Abstract
When exposed to higher Pb2+ concentration, Phanerochaete chrysosporium secreted higher content of oxalate and thiol compounds. An earlier and faster increase in oxalate was observed after short-term exposure, comparing with a gentle increase in the thiol compounds. In the extracellular polymeric substances (EPS) extract, more oxalate and T-SH were detected when the initial Pb2+ was higher, and the variations were different from the situation in the culture medium. In EPS solution, the oxalate amount was more closely related with Pb than that of thiol compounds. pH condition in the whole Pb removal process by P. chrysosporium ranged from 4 to 6.5 and was more beneficial for the binding of Pb2+ to carboxylic groups in the oxalic acid. More Pb2+ induced more EPS amount, and the increase of EPS amount influenced the immobilized oxalate more seriously. The present study can supply more comprehensive information about the metal passivation mechanism in white-rot fungi and provide meaningful references for an enhanced removal of heavy metals.
Similar content being viewed by others
References
Baldrian P (2003) Interactions of heavy metals with white-rot fungi. Enzyme Microb Technol 32:78–91
Braissant O, Decho AW, Dupraz C, Glunk C, Przekop KM, Visscher PT (2007) Exopolymeric substances of sulfate-reducing bacteria: interactions with calcium at alkaline pH and implication for formation of carbonate minerals. Geobiology 5:401–411
Braissant O, Decho AW, Przekop KM, Gallagher KL, Glunk C, Dupraz C, Visscher PT (2009) Characteristics and turnover of exopolymeric substances in a hypersaline microbial mat. FEMS Microbiol Ecol 67:293–307
Connolly JH, Jellison J (1995) Calcium translocation, calcium oxalate accumulation, and hyphal sheath morphology in the white-rot fungus Resinicium bicolor. Can J Bot 73:927–936
Dutton MV, Evans CS, Atkey PT, Wood DA (1993) Oxalate production by basidiomycetes, including the white-rot species Coriolus versicolor and Phanerochaete chrysosporium. Appl Microbiol Biotechnol 39:5–10
Fu F, Wang Q (2011) Removal of heavy metal ions from wastewaters: a review. J Environ Manage 92:407–418
Gadd GM (2000) Bioremedial potential of microbial mechanisms of metal mobilization and immobilization. Curr Opin Biotechnol 11:271–279
Galkin S, Vares T, Kalsi M, Hatakka A (1998) Production of organic acids by different white-rot fungi as detected using capillary zone electrophoresis. Biotechnol Tech 12:267–271
Gong JL, Wang B, Zeng GM, Yang CP, Niu CG, Niu QY, Zhou WJ, Liang Y (2009) Removal of cationic dyes from aqueous solution using magnetic multi-wall carbon nanotube nanocomposite as adsorbent. J Hazard Mater 164:1517–1522
Guimarães-Soares L, Pascoal C, Cássio F (2007) Effects of heavy metals on the production of thiol compounds by the aquatic fungi Fontanospora fusiramosa and Flagellospora curta. Ecotoxicol Environ Saf 66:36–43
Hasnain S, Adeli K, Storer AC (1992) Purification and characterization of an extracellular thiol-containing serine proteinase from Thermomyces lanuginosus. Biochem Cell Biol 70:117–122
Hofrichter M, Vares T, Kalsi M, Galkin S, Scheibner K, Fritsche W, Hatakka A (1999) Production of manganese peroxidase and organic acids and mineralization of 14C-labelled lignin (14C-DHP) during solid-state fermentation of wheat straw with the white rot fungus Nematoloma frowardii. Appl Environ Microbiol 65:1864–1870
Horsfall MJ, Spiff AI (2004) Studies on the effect of pH on the sorption of Pb2+ and Cd2+ ions from aqueous solutions by Caladium bicolor (wild cocoyam) biomass. Electron J Biotechnol 7:313–323
Hu GJ, Li JB, Zeng GM (2013) Recent development in the treatment of oily sludge from petroleum industry: a review. J Hazard Mater 261:470–490
Huang DL, Zeng GM, Feng CL, Hu S, Jiang XY, Tang L, Su FF, Zhang Y, Zeng W, Liu HL (2008) Degradation of lead-contaminated lignocellulosic waste by Phanerochaete chrysosporium and the reduction of lead toxicity. Environ Sci Technol 42:4946–4951
Huang DL, Zeng GM, Feng CL, Hu S, Zhao MH, Lai C, Zhang Y, Jiang XY, Liu HL (2010) Mycelial growth and solid-state fermentation of lignocellulosic waste by white-rot fungus Phanerochaete chrysosporium under lead stress. Chemosphere 81:1091–1097
Jarosz-Wilkolazka A, Gadd GM (2003) Oxalate production by wood-rotting fungi growing in toxic metal-amended medium. Chemosphere 52:541–547
Jarosz-Wilkołazka A, Grąz M, Braha B, Menge S, Schlosser D, Krauss GJ (2006) Species-specific Cd-stress response in the white rot basidiomycetes Abortiporus biennis and Cerrena unicolor. Biometals 19:39–49
Kim SJ, Jeong HJ, Myung NY, Kim M, Lee JH, So H, Park RK, Kim HM, Um JY, Hong SH (2008) The protective mechanism of antioxidants in cadmium-induced ototoxicity in vitro and in vivo. Environ Health Perspect 116:854–862
Li NJ, Zeng GM, Huang DL, Hu S, Feng CL, Zhao MH, Lai C, Huang C, Wei Z, Xie GX (2011) Oxalate production at different initial Pb2+ concentrations and the influence of oxalate during solid-state fermentation of straw with Phanerochaete chrysosporium. Bioresour Technol 102:8137–8142
Long G, Zhu P, Shen Y, Tong M (2009) Influence of extracellular polymeric substances (EPS) on deposition kinetics of bacteria. Environ Sci Technol 43:2308–2314
Mäkelä M, Galkin S, Hatakka A, Lundell T (2002) Production of organic acids and oxalate decarboxylase in lignin-degrading white rot fungi. Enzyme Microb Technol 30:542–549
Pellinen J, Abuhasan J, Joyce TW, Chang HM (1989) Biological delignification of pulp by Phanerochaete chrysosporium. J Biotechnol 10:161–170
Rhee Young J, Hillier S, Gadd Geoffrey M (2012) Lead transformation to pyromorphite by fungi. Curr Biol 22:237–241
Rivas BL, Pereira ED, Moreno-Villoslada I (2003) Water-soluble polymer–metal ion interactions. Prog Polym Sci 28:173–208
Say R, Denizli A, Yakup Arıca M (2001) Biosorption of cadmium(II), lead(II) and copper(II) with the filamentous fungus Phanerochaete chrysosporium. Bioresour Technol 76:67–70
Schuster E (1991) The behavior of mercury in the soil with special emphasis on complexation and adsorption processes—a review of the literature. Water Air Soil Pollut 56:667–680
Sedlak J, Lindsay RH (1968) Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal Biochem 25:192–205
Tang WW, Zeng GM, Gong JL, Liang J, Xu P, Zhang C, Huang BB (2014) Removal of heavy metals from aqueous solutions using nanomaterials affected by humic/fulvic acid: a review. Sci Total Environ 468–469:1014–1027
Vacchina V, Baldrian P, Gabriel J, Szpunar J (2002) Investigation of the response of wood-rotting fungi to copper stress by size-exclusion chromatography and capillary zone electrophoresis with ICP MS detection. Anal Bioanal Chem 372:453–456
Vigneshwaran N, Kathe AA, Varadarajan PV, Nachane RP, Balasubramanya RH (2006) Biomimetics of silver nanoparticles by white rot fungus, Phaenerochaete chrysosporium. Colloids Surf B Biointerfaces 53:55–59
Wang LL, Wang LF, Ren XM, Ye XD, Li WW, Yuan SJ, Sun M, Sheng GP, Yu HQ, Wang XK (2011) pH dependence of structure and surface properties of microbial EPS. Environ Sci Technol 46:737–744
Wariish H, Valli K, Renganathan V, Gold MH (1989) Thiol-mediated oxidation of nonphenolic lignin model compounds by manganese peroxidase of Phanerochaete chrysosporium. J Biol Chem 264:14185–14191
Xu P, Zeng GM, Huang DL, Feng CL, Hu S, Zhao MH, Lai C, Wei Z, Huang C, Xie GX, Liu ZF (2012) Use of iron oxide nanomaterials in wastewater treatment: a review. Sci Total Environ 424:1–10
Yetis U, Dolek A, Dilek FB, Ozcengiz G (2000) The removal of Pb(II) by Phanerochaete chrysosporium. Water Res 34:4090–4100
Zeng GM, Huang DL, Huang GH, Hu TJ, Jiang XY, Feng CL, Chen YN, Tang L, Liu HL (2007) Composting of lead-contaminated solid waste with inocula of white-rot fungus. Bioresour Technol 98:320–326
Zeng GM, Chen M, Zeng ZT (2013a) Risks of neonicotinoid pesticides. Science 340:1403
Zeng GM, Chen M, Zeng ZT (2013b) Shale gas: surface water also at risk. Nature 499:154
Acknowledgments
The study was financially supported by the National Natural Science Foundation of China (51278176, 51378190, and 51408206), the Environmental Protection Technology Research Program of Hunan (2007185), the New Century Excellent Talents in University (NECT-13-0186), the Young Teacher Growth Program of Hunan University, the Scientific Research Fund of Hunan Provincial Education Department (521293050), the Fundamental Research Funds for the Central Universities, the Hunan University Fund for Multidisciplinary Developing (531107040762), the Hunan Provincial Innovation Foundation for Postgraduate (CX2014B141), and the Program for Changjiang Scholars and Innovative Research Team in University (IRT-13R17).
Author information
Authors and Affiliations
Corresponding authors
Additional information
Responsible editor: Philippe Garrigues
Rights and permissions
About this article
Cite this article
Li, N., Zeng, G., Huang, D. et al. Response of extracellular carboxylic and thiol ligands (oxalate, thiol compounds) to Pb2+ stress in Phanerochaete chrysosporium . Environ Sci Pollut Res 22, 12655–12663 (2015). https://doi.org/10.1007/s11356-015-4429-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-015-4429-3