p-ISSN: 0972-6268 Nature Environment and Pollution Technology (Print copies up to 2016) Vol. 20 No. 2 pp. 579-585 2021 An International Quarterly Scientific Journal e-ISSN: 2395-3454

Original Research Paper Originalhttps://doi.org/10.46488/NEPT.2021.v20i02.014 Research Paper Open Access Journal

Biosorption of Cu(II) from Aqueous Solutions by a Macrofungus ( lobatum) Biomass and its Biochar

Silin Yang, Yan Wang and Yungen Liu† Faculty of Ecology and Environment, Southwest Forestry University, Kunming 650224, China †Corresponding author: Yungen Liu; [email protected]

ABSTRACT Nat. Env. & Poll. Tech. Website: www.neptjournal.com The sorption capacities of the macrofungus viz. Ganoderma lobatum (C0) and its biochar (C400) were evaluated for the biosorption of Cu(II) from aqueous solution under different conditions, including Received: 18-03-2020 adsorbent doses, pH of the solution, contact time and initial Cu(II) concentration. The results showed Revised: 25-04-2020 Accepted: 15-06-2020 that Ganoderma lobatum could be used as an efficient biosorbent for the removal of Cu(II) ions from an aqueous solution. The desired biosorbent dose in the case of C0 and C400 for Cu(II) adsorption Key Words: was 4 g/L, and the optimal pH value for biosorption was 8 for Cu(II). The Freundlich isotherm model Macrofungus fitted the absorption data of Cu(II) for both C0 and C400 better than the Langmuir isotherm model, and Biochar the adsorption capacity of C0 was better than C400. Our results indicate that C0 has a higher removal Sorption efficiency than C400 in adsorbing Cu(II) ions from aqueous solution. Biosorption kinetics were also Copper ion studied using pseudo-first-order and pseudo-second-order models, which showed that the biosorption processes of Cu(II) ions based on C0 and C400 were in accordance with the pseudo-second-order kinetics.

INTRODUCTION the case of microorganisms (Muraleedharan et al. 1994). The adsorption capacity of macrofungi clearly depends on the Water pollution by heavy metals at low concentrations is species (Nagy et al. 2014). To our knowledge, no reports in a worldwide environmental problem. Many methods have the literature have examined the biosorption of heavy metal been widely used to remove these toxic substances (Fomina using the macrofungus Ganoderma lobatum. It is a species & Gadd 2014). However, these methods have become of wood-decaying fungi in the family less effective because of low metal concentrations (Wang (order ), widely distributed in China, America & Chen 2009). Therefore, as an excellent alternative to and Mexico, growing alone or gregariously on decaying conventional techniques, biosorption has emerged as the logs and stumps of various hardwoods. The cap is flat and most promising process for treating pollutants in the aquatic up to 20 cm wide, and the flesh of the cap is dark brown to environment, especially the removal of low concentrations cinnamon-brown, woody. of heavy metals in the aqueous environment, because of its high efficiency, low cost, and non-hazardous nature (Javaid The aim of the present work was to investigate the bio- et al. 2011, Kapoor & Viraraghavan 1995). In recent years, sorption potential of the fruit body of Ganoderma lobatum macrofungi have attracted attention as biosorbents. Many and its biochar for the removal of Cu(II) from an aqueous studies have confirmed that copper ions in aqueous solutions solution. Optimum biosorption conditions were determined as a function of the biomass dose, pH, contact time, and are effectively adsorbed by the fruit bodies of macrofungi such as Pycnoporus sanguineus (Zulfadhly et al. 2001), initial metal concentration. The Langmuir and Freundlich Agaricus macrosporus (Melgar et al. 2007), Pleurotus models were employed to describe equilibrium isotherms. ostreatus (Javaid et al. 2011), Auricularia polytricha (Xinyu Biosorption mechanisms of Cu(II) onto Ganoderma lobatum et al. 2010), and Auricularia polytricha (Yu et al. 2010). and its biochar were also evaluated in terms of kinetics. Moreover, macrofungi grow prolifically and are found in many parts of the world (Vimala et al. 2011). They are MATERIALS AND METHODS visible in size, tough in texture, and have other physical Biosorbent Preparation characteristics that are conducive to their development as biosorbents without the need for immobilization or The macrofungus Ganoderma lobatum was collected from deployment of a sophisticated reactor configuration, as in Mojiang County, Yunnan Province, China. Fruit bodies were 580 Silin Yang et al. washed 3 times using distilled water, sun-dried for 3 days, studies were performed for different metal concentrations and then dried in an oven at 80°C for 48 h. The dried fruit (10-200 mg/L), pH (3-10), biosorbent doses (0.4-8 g/L), and bodies were ground and then filtered through a 2-mm nylon contact times (10-1440 min). The contents of the flask were sieve. The dried samples were placed in clean polyethene filtered, and the residual metal concentration in the filtrates sample bags, labelled C0 for future use, and a portion of the was determined by ICP-OES (VISFA-MPX). Each sample dried samples was pyrolyzed in an electrical muffle furnace was evaluated three times, and the results are presented as at 400 °C for 4 h under oxygen-limited conditions. After average values. cooling to room temperature, they were filtered through a ToTo evaluate evaluateTo theevaluate the adsorption adsorption the adsorption capacity capacity ofcapacity Cu of(II) Cu(II) ofonto Cu onto(II)C0 andonto C0 C400, C0 and the C400, amount the of amount Cu(II) of Cu(II) 2-mm nylon sieve and stored in clean polyethene sample and C400, the amount of Cu(II) adsorbed per unit mass of bags labelled C400 for future experiments. adsorbedC0 and adsorbedper C400 unit was mass per calculated unit of C0 mass and ofusing C400 C0 andthe was followingC400 calculated was calculatedequation: using the using following the following equation: equation: V (C  C ) V (C  C ) Reagents and Equipment 0 Ve(C0  Ce ) 0 V (t C0  Ct ) Qe  Q  , Qt  , Q  …(1) …(1 ) …(1) eM tM All chemicals used in this study were of analytical grade, M M Where Q (mg/g) is the amount of Cu(II) biosorbed onto and deionized water was used for all dilutions. A pH meter Where QeW (mg/g)here eQ ise (mg/g)the amount is the of amount Cu(II) ofbiosorbed Cu(II) biosorbed onto the biosorbentonto the biosorbent at equilibrium at equilibrium, C0 and C, Ce 0 and Ce (Leici, ZD-2) was used to measure pH values in the aque- the biosorbent at equilibrium, C0 and Ce respectively are the ous phase. Cu(II) concentrations in the aqueous phase were respectivelyinitial respectivelyand are equilibrium the initial are the concentrationand initial equilibrium and equilibrium (mg/L) concentration of Cu(II), concentration (mg/L V(L)) of ( mg/LCu(II),) of V Cu(L)(II), is the V(L) volume is the of volume of determined by ICP-OES (VISFA-MPX). Fourier Transform is the volume of the solution and M (g) is the biosorbent dose, the solutionthe andsolution M (g) and is theM (g)biosorbent is the biosorbent dose, Qt (mg/g)dose, Q ist (mg/g) the amount is the of amount Cu(II) of biosorbed Cu(II) biosorbed onto onto Infrared (FT-IR) spectra of C0 and C400 prepared as KBr Qt (mg/g) is the amount of Cu(II) biosorbed onto biosorbent −1 pellets were recorded in the 400-4000 cm region using a at time t (min), and Ctt (mg/L) is the concentration of Cu(II) biosorbentbiosorbent at time t (min),at time and t (min), Ctt ( mg/L)and Ct ist ( mg/L)the concentration is the concentration of Cu(II) of at Cu(II)time t (min)at time. t (min). Varian FT-IR 640 spectrometer. at time t (min).

A stock Cu(II) solution of 1000 mg/L was prepared by (C0  Ce(C) 0  Ce ) Re  Re  100%  100 % …(2) …(2) …(2) dissolving 3.8019 g Cu(NO3)2∙3H2O in 1000 mL of deionized C0 C0 water. The Cu(NO3)2∙3H2O used in this work was analytical grade and was supplied by Sinopharm Chemical Reagent Co., Where Re is the ratio between Cu(II) biosorbed at equi- Where RWe hereis the R eratio is the between ratio betweenCu(II) biosorbedCu(II) biosorbed at equilibrium at equilibrium and the andinitial the Cu(II) initial Cu(II) Ltd. (China). Stock solutions were used to prepare diluted librium and the initial Cu(II) concentration (mg/L). solutions of different working concentrations. HCl (0.1 M) concentrationconcentration (mg/L). (mg/L). and NaOH (0.1 M) volumetric solutions were used to adjust RESULTS AND DISCUSSION the solution pH. RESULTSFT-IRRESULTS Analysis AND DISCUSSION AND DISCUSSION Batch Biosorption Experiments Functional groups, such as carbonyl, carboxyl, and hydroxyl The batch biosorption experiments for C0 and C400 were groups, have been identified as potential adsorption sites FT-IR AFTnalysis-IR Analysis carried out in 150-mL stoppered conical flasks containing 0.2 responsible for binding metallic ions to the adsorbent. g of the biosorbent in 50 mL of the Cu(II) solutions (10 mg/L) The FT-IR spectra of C0 and C400 in the range from 400- Functional−1 Functional groups, such groups, as carbonyl, such as carbonyl, carboxyl, carboxyl, and hydroxyl and hydroxyl groups, havegroups, been have identified been identified as as separatelyal. at 2002). room temperature on a rotary shaker at 100 4000 cm were determined and are presented in Fig. 1. For rpm. For optimization of the experimental conditions, batch the biomass material C0, the broad and strong absorption potential potentialadsorption adsorption sites responsible sites responsible for binding for metallic binding ionsmetallic to the ions adsorbent. to the adsorbent. The FT- IRThe spectra FT-IR spectra

−1 of C0 and C400 in the range from 400-−40001 cm were determined and are presented in Fig. 1. For a of C0 and C400 in the range from 400-4000 cm were determined and are presented in Fig. 1. For b −1 the biomassthe materialbiomass C0,material the broad C0, the and broad strong and absorption strong absorption band at approximatelyband at approximately 3200-3600 3200 cm-−36001 cm

could be attributed to stretching vibrations of hydroxyl groups (–OH). The peak observed at 2925 could be attributed to stretching vibrations of hydroxyl groups (–OH). The peak observed at 2925 −1 −1 −1 cm was due to C–H stretching of CH2 groups. The band at −16391 cm indicated a fingerprint region cm was due to C–H stretching of CH2 groups. The band at 1639 cm indicated a fingerprint region Transmittance

) of C=O, C–O, and O–H groups that exist as functional groups (Wang & Chen 2009). The bands Transmittance % of C=O, C–O, and O–H groups that exist as functional groups (Wang & Chen 2009). The bands ( ) −1 %

( observed at −10741 cm were assigned to C–O stretching of alcohols and carboxylic acids (Fig.1a)

observed at 1074 cm were assigned to C–O stretching of alcohols and carboxylic acids (Fig.1a) (Fomina & Gadd 2014). For the calcined C400, the absorption bands of various functional groups (Fomina & Gadd 2014). For the calcined C400, the absorption bands of various functional groups -1 -1 Wavenumber (cm ) disappeared,Wavenumber indicating (cm that) the organic structure of the fungal biomass had been decomposed at a disappeared, indicating that the organic structure of the fungal biomass had been decomposed at a Fig. 1: FT-IR spectrum of the macrofungus (Ganoderma lobatum) (a) and its biochar (b). Fig. 1: FT-IR spectrum of the macrofungus (Ganodermahigh temperature lobatum) (a)(Fig. and 1b). its biocharAs shown (b). in Fig. 1b, the weak bands at approximately 1620 and 849 high temperature (Fig. 1b). As shown in Fig. 1b, the weak bands at approximately 1620 and 849 cm−1 were attributed to the vibrations of C=C and C–C, respectively. FT-IR studies revealed that Vol. 20, No. 2, 2021 • Nature Environment and Pollution Technology−1 Effect of the Adsorbent Dose cm were attributed to the vibrations of C=C and C–C, respectively. FT-IR studies revealed that several functional groups, which can bind transition metal ions including Cu(II), were present in C0. several functional groups, which can bind transition metal ions including Cu(II), were present in C0. The effect of the adsorbent dose on the Cu(II) ion Theseremoval functi efficiencyonal groups is presentedwere mainly in derivedFig. 2. from the cellulose, hemicellulose, and lignin of the These functional groups were mainly derived from the cellulose, hemicellulose, and lignin of the The removal efficiencies (%) were found to increase steeplyfungal with cell wall,increasing as well concentrations as some other kinds of C0 of organic components (Dashtban et al. 2009, Pérez et fungal cell wall, as well as some other kinds of organic components (Dashtban et al. 2009, Pérez et 4 and C400 up to a dose of 4 g/L. The maximum removal efficiencies of C0 and C400 respectively4

were 97.80% and 96.89% at the adsorbent dose of 4 g/L. However, beyond this dose, the increase

in removal efficiencies of C0 and C400 were marginal and became nearly constant. Similar results

have been reported for metal ion biosorption in an aqueous solution by oyster mushroom (Pleurotus

platypus) (Vimala & Das 2009). Therefore, the optimum adsorbent dose was considered to be 4 g/L

for further experiments. The above results can be explained by the finding that the biosorption sites

remain unsaturated during the biosorption reaction, whereas the number of sites available for

biosorption site increases by increasing the biosorbent dose (Sar & Tuzen 2009b). However, a high

adsorbent dose results in aggregates of adsorbent due to interference between binding sites at a

higher adsorbent dose or insufficient metal ions in the solution with respect to available binding

sites (Rome & Gadd 1987). Moreover, protons might combine with metal ions for ligands and

thereby decrease the interaction of metal ions with cell components (Ghorbani et al. 2008, Sağ &

Kutsal 1996).

5

BIOSORPTION OF CU(II) FROM AQUEOUS SOLUTIONS BY A MACROFUNGUS BIOMASS 581

band at approximately 3200-3600 cm−1 could be attributed results can be explained by the finding that the biosorption to stretching vibrations of hydroxyl groups (–OH). The peak sites remain unsaturated during the biosorption reaction, −1 observed at 2925 cm was due to C–H stretching of CH2 whereas the number of sites available for biosorption site groups. The band at 1639 cm−1 indicated a fingerprint region increases by increasing the biosorbent dose (Sar & Tuzen of C=O, C–O, and O–H groups that exist as functional groups 2009b). However, a high adsorbent dose results in aggregates (Wang & Chen 2009). The bands observed at 1074 cm−1 were of adsorbent due to interference between binding sites at a assigned to C–O stretching of alcohols and carboxylic acids higher adsorbent dose or insufficient metal ions in the solu- (Fig.1a) (Fomina & Gadd 2014). For the calcined C400, the tion with respect to available binding sites (Rome & Gadd absorption bands of various functional groups disappeared, 1987). Moreover, protons might combine with metal ions indicating that the organic structure of the fungal biomass for ligands and thereby decrease the interaction of metal had been decomposed at a high temperature (Fig. 1b). As ions with cell components (Ghorbani et al. 2008, Sağ & shown in Fig. 1b, the weak bands at approximately 1620 and Kutsal 1996). 849 cm−1 were attributed to the vibrations of C=C and C–C, respectively. FT-IR studies revealed that several functional Effect of pH groups, which can bind transition metal ions including Cu(II), The effect of initial pH on the removal efficiencies of Cu(II) were present in C0. These functional groups were mainly ions onto adsorbent were investigated from pH 3-10 for derived from the cellulose, hemicellulose, and lignin of the initial metal concentration of 10 mg/L Cu(II) solution. the fungal cell wall, as well as some other kinds of organic The results for the pH effect on the removal efficiencies of components (Dashtban et al. 2009, Pérez et al. 2002). Cu(II) are shown in Fig. 3. The removal efficiencies of C0 Effect of the Adsorbent Dose and C400 for Cu(II) ions increased from 90% to 97% and from 93% to 97%, respectively, as the pH was increased The effect of the adsorbent dose on the Cu(II) ion removal from 3 to 8. The maximum removal efficiencies of 97 % efficiency is presented in Fig. 2. The removal efficiencies (%) were found at pH 8 for the two adsorbents. Therefore, were found to increase steeply with increasing concentrations all the biosorption experiments were carried out at pH 8. of C0 and C400 up to a dose of 4 g/L. The maximum removal Previous researchers have indicated that pH is one of the efficiencies of C0 and C400 respectively were 97.80% and most important factors affecting the adsorption of heavy 96.89% at the adsorbent dose of 4 g/L. However, beyond this metal ions from aqueous solution. This parameter is directly dose, the increase in removal efficiencies of C0 and C400 related to the competition ability of hydrogen ions with metal were marginal and became nearly constant. Similar results ions for active sites on the biosorbent surface (Senthilkumar have been reported for metal ion biosorption in an aqueous et al. 2011, Tsai et al. 2007). Generally, metal biosorption solution by oyster mushroom (Pleurotus platypus) (Vimala involves complex mechanisms of ion-exchange, chelation, & Das 2009). Therefore, the optimum adsorbent dose was adsorption by physical forces, and ion entrapment in inter considered to be 4 g/L for further experiments. The above and intrafibrillar capillaries and spaces of the cell structural network of a biosorbent (Chojnacka et al. 2005). At low pH values, protons occupy most of the biosorption sites

on the biosorbent surface, and fewer copper ions can be absorbed because of the electric repulsion with protons on the

Cu(II) biosorbent. When the pH values increase, biosorbent surfaces are more negatively charged, and the biosorption of metal ions (positive charge) increases and reaches equilibrium at pH 8. Decreases in biosorption at higher pH values (> 8) are due to the formation of soluble hydroxylated complexes of the metal ions and their competition with the active sites, resulting in a repeated decrease in retention (Anayurt et al. 2009, Sar & Tuzen 2009a). Percentage Removal Percentage Removal The FT-IR spectroscopic analysis showed that the macro- (C0) had various functional groups, and these groups were involved in almost all potential binding mechanisms. Biosorbent dose (g/L) Moreover, depending on the pH value of the aqueous solu- Fig. 2: Effect of the biosorbent dose on Cu(II) removal efficiencies by the tion, these functional groups participate in metal ion binding macrofungus (Ganoderma lobatum) and its biochar. (Sar & Tuzen 2009a). Fig. 2: Effect of the biosorbent dose on Cu(II) removal efficiencies by the macrofungus (Ganoderma Nature Environment and Pollution Technology • Vol. 20, No.2, 2021 lobatum) and its biochar.

Effect of pH

The effect of initial pH on the removal efficiencies of Cu(II) ions onto adsorbent were investigated from pH 3-10 for the initial metal concentration of 10 mg/L Cu(II) solution. The results for the pH effect on the removal efficiencies of Cu(II) are shown in Fig. 3. The removal efficiencies of C0 and C400 for Cu(II) ions increased from 90% to 97% and from 93% to 97%, respectively, as the pH was increased from 3 to 8. The maximum removal efficiencies of 97 % were found at pH 8 for the two adsorbents. Therefore, all the biosorption experiments were carried out at pH 8. Previous researchers have indicated that pH is one of the most important factors affecting the adsorption of heavy metal ions from aqueous solution. This parameter is directly related to the competition ability of hydrogen ions with metal ions for active sites on the biosorbent surface (Senthilkumar et al. 2011,

Tsai et al. 2007). Generally, metal biosorption involves complex mechanisms of ion-exchange, chelation, adsorption by physical forces, and ion entrapment in inter and intrafibrillar capillaries and spaces of the cell structural network of a biosorbent (Chojnacka et al. 2005). At low pH values, protons occupy most of the biosorption sites on the biosorbent surface, and fewer copper ions can be absorbed because of the electric repulsion with protons on the biosorbent. When the pH values increase, biosorbent surfaces are more negatively charged, and the biosorption of metal ions

(positive charge) increases and reaches equilibrium at pH 8. Decreases in biosorption at higher pH values (> 8) are due to the formation of soluble hydroxylated complexes of the metal ions and their 6

Fig. 4: Effect of contact time on the Cu(II) biosorption capacity of the macrofungus (Ganoderma lobatum)

and its biochar competition with the active sites, resulting in a repeated decrease in Theretention effect (Anayurtof contact et time al. 2009on the, removal efficiencies of Cu(II) was investigated. The removal

Sar & Tuzen 2009a). efficiencies of Cu(II) by the two biosorbents as a function of time are depicted in Fig. 4. In the case

The FT-IR spectroscopic analysis showed that the macrofungusof Cu(II) (C0) removal had variousefficiencies functional by C0 and C400, the removal efficiency reached equilibrium at 480 groups, and these groups were involved in almost all potentialmin, binding which mechanisms.was chosen as Moreover, contact time for further experiments. In the initial stages, the removal depending on the pH value of the aqueous solution, these functionalefficiencies groups of participate Cu(II) by in C0 metal and C400ion increased rapidly due to the abundant availability of active binding (Sar & Tuzen 2009a). binding sites on the biosorbents, and with gradual occupancy of these sites, the sorption became less competition with the active sites, resulting in a repeated decrease in retention (Anayurt et al. 2009, 582 efficient atSilin later Yang stages et (Costaal. & Leite 1991). Sar & Tuzen 2009a).

The FT-IR spectroscopic analysis showed that the macrofungus (C0) had various functional groups, and these groups were involved in almost all potential binding mechanisms. Moreover, Cu(II) Cu(II) depending on the pH value of the aqueous solution, these functional groups participate in metal ion binding (Sar & Tuzen 2009a).

Percentage Removal Percentage Removal Percentage Removal Percentage Removal

Cu(II) pH Initial Cu(II) concentration (mg/L)

Fig. 3: Effect of the initial pH on the Cu(II) biosorption capacity of the Fig. 5: Effect of the initial Cu(II) concentration on the (II) biosorption

macrofungus (Ganoderma lobatum) and its biochar. Fig. 5: Effect ofcapacity the initial of the Cu macrofungus(II) concentration (Ganoderma on the (II)lobatum biosorption) and its capacitybiochar. of the macrofungus Fig. 3: Effect of the initial pH on the Cu(II) biosorption capacity of the macrofungus (Ganoderma lobatum) (Ganoderma lobatum) and its biochar. Effect of Contact Timeand its biochar. The initial concentration of the metal in the solution dramatically influenced the equilibrium uptake of Cu(II). The effect of contact time on the removal efficienciesThe initial of concentration of the metal in the solution dramatically influenced the equilibrium Percentage Removal Percentage Removal It was noted that the initial concentration increased the Cu(II) was investigated. The removal efficiencies of Cu(II) Effect of Contact Time uptake of Cu(II). It sorptionwas noted of thatCu(II), the whichinitial wasconcentration generally increasedexpected duethe tosorption the of Cu(II), which by the two biosorbents as a function of time are depicted in equilibrium process (Fig. 5). This increase in uptake capacity Fig. 4. In the case of Cu(II) removalpH efficiencieswas generally by C0 and expected of the due biosorbents to the equilibrium (C0 and C400)process with (Fig. the 5). increase This increase in initial in uptake capacity of C400, the removal efficiency reached equilibrium at 480 min, metal concentrations was due to the higher availability of which was chosen as contact time for furtherthe experiments. biosorbents (C0 and C400) with the increase in initial metal concentrations was due to the higher

metal ions (copper) for sorption. Moreover, the higher initial Fig. 3: Effect ofIn the the initial initial pH onstages, the Cu(II) the removalbiosorption efficiencies capacity of the of macrofungusCu(II) by C0(Ganoderma concentration lobatum )provided increased driving force to overcome availability of metal ions (copper) for sorption. Moreover, the higher initial concentration provided and C400 increased rapidly due to the abundant availability all the mass transfer resistance of metal ions between the Cu(II) and its biochar. of active binding sites on the biosorbents, and with gradual aqueous and solid phase, resulting in a higher probability of increased driving force to overcome all the mass transfer resistance of metal ions between the occupancy of these sites, the sorption became less efficient collision between metal ions and sorbents. This phenome- at later stages (Costa & Leite 1991). Effect of Contact Time aqueous and solid nonphase, also resulting results inin higher a higher metal probability uptake (Tewari of collision et al. 2005,between metal ions and Vimala & Das 2009). sorbents. This phenomenon also results in higher metal uptake (Tewari et al. 2005, Vimala & Das Biosorption Isotherm Models Sorption models are often used to predict the maximum adsorption capacity of the adsorbent. 2009).

Percentage Removal Percentage Removal Sorption models are often used to predict the maximum The Langmuir and Freundlich models are the most widely used models for the adsorption of metal adsorption capacity of the adsorbent. The Langmuir and

Cu(II) Biosorption IsothermFreundlich Modelsions models with arebiomaterials the most widely(Febrianto used et modelsal. 2009 for, Langmuir the 1918). The equilibrium adsorption data adsorption of metal ions with8 biomaterials (Febrianto et al. 2009, Langmuirwere analy 1918).sed accordingThe equilibrium to the Langmuiradsorption and data Freundlich adsorption isotherm models. The Contact time (min) were analysed according to the Langmuir and Freundlich Langmuir model suggests that monolayer sorption on a homogeneous surface occurs without adsorption isotherm models. The Langmuir model suggests that monolayerinteractions sorption between on a homogeneousabsorbed molecules. surface In occurs addition, the model assumes uniform energies of 7 without interactions between absorbed molecules. In addi- sorption onto the surface and no transmigration of the sorbate (Vimala & Das 2009). The Langmuir Percentage Removal tion, the model assumes uniform energies of sorption onto the surface and no transmigration of the sorbate (Vimala & Das model can be written in linear form. 2009). The Langmuir model can be written in linear form. C C 1 e  e  …(3) Contact time (min) …(3) Qe qm K Lqm

Fig. 4: Effect of contact time on the Cu(II) biosorption capacity of the Where q (mg/g) is the monolayer biosorption capacity m Where qm (mg/g) is the monolayer biosorption capacity of the adsorbent, and KL (L/mg) is the Ganoderma lobatum macrofungus ( ) and its biochar of the adsorbent, and KL (L/mg) is the Langmuir sorption 7 Langmuir sorption constant related to the free energy of biosorption.

Vol. 20, No. 2, 2021 • Nature Environment and Pollution Technology The Freundlich model assumes a heterogeneous sorption surface. The Freundlich model is 1 ln Q  ln C  ln K …(4) e n e F

Where, KF (mg/g) is a constant relating the biosorption capacity, and n is an empirical

parameter relating to the biosorption intensity, which varies with the heterogeneity of the material.

The linear plots of the Langmuir and Freundlich isotherm models for the sorption of Cu(II) on

C0 and C400 are presented in Fig. 6. The linear regression coefficient values (R2) were presented in

Table 1, which indicated that the Langmuir model was not able to adequately describe the

relationship between the amounts of Cu(II) adsorbed by the adsorbent and its equilibrium

concentration in solution. However, the Freundlich isotherm model exhibited a better fit to the

sorption data of Cu(II) for both C0 and C400 than the Langmuir isotherm model, since it provided

2 higher R values. Moreover, the n and KF of C0 for Cu(II) biosorption were higher than for C400.

This result indicated that C0 had greater removal efficiencies for Cu(II) than C400. It is likely that

the functional groups of C400 were destroyed during the carbonization process. A comparison of

the adsorption capacity of this biosorbent with those of different biosorbents reported by other

researchers is provided in Table 2, and it can be concluded that the macrofungus as an effective

biosorbent may play an important role in the removal of heavy metals from an aqueous environment.

Table 1: Isotherm equations and parameters for Cu(II) biosorption by the macrofungus (Ganoderma lobatum) and

9

Sorption models are often used to predict the maximum adsorption capacity of the adsorbent.

The Langmuir and Freundlich models are the most widely used models for the adsorption of metal

ions with biomaterials (Febrianto et al. 2009, Langmuir 1918). The equilibrium adsorption data

were analysed according to the Langmuir and Freundlich adsorption isotherm models. The

Langmuir model suggests that monolayer sorption on a homogeneous surface occurs without

interactions between absorbed molecules. In addition, the model assumes uniform energies of

sorption onto the surface and no transmigration of the sorbate (Vimala & Das 2009). The Langmuir

model can be written in linear form.

C C 1 e  e  …(3) Qe qm K Lqm BIOSORPTION OF CU(II) FROM AQUEOUS SOLUTIONS BY A MACROFUNGUS BIOMASS 583 Where qm (mg/g) is the monolayer biosorption capacity of the adsorbent, and KL (L/mg) is the constantLangmuir related to sorption the free constantenergy of related biosorption. to the free energy ofvalues. biosorption. Moreover, the n and KF of C0 for Cu(II) biosorption The Freundlich model assumes a heterogeneous sorption were higher than for C400. This result indicated that C0 had surface. The TheFreundlich Freundlich model model is assumes a heterogeneous sorptiongreater removalsurface. efficienciesThe Freundlich for modelCu(II) than is C400. It is likely that the functional groups of C400 were destroyed during 1 ln Qe  ln Ce  ln K F …(4) the…(4) carbonization process. A comparison of the adsorption n capacity of this biosorbent with those of different biosorbents Where, K (mg/g) is a constant relating the biosorption WF here, KF (mg/g) is a constant relating the biosorptionreported by capacity, other researchers and n is is an provided empirical in Table 2, and it capacity, and n is an empirical parameter relating to the can be concluded that the macrofungus as an effective bio- biosorptionparameter intensity, relating which to thevaries biosorption with the intensity,heterogeneity which variessorbent with may the play heterogeneity an important of rolethe material.in the removal of heavy of the material. metals from an aqueous environment. The linearThe plots linear of plotsthe Langmuir of the Langmuir and Freundlich and Freundlich iso- isotherm models for the sorption of Cu(II) on Biosorption Kinetics therm models for the sorption of Cu(II) on C0 and C400 Biosorption Kinetics C0 and C400 are presented in Fig. 6. The linear regression coefficient values (R2) were presented in are presented in Fig. 6. The linear regression coefficient To clarify the biosorption kinetics of Cu(II) ions onto C0 2 values (TableR ) were 1, presentedwhich indicated in Table that 1, which the Langmuirindicated thatmodel andwas ToC400, notclarify abletwo the biosorptionkineticto adequately models, kinetics describeofthe Cu(II) pseudo-first-order ionsthe onto C0 and C400, and two kinetic models, the the Langmuir model was not able to adequately describe pseudopseudo-second-order-first-order and pseudo model-second were-order applied model to were the applied experimental to the experimental data. The linear the relationshiprelationship between between the amounts the amounts of Cu(II) of adsorbed Cu(II) adsorbedby data. by The the linear adsorbent form of andthe pseudo-first-orderits equilibrium rate equation the adsorbent andits its biochar equilibrium. concentration in solution. formis given of the as pseudo follows-first -(Senthilkumarorder rate equation et is al. given 2011): as follows (Senthilkumar et al. 2011): concentration in solution. However, the Freundlich isotherm model exhibited a better fit to the However, the Freundlich isotherm model exhibited a better t 1 t Biosorbent Langmuir ln(Q Q )  lnFreundlichQ  K t ,   …(5) fit to the sorption data of Cu(II) for both C0 and C400 than e t e 1 2 …(5) sorption data of Cu(II) for both C0 and C400 than 2the Langmuir isotherm model, sinceQt itK pro2QevidedQe the Langmuir isotherm model, since it provided higher R 2 2 Equation qm K L R Equation n K F R 2 −1 higher R values. Moreover, the n and KF of C0 for Cu(II)W biosorptionhere K1 and Kwere2 are thehigher rate constantthan for of C400.the first -order equation (min ) and second-order Table 1: Isotherm equationsC0 and parametersy = 0.0544x for Cu(II) + biosorption18.38 0.0684 by the macrofungus0.9697 y =(Ganoderma 0.3345x + lobatum2.989) and3.364 its biochar. 0.9956 equation (g/mg min), respectively (Cheung et al. 2001). This result indicated that C0 had greater removal efficiencies for Cu(II) than C400. It is likely that Biosorbent Langmuir 0.7947 Freundlich1.2132 The values of the rate constants and correlation coefficients for the two models are shown in 2 2 the functionalEquation groups of C400qm wereK destroyedL durinR g the carbonizationEquation process.n A comparisonKF of R C400 y = 0.0609x + 16.42 0.0471 0.9408 y = 0.3822x + 2.616 2.308 0.993 C0 y = 0.0544x + 0.7947 18.38 0.0684 0.9697 Table y3. = The 0.3345x biosorption + 1.2132 mechanisms 2.989 of Cu(II)3.364 ions onto the0.9956 C0 and C400 biomass does follow the the adsorption capacity of this biosorbent with those of different biosorbents reported by other C400 y = 0.0609x + 1.29121.2912 16.42 0.0471 0.9408 pseudoy0.8368- =second 0.3822x -order + 0.8368 kinetic model2.616 (Fig. 7). The2.308 K2 value of0.993 C0 was significantly higher than C400.

researchers is12 provided in Table 2, and it can be concludedThis3.5 result that indicated the macrofungus that the sorption as rate an of effectiveC0 for Cu(II) was greater than C400. C0 C0 10 Table3 3: The equations and parameters of pseudo-first and second-order kinetics for Cu(II) biosorption by the biosorbent may playC400 an important role in the removal of heavy metalsC400 from an aqueous environment. 2.5 macrofungus (Ganoderma lobatum) and its biochar. Table 1: Isotherm8 equations and parameters for Cu(II) biosorption by the macrofungus (Ganoderma lobatum) and 2 e e Biosorbent First-order kinetics Second-order kinetics /Q 6 Q e ln C 1.5 9 Q 2 Q 2 4 Equation K1 e R Equation K2 e R 1 C0 y = -0.0017x - 0.0017 0.5242 0.9398 y = 0.2124x + 0.0233 4.7080 0.9996 2 A 0.5 B 0.6457 1.9287 0 0 0 50 100 150 -2 -1 0 1 2 3 4 5 6 C400 y = -0.0025x + 0.0025 1.2832 0.9641 y = 0.2272x + 0.0090 4.4014 0.9985 Ce lnCe 0.2494 5.7181 Fig. 6: Linear fitting of the Langmuir (A) and Freundlich (B) isotherms for Cu(II) biosorption of the macrofungus (Ganoderma lobatum) and its

Fig. 6: Linear fitting of the Langmuir (A) andbiochar. Freundlich (B) isotherms for Cu(II) biosorption of the macrofungus (Ganoderma lobatum) and its biochar. Table 2: Sorption capacity of Cu(II) on different macrofungi. 0.5 350 C0 A C0 B 0 300 Biosorbent Table 2: SorptionAdsorption capacity of capacity Cu(II) on (mg/g) different macrofungi.pH Metal concentrationC400 (mg/L) References C400 250 -0.5 Ganoderma lobatumBiosorbent 18.38 Adsorption capacity pH 8 Metal concentration10-160 (mg/L) References Present study ) t 200 t Q

Auricularia polytricha 8.36 5 - 0-250 (Xinyu et al. 2010) e -1 t/Q (mg/g) Q 150 Auricularia polytricha 18.69 6.03-6.56ln( 10-100 (Yu et al. 2010) -1.5 100 Tremella fuciformis Ganoderma lobatum20.15 18.38 8 6.03-6.5610-160 10-100 Present study(Yu et al. 2010) Pleurotus ostreatus 8.06 4.5 -2 20-100 (Javaid50 et al. 2011) Auricularia polytricha 8.36 5 0-250 (Xinyu et al., -2.5 0 0 200 400 600 800 0 200 400 600 800 1000 1200 1400 2010) Nature Environment and TimePollution（min） Technology • Vol. 20, No.2, 2021Time（min）

Auricularia polytricha 18.69 6.03-6.56 10-100 (Yu et al., 11 2010)

Tremella fuciformis 20.15 6.03-6.56 10-100 (Yu et al.,

2010)

Pleurotus ostreatus 8.06 4.5 20-100 (Javaid et al.,

2011)

10

Biosorption Kinetics

To clarify the biosorption kinetics of Cu(II) ions onto C0 and C400, two kinetic models, the

pseudo-first-order and pseudo-second-order model were applied to the experimental data. The linear

form of the pseudo-first-order rate equation is given as follows (Senthilkumar et al. 2011):

t 1 t      ln(Qe Qt ) ln Qe K1t , 2 …(5) Qt K2Qe Qe

−1 Where K1 and K2 are the rate constant of the first-order equation (min ) and second-order

equation (g/mg min), respectively (Cheung et al. 2001).

The values of the rate constants and correlation coefficients for the two models are shown in

Table 3. The biosorption mechanisms of Cu(II) ions onto the C0 and C400 biomass does follow the

pseudo-second-order kinetic model (Fig. 7). The K2 value of C0 was significantly higher than C400.

This result indicated that the sorption rate of C0 for Cu(II) was greater than C400.

Table 3: The equations and parameters of pseudo-first and second-order kinetics for Cu(II) biosorption by the

macrofungus (Ganoderma lobatum) and its biochar.

Biosorbent First-order kinetics Second-order kinetics

2 2 Equation K1 Qe R Equation K2 Qe R

584 C0 y = -0.0017x - 0.0017 0.5242Silin Yang0.9398 et al.y = 0.2124x + 0.0233 4.7080 0.9996

0.6457 1.9287 Table 3: The equations and parameters of pseudo-first and second-order kinetics for Cu(II) biosorption by the macrofungus Ganoderma( lobatum) and its biochar. C400 y = -0.0025x + 0.0025 1.2832 0.9641 y = 0.2272x + 0.0090 4.4014 0.9985 Biosorbent First-order kinetics Second-order kinetics 2 2 Equation 0.2494 K1 Qe R Equation5.7181 K2 Qe R C0 y = -0.0017x - 0.6457 0.0017 0.5242 0.9398 y = 0.2124x + 1.9287 0.0233 4.7080 0.9996 C400 y = -0.0025x + 0.2494 0.0025 1.2832 0.9641 y = 0.2272x + 5.7181 0.0090 4.4014 0.9985

0.5 350 C0 A C0 B 0 300 C400 C400 250 -0.5 ) t 200 t Q -

e -1 t/Q Q 150 ln( -1.5 100

-2 50

-2.5 0 0 200 400 600 800 0 200 400 600 800 1000 1200 1400 Time（min） Time（min）

Fig. 7: Linear fitting of the pseudo-first-order (A) and pseudo-second-order (B) kinetics for Cu(II) biosorption by the macrofungus (Ganoderma lobatum11 ) and its biochar.

Where K1 and K2 are the rate constant of the first-order C0 and C400 effectively followed the pseudo-second-order equation (min−1) and second-order equation (g/mg min), kinetic model. Further research is in progress to explore the respectively (Cheung et al. 2001). mechanism underlying the biosorption process. The values of the rate constants and correlation coeffi- cients for the two models are shown in Table 3. The bio- ACKNOWLEDGEMENTS sorption mechanisms of Cu(II) ions onto the C0 and C400 This work was supported by the National Natural Science biomass does follow the pseudo-second-order kinetic model Foundation of China (21767027). (Fig. 7). The K2 value of C0 was significantly higher than C400. This result indicated that the sorption rate of C0 for REFERENCES Cu(II) was greater than C400. Anayurt, R.A., Sari, A. and Tuzen, M. 2009. Equilibrium, thermodynamic CONCLUSION and kinetic studies on biosorption of Pb(II) and Cd(II) from aqueous solution by macrofungus (Lactarius scrobiculatus) biomass. Chemical The macrofungus as an effective biosorbent of Cu(II) was Engineering Journal, 151: 255-261. Cheung, C.W., Porter, J.F. and Mckay, G. 2001. Sorption kinetic analysis confirmed. The effects of the biosorbent dose, pH, contact for the removal of cadmium ions from effluents using bone char. Water time, and initial copper ion concentration on the removal Research, 35: 0-612. efficiencies were evaluated. The present results showed that Chojnacka, K., Chojnacki, A. and Górecka, H. 2005. Biosorption of 3+ 2+ 2+ the desired biosorbent dose in the case of Ganoderma loba- Cr , Cd and Cu ions by blue-green algae Spirulina sp.: kinetics, tum and its biochar for Cu(II) adsorption was 4 g/L, and the equilibrium and the mechanism of the process. Chemosphere, 59: 75-84. Costa, A.C.A.D. and Leite, S.G.F. 1991. Metals biosorption by sodium pH value for biosorption was found to be 8 for Cu(II). The alginate immobilized Chlorella homosphaeracells. Biotechnology Freundlich isotherm model exhibited a better fit to the sorp- Letters, 13: 559-562. tion data of Cu(II) for both C0 and C400 than the Langmuir Dashtban, M., Schraft, H. and Qin, W. 2009. Fungal bioconversion of isotherm model. The results indicated that C0 had greater lignocellulosic residues; opportunities & perspectives. Int. J. Biol. removal efficiencies for Cu(II) than C400. This finding can Sci., 5: 578-595. Febrianto, J., Kosasih, A., Sunarso, J., Ju, Y.H., Indraswati, N. and Ismadji, be interpreted as due to the decomposition of the functional S. 2009. Equilibrium and kinetic studies in adsorption of heavy metals groups of C400 during the carbonization process. Equilib- using biosorbent: A summary of recent studies. Journal of Hazardous rium data showed that the biosorption of Cu(II) ions onto Materials, 162: 616-645.

Vol. 20, No. 2, 2021 • Nature Environment and Pollution Technology Biosorption Kinetics

To clarify the biosorption kinetics of Cu(II) ions onto C0 and C400, two kinetic models, the pseudo-first-order and pseudo-second-order model were applied to the experimental data. The linear form of the pseudo-first-order rate equation is given as follows (Senthilkumar et al. 2011): t 1 t      ln(Qe Qt ) ln Qe K1t , 2 …(5) Qt K2Qe Qe

−1 Where K1 and K2 are the rate constant of the first-order equation (min ) and second-order equation (g/mg min), respectively (Cheung et al. 2001).

The values of the rate constants and correlation coefficients for the two models are shown in

Table 3. The biosorption mechanisms of Cu(II) ions onto the C0 and C400 biomass does follow the pseudo-second-order kinetic model (Fig. 7). The K2 value of C0 was significantly higher than C400.

This result indicated that the sorption rate of C0 for Cu(II) was greater than C400.

Table 3: The equations and parameters of pseudo-first and second-order kinetics for Cu(II) biosorption by the macrofungus (Ganoderma lobatum) and its biochar.

Biosorbent First-order kinetics Second-order kinetics

2 2 Equation K1 Qe R Equation K2 Qe R

C0 y = -0.0017x - 0.0017 0.5242 0.9398 y = 0.2124x + 0.0233 4.7080 0.9996 BIOSORPTION OF CU(II) FROM AQUEOUS SOLUTIONS BY A MACROFUNGUS BIOMASS 585

0.6457 1.9287 Table 3: The equations and parameters of pseudo-first and second-order kinetics for Cu(II) biosorption by the macrofungus Ganoderma( lobatum) and Fomina, M. and Gadd, G.M. 2014. Biosorption: current perspectives on and Copper(II) Ions from Binary Metal Mixtures by R. arrhizus. Process its biochar. concept, definition and application. Bioresource Technology, 160: 3-14. Biochemistry, 31: 561-572. C400 y = -0.0025x + 0.0025 1.2832 0.9641 y = 0.2272x + 0.0090 4.4014 0.9985 Ghorbani, F., Younesi, H., Ghasempouri, S.M., Zinatizadeh, A.A., Amini, Sar, A. and Tuzen, M. 2009a. Biosorption of As(III) and As(V) from aqueous Biosorbent First-order kinetics Second-order kinetics M. and Daneshi, A. 2008. Application of response surface methodology solution by macrofungus (Inonotus hispidus) biomass: Equilibrium 2 2 for optimization of cadmium biosorption in an aqueous solution and kinetic studies, Journal of Hazardous Materials, 164: 1372-1378. Equation 0.2494 K1 Qe R Equation5.7181 K2 Qe R by Saccharomyces cerevisiae. Chemical Engineering Journal, 145: Sar, A. and Tuzen, M. 2009b. Kinetic and equilibrium studies of biosorption C0 y = -0.0017x - 0.6457 0.0017 0.5242 0.9398 y = 0.2124x + 1.9287 0.0233 4.7080 0.9996 267-275. of Pb(II) and Cd(II) from aqueous solution by macrofungus (Amanita C400 y = -0.0025x + 0.2494 0.0025 1.2832 0.9641 y = 0.2272x + 5.7181 0.0090 4.4014 0.9985 Javaid, A., Bajwa, R., Shafique, U. and Anwar, J. 2011. Removal of heavy rubescens) biomass, Journal of Hazardous Materials, 164: 1004-1011. metals by adsorption on Pleurotus ostreatus. Biomass & Bioenergy, Senthilkumar, P., Ramalingam, S., Sathyaselvabala, V., Kirupha, S.D. and 0.5 350 35: 1675-1682. Sivanesan, S. 2011. Removal of copper(II) ions from aqueous solution Kapoor, A. and Viraraghavan, T. 1995. Fungal biosorption - an alternative by adsorption using cashew nutshell. Desalination, 266: 63-71. C0 C0 A B treatment option for heavy metal bearing wastewaters: a review. Tewari, N., Vasudevan, P. and Guha, B.K. 2005. Study on biosorption 0 300 C400 C400 Bioresource Technology, 53: 195-206. of Cr(VI) by Mucor hiemalis. Biochemical Engineering Journal, 23: 250 Langmuir, I. 1918. The adsorption of gases on plane surfaces of glass, 185-192. -0.5 mica and platinum. Journal of the American Chemical Society, 40: Tsai, W.T., Lee, M.K. and Chang, Y.M. 2007. Fast pyrolysis of rice husk: ) t 200 1361-1403. Product yields and compositions. Bioresource Technology, 98: 22-28. t Q - e -1 Melgar, M.J., Alonso, J. and García, M.A. 2007. Removal of toxic metals Vimala, R., Charumathi, D. and Das, N. 2011. Packed bed column studies t/Q Q 150 from aqueous solutions by fungal biomass of Agaricus macrosporus. on Cd(II) removal from industrial wastewater by macrofungus Pleurotus ln( Science of the Total Environment, 385: 12-19. platypus. Desalination, 275: 291-296. -1.5 100 Muraleedharan, T.R., Venkobachar, C. and Leela, I. 1994. Investigations of Vimala, R. and Das, N. 2009. Biosorption of cadmium (II) and lead (II) from fungal fruiting bodies as biosorbents for the removal of heavy metals aqueous solutions using mushrooms: A comparative study. Journal of -2 50 from industrial processing streams. Separation Science, 29: 1893-1903. Hazardous Materials, 168: 376-382. Nagy, B., Măicăneanu, A., Indolean, C., Mânzatu, C., Silaghi-Dumitrescu, Wang, J. and Chen, C. 2009. Biosorbents for heavy metals removal and -2.5 0 L. and Majdik, C. 2014. Comparative study of Cd(II) biosorption their future. Biotechnology Advances, 27: 195-226. 0 200 400 600 800 0 200 400 600 800 1000 1200 1400 on cultivated Agaricus bisporus and wild Lactarius piperatus based Xinyu, J., Haiwei, H., Lixiang, C. and Renduo, Z. 2010. Kinetics biocomposites. Linear and nonlinear equilibrium modelling and and equilibrium of biosorption of Cd2+, Cu2+, Pb2+, Zn2+ by Time（min） Time（min） kinetics. Journal of the Taiwan Institute of Chemical Engineers, 45: macrofungus(Auricularia polytricha) biomass. Acta Scientiae 921-929. Circumstantiae, 30(7): 1431-1438. Fig. 7: Linear fitting of the pseudo-first-order (A) and pseudo-second-order (B) kinetics for Cu(II) biosorption by the macrofungus Pérez, J., Muñoz-Dorado, J., de la Rubia, T. and Martínez, J. 2002. Yu, M., Rong, P., Hai-wei, H., Li-xiang, C. and Ren-duo, Z. 2010. (Ganoderma lobatum11 ) and its biochar. Biodegradation and biological treatments of cellulose, hemicellulose Biosorption of Cd(II), Cu(II), Pb(II) and Zn(II) in Aqueous Solutions and lignin: an overview. International Microbiology, 5: 53-63. by Fruiting Bodies of Macrofungi (Auricularia polytricha and Tremella Rome, L.D. and Gadd, G.M. 1987. Copper adsorption by Rhizopus arrhizus, fuciformis). Environmental Science, 31(7): 161-169. Cladosporium resinae and Penicillium italicum. Applied Microbiology Zulfadhly, Z., Mashitah, M.D. and Bhatia, S. 2001. Heavy metals removal & Biotechnology, 26: 84-90. in fixed-bed column by the macro fungus Pycnoporus sanguineus, Sağ, Y. and Kutsal, T. 1996. The Selective Biosorption of Chromium(VI) Environmental Pollution,a 112: 463-470.

Nature Environment and Pollution Technology • Vol. 20, No.2, 2021