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Improvement of the Nutritional Quality of Cottonseed Meal by Bacillus subtilis and the Addition of Papain.

Byline: HONG SUN, JIANG-WU TANG, XIAO-HONG YAO, YI-FEI WU, XIN WANG AND JIE FENG

ABSTRACT

To improve the nutritional quality of the cottonseed meal (CSM), it was fermented by Bacillus subtilis (FCSMB) or by B. subtilis and the addition of papain (FCSMB+A). After 48 h of fermentation, both FCSMB and FCSMB+A increased (p less than 0.05) the contents of crude protein and crude ash; whereas the contents of crude fat, crude fiber and free gossypol were sharply decreased (p less than 0.05) compared with CSM. FCSMB and FCSMB+A also raised (p less than 0.05) contents of essential and total amino acids. Moreover, both fermented products increased (p less than 0.05) the degree of hydrolysis of cottonseed protein and soluble protein content, especially in FCSMB+A. The distribution of soluble protein showed that FCSMB+A improved (p less than 0.05) the amount of small-size protein fractions ( less than 20 kDa), while decreasing (p less than 0.05) medium-size (20-50 kDa) and large-size fractions ( greater than 50 kDa) compared with FCSMB or CSM.

Additionally, 2, 2-diphenyl-1-picrylhydrazyl (DPPH) radical scavenging activity and in vitro protein digestibility were improved (p less than 0.05) in the FCSMB and FCSMB+A as compared to CSM. Collectively, CSM fermented by B. subtilis, especially with the addition of papain could substantially improve its nutritional value to some extent. (c) 2012 Friends Science Publishers

Key Words: Antioxidant activity; Bacillus subtilis; Cottonseed meal; In vitro digestibility; Papain; Solid-state fermentation

INTRODUCTION

Shortage of protein sources of good quality is a major concern in many developing countries due to the prohibitive cost of animal protein sources. Proteins of plants are alternative sources that are more economical to use (Ei-Sayed et al., 1999). Cottonseed meal (CSM), a byproduct of extracting the oil from cotton seeds, is recognized as a good protein source in China because of its high protein content (220-560 g kg-1) and wide availability (Nagalakshmi et al., 2007). However, the use of CSM in animal feeds is limited due to the detrimental effects of low lysine levels and free gossypol, which is a toxic substance. Free gossypol is associated with depressed growth performance and increased mortality in broilers (Henry et al., 2001). Study has shown that free gossypol could bind with amino acids in CSM, mainly lysine, to form non-digestible substances, further reducing the nutritional value of cottonseed protein (Watkins et al., 1993).

Therefore, methods need to be developed to reduce the harmful properties of CSM.

Solid-state fermentation is one of the most promising techniques to reduce free gossypol of CSM (Weng and Sun, 2006; Zhang et al., 2006; 2007). Bacillus subtilis is an important starter culture used in many solid-state fermentation processes (Kiers et al., 2000; Shafique et al., 2004; Zhu et al., 2008). It is easy to introduce in dry feed due to the production of spores and is generally recognized as safe recommended by the U.S. Food and Drug Administration (Kramer and Gilbert, 1989). A significant decrease in free gossypol levels after Bacillus fermentation has been demonstrated in our previous study (Tang et al., 2012).

High nutrient availability of soybean meal could also be observed by degradation of proteins during B. subtilis fermentation (Omafuvbe et al., 2002; Hong et al., 2004; Feng et al., 2007). But data on protein degradation in fermented CSM is scarce to date.

On the other hand, enzymatic hydrolysis has been widely used to enhance functional and biological properties of plant-based food and feed proteins through breakage of intact proteins (Moure et al., 2006; Chabanon et al., 2007). Moreover, proteolysis process could increase peptide contents in protein hydrolysates that are absorbed more rapidly from the intestine than free amino acids (Webb, 1990). Thus, we hypothesize that the inclusion of inoculants and proteinase together may further improve the quality of CSM as reported in similar feed ingredients (Lee et al., 2008; Xu et al., 2011).

In precious studies, papain was identified an excellent cottonseed-protein degrading enzyme (Gao et al., 2010). Therefore, the present study fermented CSM using B. subtilis alone (FCSMB) or with both incoculants and the addition of papain (FCSMB+A), to develop CSM into a high quality protein source with functional benefits and extend the use of CSM.

MATERIALS AND METHODS

Microorganism and enzyme: B. subtilis BJ-1 was first isolated from the garden soil for free gossypol degradation study and stored in China General Microbiological Culture Collection, Beijing, China (Tang et al., 2012). The culture was maintained on potato dextrose agar (PDA) slopes (CM0139, Oxoid, Beijing, China) at 4degC. Before use in an experiment, culture of B. subtilis BJ-1 was prepared by transferring a loop of bacteria from the PDA slant into a 250 mL flask containing 50 mL of nutrient broth (BD234000, Difco, Detroit, USA) and incubated at 37degC, 160 r min-1 for 18 h. The culture was diluted in sterile distilled water with 1 g L-1 peptone (LP0037, Oxoid, Beijing, China) to about 108 colony forming units mL-1. The suspension served as the inoculum for CSM fermentation.

Papain (from papaya latex, activity of 0.5-2.0 units per mg protein) was purchased from Sigma (Shanghai, China). Papain is active at acid to neutral pH and cleaves peptide bonds with alkaline amino acids and leucine, glycine. CSM contains more than 15% of these amino acids, which could be effectively hydrolysed by papain (NRC, 1994).

Fermentation of CSM with papain treatment: The CSM was purchased from Tycoon Group Co., Ltd (Xinjiang, China). CSM (100 g) was transferred into 500 mL flasks at a moisture concentration of 60% (w/w) and then inoculated with 2 mL of diluted culture of B. subtilis BJ-1. The enzyme preparations (filtration with 0.22 mm filters, Millipore, Beijing, China) were added to reach a rate of 1.0 g kg-1 of CSM with no adjustment of pH (Ghazi et al., 2010). The homogenates were incubated in a bed-packed incubator at 30degC for 48 h. After fermentation, fresh samples were dried at 50degC in a hot-air oven to about 900 g kg-1 dry matter. The dried samples were subsequently milled fitted with 1-mm mesh screen and stored in plastic bags at -20degC for chemical analysis and protein extraction. Triplicate flasks were used for each experimental variation.

Chemical analysis: Dry matter content of samples was determined by drying at 105degC for 5 h; ash content was measured by incineration at 550degC for 8 h. Contents of crude protein, crude fat crude fiber were determined according to the AOCS (2009) methods. Amino acid assay was based on the AOAC (1999) methods. Free gossypol content was determined according to AOCS (2009) based on high performance liquid chromatography technique. The degree of hydrolysis of the cottonseed protein was measured by the method of Teng et al. (2012).

Protein extraction: The soluble cottonseed proteins in CSM, FCSMB and FCSMB+A were extracted according to Chen et al. (2010) with minor modifications. For short, 500 mg samples were mixed thoroughly with 1 mL of extraction solution (50 mM phosphate buffered saline, 100 mM NaCl, pH 8.0) and vortexed for 10 min. The homogenate was centrifuged at 10,000xg for 15 min and the supernatant was collected for electrophoresis.

Electrophoresis: Tricine-sodium dodecyl sulphaye-polyacrylamide gel electrophoresis (Trincine-SDS-PAGE) was performed as previously described (Schagger, 2006) using a 5% stacking gel and 16% separating gel. The soluble cottonseed protein was denatured with sampling buffer (50 mM Tris-HCl, 25% (w/v) glycerol, 2% (w/v) SDS and 0.1% (w/v) bromophenol blue) and boiled for 5 min. Protein bands were stained in a Coomassie brilliant blue G-250 solution for 2 h then discolored with acetic acid (methanol: acetic acid: water, 4:0.8:5.2, v/v/v) over night. The protein markers were purchased from FermentasTM (SM1881, Shenzhen, China).

Free radical-scavenging assay: The antioxidant activity of the protein extracts was determined as hydrogen-donating or radical-scavenging ability by the 2, 2-diphenyl-1-picrylhydrazyl (DPPH) method according to Shyu and Hwang (2002). Briefly, 1 mL of protein extracts at a concentration of 10 mg mL-1 was added to 2 mL of 100 mM methanolic solution of DPPH (Sigma). After immediately shaken, the mixture was kept at room temperature in dark. The decrease in absorbance at 517 nm was measured at 10 min interval until a plateau was detected. The inhibitory percentage of DPPH was calculated according to the following equation: Scavenging effect (%) = (Acontrol - (Asample - Ablank))/Acontrol x 100, where Acontrol was the absorbance of DPPH without samples, Asample was the absorbance of samples mixed with DPPH, and Ablank was the absorbance of sample without DPPH addition.

Determination of in vitro protein digestibility: The procedure of the in vitro protein digestibility was according to the method of Chen et al. (2010). Ten gram of sample was put in a 250 mL flask with 50 mL pepsin-HCl solution (200 mg of pepsin (250 units mg-1, sigma, Beijing, China) and 0.01 M HCl) and incubated at 39degC for 4 h. After adjusted pH to 7.0 by Na2CO3 (50 mg mL-1), 30 mL of artificial pancreatin solution was added and re-incubated at 39degC for 4 h. Digestion was stopped by adding 10 mL of 5% trichloroaceric acid (TCA) into the flask and the digesta solution was centrifuged at 1,000xg for 15 min. The TCA-insoluble residue was oven dried and the crude protein content was analyzed. In vitro digestibility (%) = (content of crude protein of sample - content of crude protein of TCA-insoluble residue)/content of crude protein of samplex100.

Statistical analysis: Each determination was performed on three separate samples and analyzed in triplicate and results were then averaged. Data were assessed by the analysis of variance (ANOVA), and significant difference between the treatments was determined with Duncan's multiple range test procedure (SAS, 1999). A significance level of 0.05 was used.

RESULTS AND DISCUSSION

Chemical parameters of treated and untreated CSM: FCSMB and FCSMB+A changed the chemical characteristics of CSM (Table I). Contents of crude protein and crude ash increased (p less than 0.05) after fermentation. This may be partly due to the use of carbon sources in CSM during the fermentation process, leading to the concentration of other nutrients (Weng and Sun, 2006; Zhang et al., 2007; Khalaf and Meleigy, 2008). The increase in Bacillus counts (data not shown) may also account for the elevated level of crude protein, for it constitutes about 63% protein of its biomass (Terlabie et al., 2006). The contents of crude fiber and crude fat of FCSMB and FCSMB+A were decreased (p less than 0.05) compared with CSM. Similarly, Tang et al. (2012) demonstrated decreased (p less than 0.05) contents of these nutrients in fermented CSM. The reduction may be attributed to the production of lipase (Terlabie et al., 2006) and cellulose (Amartey et al., 1999) by Bacillus strains.

The free gossypol contents in FCSMB and FCSMB+A were reduced (p less than 0.05) by 61.9% and 54.7%, respectively (Table I). In accordance with our results, free gossypol content was decreased during solid-state fermentation by fungi (Weng and Sun, 2006; Zhang et al., 2006). More importantly, free gossypol contents of FCSMB and FCSMB+A are lower than the levels (400 mg kg-1) which can adversely affect broiler performance (Henry et al., 2001).

The decrease in free gossypol likely is the result of the binding of proteins, and/or degrading enzymes secreted by microbes (Zhang et al., 2007). However, detoxification of

Table I: Nutrient composition and free gossypol content of cottonseed meals fermented with Bacillus subtilis (FCSMB) or with B. subtilis and papain (FCSMB+A)

Items###Unfermented###FCSMB###FCSMB+A###SEM###p

Dry matter (g kg-1)###903.9###922.0###899.3###5.90###0.273

Crude fat (g kg-1)###14.9a###11.3b###10.8b###0.71###less than 0.001

Crude protein (g kg-1)###468.6b###525.9a###513.4a###9.01###less than 0.001

Crude fiber (g kg-1)###101.2a###93.3b###92.7b###1.54###0.003

Crude ash (g kg-1)###54.9b###61.9a###61.7a###1.22###less than 0.001

Free gossypol (mg kg-1) 745.67a###284.00b###337.66b###74.93###less than 0.001

Free gossypol (mg kg-1) 745.67a 284.00b 337.66b 74.93 less than 0.001

Note: SEM = standard error of the mean; Means obtained from triplication (n=3) not sharing a common superscript in a same row are significantly different at p less than 0.05

Table II: Amino acids (AA) profile of cottonseed meals fermented with Bacillus subtilis (FCSMB) or with B. subtilis and papain (FCSMB+A) (g kg-1 dry basis)

Amino acids###Unfermented###FCSMB###FCSMB+A###SEM###p

Lysine###20.93b###22.82a###22.57a###0.33###0.029

Methionine###4.90###5.20###5.01###0.14###0.586

Threonine###15.51b###17.74a###17.55a###0.41###0.003

Arginine###51.64b###56.02a###58.68a###1.32###0.070

Leucine###28.94c###34.26a###31.88b###1.81###less than 0.001

Isoleucine###17.13###19.11###18.20###0.50###0.054

Valine###22.26###22.71###22.93###0.31###0.670

Histidine###16.99c###20.33a###18.79b###0.53###0.001

Phenylalanine###27.72c###33.05a###30.71b###0.80###less than 0.001

Serine###22.54b###26.01a###25.11a###0.63###less than 0.001

Proline###20.71###22.89###21.04###0.55###0.149

Glycine###20.85c###23.82a###22.63b###0.50###less than 0.001

Alanine###20.52b###23.11a###22.84a###0.43###0.011

Tyrosine###11.61b###14.28a###13.23a###0.43###0.008

Aspartic acid###44.20b###51.14a###48.90a###2.12###0.001

Glutamic acid###111.41b###126.92a###123.77a###2.65###0.007

Essential AA###206.02b###231.24a###226.32a###3.61###0.012

Total AA###457.86b###519.41a###503.84a###13.22###less than 0.001

Note: SEM = standard error of the mean; Means obtained from triplication (n=3) not sharing a common superscript in a same row are significantly different at p less than 0.05; Essential AA: Lys, Met, Thr, Arg, Leu, Iso, Val, His and Phe

Table III: Hydrolysis degree, soluble protein content and protein distribution by size in cottonseed meals fermented with Bacillus subtilis (FCSMB) or with B. subtilis and papain (FCSMB+A)

###Unfermented###FCSMB###FCSMB+A###SEM###p

Hydrolysis degree (%)###0c###5.81b###20.12a###2.99###less than 0.001

Soluble protein (g kg-1)###177.15c###254.83b###390.45a###31.11###less than 0.001

Molecular weight range (%)

greater than 50 kDa###35.6a###33.0a###19.7b###2.52###less than 0.001

20 kDa to 50 kDa###36.6a###36.4a###32.5b###0.71###0.001

less than 20 kDa###27.8b###30.6b###47.8a###3.20###less than 0.001

Note: SEM = standard error of the mean; Means obtained from triplication (n=3) not sharing a common superscript in a same row are significantly different at p less than 0.05

free gossypol is less than those observed by Weng and Sun (2006) and Zhang et al. (2006), which probably due to the differences between strains.

The nutritional value of a protein is highly correlated with its amino acid composition, especially essential amino acids required in the diet of animals. The total amino acid content of both FCSMB and FCSMB+A was increased (p less than 0.05) by 13.4% and 10.0%, respectively (Table II). This is in agreement with the increase of crude protein content after fermentation. Moreover, both FCSMB and FCSMB+A improved (p less than 0.05) the contents of some essential amino acids, including lysine, threonine, leucine, arginine, histidine and phenylalanine. The content of non-essential amino acid was also increased (p less than 0.05) after fermentation, except proline. Thus, FCSMB and FCSMB+A potentially improve the nutritional value of CSM from the point view of amino acids. This is partly agrees with Zhang et al. (2007) and Khalaf and Meleigy, (2008), who reported a significant increase in total and essential amino acids of CSM fermented with Candida tropicalis.

The increase in amino acid levels may be ascribed to certain microbial metabolism that occurs during fermentation. Interestingly, FCSMB+A decreased (p less than 0.05) the levels of leucine, histidine, phenylalanine and glycine, compared with FCSMB. Since papain breaks the bonds in proteins rather than affect the total amount of amino acids, the significant drop of amino acids in FCSMB+A may be attributed to the excessive utilization of some amino acids by B. subtilis.

Degradation of protein: To access the effects of FCSMB and FCSMB+A on protein degradation of CSM, protein solubility and degree of hydrolysis were determined. Bacillus ferments showed higher (p less than 0.05) protein solubility and hydrolysis degree, especially in FCSMB+A, compared with the CSM (Table III). Degree of hydrolysis is one of the determinant parameter for monitoring the protein hydrolysis. The use of protease (papain) as additives is expected to degrade cottonseed protein, contributing to the increase of hydrolysis degree. The increase of protein solubility could result from the breakdown of protein into water-soluble molecules (Chabanon et al., 2007). Interestingly, FCSMB sharply increased the degree of hydrolysis and the soluble protein content, compared with CSM.

Teng et al. (2012) repoarted similar result in soybean meal fermented with B. subtilis. These observations suggest that proteolytic activity has been involved in the fermentation with B. subtilis (Omafuvbe et al., 2002; Terlabie et al., 2006).

However, the proteolysis during fermentation in the current study is much less than those reported in other studies (Phromraksa et al., 2009; Teng et al., 2012). The lack of agreement may be attributed to differences between strains and substrates (soybean meal and CSM, respectively).

The subunit profile of cottonseed protein in FCSMB and FCSMB+A was assayed by Tricinie-SDS-PAGE (Fig. 1). The unfermented CSM exhibited major protein subunits, including globulin 9S (55 kDa and 49 kDa), globlin 5S (24 kDa and 22 kDa) and albumin 2S (20 kDa, 15 kDa and 14 kDa), which are in agreement with those of previously reported (Sadeghi and Shawrang, 2007). The subunits of globulin 9S degraded to some extent, after fermentation with B. subtilis. More or less complete breakdown of all two subunits (9S and 5S) to low-molecular weight fractions was observed in FCSMB+A. These observations are consistent with the protein solubility and the degree of hydrolysis, reflecting the proteolytic activity of B. subtilis (Kiers et al., 2000; Zhu et al., 2008) and papain. The ratio of each band was determined by densitometric analysis with the sizes of peptides grouped as large ( greater than 55 kDa), medium (20-55 kDa) and small ( less than 20 kDa) (Table III).

The ratio of small-size fraction increased by 10.1% (p greater than 0.05) and 71.9% (p less than 0.05) in FCSMB and FCSMB+A, respectively. The large-size protein fraction was decreased by 7.3% in FCSMB and 44.7% in FCSMB+A, respectively. The increased amount of small-size proteins is most likely due to the digestion of large-size proteins in CSM. However, the distribution profile of cottonseed protein has not been significantly affected in FCSMB, which is in conflict with results obtained in fermented soybean meals (Feng et al., 2007; Zhu et al., 2008). The differences in substrates (CSM versus soybean meal) and bacteria probably account for the discrepancy, suggesting that B. subtilis BJ-1 could not degrade some protein subunits in cottonseed protein. On the other hand, Ghazi et al. (2010) demonstrated that protease improved the digestion of soybean meal though the improvement of nitrogen usage before to the terminal of the small intestine of broilers.

Feng et al. (2007) indicated that degradation of soybean protein could improve the digestive function of piglets. Therefore, the increase in small-molecule proteins of FCSMB+A may improve the digestibility of cottonseed protein. The result also suggests that papain could be use as a suitable enzyme in the fermentation of CSM, which sheds new lights on the strategy for improving the nutritional value of plant-source proteins.

In vitro protein digestibility and free radical-scavenging activity: In vitro digestibility of fermented samples was increased (p less than 0.05), compared with CSM (Fig. 2). Similar improvement was observed in fermented CSM with fungi (Zhang et al., 2007). The increase in protein digestibility can be a result of the partial degradation of storage protein into more simple and soluble molecules by enzymatic reactions during the fermentation (Sadeghi and Shawrang, 2007; Zhang et al., 2007). However, it would translate to added nutritional value only if it gives rise to better performance in animal feeding trials, which needs to be further investigated.

DPPH is a stable free radical which is used as a substrate to evaluate the in vitro antioxidant activities. The scavenging effect increased with the incubation time up to 60 min (Fig. 3). Protein extracts from both FCSMB and FCSMB+A showed radical-scavenging activity superior (p less than 0.05) to the CSM during the whole reaction period, with the peak level reached by papain supplement. Similarly, antioxidant activity has been significantly increased in fermented soybean products (Zhu et al., 2008; Teng et al., 2012). The increased degradation of cottonseed protein can contribute to the increment of antioxidant activity in FCSMB and FCSMB+A (Zhu et al., 2008; Gao et al., 2010). This may explain why FCSMB+A depicted a higher antioxidant activity than FCSMB. The improvement of antioxidant activity may be also associated with the increase of amino acids including histidine, alanine, leucine, which play important roles in scavenging free radicals (Kim et al., 2001).

Other factors cannot be ruled out including the hydrogen-donating ability of microorganisms and other antioxidant components (phenolic compounds, polysaccharides and vitamin) (Yang et al., 2000). Since high antioxidant activity is beneficial for inhibiting the oxidation of nutrients in feedstuffs, the fermented CSM may be used as a functional feed ingredient.

CONCLUSION

Fermentation processes with B. subtilis BJ-1 could increase the nutritional value, degrade the cottonseed protein which is beneficial for protein utilization and enhance the antioxidant activity of CSM, especially with the supplement of papain. Fermentation with papain may offer a novel strategy to improve the value of CSM.

Acknowledgement: This study was financially supported by the Key Science Project Award of Zhejiang Province Science and Technology Committee (2011C12010) of the P. R. China. The work was also supported by the New-Century Training Program Foundation for Talents from the Ministry of Education of China (Grant No. NCET-10-0727 ), and the Natural Science Foundation for Distinguished Young Scholars of of Zhejiang pvovince, China(Grant No. R3110085).

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College of Animal Sciences, Zhejiang University, Hangzhou, 310058, PR China, +Institute of Plant Protection and Microbiology, Zhejiang Academy of Agriculture Sciences, Hangzhou, 310021, PR China, 1Corresponding author's e-mails: fengj@zju.edu.cn; gearyou@gmail.com, To cite this paper: Sun, H., J.W. Tang, X.H. Yao, Y.F. Wu, X. Wang and J. Feng, 2012. Improvement of the nutritional quality of cottonseed meal by Bacillus subtilis and the addition of papain. Int. J. Agric. Biol., 14: 563-568
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Author:Hong Sun; Jiang-Wu Tang; Xiao-Hong Yao; Yi-Fei Wu; Xin Wang; Jie Feng
Publication:International Journal of Agriculture and Biology
Article Type:Report
Geographic Code:9CHIN
Date:Aug 31, 2012
Words:4868
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