Abstract
In this paper, a highly copper-resistant fungal strain NT-1 was characterized by morphological, physiological, biochemical, and molecular biological techniques. Physiological response to Cu(II) stress, effects of environmental factors on Cu(II) biosorption, as well as mechanisms of Cu(II) biosorption by strain NT-1 were also investigated in this study. The results showed that NT-1 belonged to the genus Gibberella, which exhibited high tolerance to both acidic conditions and Cu(II) contamination in the environment. High concentrations of copper stress inhibited the growth of NT-1 to various degrees, leading to the decreases in mycelial biomass and colony diameter, as well as changes in morphology. Under optimal conditions (initial copper concentration: 200 mg L−1, temperature 28 °C, pH 5.0, and inoculum dose 10%), the maximum copper removal percentage from solution through culture of strain NT-1 within 5 days reached up to 45.5%. The biosorption of Cu(II) by NT-1 conformed to quasi-second-order kinetics and Langmuir isothermal adsorption model and was confirmed to be a monolayer adsorption process dominated by surface adsorption. The binding of NT-1 to Cu(II) was mainly achieved by forming polydentate complexes with carboxylate and amide group through covalent interactions and forming Cu-nitrogen-containing heterocyclic complexes via Cu(II)-π interaction. The results of this study provide a new fungal resource and key parameters influencing growth and copper removal capacity of the strain for developing an effective bioremediation strategy for copper-contaminated acidic orchard soils.






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Abdolali A, Ngo HH, Guo W, Zhou JL, du B, Wei Q, Wang XC, Nguyen PD (2015) Characterization of a multi-metal binding biosorbent: chemical modification and desorption studies. Bioresour Technol 193:477–487. https://doi.org/10.1016/j.biortech.2015.06.123
Amirnia S, Ray MB, Margaritis A (2015) Heavy metals removal from aqueous solutions using Saccharomyces cerevisiae in a novel continuous bioreactor–biosorption system. Chem Eng J 264:863–872. https://doi.org/10.1016/j.cej.2014.12.016
Andreazza R, Pieniz S, Wolf L, Lee M-K, Camargo FA, Okeke BC (2010) Characterization of copper bioreduction and biosorption by a highly copper resistant bacterium isolated from copper-contaminated vineyard soil. Sci Total Environ 408:1501–1507. https://doi.org/10.1016/j.scitotenv.2009.12.017
Besnard E, Chenu C, Robert M (2001) Influence of organic amendments on copper distribution among particle size and density fractions in Champagne vineyard soils. Environ Pollut 112:329–337. https://doi.org/10.1016/S0269-7491(00)00151-2
Chen C, Wang J (2016) Uranium removal by novel graphene oxide-immobilized Saccharomyces cerevisiae gel beads. J Environ Radioact 162:134–145. https://doi.org/10.1016/j.jenvrad.2016.05.012
Cooksey DA (1994) Molecular mechanisms of copper resistance and accumulation in bacteria. FEMS Microbiol Rev 14:381–386
Dhillon GS, Kaur S, Brar SK, Verma M (2013) Green synthesis approach: extraction of chitosan from fungus mycelia. Crit Rev Biotechnol 33:379–403. https://doi.org/10.3109/07388551.2012.717217
Dixit R, Wasiullah, Malaviya D, Pandiyan K, Singh U, Sahu A, Shukla R, Singh B, Rai J, Sharma P, Lade H, Paul D (2015) Bioremediation of heavy metals from soil and aquatic environment: an overview of principles and criteria of fundamental processes. Sustainability 7:2189–2212. https://doi.org/10.3390/su7022189
Evangelou V, Marsi M, Chappell M (2002) Potentiometric–spectroscopic evaluation of metal-ion complexes by humic fractions extracted from corn tissue. Spectrochim Acta Part A 58:2159–2175. https://doi.org/10.1016/S1386-1425(01)00690-4
Franco LO, Maia RCC, Porto ALF, Messias AS, Fukushima K, Campos-Takaki GM (2004) Heavy metal biosorption by chitin and chitosan isolated from Cunninghamella elegans (IFM 46109). Braz J Microbiol 35:243–247. https://doi.org/10.1590/S1517-83822004000200013
Fu C, Zhang H, Tu C, Li L, Luo Y (2018) Geostatistical interpolation of available copper in orchard soil as influenced by planting duration. Environ Sci Pollut Res 25:52–63. https://doi.org/10.1007/s11356-016-7882-8
Gimeno-García E, Andreu V, Boluda R (1996) Heavy metals incidence in the application of inorganic fertilizers and pesticides to rice farming soils. Environ Pollut 92:19–25. https://doi.org/10.1016/0269-7491(95)00090-9
Gutierrez T, Biller DV, Shimmield T, Green DH (2012) Metal binding properties of the EPS produced by Halomonas sp. TG39 and its potential in enhancing trace element bioavailability to eukaryotic phytoplankton. Biometals 25:1185–1194. https://doi.org/10.1007/s10534-012-9581-3
Khan Z, Rehman A, Hussain SZ (2016) Resistance and uptake of cadmium by yeast, Pichia hampshirensis 4Aer, isolated from industrial effluent and its potential use in decontamination of wastewater. Chemosphere 159:32–43. https://doi.org/10.1016/j.chemosphere.2016.05.076
Kiran MG, Pakshirajan K, Das G (2017) Heavy metal removal from multicomponent system by sulfate reducing bacteria: mechanism and cell surface characterization. J Hazard Mater 324:62–70. https://doi.org/10.1016/j.jhazmat.2015.12.042
Klis FM, Mol P, Hellingwerf K, Brul S (2002) Dynamics of cell wall structure in Saccharomyces cerevisiae. FEMS Microbiol Rev 26:239–256. https://doi.org/10.1016/S0168-6445(02)00087-6
Letnik I, Avrahami R, Port R, Greiner A, Zussman E, Rokem JS, Greenblatt C (2017) Biosorption of copper from aqueous environments by Micrococcus luteus in cell suspension and when encapsulated. Int Biodeterior Biodegrad 116:64–72. https://doi.org/10.1016/j.ibiod.2016.09.029
Li D, Xu X, Yu H, Han X (2017) Characterization of Pb2+ biosorption by psychrotrophic strain Pseudomonas sp. I3 isolated from permafrost soil of Mohe wetland in Northeast China. J Environ Manag 196:8–15. https://doi.org/10.1016/j.jenvman.2017.02.076
Li WW, Yu HQ (2014) Insight into the roles of microbial extracellular polymer substances in metal biosorption. Bioresour Technol 160:15–23. https://doi.org/10.1016/j.biortech.2013.11.074
Luo Y, Tu C (2018) Twenty years of research and development on soil pollution and remediation in China. Springer, Singapore. https://doi.org/10.1007/978-981-10-6029-8
Mullen M, Wolf D, Beveridge T, Bailey G (1992) Sorption of heavy metals by the soil fungi Aspergillus niger and Mucor rouxii. Soil Biol and Biochem 24:129–135. https://doi.org/10.1016/0038-0717(92)90268-3
Ozdemir G, Ceyhan N, Ozturk T, Akirmak F, Cosar T (2004) Biosorption of chromium (VI), cadmium (II) and copper (II) by Pantoea sp. TEM18. Chem Eng J 102:249–253. https://doi.org/10.1016/j.cej.2004.01.032
Öztürk A, Artan T, Ayar A (2004) Biosorption of nickel (II) and copper (II) ions from aqueous solution by Streptomyces coelicolor A3 (2). Colloids Surf B 34:105–111. https://doi.org/10.1016/j.colsurfb.2003.11.008
Ozturk S, Aslim B, Suludere Z (2009) Evaluation of chromium (VI) removal behaviour by two isolates of Synechocystis sp. in terms of exopolysaccharide (EPS) production and monomer composition. Bioresour Technol 100:5588–5593. https://doi.org/10.1016/j.biortech.2009.06.001
Paraszkiewicz K, Bernat P, Długoński J (2009) Effect of nickel, copper, and zinc on emulsifier production and saturation of cellular fatty acids in the filamentous fungus Curvularia lunata. Int Biodeterior Biodegrad 63:100–105. https://doi.org/10.1016/j.ibiod.2008.03.015
Paraszkiewicz K, Frycie A, Słaba M, Długoński J (2007) Enhancement of emulsifier production by Curvularia lunata in cadmium, zinc and lead presence. Biometals 20:797–805. https://doi.org/10.1007/s10534-006-9043-x
Park JH, Chon HT (2016) Characterization of cadmium biosorption by Exiguobacterium sp. isolated from farmland soil near Cu-Pb-Zn mine. Environ Sci Pollut Res 23:11814–11822. https://doi.org/10.1007/s11356-016-6335-8
Pietrzak U, McPhail DC (2004) Copper accumulation, distribution and fractionation in vineyard soils of Victoria, Australia. Geoderma 122:151–166. https://doi.org/10.1016/j.geoderma.2004.01.005
Puig S, Lee J, Lau M, Thiele DJ (2002) Biochemical and genetic analyses of yeast and human high affinity copper transporters suggest a conserved mechanism for copper uptake. J Biol Chem 277:26021–26030. https://doi.org/10.1074/jbc.M202547200
Sun F, Yan Y, Liao H, Bai Y, Xing B, Wu F (2014) Biosorption of antimony (V) by freshwater cyanobacteria Microcystis from Lake Taihu, China: effects of pH and competitive ions. Environ Sci Pollut Res 21:5836–5848. https://doi.org/10.1007/s11356-014-2522-7
Sun XF, Wang SG, Zhang XM, Chen JP, Li XM, Gao BY, Ma Y (2009) Spectroscopic study of Zn2+ and Co2+ binding to extracellular polymeric substances (EPS) from aerobic granules. J Colloid Interface Sci 335:11–17. https://doi.org/10.1016/j.jcis.2009.03.088
Suresh K, Subramanyam C (1998) Polyphenols are involved in copper binding to cell walls of Neurospora crassa. J Inorg Biochem 69:209–215. https://doi.org/10.1016/S0162-0134(97)10001-0
Tyagi M, Da FM, de Carvalho CC (2011) Bioaugmentation and biostimulation strategies to improve the effectiveness of bioremediation processes. Biodegradation 22:231–241. https://doi.org/10.1007/s10532-010-9394-4
Vesentini D, Dickinson DJ, Murphy RJ (2007) The protective role of the extracellular mucilaginous material (ECMM) from two wood-rotting basidiomycetes against copper toxicity. Int Biodeterior Biodegrad 60:1–7. https://doi.org/10.1016/j.ibiod.2006.11.006
Wang QY, Zhou DM, Cang L (2009) Microbial and enzyme properties of apple orchard soil as affected by long-term application of copper fungicide. Soil Biol Biochem 41:1504–1509. https://doi.org/10.1016/j.soilbio.2009.04.010
Wang T, Yao J, Yuan Z, Zhao Y, Wang F, Chen H (2018) Isolation of lead-resistant Arthrobactor strain GQ-9 and its biosorption mechanism. Environ Sci Pollut Res 25:3527–3538. https://doi.org/10.1007/s11356-017-0694-7
Wang Z, Liu G, Zheng H, Li F, Ngo HH, Guo W, Liu C, Chen L, Xing B (2015) Investigating the mechanisms of biochar’s removal of lead from solution. Bioresour Technol 177:308–317. https://doi.org/10.1016/j.biortech.2014.11.077
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics PCR protocols. In: PCR protocols, a guide to methods and applications, 315–322
Wightwick AM, Mollah MR, Partington DL, Allinson G (2008) Copper fungicide residues in Australian vineyard soils. J Agric Food Chem 56:2457–2464
Wuana RA, Okieimen FE (2011) Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. ISRN Ecol 2011:1–20. https://doi.org/10.5402/2011/402647
Wu G, Kang H, Zhang X, Shao H, Chu L, Ruan C (2010) A critical review on the bio-removal of hazardous heavy metals from contaminated soils: issues, progress, eco-environmental concerns and opportunities. J Hazard Mater 174:1–8. https://doi.org/10.1016/j.jhazmat.2009.09.113
Yahaya YA, Don MM, Bhatia S (2009) Biosorption of copper (II) onto immobilized cells of Pycnoporus sanguineus from aqueous solution: equilibrium and kinetic studies. J Hazard Mater 161:189–195. https://doi.org/10.1016/j.jhazmat.2008.03.104
Yang J, Wei W, Pi S, Ma F, Li A, Wu D, Xing J (2015) Competitive adsorption of heavy metals by extracellular polymeric substances extracted from Klebsiella sp. J1. Bioresour Technol 196:533–539. https://doi.org/10.1016/j.biortech.2015.08.011
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The current research was funded by the National Key R&D Program of China (2016YFE0106400), and the National High Technology Research and Development Program (2012AA06A204-4, 2013AA06A211-4).
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Tu, C., Liu, Y., Wei, J. et al. Characterization and mechanism of copper biosorption by a highly copper-resistant fungal strain isolated from copper-polluted acidic orchard soil. Environ Sci Pollut Res 25, 24965–24974 (2018). https://doi.org/10.1007/s11356-018-2563-4
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DOI: https://doi.org/10.1007/s11356-018-2563-4


