Abstract
In this research, adsorption properties of bovine serum albumin (BSA) on diatomite clay, which is an oxide mineral, were studied as a function of BSA, sodium phosphate buffer and protein concentration and pH and the thermodynamic parameters of adsorption process were investigated. The BSA adsorption experiment onto diatomite clay indicated that the BSA solution reached the maximum adsorption value at pH 5.5. It was observed that the maximum adsorption capacity (qm) of the data obtained from the adsorption studies showed a great dependence on pH. The maximum amount of adsorption in adsorption experiments can be considered as points where the electrostatic interaction for pH is appropriate. Both structural and electrostatic interaction in regions outside of the isoelectric point may have caused a decrease in BSA absorbance. The structural influences were associated with different conformational states that while BSA molecules accept changes with pH, electrostatic effects can be observed in BSA molecules behaved like soft particles. In this case, it is not possible to explain the independence of the qm–pH curves of the amount of adsorption. The protein molecules at this point are very stable. Because this value is close to the isoelectric point of serum albumin. The surface structural change of BSA and diatomite clay was studied. For this, Fourier transform infrared spectroscopy (FTIR) spectroscopy values were compared before and after the experiment. The diatomite samples used as support material were characterized by FTIR, scanning electron microscopy, thermogravimetric analysis and Brunauer Emmett–Teller surface area analysis. The thermodynamic functions such as enthalpy, entropy, Gibbs free energy and activation energy were investigated in their experimental work. The thermodynamic parameters such as Gibbs free energy (ΔG*), Ea, ΔH* and ΔS* were calculated as − 67.45, 15.41, − 12.84 kJ mol−1 and − 183.28 J mol−1 K−1 for BSA adsorption, respectively. We can deduce that the adsorption process from the data obtained from the thermodynamic parameters is spontaneous and exothermic. The adsorption of the process was investigated using Eyring and Arrhenius equations, and its adsorption kinetic found to be coherent with the pseudo-second-order model. As a result, we reached that the diatomite clay is a suitable adsorbent for the BSA. Experimental results showed that diatomite clay has the potency to be used for rapid pretreatment in the process of identifying proteins.
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Introduction
The biotechnological and nanotechnological advances have recently begun to be used in many areas such as biosensors, artificial implants, nanocatalysts, purification strategies and drug delivery system (Demirci et al. 2016; Ayranci et al. 2017a, b; Sahin et al. 2018; Karatepe et al. 2016; Aday et al. 2016a, b; Yildiz et al. 2016a, b, c, d, e, 2017a, b, c; Erken et al. 2015; Baskaya et al. 2017a, b; Celik et al. 2016a, b, c; Abrahamson et al. 2013; Demir et al. 2017a, b; Erken et al. 2016a, b; Akocak et al. 2017; Eris et al. 2018a, b, c; Esirden et al. 2015; Goksu et al. 2016a, b, c, 2017; Sen et al. 2007, 2011a, b, 2012a, b, c, 2013a, b, c, 2014a, b, 2017a, b, c, d, e, f, 2018a, b; Mittal et al. 2010; Gupta et al. 2011, 2014a, b, 2015; Saleh and Gupta 2011, 2012a, b, 2014; Khani et al. 2010; Saravanan et al. 2013a, b, c, d, e, 2015a, b, 2016a, b; Devaraj et al. 2016; Gupta and Saleh 2013; Erkan et al. 2006; Bozkurt et al. 2017; Pamuk et al. 2015; Sahin et al. 2017; Dasdelen et al. 2017; Iverson et al. 2013; Koskun et al. 2018; Sen and Gokagac 2007, 2008, 2014; Gezer et al. 2017; Giraldo et al. 2014; Ahmaruzzaman and Gupta 2011; Mohammadi et al. 2011; Robati et al. 2016; Ghaedi et al. 2015; Asfaram et al. 2015; Topuz et al. 2010; Zhang et al. 2013). In biosensor systems, protein molecules are extremely effective in transduction events and the structural properties of adsorbed protein molecules are particularly influenced by the biocompatibility of the materials. The besides protecting the structure of protein molecules practically in adsorption processes furthermore, new changes in protein structure to perform adsorption are crucial to understand the structural changes in adsorption induction (Celik et al. 2016d; Giacomelli and Norde 2001). The interaction of any support molecules of biomolecules has intensively worked in the past (Norde et al. 2000; Rigou et al. 2006). The bovine serum albumin (BSA), which is used as a biomolecule, has spherical dimensions of about 4 nm · 4 nm · 14 nm (Violante et al. 1995). The BSA represents 52–62% of total protein in blood plasma (McClellan and Franses 2003). The most important physiological characteristic of serum albumin is to play a role in adjusting osmotic pressure and blood pH, and BSA also plays a role in the transport of compounds such as fatty acids, metals, amino acids, steroids and drugs (Brandes et al. 2006). The isoelectric point of BSA is at pH 4.7. We can take it that the pH solutions prepared on BSA isoelectric point are loaded with negative (Huang and Kim 2004). The BSA molecules have the ability to bind especially strongly negatively charged support materials. For this reason, it takes an active role in transportation (Kudelski 2003). Protein adsorption is important from the complex nature of the system when viewed from a more fundamental perspective and ideally, a protein adsorption can be affected by pH, ionic strength, protein concentration and buffer solution states. For this reason, protein adsorption studies have recently been extensively studied on experimental conditions (Hu and Su 2003; Hunter 1999). The diatomite consists of siliceous rocks in sedimentary construction of a small part of crystalline material (SiO2·nH2O) in the form of an amorphous silica. It possesses extremely important physical and chemical properties such as high permeability large pore structure, low thermal conductivity, wide surface area and small particle size. The diatomite clay is found in high quantities in Turkey and in various regions of the world (Vroman and Adams 1969; Khraisheh et al. 2004). Diatomite clay is a micro/nanostructured material that is derived from sedimentary silicon, low cost, harmless and environmentally sensitive and natural (Sheng et al. 2009). The purpose of this work is to determine the physicochemical adsorption kinetics of the BSA molecule on diatomite clay under certain conditions. In this sorption process, many experimental parameters were analyzed including the pH, ionic strength, protein concentration and buffer solution concentration. The kinetic analysis studies were carried out after the amount of BSA adsorbed on the diatomite clay was determined. Thermodynamic parameters such as Gibbs free energy (ΔG*), Ea, ΔH* and ΔS* were calculated. The purpose of this work was to study the kinetics and mechanism of adsorption of BSA on diatomite clay as support material under optimum experimental conditions. Thus, this investigation is aimed at to study the kinetics and dynamics of adsorption of BSA on diatomite clay.
Experimental
Materials and methods
The bovine serum albumin (BSA) was purchased from Sigma (with purity > 99.9%, USA). In this research, the sample of diatomite clay and some analyzes were performed for its characterization. The bovine serum albumin used in the study was purchased from Sigma. The solvents and chemicals were purchased from Merck AG (Darmstadt, Germany). The diatomite clay was obtained from the Seller Company. The SEM (SCM 5000) was used to clarify the microstructural and morphological structure of the clay sample. The water was passed from Milli-Q system and distilled two times. The elements contained in the clay sample and the percentages of these elements are given in Table 1. The BET N2(Micromeritics Flow Sorb II 2300) was used to investigate the specific surface area of the clay, and some properties of the diatomite clay are given in Table 2. The agitation was done for 120 min. The adsorption experiment was performed in the main parameters at pH 7, 298 K and 0.5 g L−1). NaOH (0.05 N) and HCl (0.05 N) were used to adjust pH. Four milliliters of samples was taken from the sample to get measure at certain time intervals during the experiment. The centrifugation was performed at 8000 rpm for 5 min, and then concentrations of the residual serum albumin were determined using a UV–Vis spectrophotometer (Carry 1EUV-VİS). The amount of serum albumin adsorbed on diatomite clay surface was found by using Eq. (1) (Lemonas 1997).
Adsorption experiments
The protein adsorption experiments were performed in the water bath to adsorption study of BSA on diatomite clay. The experiments were performed using protein mechanic stirrer by diatomite clay samples with 100 ml aqueous solution at various concentrations (0.10–0.35 g L−1), sodium phosphate buffer concentrations (2.5.10−2–7.5.10−2 mol L−1), pH (5.5–9) and temperature (288–318 K). The suspensions used in the experiment was stirred at 288 K and 700 (rpm) for 4 h in an incubator-shaker. In adsorption experiments, blind experiments were performed under the same experimental conditions. Every protein adsorption experiment was repeated three times. The since the data obtained from the study were very close to each other, the averages were taken. The concentration of the protein molecule in the initial solutions and the post-adsorption concentration were carried out by UV–Vis spectrophotometer.
where in this equation, qt is enzyme concentration, m is the mass of the clay, V is the volume of the mixture, Co is the concentration of enzyme solution and Ct is at any time concentration of enzyme solution (Lemonas 1997).
Results and discussion
Protein adsorption experiments
The changing adsorption kinetic rate with the initial concentration of the bovine serum albumin is shown in Fig. 1. It is observed that the adsorption rate increases with increasing bovine serum albumin initial concentration. It can be seen in Fig. 1 that when the initial of concentration bovine serum albumin increased from 0.25 to 0.75 g L−1, the absorption of the protein increased from 0.077 to 0.1748 mg g−1. The adsorption effect of the initial pH of BSA on diatomite clay the amount of BSA was investigated by changing under constant process parameters. As shown in Fig. 1a, the increase in pH decreases the amount of adsorption of protein molecules. The zero-load point, in which hydroxyl and proton ions are equal, has an important effect on the pH effect, especially in protein adsorption processes (Akkuş 2006). Because the net charge is zero at the isoelectric point in which enzymes or proteins have a very stable structure. The protein is more active at this point or near these points, preserving their three-dimensional structure. But these structures will start to decompose stable values below or above the isoelectric point (Fig. 2). This situation adversely affects the amount of adsorption (Hunter 1999). Loads on the surface of proteins that are biomolecules are not homogeneous. When the pH of the solution changes, the charge on the protein surface changes. The pH values below the isoelectric point of the BSA are usually positively charged, and the pH values above the isoelectric point of the BSA are usually negatively charged (Doğan et al. 2006). The isoelectric point of the BSA used as an adsorbent in the work is about pH 4.7 (Mansch and Chapman 1996). The adsorption of BSA onto diatomite clay reached a maximum value of pH 5.5. Therefore, at this pH, the interaction between serum albumin and diatomite clay is greater. The same is the enzyme lipase which biomolecules have negative charges increases at pH values above the isoelectric point leads to an increase in negative charge in the surface of krill clay as it. Demirbaş et al. stated this situation in a nice way (Tasman and Ajaeger 1998). SEM microphotographs of DC, BSA and BSA adsorbed DC after 120 min are shown in Fig. 3. Besides, as shown in Fig. 4, the increase in the amount of sodium phosphate salts resulted in an increase in the amount of adsorption. The addition of sodium phosphate in the adsorption process causes two influences. In the first case, the amount of salt added to solution medium decreases the interaction by entering between diatomite clay and protein molecules. In the latter case, the surface contact area between diatomite clay and protein molecules increases with the increase in phosphate salt. It can be said that the increase in the adsorption capacity of the adsorption process of these two processes in the second case is a more dominant effect. The similar results are observed in adsorption of biomolecules and dyestuffs on the clay surface (Demirbas 2006; Tekin et al. 2005; Vermöhlen et al. 2000; Vecchia et al. 2005). As shown in Fig. 5, in the adsorption of BSA molecules, temperature effect can be used as an important function. Adsorption experiments were performed to determine the effect of temperature (288, 298, 309.5 and 318 K) on the specific pH, concentration and at all times. The adsorption of protein on the surface of diatomite clay is increased by the increase in the temperature. However, maximum adsorption yield was obtained at a temperature of 36.5. The protein molecules are very sensitive to temperature. Its structure begins to deteriorate at very high temperatures. The adsorbing zones lose their activity at high temperatures. Therefore, interaction of BSA molecules with support materials is insufficient at very high temperatures which leads to a reduction in the adsorption effect. It shows that the adsorption does not occur chemically but physically. In addition, the increase in adsorption with temperature may decrease the pores of the support material, which may affect support material adsorption capacity (Pronk et al. 1988). It was determined that the increase in temperature caused a serious increase in the amount of adsorption (Bhattacharya et al. 2008; Sariri and Tighe 1996). The protein molecules are usually very active in the temperature range of 35.5–37 °C. The data obtained from the experimental data confirm these expressions. In parallel with his work, Vecchia et al. found that the maximum adsorption of the immobilized lipase enzyme with different support materials was found to be 37 °C (Vermöhlen et al. 2000). The optimum conditions for enzyme immobilization are obtained at these near temperature values (Vecchia et al. 2005). Sharma 2001 and Xu et al. various investigators have reported an optimal temperature for the lipase enzyme of 37 °C (Sharma 2001; Xu et al. 1995).
FTIR, SEM images and thermogravimetric (TG–DTA) analyses
As indicated in Fig. 4a–c, thermogravimetric analysis (TGA) of DC, BSA and BSA adsorbed on DC was performed. Figure 4a–c deduces the following results from the TGA curves. For Fig. 4a; when the temperature is increased from 25 to 105 °C, the weight loss of water in clay structure was impregnated with 6.8% for Fig. 4a, 9.6% for BSA Fig. 4b and 6.1% for BSA adsorbed DC Fig. 4c. As indicated in Fig. 4a, the temperature range of the dehydration event falls at 105–400 °C which falls due to the release of water in the intermediate layers at this temperature range. The rapid weight loss (4.5%) in the temperature range from 400 to 550 °C is striking with the steep slope of the TGA curve. This can be explained by the dehydroxylation of the sample. As can be seen from the curves of Fig. 4b, c, for SBA and for BSA adsorbent DC, there are two weight loss stages at temperatures of 25–100 °C and 250–450 °C, respectively. The first stage can be explained by the loss of water, the second stage can be attributed to the dissociation of BSA. Therefore, comparing the TGA scan of BSA adsorbed on DC and DC, extra weight loss of BSA adsorbed on DC can be explained by the deterioration of BSA structure. The results of the FTIR spectra of the samples used in the study (Fig. 4a–c) can be explained as follows. As indicated in Fig. 5a, for diatomite, the band at ~ 1634 cm−1 is caused by OH bending vibrations of water adsorbed in silicate minerals. The ~ 1021 cm−1 band originated from the Si–O–Si vibration. In the ~ 794 cm−1 band, it caused an OH translational vibration (Montero et al. 1993). FTIR-ATR spectrum analysis of BSA molecule adsorbed on diatomite clay was performed. Unlike the pure diatomite clay structure, the peak in the amide II (~ 1544 cm−1) band was observed. Amid II band is due to the N–H bend at the peptide bond. In this range band, a similar phenomenon has been observed as a result of the adsorption of some biomolecules on the clay (Ilia et al. 2009; Lu et al. 1994).
Kinetic analysis
The adsorption kinetics between BSA and diatomite clay, which is an oxide mineral, is well defined by the so-called second-order and in-particle diffusion model (Montero et al. 1993). This can be explained by the fact that the clay mineral, an oxide mineral, is more exposed to the interaction of BSA molecules along the open surface area and in the support material with increasing temperature. The kinetic analyzes at adsorption processes were performed at 298 K and pH 7. The adsorption is particularly rapid at the beginning (contact time < 30 min) and then slows down. The surface area for adsorption at the initial stage of the reaction may be smaller and then, the remaining surface areas affect the adversely propulsive forces between the BSA molecules on the surfaces of the support material bulk phase (Ilia et al. 2009). First, second and intraparticle diffusion models have been tried to determine which model-compatible phenomena of the adsorption phenomenon using experimental data and we can understand which model of adsorption process is being carried out. Equation (4.5) gives equations of equality in the first and second degrees, where qe is the equilibrium value of the adsorption value between diatomite clay and BSA. The qt is the value of the adsorption of bovine serum albumin and diatomite clay, which is an oxide mineral, at a given time (mg/g) and k1 represents the constant coefficient value from the so-called first-order equation at Eq. (2) (Lu et al. 1994). To understand the kinetic mechanism of the rate of the adsorption process, the pseudo-second-order equation is expressed by Eq. (3) (Giacmelli et al. 1999), where qe and k2 values are obtained from the slope of the linear line of T/q relative to t. Furthermore, \(Eq.(4).\) is used to obtain the initial adsorption rate of the experimental process.
kint values are obtained from the slope of the linear line of qt relative to t1/2 (Li et al. 2006). Table 3 presents the coefficients of the pseudo-first and second-order adsorption kinetic models and the intraparticle diffusion model at pH 5.5, 7 and 9, respectively. By looking at the R2 coefficient values, it was investigated which model was suitable. Therefore, this study suggests that the second-order-model represents better the adsorption kinetics. The parallel studies have been observed in adsorption studies (Li et al. 2006; Mall et al. 2006). These studies also show that thermodynamic analysis studies give us an idea of whether the adsorption process is physical or chemical. The various mechanisms such as external diffusion, boundary layer diffusion and intraparticle diffusion limit the adsorption kinetic mechanism (El-Naggar et al. 2012). For this reason, the intraparticle diffusion model provides information on the rate-limiting limit of the adsorption process as shown in Fig. 6. If the intraparticle diffusion occurs in a single step of limiting the velocity, then t1/2 against Q regression is linear and passes through origin (Ho and McKay 1999). Regression can be linear if the plot does not pass directly through the origin, suggesting that adsorption process involved intraparticle diffusion, but this means that the adsorption mechanism is not the only control step. In which case the adsorption rate controls the other kinetic model, the finding of which is similar to that made in previous works on adsorption (Li et al. 2006; Mall et al. 2006; El-Naggar et al. 2012; Ho and McKay 1999). The kint values increased with the temperature (288–318 K), as a result of enhancing the mobility of BSA molecules in the adsorption process. In addition, the value of C, like kint values varied with temperature (Table 4). Determination of the boundary thickness can be understood by C value. The magnitude of a boundary layer diffusion effect is proportional to the magnitude of the corresponding value of C (Ozcan et al. 2006). The results of this study show that the temperature factor is influenced by diffusion boundary layer diffusion (Chiou et al. 2004).
Thermodynamic parameters
The values of k2 are used to the finding of Ea (activation energy) from Arrhenius Eq. (6). In this equation, A is the factor of Arrhenius equation (g mol−1 s−1), Ea is activation energy (J mol−1), T is the temperature of the solution (K), R is the constant of gas (J K−1 mol−1). The activation energy was calculated from the slope of equation as 15.41 kJ mol−1. Low activation energies (5–40 kJ / mol) indicate that the process is physical and that higher activation energies (40–800 kJ / mol) are chemisorption (Guibal et al. 2003). For this reason, the thermodynamic activation parameters of the process such as free energy Δg, enthalpy ΔH and entropy ΔS were determined using the Eyring equation as shown in Fig. 7 (7) (Kannan and Sundaram 2001; Ho et al. 2002; Mall and Upadhyay 1995; Laidler and Meiser 1999).
In the Eyring Eq. (7), T is the temperature of the solution, k2 is constant of rate sorption, ∆S is entropy, ∆ is enthalpy, R is constant of gas, kb is the constant of Boltzmann (1.3807 × 10−23 JK−1) and h is the constant of Planck (6.6261 × 10−34 Js). The calculated thermodynamic parameters are given in Table 5. The value of ∆S (entropy change) was founded as—183.28 J K mol−1. This value indicates that the serum albumin was distributed regularly on the diatomite clay. The value of Ea is less than 40 kJ, indicating that the adsorption serum albumin on the diatomite clay is physical. The values of ∆G were found as negative. These values indicate that the adsorption process occurs spontaneously.
Conclusions
The diatomite clay mineral is very important for the adsorption of BSA molecules because of its low cost, high selectivity, high retention capacity and non-toxicity, and clay mineral can be used as a good adsorbent to retain proteins found in milk industry by-products. The diatomite clay as support material in adsorption processes is strong effective for adsorbing BSA molecules from aqueous media. The data obtained in the adsorption process are specifically dependent on the initial BSA concentration, duration of contact, pH and the temperature. It was clearly seen that the amount of adsorption increased proportionally with increasing contact time and becomes gradual after 30 min. The BSA adsorption amount adsorbed by the diatomite clay had a maximum value at a pH of 5.5 and decreases with increasing the solution pH. The amount of adsorption increased with increasing BSA molecule concentration and as indicated in Fig. 5, the highest adsorption takes place at 309.5 K. Also, the diatomite clay mineral is very important for the adsorption of BSA molecules because of its low cost, high selectivity, high retention capacity and non-toxicity, and clay mineral can be used as a good adsorbent to retain proteins found in milk industry by-products. The adsorption of serum albumin on diatomite clay was investigated. Herein, values of free Gibbs energy were found as negative. The negative value of the Gibbs energy change of the adsorption indicates that the adsorption is spontaneous. This indicates that the adsorption event takes place without the need for an outside energy. The process of the adsorption of the diatomite clay was found to be physical due to the value of activated energy. According to the value entropy, the process has occurred regularly on the diatomite clay. Value of enthalpy was found as − 12.84 kJ mol−1. This value indicates that the process of adsorption lipase enzyme on diatomite clay is exothermic. The adsorption process increased with increasing of initial concentration of the BSA, ionic strength and increasing contact time. The diatomite clay has a high potential to adsorb these BSA from aqueous solutions. Therefore, it can be effectively used as an adsorbent for the adsorption of BSA. The additional work on this area leads to the development of support materials for recovery of existing biomolecules from food industry wastes.
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Çalımlı, M.H., Demirbaş, Ö., Aygün, A. et al. Immobilization kinetics and mechanism of bovine serum albumin on diatomite clay from aqueous solutions. Appl Water Sci 8, 209 (2018). https://doi.org/10.1007/s13201-018-0858-8
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DOI: https://doi.org/10.1007/s13201-018-0858-8