cobbett C, Goldsbrough P., Phytochelatins metallothioneins roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol. 2002;53:159–182.
109. Kang SH, Singh S, Kim JY, et al. Bacteria metabolically engineered for enhanced phytochelatin production and cadmium accumulation. Appl Environ Microbiol. 2007;73:6317–6320.
110. Liu P, Luo L, Guo J, et al. Farnesol induces apoptosis and oxidative stress in the fungal pathogen Penicillium expansum. Mycologia. 2010;102:311–318.
111. Sutherland DE, Stillman MJ., Challenging conventional wisdom: single domain metallothioneins. Metallomics. 2014;6:702–728.
112. Das D, Chakraborty A, Santra S., Characteristics of metabolic changes and antioxidative response in a potential zinc tolerant fungal strain, Aspergillus terreus. Proc Natl A Sci India B. 2015;87:1-8.
113. Pan F, Wang R, Englert U., Switching from bonding to nonbonding: temperature-dependent metal coordination in a zinc (II) sulfadiazine complex. Inorg Chem. 2011;51:769–771.
114. Baldrian P., Interactions of heavy metals with white-rot fungi. Enzyme Microb Technol. 2003;32:78–91.
115. Wan J, Zeng GM, Huang DL, et al. The oxidative stress of Phanerochaete chrysosporium against lead toxicity. Appl Biochem Biotechnol. 2015;175:1981–1991.
116. Forney LJ, Reddy CA, Tien M, et al. The involvement of hydroxyl radical derived from hydrogen peroxide in lignin degradation by the white rot fungus Phanerochaete chrysosporium. J Biol Chem. 1982;257:11455–11462.
117. Park JS, Wood PM, Davies MJ, et al. A kinetic and ESR investigation of iron (II) oxalate oxidation by hydrogen peroxide and dioxygen as a source of hydroxyl radicals. Free Radic Res. 1997;27:447–458.
118. Vallino M, Martino E, Boella F, et al. Cu,Zn superoxide dismutase and zinc stress in the metal-tolerant ericoid mycorrhizal fungus Oidiodendron maius Zn. FEMS Microbiol Lett. 2009;293:48–57.
119. Erill I, Campoy S, Barbé J., Aeons of distress: an evolutionary perspective on the bacterial SOS response. FEMS Microbiol Rev. 2007;31:637–656.
120. Godon C, Coullet S, Baus B, et al. Quantitation of p53 nuclear relocation in response to stress using a yeast functional assay: effects of irradiation and modulation by heavy metal ions. Oncogene. 2005;24:6459–6464.
121. Hakem R. DNA-damage repair; the good, the bad, and the ugly. EMBO J. 2008;27:589–605.
122. Shen M, Zhao DK, Qiao Q, et al. Identification of glutathione S-transferase (GST) genes from a dark septate endophytic fungus (Exophiala pisciphila) and their expression patterns under varied metals stress. PLoS One. 2015;10:e0123418.
123. Jin B, Robertson KD., DNA methyltransferases, DNA damage repair, and cancer. Epigenetic Alterations in Oncogenesis, vol. 754. New York: Springer; 2013. p. 3–29.
124. Marteijn JA, Lans H, Vermeulen W, et al. Understanding nucleotide excision repair and its roles in cancer and ageing. Nat Rev Mol Cell Biol. 2014;15:465–481.
125. Gong XM, Huang DL, Liu YG, et al. Remediation of contaminated soils by biotechnology with nanomaterials: bio-behavior, applications, and perspectives. Crit Rev Biotechnol. 2017. DOI:10.1080/07388551.2017.1368446
126. Žgur-Bertok D., DNA damage repair and bacterial pathogens. PLoS Pathog. 2013;9:e1003711.
127. Zheng G, Fu Y, He C., Nucleic acid oxidation in DNA damage repair and epigenetics. Chem Rev. 2014;114:4602–4620.
128. Luna A, Aladjem MI, Kohn KW., SIRT1/PARP1 crosstalk: connecting DNA damage and metabolism. Genome Integr. 2013;4:6.
129. 2/graphene photocatalyst and its highly efficient photocatalytic degradation of target pollutant under visible light irradiation. Appl Surf Sci. 2016;390:368–376.
130. Wang H, Yuan XZ, Wu Y, et al. Plasmonic Bi nanoparticles and BiOCl sheets as cocatalyst deposited on perovskite-type ZnSn(OH) 6 microparticle with facet-oriented polyhedron for improved visible-light-driven photocatalysis. Appl Catal B Environ. 2017;209:543–553.
131. Wang H, Yuan XZ, Wu Y, et al. In situ synthesis of In2S3@MIL-125(Ti) core-shell microparticle for the removal of tetracycline from wastewater by integrated adsorption and visible-light-driven photocatalysis. Appl Catal B Environ. 2016;186:19–29.
132. Wang H, Yuan X, Zeng GM, et al. Three dimensional graphene based materials: synthesis and applications from energy storage and conversion to electrochemical sensor and environmental remediation. Adv Colloid Interface Sci. 2015;221:41–59.
133. Wang H, Yuan X, Wu Y, et al. Adsorption characteristics and behaviors of graphene oxide for Zn(II) removal from aqueous solution. Appl Surf Sci. 2013;279:432–440.
134. Yi H, Zeng G, Lai C, et al. Environment-friendly fullerene separation methods. Chem Eng J. 2017;330:134–145.
135. Xu P, Zeng GM, Huang DL, et al. Use of iron oxide nanomaterials in wastewater treatment: a review. Sci Total Environ. 2012;424:1–10.
136. Kim Y, Lee BG, Roh Y., Microbial synthesis of silver nanoparticles. J Nanosci Nanotechnol. 2013;13:3897–3900.
137. Xu P, Zeng GM, Huang DL, et al. Adsorption of Pb(II) by iron oxide nanoparticles immobilized Phanerochaete chrysosporium: equilibrium, kinetic, thermodynamic and mechanisms analysis. Chem Eng J. 2012;203:423–431.
138. Zuo Y, Chen GQ, Zeng GM, et al. Transport, fate, and stimulating impact of silver nanoparticles on the removal of Cd(II) by Phanerochaete chrysosporium in aqueous solutions. J Hazard Mater. 2015;285:236–244.
139. Guo Z, Chen GQ, Liu L, et al. Activity variation of Phanerochaete chrysosporium under nanosilver exposure by controlling of different sulfide sources. Sci Rep. 2016;6:20813.
140. Wirth SM, Lowry GV, Tilton RD., Natural organic matter alters biofilm tolerance to silver nanoparticles and dissolved silver. Environ Sci Technol. 2012;46:12687–12696.
141. Mukherjee P, Roy M, Mandal BP, et al. Green synthesis of highly stabilized nanocrystalline silver particles by a non-pathogenic and agriculturally important fungus T. asperellum. Nanotechnology. 2008;19:075103.
142. Espinosa-Ortiz EJ, Shakya M, Jain R, et al. Sorption of zinc onto elemental selenium nanoparticles immobilized in Phanerochaete chrysosporium pellets. Environ Sci Pollut Res. 2016;23:1–12.
143. Dhanjal S, Cameotra SS., Aerobic biogenesis of selenium nanospheres by Bacillus cereus isolated from coalmine soil. Microb Cell Fact. 2010;9:11.
144. Espinosa-Ortiz EJ, Gonzalez-Gil G, Saikaly PE, et al. Effects of selenium oxyanions on the white-rot fungus Phanerochaete chrysosporium. Appl Microbiol Biotechnol. 2015;99:2405–2418.
145. Jain R, Dominic D, Jordan N, et al. Preferential adsorption of Cu in a multi-metal mixture onto biogenic elemental selenium nanoparticles. Chem Eng J. 2016;284:917–925.
146. Kim YH, Lee HS, Kwon HJ, et al. Effects of different selenium levels on growth and regulation of laccase and versatile peroxidase in white-rot fungus, Pleurotus eryngii. World J Microbiol Biotechnol. 2014;30:2101–2109.
147. Espinosa-Ortiz EJ, Rene ER, Pakshirajan K, et al. Fungal pelleted reactors in wastewater treatment: applications and perspectives. Chem Eng J. 2016;283:553–571.
148. 2 nanoparticles: the role of the minority (001) surface. J Phys Chem B. 2005;109:19560–19562.
149. 2 nanoparticles. Appl Microbiol Biotechnol. 2013;97:3149–3157.
150. 2 nanoparticles after exposure to toxic pollutants in solution. Chemosphere. 2015;128:21–27.
151. Kamwilaisak K, Wright PC., Investigating laccase and titanium dioxide for lignin degradation. Energy Fuels. 2012;26:2400–2406.