Biogeneration of Silica Nanoparticles from Rice Husk Ash Using

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Biogeneration of Silica Nanoparticles from Rice Husk Ash Using Fusarium oxysporum in Two Different Growth Media Tatiana G. Pineda-Vásquez,†,‡ Ana E. Casas-Botero,† Margarita E. Ramírez-Carmona,† Mabel M. Torres-Taborda,† Carlos H. L. Soares,§ and Dachamir Hotza‡,* †

Department of Chemical Engineering, Pontifical Bolivarian University (UPB), Circular 1 #70-01, Medellin, Colombia Department of Chemical and Food Engineering, Federal University of Santa Catarina (UFSC), 88040-900 Florianópolis, Brazil § Department of Biochemistry, Federal University of Santa Catarina (UFSC), 88040-900 Florianópolis, Brazil ‡

ABSTRACT: The biotransformation of rice husk ash (RHA) by Fusarium oxysporum to generate silica nanoparticles was carried out using two different commercial growth media: malt-glucose (MG) and malt-glucose-yeast-peptone (MGYP). Biomass production, substrate consumption, organic acids production, and solubilized silica were measured during RHA biotransformation. Extracellular proteins were analyzed by SD-PAGE. Silica nanoparticles were analyzed by XRD, zeta potential, SEM, and TEM. The results showed that the production of organic acids was not directly related to the solubilization of silica. Solubilization and stabilization of silica occur mainly in the exponential growth phase of F. oxysporum, which are associated with the action of extracellular proteins with sizes 24, 55, and 70 kDa. MG medium presented the best performance for the growth of F. oxysporum and production of semicrystalline, quasi-spherical silica nanoparticles in the range of 2−8 nm.

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INTRODUCTION Silica is an important material widely used for industrial and commercial purposes. High surface area silica nanoparticles have been successfully used as resins,1−4 catalytic supports,5−10 molecular filters,11−13 biomedical applications,14−18 rubber fillers,19,20 construction materials,21−24 among others.24−26 Silica nanoparticles can be synthesized by numerous methods or obtained from several residues, such as silicon sludge, rice husk (RH), or rice husk ash (RHA).23 RHA is one of the most common sources of silica, which is an industrial waste produced by burning RH as a sustainable biomass energy resource. RH, the hard protective shell of rice grains, is an agricultural byproduct of rice mills.27 In 2012 almost 243 millions of tonnes of rice husk were produced in the world and used for several processes as combustion,28−31 gasification,32−34 and pyrolysis.32,35,36 Almost 15% of rice husks are ashes that can be used as a cheap source for silica synthesis, contributing to the industrial scale production of several materials. The silica present in rice husk is in a hydrated amorphous form. Thermal and chemical treatments have been used to produce silica micro and nanoparticles.25,29,37,38 However, those processes can be expensive and have a low productivity. Bansal et al. presented a biological route for the generation of silica nanoparticles from rice husk using the fungus Fusarium oxysporum.23 This technique has a great potential because it can use soft conditions of temperature and pressure, being environmentally friendly. Moreover, Pineda et al.39 synthesized silica particles from RHA using cultures of F. oxysporum. They observed that before and after reaction with the fungus, the morphology of silica particles in RHA changed and the average size decreased from ∼600 to ∼5 μm. Different authors have established that microorganisms can modify their interaction with minerals according to the culture media.40,41 The process conditions regarding the action of F. oxysporum, such as concentration of substrate and protein, and © 2014 American Chemical Society

the addition of minerals containing silica to the growth media may influence the biotransformation process.42 The amorphous silica in RHA can be simultaneously leached and transformed into crystalline silica nanoparticles by F. oxysporum. The leaching step has been associated with the production of organic acids and the biotransformation step with a hydrolyzation reaction due to the action of specific proteins.43 Both steps depend on growing conditions and culture media, which may exhibit different composition in special different sugar/protein ratio. In this context, the aim of this work was to analyze the influence of two different commercial culture media supplemented with RHA on the F. oxysporum capacity in producing nanosilica particles. The respective growing curves were compared and the best conditions were established for the production of silica particles. Special attention was dedicated to the effects of organic acids on the hypothetical first step of the leaching process.

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EXPERIMENTAL SECTION Materials. Rice husk ash (RHA) was obtained from Arroz Fumacense (Morro da Fumaça, SC, Brazil), without pretreatment. F. oxysporum was obtained from UPB (Medellin, Colombia) and maintained at 25 °C with potato dextrose agar (Merck). Spores were harvested with distilled sterile water to prepare a solution with a final concentration of 108 spores/ mL. Silica Biotransformation. Silica biotransformation was carried out using two different liquid culture media. A maltglucose (MG) medium was composed by 1.5 wt % malt extract Received: Revised: Accepted: Published: 6959

December 19, 2013 April 3, 2014 April 3, 2014 April 3, 2014 dx.doi.org/10.1021/ie404318w | Ind. Eng. Chem. Res. 2014, 53, 6959−6965

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organic acid production capacity.50,51 Based on this, two media containing different initial concentration of glucose, malt extract, and RHA were selected. The intention was to obtain information on the mechanism of production of silica nanoparticles, particularly to investigate how microbial organic acid production can affect the solubilization of silica particles in amorphous silica containing RHA. The CO2 production can be related to microbial metabolic activity during growth.52 This method was selected due to the interference of RHA in biomass measurements when the dry weight method is used. The CO2 production is associated with microbial metabolism and it can be used as an indirect method to follow the growth of F. oxysporum although it also includes the CO2 production during maintenance stage. CO2 production in both media was fitted using nonlinear sigmoid growth functions. For MG media the Gompertz model (eq 1) fitted the experimental results of CO2 production with an adjusted determination coefficient (R2 adjusted) of 0.99 and the root mean squared error (RMSE) of 0.076. Experimental data for MGYP media was better adjusted by the MorganMercer-Flodin (MMF) model (eq 2), with R2 adjusted of 0.99 and RMSE of 0.155. Figure 1 shows the results obtained for CO2 produced from F. oxysporum growing in MG and MGYP media, both supplemented with RHA.

and 0.3 wt % glucose; and a malt-glucose-yeast-peptone (MGYP) medium was composed by 0.3 wt % malt extract, 1 wt % glucose, 0.3 wt % yeast extract, and 0.5 wt % peptone. The pH value was adjusted to 6.8 with NaOH 0.1 M and HCl 0.1 M solutions. Both culture media were supplemented with RHA, MG (2 wt % RHA) and MGYP (10 wt % RHA). Media were autoclaved for 20 min at 121 °C. The microbiological process was started by inoculation of 10 mL of F. oxysporum spores solution (108 spores/mL) into 250 mL erlenmeyer flasks containing 100 mL of media (MG or MGYP) supplemented with RHA. The flasks were incubated at 25 °C on a rotating shaker (150 rpm) during 4 days. Characterization of Biotransformation Process. Microbial growth was evaluated by CO2 production, using an Oxitop device (WTW) every 30 min. Samples were collected during the course of reaction by separating fungal mycelia and the remaining RHA from the aqueous component by filtration. The filtrate was used to measure glucose consumption and organic acids production by high performance liquid chromatography (HPLC). The PerkinElmer HPLC system was equipped with a refraction index detector (RID) and a 300 mm ion exclusion column (7.8 × 150 mm, Waters). The mobile phase consisted of 0.005 N sulfuric acid. The flow rate was 0.6 mL/min. In order to quantitatively evaluate the CO2 production by F. oxysporum in MG and MGYP media, two models were used: Gompertz44−46 (eq 1) and Morgan-Mercer-Flodin45,46 (MMF, eq 2): ln(CCO2) = aexp( −exp(b − ct )) ln(CCO2) = A −

(1)

(A − B ) (1 + Kt D)

(2)

where a, b, c, A, B, K, and D are model parameters, CCO2 is the CO2 concentration, and t is the time. The extracellular proteins in culture media were analyzed using 12 wt % sodium dodecyl sulfate polyacrylamide gel electrophoresis (SDS-PAGE), after centrifugation at 10 000 rpm for 30 min. Concentration of solubilized silica was measured from the aqueous phase by UV−vis spectrophotometry using the standard molybdate method.47 Samples for transmission electron microscopy (TEM, JEM-2100) were prepared by dropping water-dispersed bioleached nanoparticles onto carbon-coated copper grids. Also, samples of solubilized silica were evaporated under reduced pressure to powder, and this powder and RHA were characterized after calcination at 400 °C during 2 h by scanning electronic microscopy (SEM, JEOL JSM-6390LV),48 and X-ray diffractometry (XRD, Philips XPert) with rotating anode generators and monochromatic detector using Cu Kα radiation from a 2θ of 0−120° with the step 0.05°. Zeta potential measurements of silica particles were performed (Zeta Nano Sizer ZEN-3600, Malvern) before and after the biotransformation process. The concentration of RHA and the suspension of silica nanoparticles were both 100 mg/L. According to the literature,49 NaCl 0.01 M was used as a neutral electrolyte. The isoelectric point (IEP) was determined by varying pH values through NaOH and HCl titration.

Figure 1. CO2 production from F. oxysporum growing in media MG and MGYP, supplemented with RHA.

The Gompertz model was rewritten in terms of three parameters microbiologically significant according to Zwiettering et al.44 (eq 3): the maximum specific growth rate, μmax, calculated as the slope of a tangent line at the inflection point; the lag time, λ, defined as the intercept with x-axis of this tangent line; and the asymptote, CCO2max, the maximum value of CO2 reached. Equation 4 shows the parametrization proposed for the MMF model:46 CCO2max, corresponding to the maximum CO2 production; CCO20, the initial concentration of CO2 at t = 0; δ, a parameter that controls the inflection point; and k, a scale parameter.

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⎤ ⎡ μ exp(1) ln(CCO2) = ln(CCO2max ) exp⎢ max (λ − t ) + 1⎥ ⎢⎣ ln(CCO2max ) ⎦⎥

RESULTS AND DISCUSSION It is well-known that the chemical composition of culture media can affect the enzyme production by the fungus as well as its

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dx.doi.org/10.1021/ie404318w | Ind. Eng. Chem. Res. 2014, 53, 6959−6965

Industrial & Engineering Chemistry Research ln(CCO2) = ln(CCO2max ) −

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glucose, respectively. The initial glucose content of the culture media and the behavior of its depletion rate across the time is an important element to establish the substrate yield and the uptake of essential nutrients. As it can be seen in Figure 2 that most of the total glucose was consumed during the second day for the fungus growing in MGYP medium (85%) and between the first and the third day when it grew in MG media (95%), when the fungus achieved the stationary phase, and the total glucose was fully consumed. Comparing the Figures 1 and 2, and taking into account that the composition of MG culture media contains less initial glucose concentrations than MGYP, the glucose consumption curves indicated that in MG medium the fungus can produce more CO2 using a lower concentration of glucose. This result may indicate that carbon sources other than glucose are being used for growing and producing CO2 especially after 3 days of incubation period. In this case, the production of hydrolyze enzymatic activity is required. On the other hand, the results obtained for the MGYP media seems to indicate that the higher rate of glucose consumption in the first 2 days instead of CO2 production was followed for other metabolites production, for example, by organic acids production. The latter hypothesis seems to be correct if it takes into account the curve of organic acid production observed in Figure 3 which it may the reason for the discrepancy observed between CO2 and glucose consumption curves in MGYP media case.

ln(CCO2max ) − ln(CCO20) 1 + (kt )δ

(4)

For the MMF model, the parameters μmax and λ were calculated in the same way as proposed for Gompertz model.44 Table 1 presents the results for growth parameters in both culture media. Table 1. Predicted Specific Growth Rate (μ, days−1), Lag Phase (λ, days), and Maximum CO2 Concentration (CCO2max, mg/L) MG media

MGYP media

parameter

Gompertz model

MMF model

μmax (days−1) λ (days) CCO2max (mg/L)

1.882 0.441 523.76

5.960 1.182 216.60

The results in Figure 2 and Table 1 show that the CO2 production curves for both media culture exhibited different

Figure 2. Glucose consumption curve by F. oxysporum growing in MG and MGYP media. Figure 3. Organic acids production curves compared to soluble silica for the MGYP and MG culture media.

phases of microbial growth in a closed system. The first phase represents the time needed for microorganisms to adapt to the media culture (latency phase). In this case, F. oxysporum presented a latency phase of 1 day for the MGYP medium and about 0.4 days for MG medium. During the second phase the microorganism presented an exponential growth until it achieved the stationary phase and exhibited the maximum growth rate. For F. oxysporum the maximum specific growth rate was 1.88 days−1 in MG and 5.96 days−1 in MGYP, showing a faster CO2 production in MGYP related with a higher concentration and uptake of substrate in this media. The amount of CO2 produced in MG media was higher than in MGYP media after 4 days of incubation period. According to the CO2 production, the results showed that the F. oxysporum grew better in MG media. The results are important due to economic considerations for industrial production of biotransformed silica. Figure 2 shows the glucose consumption by F. oxysporum in MG and MGYP media, which contained 0.3 and 1 wt %

Figure 3 shows organic acids production results compared to the soluble silica production curves for MGYP and MG culture media. The concentration of solubilized silica increased in the time period that the organic acid concentration decreased for MG culture media. For MGYP media, an opposite effect was observed. In this case, the organic acid production increased and the concentration of solubilized silica decreased. First, these results clearly indicate that the metabolic routes for glucose transformation were different in each medium. In MGYP, higher intermediate production of organic acids was observed. Additionally, regardless of the operative mechanisms with respect to glucose consumption, the results showed that an increase in silica nanoparticles solubilization was not directly associated with the organic acids production. Frequently it has been suggested that the leaching step may be related to the organic acids production.53 The organic acids are synthesized 6961



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on gel electrophoresis by Mukherjee et al. They suggested that out of four proteins of that study, one was responsible for the reduction of ions and the subsequent formation of gold nanoparticles.55 According to the former results, MG was selected as the culture medium to evaluate the nanoparticle production by XRD and zeta potential measurements, both before and after microbial process. Figure 5 shows the XRD results for RHA and silica nanoparticles after the fungal transformation. According to

by the fungi in the glycolytic pathway and could promote the bioleaching process due to chemical attack. Studies have been reported for bioleaching processes of metals, where organic acids promote the mineral dissolution by lowering the pH and increase the load of soluble metals by complexion-chelating into soluble metallic complexes.53 However, for the silica biotransformation, the organic acid production does not seem to contribute for silica bioleaching process. Bansal et al. found that the silica biotransformation is associated with proteins present in fungal biomass.54 Considering the growth curves, the glucose consumption and the organic acids production, it can be established that the MG medium is more suitable for the transformation of silica nanoparticles when compared to MGYP medium. Those results are important due to the economic considerations for the scale up of the processes. Figure 4 shows the electrophoretic profile of extracellular proteins produced by F. oxysporum growing in MG medium

Figure 5. XRD diffractograms for RHA and silica nanoparticles after the biotransformation using F. oxysporum.

the literature, a low intensity halo between 15° and 30° is typical for RHA, and a peak at 22° corresponds to cristobalite.36 After biotransformation, the XRD presented a small fraction of silica crystals, and the intensity of peaks 28.2°, 31.78°, and 40.42° increased. This suggests that a fraction of the amorphous phase is converted into crystalline phase. According to Bansal et al., biomolecules and proteins released by the fungus first leach out the amorphous silica from the rice husk ash and then biotransform the amorphous silica into crystalline silica particles.23 Figure 6 shows the zeta potential curves of silica particles as a function of pH before and after the interaction with F. oxysporum. The results correspond to negative surface charges for both materials for all of the tested pH values. The isoelectric point (IEP) value of RHA particles was around pH 2.8; this value is slightly more basic than the PIE of pure silica, probably due to the presence of other oxides such as CaO, K2O, and Na2O and to other impurities, organic in nature, remnants of burning rice husk, such as hemicelluloses and celluloses.38 These impurities are characterized by having IEP between 2.9 and 7.5.56 The RHA surface is electronegative when the pH is above 3.0. The zeta potential decreases with increasing pH value up to pH 10, which is in good agreement with Ma et al.57 Observing Figure 6, it is interesting to become aware of the zeta potential alteration profiles after the fungal contact with the particle surfaces, which can be related to the secretion of protein fungal compounds that interact with RHA and modify the particles surface. The pH value at the IEP of silica nanoparticles decreased to around 1.3. This value is similar to IPE of pure SiO2 (1.7−2.0).58−60 IEP may present some

Figure 4. Electrophoresis results: (A) Extracellular proteins of F. oxysporum growing in MG medium page, (B) extracellular proteins of F. oxysporum growing in MG medium supplemented with RHA, (C) page ruler prestained 10−170 kDa (Thermo).

supplemented with RHA after 4-day incubation period. These proteins were analyzed using 12% SDS-PAGE. For fungi growing in MG with RHA (Figure 4, B) a band corresponding to a low molecular weight protein was observed at 10−15 kDa and around 24 kDa, as well as two bands between 55 and 70 kDa and a very high molecular weight protein of more than 200 kDa. It was noticed that the exposure of F. oxysporum to MG medium containing RHA induced the secretion of proteins of molecular weights around 24 kDa and 55−70 kDa, which are lacking in the MG media. The presence of a low molecular weight protein around 24 kDa is in agreement with Bansal et al.ś work.54 They established that this low molecular weight protein might be acting as hydrolyzing/capping proteins and that the high molecular weight proteins could be acting as a template for nanosilica synthesis.23 Proteins of 55−70 kDa have not been reported for this system, but four proteins of molecular masses between 66 and 10 kDa have been detected 6962



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decreased. This was also reported by Rozainee et al.62 and Martinez et al.29 Heterogeneously distributed silica particles on upper and lower surfaces of rice husk ash can be seen as bright dots (Figure 7B). Moreover, after bioprocessing Si peaks detected by EDX presented a stronger signal (Figure 7D) when compared to the RHA before bioprocessing (Figure 7C). Although many variables could affect the signal intensity, EDX of samples after biotransformation consistently presented spectra showing a larger amount of silica particles leached out. To further investigate the primary particle size distribution of biogenerated silica, a sample of particles from reaction products formed during 4 days was taken, diluted into ethanol and analyzed by TEM (Figure 8A). A statistical analysis of 200 random silica particles indicated that the primary particle size ranged from 1 to 7 nm, with an average of 4 ± 2 nm (Figure 8B). In this way, the extracellular bioprocess led to the generation of silica nanoparticles from rice husk ash at room temperature.

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Figure 6. Zeta potential of silica particles in RHA before and after the interaction with F. oxysporum.

CONCLUSIONS Taking into account growth curves, CO2 production, glucose consumption, and organic acids production, it may be concluded that the MG medium is more suitable for biogeneration of silica nanoparticles when compared to MGYP medium. Considering the composition of culture media, these results are important due to the economic considerations for the scale up of processes. Based on the organic acids and the soluble silica production curves, the results showed an increase in silica nanoparticles solubilization that was not associated with the organic acids production. It was rather correlated to proteins associated with the exposure of F. oxysporum to RHA. Changes in XRD angles with the fungal biotransformation correspond to the surface modification on silica particles due to the fungal action. Likewise, an alteration on zeta potential profiles was observed after fungal contact with the particle

dispersion in values depending on the method of silica synthesis, conditions of storage and surface properties. In this case, the electrokinetic curves mean that silica particles dispersed in water present a positive charge in a strongly acidic environment (pH < 1). On the other hand, at pH values higher than the IEP, negative values of zeta potential are related to the increased dissociation of silanol groups on the SiO2 surface.61 Figure 7 shows SEM micrographs of rice husk ash obtained by extracellular process using F. oxysporum at 28 °C and atmospheric pressure. Particles before treatment are irregular in shape with average size of 610 ± 60 μm (Figure 7A). After fungal treatment, the structure of RHA was broken down, the morphology of silica particles changed, and the average size

Figure 7. SEM micrographs and EDX of lower surface RHA before (A, C) and after (B, D) the interaction with F. oxysporum. 6963



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surfaces. This change could be due to the secretion of fungal proteins that interact with the RHA surfaces and modifies the superficial particles. SEM images showed different average sizes in silica nanoparticles, after fungal treatment indicating a morphological change in silica nanoparticles.

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Phone/Fax: +55 48 3721 9448/ 9687. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS The support from CNPq/Brazil and COLCIENCIAS/ Colombia is gratefully acknowledged.

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Biogeneration of Silica Nanoparticles from Rice Husk Ash Using

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