Article pubs.acs.org/JAFC
Improving Digestibility of Feather Meal by Steam Flash Explosion Yiqi Zhang,† Ruijin Yang,*,‡ and Wei Zhao‡ †
State Key Laboratory of Food Science and Technology, and ‡School of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu 214122, People’s Republic of China ABSTRACT: Poultry feathers are available in large quantities. However, natural feathers have poor digestibility and are often considered as solid wastes. To improve the digestibility of poultry feathers, steam flash explosion (SFE) was applied to duck feathers at different pressures ranging from 0.5 to 2.5 MPa for 1 min. The pepsin digestibility, disulfide bond content, and major secondary structure component (β-sheets) of duck feathers before and after the process were examined. The results showed that SFE could effectively increase pepsin digestibility of feather meal. Under the optimal conditions (1.8 MPa for 1 min), the pepsin digestibility of exploded feather meal achieved approximately 91%, which was about 9 times higher than that of the original feathers. The pepsin digestibility was highly correlated with the degree of reduction of disulfide bonds (R2 = 0.98) and slightly negatively correlated with β-sheet structure. SFE is an effective method to improve the bio-utilization of feather meal. KEYWORDS: feather meal, pepsin digestibility, steam flash explosion, disulfide bond, β-sheets
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INTRODUCTION Feathers represent 5−7% of the body weight of domestic fowl. An estimated 1.5−2 million tonnes are produced annually from the poultry industry in the United States, and over 65 million tonnes are produced worldwide.1,2 It is a valuable protein source that could be beneficially harnessed as animal feedstuff. However, there is limited use of feathers for industrial applications, and most of the feathers are currently disposed as solid wastes by incineration or landfilling.3,4 Feathers contain about 90% protein called keratin. With extensive disulfide bonds and cross-linkages, feather keratin forms filamentous structures made of polypeptide chains folded into β-sheets, which are stacked and twisted to form a helical structure.5 This highly rigid structure of feather keratin renders it insoluble and resistant to most proteolytic enzymes. Thus, without appropriate processing, feather meal has poor digestibility (only 10%) and low nutritive value. Many treatments have been developed to increase the digestibility of feather meal, including hydrothermal treatment, chemical (strong acidic, alkalic, or catalytic) hydrolysis, and enzymatic hydrolysis.4,6−8 However, the hydrothermal treatment achieves limited and varying nutritional improvement. The chemical hydrolysis often brings serious pollution to the environment. The higher cost of enzymes themselves, with a long production cycle, has thus far limited the development of industrial processes. Hence, investigation into alternative technology with prospects for nutritional enhancement, environmental friendliness, and cost-effectiveness seems justifiable. Steam explosion is an innovative method for pretreatment of renewable resources into value-added materials for bioconversion, e.g., barley bran, wood, feather, and other agricultural byproducts.9−12 Steam explosion is based on short-time steam cooking of biomasses at high temperatures, followed by rapidly releasing to ambient, the advantages of which include a significantly lower environmental impact, lower capital investment, and less hazardous process chemicals.13 Steam flash explosion (SFE) is developed from conventional steam © 2014 American Chemical Society
explosion, steam spout, or swollen technologies, but it is dramatically different from these physicochemical methods in steam deflation time. SFE adopts a structure in catapult explosion mode that is principally composed of a cylinder and piston, which could complete the explosion within 0.00875 s. However, conventional steam explosion technologies adopt a classical structure in valve blow mode, which need at least tens of seconds or minutes to finish the release of high-pressure steam.14 The rapid pressure release could achieve a physical tearing effect, which functions as a conversion process of thermal energy into mechanical energy to enhance the biomass dissociation.14,15 Meanwhile, the residence time of the materials with the high-pressure steam causes various chemical reactions. The objectives of this study were (1) to investigate the possibility of developing feather meal with high digestibility using SFE and (2) to gain additional information about the relationship between the structure of feather keratin and pepsin digestibility. It was anticipated that the results from this work would provide a new understanding of the application prospect of SFE in feather meal for industrial development.
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MATERIALS AND METHODS
Materials. Dry and clean duck feathers were supplied by Hangzhou Venus Biological Nutrition Co., Ltd., China. The feathers had 6.0% moisture content (w/w, wet basis), 90.2% crude protein, and 1.6% crude fat (w/w, dry basis). All chemicals were of analytical grade. SFE Treatment. The experiments were carried out on a QBS-200B SFE test bed with a 5 L chamber from Gentle Science and Technology Co. Ltd., China. The diagram of the SFE process is shown in Figure 1. The apparatus consists of a steam generator, material vessel, receiver, and rapid-opening piston valve. About 100 g of air-dried feathers were placed inside the vessel and exposed to the saturated steam in each bath. SFE was performed at 0.5, 1.0, 1.4, 1.6, 1.8, 2.0, 2.2, and 2.5 MPa for 1 min. After the elapsed time, the piston valve was opened and the
Received: Revised: Accepted: Published: 2745
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Figure 1. Structural diagram of the QBS-200B SFE test bed: (a) SFE system, (b) status of the piston in the steam boiling phase, and (c) status of the piston in the explosion phase. pressure decreased dramatically in a very short time (within 0.00875 s). The exploded materials, together with a little water, were recovered in the receiver and frozen at −20 °C until the analyses. Morphological Characterization. The morphology of feather fibers was observed using scanning electron microscopy (SEM, FEI Quanta 200, Eindhoven, Netherlands). The specimens were mounted on conductive adhesive tape, sputter-coated with gold palladium, and observed using a voltage of 5.0 kV. Protein Solubility and Pepsin Digestibility. A total of 1 g of ground samples was suspended in 25 mL solutions. The suspensions were shaken in a water bath for 4 h according to the method described by Li and Lee.16 The mixture was centrifuged at 10000g for 20 min at 4 °C. The soluble protein content of the supernatant was then determined using a modified Lowry procedure.17 The total nitrogen in the original samples was measured by the Kjeldahl method. All analyses were conducted in duplicate. Pepsin digestibility of each sample was determined by the procedure of the AOAC International using 0.2% pepsin (activity of 1:10 000) in 0.075 M HCl.18 In this assay, 1.000 g (±0.010 g) of sample was incubated in 150 mL of pepsin solution at 45 °C for 16 h. Protein digestibility was expressed as the difference between the nitrogen content of the sample and the residual nitrogen content after pepsin digestion, divided by the nitrogen content of the sample. Disulfide−Sulfhydryl Quantification. Disulfide (SS) and sulfhydryl (SH) contents of unexploded and exploded samples were determined according to the method of the solid-phase assay by Chan et al.,19 with some modifications. For free sulfhydryl content determination, approximately 15 mg of the ground sample with a particle size smaller than 40 mesh was suspended in 0.8 mL of reaction
buffer consisting of 8 M urea, 3 mM ethylenediaminetetraacetic acid (EDTA), 1% sodium dodecyl sulfate (SDS), and 0.2 M tris(hydroxymethyl)aminomethane) (Tris)−HCl (pH 8.0) (buffer A). The reaction mixture was vortexed for various intervals at room temperature. After 2.5 h, 0.2 mL of 50 mM 5,5′-dithiobis(2nitrobenzoic acid) (DTNB) in 0.2 M Tris−HCl (pH 8.0) (buffer B) was added to each sample, vortexed for 1 h, and then centrifuged at 13600g for 10 min at room temperature. Concurrently, a sample was incubated without DTNB as a blank. The supernatant was collected and diluted at a ratio of 1:10. The absorbance of the supernatant was read at 412 nm. An extinction coefficient of 13 600 M−1 cm−1 was used to calculate the number of thiol-containing groups. For determination of the total sulfhydryl (SH + reduced SS) content, the assay procedure was as described for the SH assay, except for the use of different reaction buffers. The buffer consisted of 8 M urea, 3 mM EDTA, 1% SDS, and 0.2 M Tris−HCl (pH 9.5), 0.1 M Na2SO3, and 50 mM 2-nitro-5-thio-sulfobenzoic acid (NTSB2−), synthesized from DTNB according to the procedure by Thannhauser et al.20 The disulfide group content was calculated as the difference between the thiol group content before and after reduction of disulfide bonds with sulfite. From each replicate of each treatment, three measurements were taken. Fourier Transform Infrared (FTIR) Spectroscopy. FTIR spectra of the steam-exploded samples, dried at 105 °C for 2 h, were obtained from 4000 to 400 cm−1 by a Nexus Thermo Nicolet spectrometer. The KBr pellet sampling method was used to prepare the thin film for testing. All sample spectra were recorded at 128 scans and 4 cm−1 resolution, and spectra of two replicate measurements for each sample were averaged. The infrared (IR) spectra were acquired and analyzed 2746
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using Thermo Scientific OMNIC software package (version 8.2). Spectra were baseline-corrected, smoothed with a nine-point Savitsky−Golay function, and normalized using the amide I absorption intensity peak. Amide I was shown after band narrowing by Fourier self-deconvolution (FSD) to resolve overlapping IR bands using a half bandwidth of 30.0 cm−1 and enhancement factor k = 3.0. Secondderivative spectra were obtained to support the initial identification of band positions by deconvolution. The band positions obtained from the above steps were then used as the initial guess for curve-fitting of the original spectra with Gaussian bands. For the final fits, the positions, heights, and widths of all bands were varied simultaneously. The curve-fitting procedure was calculated on Peakfit version 4.12 software (SeaSolve Software, Inc.). Statistical Analysis. Data are expressed as the mean ± standard deviation (SD). The difference between groups were tested by analysis of variation (ANOVA) and Duncan’s multiple range tests (SPSS version 19.0 for Windows, SPSS, Inc., Chicago, IL). Means were compared and considered significant when p < 0.05.
with shrinkage folds appearing occasionally (panels b and c of Figure 2). As the pressure increased, the central axis of the feather disappeared and the original structure could not be identified. The samples gave cross-interconnected pores, which were sponge-like and had more cracks and cavities (panels d−f of Figure 2). In SFE treatment, saturated steam with a powerful seepage force penetrates into the fibrous tissues of the materials. The material is maintained at the desired pressure for a short time and undergoes hydrolysis and other chemical processes. At the end of this period, the pressure rapidly decreases to atmosphere and most of the steam in the material will quickly expand. Accordingly, the resulting mechanical effect plays a role in forming the cavities in the surface of feather when the steam rushes out. Yu et al.14 also demonstrated the mechanical effect of steam explosion through the characterization of the morphological changes of maize stalks in different steam pretreatment methods. We prolonged the time of the feather at 1.8 MPa to 8 min and then carried out SFE, but no additional effect was found on the treatment efficiency, indicating that the mechanical effect played an important role on the exploded feathers. Protein Solubility and Pepsin Digestibility of Feathers Treated by SFE. Four solvents [0.05 M sodium phosphate buffer (pH 8.0), 0.05 M sodium phosphate buffer (pH 8.0) + 6 M urea, 0.2% potassium hydroxide, and 0.2% pepsin] were used to monitor dissolubility changes of the exploded samples. As shown in Figure 3, the dissolubility of feather meal in all of the
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RESULTS AND DISCUSSION Morphological Changes of Feathers Treated by SFE. The effect of SFE on the morphology of feathers was illustrated in Figure 2. SEM of untreated and treated feathers showed
Figure 3. Solubility and pepsin digestibility of feather meal treated by SFE treatment. The dotted line is the minimum digestible protein level recommended as feather meal by the Association of American Feed Control Officials. The data are expressed as the mean ± SD (n = 3). Figure 2. Scanning electron micrographs of untreated and treated feathers by SFE treatment: (a) feather fiber without treatment (50×), (b) steam exploded at 0.5 MPa (50×), (c) steam exploded at 1.0 MPa (50×), (d) steam exploded at 1.4 MPa (50×), (e) steam exploded at 1.8 MPa (50×), and (f) steam exploded at 1.8 MPa (500×).
solvents tested in this study dramatically increased with the increase of steam pressure. The protein solubility in 0.2% potassium hydroxide solution is always the common procedure to evaluate the intensity of treatment.21 After SFE treatment, the solubility of feather meal could reach 89.3% at 2.5 MPa from only 3.0% in the original sample. The increase may be ascribed to the increasing repulsive forces between surface groups of the exploded sample that mainly exists as the anion form. From the point of view of eco-friendly conversion and utilization of extracted keratins, it is not necessary to use 0.2% potassium hydroxide to extract feather keratins. Figure 3 also
obvious morphological changes induced by SFE treatment. As shown in Figure 2a, feathers showed a smooth surface and had a hierarchical structure beginning with the level of the central barbs, which grow directly from the quill. These central barbs are tiny “quills” that also grow barbs.12 At lower steam pressures, feathers showed the regular and compact structure, 2747
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of the disulfide bond and free SH in feather keratins treated by SFE treatment. Obviously, SFE treatment could significantly decrease the content of the disulfide bond, which is the major factor resistant to proteolytic cleavage. With the increasing severity of the treatment, the disulfide bonds decreased from 330 to 93 nmol mg−1. Because 1 mol of disulfide reacts quantitatively to yield 2 mol of cysteine residues, the free sulfhydryl increase should be accounted for the decreased disulfide cross-linking. However, as shown in Figure 4, the free sulfhydryl significantly (p < 0.05) decreased from 10 nmol mg−1 for the control to 2 nmol mg−1 for the exploded sample (1.0 MPa) and then increased to 31 nmol mg−1 at higher steam pressures. Although the sample showed the greatest increase in free sulfhydryl with the greatest decrease in disulfides, the changes were not proportional. The decrease in free sulfhydryl content of exploded samples at low pressures and then increases with increasing steam pressures, concomitant with decreases in disulfide bonds, are in general agreement with the findings among extruded samples. These authors showed large reductions in disulfide bond content and slightly increased sulfhydryl content among the extrusion of wheat meal and lentil meal.25,26 The results indicated that feather keratins containing a high level of cysteine/cystine residues were easily denatured by SFE treatment. It is also likely that some of the free sulfhydryl groups were oxidized to sulfoxyl compounds or formed sulfurcontaining volatiles, such as hydrogen sulfide, volatile organic compounds, or flavor compounds, during the process.27,28 Furthermore, because of the involvement of mechanical force in the explosion phase, cysteine might be more prone to oxidation and then the keratin molecules was susceptible to the extrinsic factors, such as the temperature and humidity. FTIR Spectroscopy of Feathers Treated by SFE. The secondary molecular structure of feather keratin can be changed under the influence of physicochemical forces, such as mechanical forces or chemical processes.29 FTIR investigation can be used as an effective tool to assess the structural changes in proteins. Particularly, the amide I band in the range between 1600 and 1700 cm−1 and amide II band in the region of 1510 and 1580 cm−1 provide useful information. Amide I, the most intense absorption band in proteins, is useful for the analysis of the protein secondary structure and arises mainly from CO stretching, with a minor contribution from C−N stretching, while the amide II band originates from the N−H bending and C−H stretching vibrations.30 In Figure 5, the IR spectra of feather keratin are reported. As previously reported1 and evident from the amide I peak at 1627 cm−1, the feather mainly consists of β-sheet structure. A peak shift of the amide I band was observed as a function of the steam pressure from approximately 1627 cm−1 to a strong, broad maximum at approximately 1633 cm−1, which was indicative of decreased amounts of ordered β-sheet structures and the promotion of disordered structures.1,31 The amide II band, much less conformationally sensitive than amide I, is related to N−H bending and C−H stretching vibrations. However, it is much more sensitive to the environment of the N−H group. Therefore, the amide II band can be used to deduce changes to the environment of the N−H groups and respond to differences in hydrogen-bonding environments.32 In general, stronger hydrogen-bonded N−H groups absorb at higher frequencies.1 In amide II of the steamexploded samples, it is worth noting a significant decrease in the intensity of the absorption band at 1540 cm−1 with respect
showed that there was 16.2% of the exploded sample soluble in a 0.05 M sodium phosphate (pH 8.0) system and 64.6% of the protein soluble in a 6 M urea system at 2.5 MPa. However, the original feathers are almost insoluble in the above mild solvents. The present work also provides a mild way to extract feather keratin for exploitation of innovative biopolymers. Feathers are rich in crude protein (90%), while without pretreatment, only 10.5% of feathers could be hydrolyzed by pepsin, because of their intact and compact structures.4 As shown in Figure 3, pepsin digestibility sharply increased to 91.9% at 1.8 MPa, which was nearly 9 times higher than that of untreated feathers, while it changed not significantly at higher conditions (p > 0.05). This result reflects the very high effectiveness of SFE treatment for the improvement of the bioutilization of feather meal. Moreover, only cysteine decreased significantly from 5.07 g/100 g of crude protein for the control to 1.66 g/100 g of crude protein for the exploded sample at 1.8 MPa, while the changes of other amino acids in feather meal were not obvious during SFE treatment (data not shown). Several researchers have employed chemical treatments or screened microorganisms to increase the enzymatic accessibility of feathers.7,22,23 Obviously, it is not environmentally friendly or requires a long production cycle and tedious preparation. SFE is a physicochemical process, which includes three phases: the steam penetration phase (3−5 s), the boiling phase (1−3 min), and the explosion phase (within 0.00875 s). The total time in high temperatures is very short, and the temperature of materials could decrease to 50 °C or lower immediately after SFE treatment, indicating that SFE treatment is a highefficiency and environmentally friendly process for production of feather meal. When steam pressure rose higher than 2.2 MPa, the colors of the samples were dark yellow, indicating degradation and a chemical modification of feather keratin, as demonstrated by Senoz et al.24 The author suggested that undesired materials formed via cross-linking reactions to provide a high-temperature-resistant nature to the keratin, even when disulfide bonds were broken. In the present work, SFE allowed use of a low steam pressure (1.8 MPa) and short time (1 min) to effectively increase pepsin digestibility of feather meal. Disulfide Bonds and Free Sulfhydryl of Feathers Treated by SFE. Figure 4 illustrated the quantitative change
Figure 4. Changes of disulfide bonds and free thiol groups of feather keratins in SFE treatment. The data are expressed as the mean ± SD (n = 3). 2748
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significantly (83.7%). When the pressure rose higher than 1.4 MPa, β-sheet and disulfide bond contents decreased gradually. Hence, there was a synergistic effect between hydrogen and disulfide bonds on the stability of feather keratin. Disulfide bonds have the lowest covalent bond energy in proteins, making them the most susceptible for cleavage by thermal effect and mechanical force.35,36 In the present work, a high negative linear correlation coefficient (R2 = 0.98) was found between disulfide bond contents of feather keratin and pepsin digestibility, over the full investigated steam pressure range (Figure 7a). Reduction of disulfide bonds caused
Figure 5. FTIR spectra of (a) feather and samples of the SFE process at (b) 1.0 MPa for 1 min and (c) 2.2 MPa for 1 min. For easier comparison, intensities have been normalized in all spectra. Spectra are offset, and curves are shifted vertically for clarity.
to the component at 1515 cm−1. This means that less hydrogen-bonded peptide groups were contained in the samples resulting from SFE with respect to the original feather, which is in line with the solubility, as shown in Figure 3. Under high temperature and humidity, most of the hydrogen bonds in the feather were broken, as demonstrated by Xu et al.,33 increasing accessibility of the protein bodies to enzymatic attack. Effect of Protein Structure Modification on Pepsin Digestibility. A high cystine content (7%) is the most important property that differentiates keratins from other structural proteins, such as collagen and elastin.34 Feather proteins in their native form are resistant to most proteases when fed to an animal. Thus, destruction of cystines to a certain extent is desirable in production of feather meal. As shown in Figure 6, when steam pressure was below 1.4 MPa, disulfide bonds of feather keratin decreased dramatically and the β-sheet contents changed slightly, with pepsin digestibility increasing
Figure 7. Correlation between pepsin digestibility and (a) disulfide bond content and (b) relative spectral weights of the β-sheet of steamexploded samples.
disruption of the feather keratin structure and, as a consequence, an enhanced accessibility of sites susceptible to proteolysis. A similar study also found that the degree of hydrolysis by trypsin and pancreatin was strongly correlated to the degree of disulfide reduction of soy flour.37 In contrast, Figure 7b showed that, at a lower steam pressure, a linear relationship was observed between the relative spectral weights of the β-sheet structures and pepsin digestibility (R2 = 0.94). As steam pressure increased, the digestibility became independent of the β-sheet contents. The results partly agreed with the findings of Yu et al.,38 who suggested that the difference in the percentage of protein secondary structure might be responsible for different feed protein digestive behaviors. Obveriously, the
Figure 6. Changes of the relative spectral weights of the β-sheet of feather keratins in SFE treatment. 2749
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(9) Gong, L.; Huang, L.; Zhang, Y. Effect of steam explosion treatment on barley bran phenolic compounds and antioxidant capacity. J. Agric. Food Chem. 2012, 60, 7177−7184. (10) Martin-Sampedro, R.; Capanema, E. A.; Hoeger, I.; Villar, J. C.; Rojas, O. J. Lignin changes after steam explosion and laccase-mediator treatment of eucalyptus wood chips. J. Agric. Food Chem. 2011, 59, 8761−8769. (11) Zhang, Y. P.; Yang, R. J.; Zhao, W.; Hua, X.; Zhang, W. B. Application of high density steam flash-explosion in protein extraction of soybean meal. J. Food Eng. 2013, 116, 430−435. (12) Zhao, W.; Yang, R. J.; Zhang, Y. Q.; Wu, L. Sustainable and practical utilization of feather keratin by an innovative physicochemical pretreatment: High density steam flash-explosion. Green Chem. 2012, 14, 3352−3360. (13) Wang, K.; Jiang, J. X.; Xu, F.; Sun, R. C. Influence of steaming pressure on steam explosion pretreatment of Lespedeza stalks (Lespedeza cyrtobotrya). II. Characteristics of degraded lignin. J. Appl. Polym. Sci. 2010, 116, 1617−1625. (14) Yu, Z.; Zhang, B.; Yu, F.; Xu, G.; Song, A. A real explosion: The requirement of steam explosion pretreatment. Bioresour. Technol. 2012, 121, 335−341. (15) Zhang, Y. Z.; Chen, H. Z. Multiscale modeling of biomass pretreatment for optimization of steam explosion conditions. Chem. Eng. Sci. 2012, 75, 177−182. (16) Li, M.; Lee, T. C. Effect of extrusion temperature on solubility and molecular weight distribution of wheat flour proteins. J. Agric. Food Chem. 1996, 44, 763−768. (17) Peterson, G. L. A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal. Biochem. 1977, 83, 346−356. (18) AOAC International. Official Methods of Analysis, 17th ed.; AOAC International: Gaithersburg, MD, 2000. (19) Chan, K.; Wasserman, B. P. Direct colorimetric assay of free thiol groups and disulfide bonds in suspensions of solubilized and particulate cereal proteins. Cereal Chem. 1993, 70, 22−26. (20) Thannhauser, T. W.; Konishi, Y.; Scheraga, H. A. Analysis for disulfide bonds in peptides and proteins. Methods Enzymol. 1987, 143, 115−119. (21) Parsons, C.; Hashimoto, K.; Wedekind, K.; Baker, D. Soybean protein solubility in potassium hydroxide: An in vitro test of in vivo protein quality. J. Anim. Sci. 1991, 69, 2918. (22) Mokrejs, P.; Svoboda, P.; Hrncirik, J.; Janacova, D.; Vasek, V. Processing poultry feathers into keratin hydrolysate through alkalineenzymatic hydrolysis. Waste Manage. Res. 2011, 29, 260−267. (23) Rahayu, S.; Syah, D.; Thenawidjaja Suhartono, M. Degradation of keratin by keratinase and disulfide reductase from Bacillus sp. MTS of Indonesian origin. Biocatal. Agric. Biotechnol. 2012, 1, 152−158. (24) Senoz, E.; Wool, R. P.; McChalicher, C. W. J.; Hong, C. K. Physical and chemical changes in feather keratin during pyrolysis. Polym. Degrad. Stab. 2012, 97, 297−307. (25) Li, M.; Lee, T. C. Effect of extrusion temperature on the solubility and molecular weight of lentil bean flour proteins containing low cysteine residues. J. Agric. Food Chem. 2000, 48, 880−884. (26) Anderson, A.; Ng, P. Changes in disulfide and sulfhydryl contents and electrophoretic patterns of extruded wheat flour proteins. Cereal Chem. 2000, 77, 354−359. (27) Rebello, C.; Schaich, K. Extrusion chemistry of wheat flour proteins: II. Sulfhydryl−disulfide content and protein structural changes. Cereal Chem. 1999, 76, 756−763. (28) Zhang, Y.; Chien, M.; Ho, C. T. Comparison of the volatile compounds obtained from thermal degradation of cysteine and glutathione in water. J. Agric. Food Chem. 1988, 36, 992−996. (29) Bragulla, H. H.; Homberger, D. G. Structure and functions of keratin proteins in simple, stratified, keratinized and cornified epithelia. J. Anat. 2009, 214, 516−559. (30) Jackson, M.; Mantsch, H. H. The use and misuse of FTIR spectroscopy in the determination of protein structure. Crit. Rev. Biochem. Mol. Biol. 1995, 30, 95−120.
application of heat energy or mechanical energy during SFE breaked hydrogen bonds, which stabilized the β-sheet conformation, and consequently, more protein could disolve in the 6 M urea system (Figure 3). We also observed that a random coil structure was detected among the exploded samples (not shown), suggesting a good amino acid availability from the unordered secondary structure. SFE equipment with a 5 m3 chamber has been developed; hence, SFE treatment could be performed on a large scale.14 Because of the structural features of the catapult explosion mode of SFE, the effective gas deflation passage of the mode has the same area as the cylinder cross-section, which ensures that the deflation time will not be prolonged. Therefore, the treatment efficiency in scale-up applications of SFE can remain consistent with the small equipment. This environmentally friendly technology, requiring little or no chemical input, is a promising route for commercial production of feather meal.
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AUTHOR INFORMATION
Corresponding Author
*Telephone/Fax: +86-510-85919150. E-mail: yrj@jiangnan. edu.cn. Funding
The authors gratefully acknowledge the support by the National Natural Science Foundation of China (31271977). Notes
The authors declare no competing financial interest.
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ABBREVIATIONS USED SFE, steam flash explosion; SS, disulfide; SH, sulfhydryl; DTNB, 5,5′-dithiobis(2-nitrobenzoic acid); NTSB, 2-nitro-5thio-sulfobenzoic acid; FTIR, Fourier transform infrared; FSD, Fourier self-deconvolution
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REFERENCES
(1) Ullah, A.; Vasanthan, T.; Bressler, D.; Elias, A. L.; Wu, J. Bioplastics from feather quill. Biomacromolecules 2011, 12, 3826−3832. (2) Poole, A. J.; Church, J. S.; Huson, M. G. Environmentally sustainable fibers from regenerated protein. Biomacromolecules 2009, 10, 1−8. (3) Jin, E.; Reddy, N.; Zhu, Z.; Yang, Y. Graft polymerization of native chicken feathers for thermoplastic applications. J. Agric. Food Chem. 2011, 59, 1729−1738. (4) Onifade, A. A.; Al-Sane, N. A.; Al-Musallam, A. A.; Al-Zarban, S. A review: Potentials for biotechnological applications of keratindegrading microorganisms and their enzymes for nutritional improvement of feathers and other keratins as livestock feed resources. Bioresour. Technol. 1998, 66, 1−11. (5) Fraser, R. D.; Parry, D. A. The structural basis of the filamentmatrix texture in the avian/reptilian group of hard β-keratins. J. Struct. Biol. 2011, 173, 391−405. (6) Daroit, D. J.; Correa, A. P. F.; Brandelli, A. Production of keratinolytic proteases through bioconversion of feather meal by the Amazonian bacterium Bacillus sp. P45. Int. Biodeterior. Biodegrad. 2011, 65, 45−51. (7) Coward-Kelly, G.; Chang, V. S.; Agbogbo, F. K.; Holtzapple, M. T. Lime treatment of keratinous materials for the generation of highly digestible animal feed: 1. Chicken feathers. Bioresour. Technol. 2006, 97, 1337−1343. (8) Martins, V. G.; Costa, J. A. V.; Silveira, S. T.; Brandelli, A.; Prentice, C. Protein and amino acid solubilization using Bacillus cereus, Bacillus velesensis, and Chryseobacterium sp. from chemical extraction protein residue. Food Bioprocess Technol. 2011, 4, 116−123. 2750
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Article
(31) Khurana, R.; Fink, A. L. Do parallel β-helix proteins have a unique Fourier transform infrared spectrum? Biophys. J. 2000, 78, 994−1000. (32) Almutawah, A.; Barker, S. A.; Belton, P. S. Hydration of gluten: A dielectric, calorimetric, and Fourier transform infrared study. Biomacromolecules 2007, 8, 1601−1606. (33) Xu, W. L.; Ke, G. Z.; Wu, J. H.; Wang, X. G. Modification of wool fiber using steam explosion. Eur. Polym. J. 2006, 42, 2168−2173. (34) Kornillowicz-Kowalska, T.; Bohacz, J. Biodegradation of keratin waste: Theory and practical aspects. Waste Manage. 2011, 31, 1689− 1701. (35) Aslaksen, M. A.; Romarheim, O. H.; Storebakken, T.; Skrede, A. Evaluation of content and digestibility of disulfide bonds and free thiols in unextruded and extruded diets containing fish meal and soybean protein sources. Anim. Feed Sci. Technol. 2006, 128, 320−330. (36) Zhu, X.; Jin, Z.; Liu, D. Study on the mechanism of feather keratin extrusion. J. Chin. Cereals Oils Assoc. 1998, 13, 16−19. (37) Faris, R. J.; Wang, H.; Wang, T. Improving digestibility of soy flour by reducing disulfide bonds with thioredoxin. J. Agric. Food Chem. 2008, 56, 7146−7150. (38) Yu, P. Q.; McKinnon, J. J.; Christensen, C. R.; Christensen, D. A. Using synchrotron-based FTIR microspectroscopy to reveal chemical features of feather protein secondary structure: Comparison with other feed protein sources. J. Agric. Food Chem. 2004, 52, 7353− 7361.
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