Abstract
The wastes from the macro-fungus Agaricus bisporus were used as an eco-friendly and low-cost adsorbent for the treatment of colored effluents containing the recalcitrant dyes, acid red 97 (AR97) and crystal violet (CV). The macro-fungal waste presented an amorphous structure, composed of particles with different sizes and shapes. Also, it presents typical functional chemical groups of proteins and carbohydrates with a point of zero charge of 4.6. The optimum conditions for the dosage were found to be as follows: 0.5 g L−1 with an initial pH at 2.0 for the AR97 and 8.0 for the CV. From the kinetic test, it was found that it took 210 min and an adsorption capacity of 165 mg g−1 for the AR97. Concerning the CV kinetics, it took 120 min to reach the equilibrium and it achieved an adsorption capacity of 165.9 mg g−1. The Elovich model was the most proper model for describing the experimental data, achieving an R2 ≥ 0.997 and MSE ≤ 36.98 (mg g−1)2. The isotherm curves were best represented by the Langmuir model, predicting maximum adsorption capacity of 372.69 and 228.74 mg g−1 for the AR97 and CV, respectively. The process was spontaneous and favorable for both dyes. The ∆H0 values were 9.53 and 10.69 kJ mol−1 for AR97 and CV, respectively, indicating physical and endothermic adsorption. Overall, the wastes from Agaricus bisporus have the potential to adsorb cationic and anionic dyes, thus solving environmental problems related to water quality and residue disposal.
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Introduction
Currently, the industrial activities are more intensive, thereby the consumption of tons of dyes in different industrial processes has been growing. It is recognized that after each of these processes, a considerable number of effluents are generated, which need proper treatment before being disposed into the environment. The key problem is due to high toxicity, which affects the aquatic biome and other living beings (Gupta et al. 2013). Among the employed dyes, the crystal violet (CV) is known to be carcinogenic and mutagenic. However, it is still highly used in diverse sections of the textile industry, biological coloration, and dermatological agent. At lower concentrations, it can penetrate the skin, causing irritation and problems in the digestive system; in extreme cases, it can lead to breathing difficulties, kidney failure, and permanent blindness (Sarma et al. 2016). Another highly used dye in the textile and leather industries is the acid red 97 (AR97). Living organisms cannot degrade it, so in small concentrations, it can already damage animals and humans (Bankole et al. 2018). In this sense, the removal of these dyes from water resources is of great importance (Rigueto et al. 2020).
The adsorption is an efficient and easy operation method and is economical when employing low-cost adsorbents (Dotto and McKay 2020). Several studies utilizing different biomass based on macro-fungi for the removal of dyes have been reported. These fruiting bodies present great advantages: high availability, low cost, good texture, and physical and chemical resistance, showing good properties for the development of adsorbents (Maurya et al. 2006). Fu and Viraraghavan (2002) used the fungal biomass of Aspergillus niger for the removal of several dyes. Bayramoğlu and Yakup Arıca (2007) utilized the Trametes versicolor inactive biomass for the removal of direct blue 1 and direct red 128. Akar et al. (2009) have used a mixture of A. bisporus and Theileria orientalis for adsorption of reactive blue 49. Fomes fomentarius and Phellinus igniarius were used for the removal of rhodamine B and methylene blue (Maurya et al. 2006). Last, Georgin et al. (2019a) used the residues of the filamentous fungus Beauveria bassiana in the adsorption of the acid red 97 dye.
The Agaricus bisporus macro-fungus, commonly known as champignon mushroom, is an eatable and traded Basidiomycota. The principal components of the fungal cell wall are polysaccharides, chitin being a characteristic component of basidiomycetes (Vetter 2007). The production of these mushrooms generates high quantities of residues. The commercialized part is the upper rounded structure, which is above the ground, whereas the roots and stalk are discarded. Until the present data, no studies were observed that utilize the wastes from Agaricus bisporus macro-fungi as adsorbent. This work is aimed at studying the possibility of using the wastes from the macro-fungus Agaricus bisporus as a low-cost and eco-friendly adsorbent for the treatment of ideal colored effluents containing AR97 and CV. The fungal biomass wastes were prepared and characterized by different techniques. The kinetics, equilibrium, and thermodynamics of the adsorption operation were analyzed.
Materials and methods
Preparation of the Agaricus bisporus macro-fungal wastes
The Agaricus bisporus macro-fungal wastes, composed of roots and stalks (Fig. 1), were collected at local producers in the southern Brazil. Initially, the material was washed to remove impurities and dirt, mostly constituted by the substrate used in culture growth. Second, the samples were dried at 50 °C for 48 h. After this step, around 60% of the mass was lost, considering that it is predominantly composed of water. Last, the material was grounded and sieved (60 mesh), therefore obtaining a gray power with a particle diameter inferior to 150 μm. The material was stored for further utilization and labeled ABR (Agaricus bisporus residue).
Characterization of the ABR adsorbent
ABR was characterized by scanning electron microscopy (SEM) (Duarte et al. 2019), X-ray powder diffraction (XRD) (Oliveira et al. 2019), Fourier transform infrared spectroscopy (FT-IR) (Rojas et al. 2019), and point of zero charge (pHpzc) (Postai et al. 2016).
Adsorption assays using the ABR
For the adsorption experiments, the AR97 (empirical formula C32H20N4Na2O8S2, Mw 698.6 g mol−1, CAS number 10169-02-05) and CV (empirical formula C25H30N3Cl, Mw 407.9 g mol−1, CAS number 548-62-9) dyes were utilized, which were acquired from Sigma-Aldrich (Germany). At first, stock solutions of the dyes were prepared by dissolving 1.00 g onto 1000 mL of distilled water. The experimental solutions were prepared by diluting the stock solution until reaching the desired concentration. All tests described below were performed separately for each dye under identical experimental conditions. The dye concentrations were determined using a UV-Vis spectrophotometer from Shimadzu (model UV1700, Japan) at the wavelengths of 497 and 590 nm for the AR97 and CV, respectively.
The influence of pH was tested for the range of 2 to 10. The pH values were adjusted using NaOH or HCl solutions (0.1 mol L−1). The dosage of 0.75 g L−1 was added to 50 mL of the dye with an initial concentration of 100 mg L−1 and stirred for 120 min at 298 K. The ABR dosage effect was evaluated for the 0.25, 0.5, 0.75, 1.0, and 1.25 g L−1, at 298 K at the optimum pH. For this, the adsorbent was put in contact with 50 mL of dye solution with the initial concentration of 100 mg L−1. The solutions were agitated for 2 h at 150 rpm.
The kinetic tests were conducted using the optimum dosage and pH conditions. The kinetic curves were evaluated for the different initial concentrations (50, 100, and 200 mg L−1). The samples were collected at various times (from 0 to 240 min). The equilibrium data were obtained for four different temperatures (298, 308, 318, and 328 K) with different initial concentrations (0, 25, 50, 100, 200, 300, 400, and 500 mg L−1).
After all the experiments, the samples were centrifuged (Cenrtibio, 80-2B, Brazil) at 4000 rpm for 20 min, to ensure the separation between the phases. All tests were made in triplicate. The percentage of dye removal (R, %), adsorption capacity at any time (qt, mg g−1), and equilibrium (qe, mg g−1) were used to evaluate the adsorption operation.
Kinetics, equilibrium, and thermodynamics
The kinetic curves were evaluated by the pseudo-first-order (Lagergren 1898), pseudo-second-order (Ho and Mckay 1999), general order (Liu and Shen 2008), and Elovich models (Elovich and Larinov 1962) (supplementary material (S.1)). For the adsorption isotherms, the models of Langmuir (1918) and Freundlich (1906) were tested (supplementary material (S.2)). The estimation of the thermodynamic parameters was done according to Lima et al. (2018) (supplementary material (S.3)). The parameter estimation and fit quality evaluation were made using scripts on MATLAB 2017. The fit quality evaluation was performed through the coefficient of determination (R2), adjusted determination coefficient (R2adj), average relative error (ARE), and minimum squared error (MSE) (supplementary material (S.4)).
Results and discussion
Features of ABR adsorbent
The SEM images with different magnifications were done for studying the surface morphology of the ABR, as presented in Fig. 2. It was verified that ABR is composed of particles with distinct irregular shapes and sizes, with a rugous surface. Similar characteristics have been reported by Akar et al. (2009) using the same fungi and by Grassi et al. (2019) for Diaporthe schini.
The XRD pattern for the ABR is exhibited in Fig. 3, variating the 2θ from 0 to 100°. In this case, the pattern presented a broad peak between 10 and 50°, without the presence of crystalline phases. These arrangements are composed of functional groups present on the fungal cell wall, containing amide, carboxyl, and phosphate (Li et al. 2018). These disorganized structures can facilitate the adsorption of dyes on the mushroom (Zazycki et al. 2018). The profile of this structure was equally found by Georgin et al. (2019a), in the fungus Beauveria bassiana.
The FT-IR spectrum for the ABR adsorbent is presented in Fig. 4. The broadband at 3420 cm−1 is related to the elongation of OH (Pavan et al. 2008). The band at 2932 cm−1 can be attributed to the CH bonds; after this, the intense bands at 1640 and 1465 cm−1 are related to the amide and ether group vibrations (Kumar and Ahmad 2011). The following band is 1015 cm−1, which is related to the C–OH and C–O– vibrations. The latter bands 710 and 498 cm−1 are associated with the C–H and C–N–C bonds, respectively (Román et al. 2013). From this spectrum, it is expected that ABR contains functional groups of natural chitin, including the hydroxyl, amide I (carbonyl vibration C–N), and amide II (NH deformation) groups. These groups on the ABR surface contain elements present in proteins and carbohydrates that can facilitate the adsorption of the dyes.
The point of zero charge (pHpzc) is the value where the charges at the surface of the materials tend to be zero or equivalent. In this case, the ABR presented a pHpzc of 4.6, according to Fig. 5. Therefore, the surface of the adsorbent is positively charged for pH values below 4.6. On the other hand, the surface is negatively charged for pH values above 4.6.
Evaluation of pH and adsorbent dosage
It is recognized that pH is one of the most relevant parameters in the adsorption process. It is a controller of the superficial charge, ionization degree, and the dissociation of functional groups (Bairagi et al. 2011; Nekouei et al. 2015). Figure 6 shows the adsorption capacity of AR97 and CV as a function of pH. In this figure, an inverse behavior of the dyes concerning the pH was obtained, mainly due to their contrary ionic nature. Concerning the AR97, the adsorption capacity decreased from 99.3 to 3.3 mg g−1 with an increase of pH. The optimum adsorption occurred at pH 2. This trend occurred because AR97 is an anionic dye, being negatively charged in the solution. In parallel, the ABR adsorbent is positively charged at pH values lower than 4.6 (Fig. 5). Hence, at a pH of 2, the interactions are facilitated. For the CV dye, the adsorption increased from 35.6 to 117.4 mg g−1 with the increase of the solution pH. The better pH for CV adsorption was 8. This behavior occurred because CV is a cationic molecule, being positively charged in solution. In parallel, the ABR adsorbent is deprotonated, leading to a notable attraction with the CV dye (Gupta et al. 2012). From these results, the ideal initial pH of the solution was selected as 2.0 for AR97 and 8.0 for CV.
The effect of ABR dosage in the adsorption of AR97 and CV (adsorption capacity and removal percentage) is presented in Fig. 7. For the AR97 (Fig. 7a), the ABR dosage increase led to an increase in removal percentage from 53.4 to 84.9% and a decrease in the adsorption capacity from 213.4 to 67.9 mg g−1. A similar trend was observed for the adsorption of CV (Fig. 7b), where the removal percentage increased from 66.5 to 88% and the adsorption capacity decreased from 266.0 to 70.4 mg g−1. The substantial increase in the removal percentage (R), for both dyes, at ABR dosage until 0.7 g L−1, is due to the greater number of vacant sites on the adsorbent surface, so the dye molecules are easily allocated. In contrast, the modest increase in removal percentage at higher ABR dosages is due to the lack of available sites (Pathania et al. 2016). Similar behavior has also been found by Mittal et al. (2010) when studying the adsorption of chrysodine. In this case, the ABR dosage of 0.5 g L−1 was adopted, because this dosage provides good values of both removal percentage and adsorption capacity.
Adsorption of AR97 and CV on ABR: kinetics, isotherms, and thermodynamics
The kinetic profiles for the adsorption of AR97 and CV onto the ABR are presented in Figs. 8 a and b, respectively. It can be noted in Fig. 8 that, for both dyes, the adsorption capacity increased with the contact time, attaining a constant value. Besides, for both dyes, the equilibrium time was little dependent on the initial concentration. For AR97, the equilibrium was achieved at 210 min for all initial concentrations, with a maximum adsorption capacity of 165.91 mg g−1 for 200 mg L−1. For the CV dye, the equilibrium time was reached at 125 min for all concentrations, reaching an adsorption capacity of 259.57 mg g−1 for the initial concentration of 200 mg L−1. Through a comparative evaluation between the dyes, it was observed that the adsorption occurred faster for CV than for AR97. This trend occurred because CV has little molecular volume and size in comparison with AR97, facilitating the mass transfer aspects. Similar tendencies were found in the adsorption of methyl orange using mesoporous carbon material (Mohammadi et al. 2011).
For describing the adsorption kinetics of both dyes onto the ABR, the pseudo-first-order, pseudo-second-order, general order, and Elovich models were adjusted. The parameters are presented in Tables 1 and 2 (AR97 and CV, respectively). The Elovich model was the most suitable for describing the kinetic behavior for both adsorbate/adsorbent systems. In the case of AR97, the statistical indicators were R2adj ≥ 0.975 and MSE ≤ 24.6 (mg g−1)2. For the CV, an R2adj ≥ 0.981 and MSE ≤ 37.0 (mg g−1)2 were found. According to Wu et al. (2009), this model is suitable for adsorption on heterogeneous surfaces. This behavior is following the system proposed in this work, where the adsorbent (ABR) has adsorption sites of different natures and energies. The parameter “b” is the initial adsorption rate because (dqt/dt) tends to “b” when qt tends to 0. In this work, for all initial concentrations, the parameter “b” was higher for CV than for AR97. This trend is an indication that at the initial stages, the CV adsorption is faster than the AR97 adsorption. This behavior can be easily observed comparing Fig. 8 a and b. This behavior is also associated with the little molecular volume and size of the CV dye.
The equilibrium data for the adsorption of AR97 and CV are presented in Fig. 9a, b, respectively. According to Giles et al. (1974), the isotherms can be classified as L2 type. For both cases, the temperature increase caused an increase in the adsorption capacity, indicating endothermic adsorption. However, the inclination of the curves differs according to the system, being more favorable for the AR97, where the adsorption capacity achieved 362.09 mg g−1 at 328 K. For the CV, adsorption capacity reached 202 mg g−1 at 328 K. The temperature effect on the adsorption capacity can be explained by the increase in the dispersion of the dye molecules through the outer boundary layer and the internal pores of the adsorbent particles, as a result of the solution viscosity reduction (Güzel et al. 2015). Similar behavior has been observed by Akar et al. (2009) in the adsorption of acid red 44 on the biomass of the fungus Agaricus bisporus. Grassi et al. (2019) also found that the adsorption capacity of CV onto Diaporthe schini fungi increased with the temperature. Streit et al. (2019), studying the adsorption of allura red and CV on activated carbon, identified a similar trend concerning the temperature. According to these authors, this behavior is also associated with the desolvation of the dye molecules.
The estimated parameters for the equilibrium models are presented in Tables 3 and 4. From the statistical indicators, it was found that the Langmuir model is the most suitable for describing the adsorption isotherms for both adsorbate/adsorbent systems. For the AR97, the Langmuir model presented an R2adj ≥ 0.941 and an MSE ≤ 523.45 (mg g−1)2. Following the same criteria, for the CV, the Langmuir model achieved an R2adj ≥ 0.984 and an MSE ≤ 48.83 (mg g−1)2. The model parameters (qL and KL) agree to the experimental data, increasing with the temperature. This trend shows that the adsorption capacity and also the affinity adsorbate/adsorbent have increased with the temperature. Furthermore, the parameters qL and KL were higher for the AR97 dye. This behavior shows that the adsorption capacity for this dye was higher, and also, its affinity for ABR was higher. This trend can be attributed to the more ramified structure of the AR97 dye, which, in turn, leads to a more significant probability of interacting with the ABR surface.
Take into account the literature and the results found in this work; a comparison was considered for the adsorption capacity, presented in Table 5 (AR97). Several adsorbents used for the removal of AR97 and CV were analyzed (Table 5). For both dyes, the ABR adsorbent reached the third-best adsorption capacity, being 372.69 and 228.74 mg g−1, respectively. These results demonstrate that in addition to the low cost of obtaining the material, since it is a residue and requires practically not even a reagent for its preparation, the ABR demonstrates the considerable potential for removing textile dyes, making it a promising adsorbent material.
The computed thermodynamic parameters for both systems are presented in Table 6. The estimate has to use the Langmuir constant (KL) for the determination of the equilibrium constant (Ke). For both systems, it was found that the adsorption was a spontaneous process since ΔG0AR97 and ΔG0CV were negative. Both systems were endothermic with ΔH0AR97 = 9.53 and ΔH0CV = 10.69 kJ mol−1 (Gupta et al. 1997). The magnitude of ΔH0 indicates that the ion-dipole, dipole-dipole, or hydrogen bonds can be involved in the adsorption of CV and AR97 on ABR (Chang and Thoman 2014). Minor rearrangements occurred at the surface of the adsorbent for both systems, considering the positive ΔS0 values.
Conclusion
The macro-fungal (Agaricus bisporus) wastes were evaluated as an adsorbent in the removal of the acid red 97 and crystal violet dyes from ideal colored effluents. It was obtained that the Agaricus bisporus wastes presented an amorphous structure composed of irregular particles, formed by chemical elements present in proteins and carbohydrates. The adsorbent presented a pHpzc of 4.6. The adsorption was favorable at acidic pH (2) for AR97 and basic pH (8) for CV with the optimum ABR dosage of 0.5 g L−1. The adsorption equilibrium has been achieved at 210 and 125 min, for the AR97 and CV. The Elovich model is the proper model to describe the kinetic data for both systems. For the isothermal studies, the Langmuir model showed strong affinity of the dyes with the ABR, obtaining a maximum capacity of 372.69 mg g−1 for AR97 and 228.74 mg g−1 for CV. The adsorption for both systems was spontaneous, favorable, and endothermic. All these results show that the wastes from the cultivation of Agaricus bisporus have great potential in the treatment of ideal colored effluents.
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Drumm, F.C., Franco, D.S.P., Georgin, J. et al. Macro-fungal (Agaricus bisporus) wastes as an adsorbent in the removal of the acid red 97 and crystal violet dyes from ideal colored effluents. Environ Sci Pollut Res 28, 405–415 (2021). https://doi.org/10.1007/s11356-020-10521-9
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DOI: https://doi.org/10.1007/s11356-020-10521-9