Indian Journal of Animal Research

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Indian Journal of Animal Research, volume 57 issue 7 (july 2023) : 868-874

Solid-state Fermentation of Cottonseed Meal with Saccharomyces cerevisiae for Gossypol Reduction and Nutrient Enrichment

Padala Dharmakar1,4, S. Aanand1,*, Stephen Sampath Kumar2, Muralidhar P. Ande3, P. Padmavathy4, Jaculine Periera4, Ch. Balakrishna5
1Erode Bhavanisagar Centre for Aquaculture (EBCeSA), Tamil Nadu Dr. J. Jayalalithaa Fisheries University, Bhavanisagar-638 451, Tamil Nadu, India.
2Directorate of Sustainable Aquaculture, Tamil Nadu Dr. J. Jayalalithaa Fisheries University, Nagapattinam-611 002, Tamil Nadu, India.
3ICAR-Central Institute of Fisheries Education (CIFE), Kakinada Regional Centre, Kakinada-533 007, Andhra Pradesh, India.
4Fisheries College and Research Institute, Tamil Nadu Dr. J. Jayalalithaa Fisheries University, Thoothukudi-638 008, Tamil Nadu, India.
5ICAR-Krishi Vigyan Kendra, Acharya N.G Ranga Agricultural University, Amadalavalasa-532 185, Andhra Pradesh, India.
Cite article:- Dharmakar Padala, Aanand S., Kumar Sampath Stephen, Ande P. Muralidhar, Padmavathy P., Periera Jaculine, Balakrishna Ch. (2023). Solid-state Fermentation of Cottonseed Meal with Saccharomyces cerevisiae for Gossypol Reduction and Nutrient Enrichment . Indian Journal of Animal Research. 57(7): 868-874. doi: 10.18805/IJAR.B-5080.
Background: An experiment was conducted to study the effect of solid-state fermentation (SSF) of cottonseed meal (CSM) with Saccharomyces cerevisiae on anti-nutritional factors and amino acid profile. 

Methods: A finely ground CSM was fermented with baker’s yeast for 48 h at room temperature with periodic observations of pH, temperature and moisture. The fermented substrate was partially sun-dried and nutritional values were observed.

Result: After the SSF process on dry basses, the protein content of CSM increased from 8.74% to 12.67%. Besides increasing the nutritional value, the SSF showed a clear significant effect in reducing the anti-nutritional factors content of raw CSM like total gossypol from 0.28% to 0.21%, phytic acid from 3.3% to 0.3% and total tannin from 1.42% to 0.68%. CSM fermented with S. cerevisiae improved concertations of essential amino acids viz., histidine, isoleucine, valine, methionine and phenylalanine. The protein quality evaluation showed a significant increase in its nutritional value. Based on the present result, it can be concluded that the fermentation of CSM with S. cerevisiae decreases the anti-nutritional factors and improves essential nutrients.
Growing demand and cost and reduced availability of quality fishmeal in the required quantity have emphasised in search for alternative protein sources in the diets of fish and farmed animals (Fournier et al., 2004; Ramachandran and Ray, 2007). Therefore, research is directed towards finding quality alternative protein sources that are ideally less expensive and readily available natural resources (Currie, 2000). Such research work has been intensified in the last decade to determining the efficiency of alternative ingredients in terms of growth and production with better feed supply (Adeniji, 2007). In the current scenario, using non-conventional feed ingredients has been reported with good growth and economic benefits. Various by-products from agro-industries are gaining interest to use as feed ingredients in feed formulations since these by-products possess significant amounts of bioactive compounds. These processed end products are considered promising source of protein and energy for formulating economic and environment-friendly fish diets (Herrero et al., 2013).

Among the plant protein sources, oil seed cakes/meals are predominant choices for feed formulations. After oil extraction from the seeds, the leftover meals form the best by-products. Oil cakes are available in two forms, such as edible and non-edible (Sarker et al., 2015) and are the primary source of protein in animal feeds (Elzubeir et al., 1990; Mohmmed et al., 1995). The high content of protein in the oil cake meal offers an array of rich essential amino acids (Smith et al., 1959; Patel et al., 1970). These industrial by-products are used extensively in fish, livestock and poultry feed to provide protein worldwide (Ensminges, 1980; Tekeli, 2014; Zhao et al., 2016). These plant-based agro-industrial waste have limited use as feed ingredients owing to their high fibre content and presence of anti-nutritional factors (ANFs). These anti-nutritional factors negate the growth and other physiological responses of the organism during high rate of inclusion. Further, these are also deficient in certain essential amino acids like lysine and methionine (Eyo, 2003), have lower biological values, high indigestibility rate and experience loss of quality during storage (Lji et al., 2017).

Cotton is the backbone of the textile industry, supporting 70% of the country’s total fibre production. The cotton plant contributes to more food for humans and feed for animals than as a fibre source (Dinesh et al., 2003). Among all the plant protein sources, cottonseed a by-product of the textile industry, provides a significant quantity of edible oil and protein-rich meal for livestock (Munro, 1987). Cottonseed meal (CSM) is a by-product generated from decortications of the seed after oil extraction, (Paiano et al., 2006). CSM is the second-largest protein source used in animal feed (Smith, 1972) due to its relatively higher content of protein and balanced amino acid profile. CSM is nutritionally valuable feed that contains 51.20% crude protein, 7.02% crude fiber, 1.6% ether extract, 9.3% ash and 2.71 ME (kcal/kg) Obioha, (1992).

CSM can fill the scarcity of conventional feed ingredients for fed aquaculture systems. However, the utilisation of these plant proteins in fish diets is limited due to their low levels of digestible protein and anti-nutritional factors, which interfere with nutrient bio-availability and utilisation in unprocessed form (Abowei and Ekubo, 2011; Kumar et al., 2021). CSM contains anti-nutritional factors viz., gossypol (Withers and Carruth, 1915), phytic acid and tannin (Tacon, 1990), leading to limitations of its use as a feed ingredient. Gossypol is available in either bound gossypol (BG) or free gossypol (FG) form, the bound form being non-toxic and of little significance, since it is unavailable and passes through the gastrointestinal tract unabsorbed (Tanksley, 1990). FG binds with protein (amino group of lysine) and hinders its availability to animals (Mahmood et al., 2011). FG of CSM has anti-nutritional properties (Romano and Scheffler, 2008); it affects growth (Wan et al., 2018) and causes infertility in fish (Liu et al., 2020). Therefore, lowering the effect of gossypol from CSM is necessary to improve the quality of protein for the fish.

Solid-state fermentation (SSF) of agro-industrial residues has become a suitable pre-treatment that could allow their use as biologically active secondary metabolites, especially as animal feed (Singhania et al., 2009). SSF is defined as the fermentation involving solids in the absence (or near absence) of free water; however, the substrate must hold enough moisture to maintain the microorganism’s growth and metabolism. (Pandey et al., 1995 and 2000). In recent years SSF has gained importance due to its simple design, reduced energy requirements and minimum wastewater discharge (Manzanares et al., 2012; Andreaus et al., 2016; Meghavarnam and Janakiraman, 2017). Microbial degradation of the residues improves the substrate value as animal feed (Pandey, 2003) by increasing the probiotics content in the feed (Dawood and Koshio, 2020). SSF of agro-industrial by-products and plant ingredients reduces these products’ crude fibre content and increases the nutrients’ bio-availability (Onyimba et al., 2015; Meshram et al., 2018). The present work was conducted to study the utilisation of the CSM as an alternative feed ingredient by SSF to reduce the effect of the anti-nutritional factor gossypol and nutrient enrichment with S. cerevisiae.
Cottonseed meal
 
Commercial cottonseed meal (CSM) was finely ground in a pulveriser and sieved to get a uniform particle size for solid-state fermentation.
 
Inoculum preparation
 
Commercial baker’s yeast (Saccharomyces cerevisiae) was used to ferment CSM. The baker’s yeast was activated on potato dextrose agar (PDA, Himedia) and the culture was maintained at 4oC. Spores from six-day-old cultures were grown at room temperature (28oC) to use as inoculum for SSF of CSM (Costa et al., 1998).
 
Solid-state fermentation (SSF)
 
SSF was conducted in a customised tray fermenter (Viesturs et al., 1987) with 2 kg dried (moisture<10%) and powdered cotton seed meal. 20 ml of water was sprayed at each tray to adjust the final moisture content of the fermentation mixture by about 50%. The mixed substrate was then sterilised in an autoclave at 121oC for 15 min. Trays were inoculated with 60 mg of S. cerevisiae and thoroughly mixed using a sterile glass rod. The mixture was allowed to ferment for 48 h at room temperature. The variations in pH, temperature and moisture monitored the fermentation process. The standardisation of the SSF of CSM was carried out until complete fermentation was achieved. After fermentation, the fermented substrate was partially sun-dried for 12 h to obtain a homogenous material (Hassaan et al., 2015). The dried substrate was ground and kept in the refrigerator.
 
Evaluation of anti-nutritional components
 
Gossypol             
 
Before and after fermentation, the anti-nutritional factors of free and bond gossypol in the CSM were analysed at Central Institute for Research on Cotton Technology (ICAR), Matunga, Mumbai, India.
 
Phytic acid
 
The phytic acid content of CSM was estimated by using the spectrophotometric procedure (Gao et al., 2007). The assay comprises of addition of 10 ml, 3.5% HCl to 0.5 g sample followed by shaking for one h at 200 rpm (ORBITEK shaker; Scigenics, India). Then this sample extract was centrifuged (Heraeus Megafuge 8R, Thermo Fisher Scientific, USA) at 1600 g for 10 min and the supernatant was collected and mixed with 1 ml, wade reagent (0.03% FeCl3.6H2O + 0.3% sulphosalicylic acid) and centrifuged at 1600 g for 10 min. The absorbance of the collected supernatant was recorded at 500 nm using a UV-visible spectrophotometer (Thermo Scientific, USA) and a blank with each sample was run.
 
Total tannin
 
The concentration of tannin in the CSM and FCSM was determined by following by Folin-Denis method (Schanderi, 1970). The crude extract (0.2 ml) was diluted with 8.3 ml of distilled water and then mixed with 0.5 ml of Folin-Denis reagent. The reaction mixture was alkalinised by adding 1 ml of 15% (w/v) sodium carbonate solution and kept in the dark for 30 min at room temperature. The absorbance of the solution was read at 700 nm using a spectrophotometer (Shimadzu UV-1800) and the concentration of tannin in the extracts was determined using pure tannic acid (MERCK, India) as standard.
 
Amino acid profile analysis
 
The amino acid profile was carried out using 5 g dry powder of CSM and FSFM of feed with HPLC, LACHROM L-7000 ATOZ Pharmaceuticals PVT.LTD., Chennai, Tamil Nadu. The amino acid profile was done with the Chrom NAV software system from JASCO-HPLC analysis.
 
Statistical analysis
 
Statistical Package for Social Sciences (SPSS) version 25.0 (IBM Corp.) was used to test the differences between various treatments by one-way analysis of variance (ANOVA). Duncan’s multiple range test (p<0.05) was used to find the significant difference between treatments.
Effect of fermentation on anti-nutritional factors present in CSM
 
Cottonseed meal utilisation in mono-gastric animals is generally limited. In the present study, fermentation of CSM with commercial baker’s yeast (S. cerevisiae) has resulted in a significant decrease in the anti-nutritional factors (p<0.05) shown in Table 1. The results showed that the gossypol (%) content in CSM was reduced from 0.28% to 0.21% by SSF. Feeding diets containing gossypol causes adverse effects, such as growth depression and intestinal and other internal organ abnormalities in feed animals (Berardi and Goldblatt, 1980). Further, the gossypol in the pigment glands of the cottonseed is released during the mechanical process. It reacts with the amino groups of lysine, rendering its non-availability to the fish (Jackson et al., 1982). Tang et al., (2012) reported the fermentation of CSM with Bacillus subtilis BJ-1 had reduced the gossypol content from 0.82 to 0.21 g/kg. A similar finding showed decreased gossypol level from 90 to 30 mg/kg when fermented with Candida utilis (Xiong et al., 2016). Microbes or microbial enzymes growing during SSF utilise or bind the undesirable anti-nutrients like gossypol, reducing their availability in the free form. The optimum temperature and incubation period of CSM by yeast during fermentation are responsible for the biodegradation of gossypol in CSM. Similar observations at 30oC and 24 to 48 h fermentation have shown the detoxification of gossypol in CSM (Zhang et al., 2007; Khalaf et al., 2008; Zhang et al., 2022).

Table 1: Effect of solid-state fermentation of CSM and thier anti-nutritional factors.



Oilseeds contain 3-6% phytic acid (Graf, 1983). They exhibit their anti-nutritional property by binding phosphorous and other essential nutrients, thereby decreasing their availability in feed for most monogastric animals, including fish (Canibe et al., 1999). In the present study, fermentation of CSM with S. cerevisiae resulted in a significant decrease (p<0.05) in the phytate activity (Table 1). The phytic acid content was reported as 2.55 and 1.05 mg/kg in CSM and FCSM, respectively and a 58.8% reduction was observed. Apparently, SSF of CSM by S. cerevisiae could reduce the phytic acid. The decrease in phytic acid was mediated through phytate degrading yeast phytase, preventing the formation of protein-phytate complexes during the SSF process, making nutrients and minerals bio-available (Hirabayashi et al., 1998). In corroboration to our finding, S. cerevisiae fermentation effectively removed phytic acid in Mutuo plant tubers (Icacina mannii), a West African tropical plant (Antai and Nkwelang, 1998). S. cerevisiae also decreased phytic acid in de-oiled soybean meal after SSF (Hassaan et al., 2015). Similar reports revealed that fermentation of black gram seed meal with Bacillus sp. (Ramachandran and Ray, 2007), rice bran with S. cerevisiae reduced its phytic acid content (Geetha et al., 2015) and gossypol reduction of CSM with Bacillus coagulans (Zhang et al., 2022).

Tannins, like gossypol, are a diverse polyphenolic compound associated with toxic and anti-nutritional effects, including reduced feed intake and growth and impaired nutrient absorption (Butler et al., 1986). Several researchers reported the toxicity of tannin and interference with the digestive enzymes in fish (Krogdahl, 1989; Mukhopadhyay and Ray, 1999) and higher animals (Reddy and Pierson, 1994). Tannins have been found to interfere with digestion by displaying anti-trypsin and anti-amylase activity (Helsper et al., 1993). Tannin also inhibits the protein and dry matter digestibility by impending the protease and forming indigestible complexes that might lead to growth retardation (Krogdahl, 1989; Joye, 2019). Tannins also can be complex with vitamin B12 (Liener, 1980). Reduction in polyphenol compounds like tannins during the SSF might be due to microbial fermentation of phenolic oxidase (Tajoddin et al., 2014; Tian et al., 2019). Similar findings of fermentation by lactic acid bacteria showed a reduction in the tannin content of sesame seed meal from 20 to 10 g kg-1 was noticed by Mukhopadhyay and Ray (1999) and tannin degrading fungal enzymes during the fermentation process (Jacqueline and Visser, 1996). In the present study, fermentation of CSM with brewery’s yeast significantly reduced (p<0.05) tannin activity, as shown in Table 1. A decrease of 89.1% in the tannin activity of CSM was recorded following solid-state fermentation with S. cerevisiae.

Amino acid content is also one of the significant factors in determining the quality of feeds. The requirements for amino acids in animals are well defined in various sets of recommendations such as those of National Research Council (1993). Amino acids requirements vary depending on the species and age of animals (Agbo, 2008). Fermentation of CSM with S. cerevisiae increased the lysine and methionine content (11.3% and 14.2%, respectively) of FCSM after 48 h of fermentation. Other essential amino acids in FCSM, like arginine, isoleucine and threonine, also increased compared to CSM. However, some essential amino acids like leucine, phenylalanine and valine decreased after the fermentation of CSM (Table 2). Microbial fermentation with brewery yeast and reduction of phytic acid might be shown an increased level of essential amino acids in the FCSM. Gossypol binds with the epsilon group of amino acids, primarily lysine, possibly arginine and cysteine, of proteins during heating in oil extraction and makes these amino acids unavailable to the animals (Fernandez et al., 1995).

Table 2: Amino acid profile of CSM and FCSM after 48 h fermentation with Saccharomyces cerevisiae.

Enzymatic and fermentative treatment with S. cerevisiae has enhanced the nutritional value of CSM are being explored in terms of cost, high product yield and efficient recovery. Solid-state fermentation of CSM has been demonstrated as a promising method since biodegradation of gossypol occurs during the fermentation process. It can reduce other anti-nutrients like phytic acid and total tannin. The nutritionally enriched with enzymes, proteins and other active substances like essential nutrients and amino acids in the CSM. SSF of the Agro-industrial waste can improve protein quality, increase essential nutrients like lysine and methionine and be an eco-friendly process to utilise the non-conventional feed ingredients as the best alternative protein supplement for non-ruminants.
The authors gratefully acknowledge the Vice-Chancellor and Director, Tamil Nadu, Dr J. Jayalalithaa Fisheries University, Nagapattinam, Tamil Nadu, India, for providing all the required facilities for the research.
None.

  1. Abowei, J.F.N. and Ekubo, A.T. (2011). A review of conventional and unconventional feeds in fish nutrition. British Journal of Pharmacology and Toxicology. 2(4): 179-191.

  2. Adeniji, A.A. (2007). Effect of replacing groundnut cake with maggot meal in the diet of broilers. International Journal of Poultry Science. 6(11): 822-825.

  3. Agbo, N.W. (2008). Oilseed meals as dietary protein sources for juvenile Nile tilapia (Oreochromis niloticus L.). STORRE: Stirling Online Research Repository. http://hdl.handle.net/ 1893/984.

  4. Andreaus, J., Bon, E.P.D.S. and Ferreira-Leitao, V.S. (2016). Sustainable technology supported by enzymes-prevention and valorisation of agroindustrial residues. Biocatalysis and Biotransformation. 34(2): 54-56.

  5. Antai, S.P. and Nkwelang, G. (1998). Reduction of some toxicants in Icacina mannii by fermentation with Saccharomyces cerevisiae. Plant Foods for Human Nutrition. 53(2): 103-111.

  6. Benjamin, U.A., Emmanuel, K.A. and Bamidele, O.O. (2016). Dietary phytase improves growth and water quality parameters for juvenile Clarias gariepinus fed soyabean diet-based diets. International Journal of Aquaculture. 5. DOI: 10.13140/ RG.2.1.3524.2001.

  7. Berardi, L.C. and Goldblatt, L.A. (1980). Gossypol. In: Toxic Constituents of Plant Food Stuffs. (Edited by I. E. Liener). New York, USA: Academic Press. Pp. 183-237.

  8. Butler, L.G., Rogler, J.C., Mehansho, H. and Carlson, D.M. (1986). Dietary Effects of Tannins. Plant Flavonoids in Biology and Medicine, Buffalo, New York (USA), 22-26.

  9. Canibe, N., Pedrosa, M.M., Robredo, L.M. and Bach Knudsen, K.E. (1999). Chemical composition, digestibility and protein quality of 12 sunflower (Helianthus annuus L.) cultivars. Journal of the Science of Food and Agriculture. 79(13): 1775-1782.

  10. Costa, J.A., Alegre, R.M. and Hasan, S.D. (1998). Packing density and thermal conductivity determintion for rice bran solid- state fermentation. Biotechnology Techniques. 12(10): 747-750.

  11. Currie, D.J. (2000). Aquaculture: Opportunity to Benefit Mankind. World Aquaculture. 44-49.

  12. Dawood, M.A. and Koshio, S. (2020). Application of fermentation strategy in aquafeed for sustainable aquaculture. Reviews in Aquaculture. 12(2): 987-1002.

  13. Dinesh, K.P., Sachin, M., Veena, B.J., Kumar, P.K.V. et al. (2003). Evaluation of botanicals against mealybug Planococcus citri Risso and its effect on parasitoid and attendant. Journal of Coffee Research. 31(2): 139-152.

  14. Ensminges, M.E. (1980) Dairy Cattle Science, 2nd ed., the Interstate Printers and Publishers, INC., Danville, Illnois, U.S.A.

  15. Eyo, A.A. (2003). Fundamentals of Fish Nutrition and Diet Development. An Overview. National Workshop on Fish Feed Development and Feeding Practices in Aquaculture Organized by Fisheries Society of Nigeria (FISON) in Collaboration with National Institute of Fresh Water Fisheries Research (NIFFR) and FAO National Special Programme for Food Security (FAO-NSPFS). 1-33.

  16. Fernandez, S.R., Zhang, Y.E. and Parsons, C.M. (1995). Dietary formulation with cottonseed meal on a total amino acid versus a digestible amino acid basis. Poultry Science. 74(7): 1168-1179.

  17. Fournier, V., Huelvan, C. and Desbruyeres, E. (2004). Incorporation of a mixture of plant feedstuffs as substitute for fish meal in diets of juvenile turbot (Psetta maxima). Aquaculture.  236(1-4): 451-465.

  18. Gao, Y., Shang, C., Maroof, M.S. et al. (2007). A modified colorimetric  method for phytic acid analysis in soybean. Crop Science.  47(5): 1797-1803.

  19. Geetha, P.S., Maheswari, I., Anandham, R. and Nallakurumban, B. (2015). Heat stabilised defatted rice bran (HDRB) fermented with Saccharomyces cerevisiae var MTCC 3813 to enhance the protein content with bio activity. International Journal of Scientific and Research Publication. 5: 1-7.

  20. Graf, E. (1983). Applications of phytic acid. Journal of the American Oil Chemists’ Society. 60 (11): 1861-1867.

  21. Hassaan, M.S., Soltan, M.A. and Abdel-Moez, A.M. (2015). Nutritive value of soybean meal after solid state fermentation with Saccharomyces cerevisiae for Nile tilapia, Oreochromis niloticus. Animal Feed Science and Technology. 201: 89-98.

  22. Helsper, J.P., Hoogendijk, J.M., Van Norel, A. and Burger-Meyer, K. (1993). Anti-nutritional factors in faba beans (Vica faba L.) as affected by breeding toward the absence of condensed tannins. Journal of Agricultural and Food Chemistry. 41(7):  1058-1061.

  23. Herrero, M., Havlík, P., Valin, H., Notenbaert, A. et al. (2013). Biomass use, production, feed efficiencies and greenhouse gas emissions from global livestock systems. Proceedings of the National Academy of Sciences. 110(52): 20888-20893.

  24. Hirabayashi, M., Matsui, T. and Yano, H. (1998). Fermentation of soybean meal with Aspergillus usamii improves zinc availability in rats. Biological Trace Element Res. 61: 227-234.

  25. Iji, P.A., Toghyani, M., Ahiwe, E.U., Omede, A.A. and Applegate, T. (2017). Alternative sources of protein for poultry nutrition. Achieving Sustainable Production of Poultry Meat. 2: 1-13.

  26. Jackson, A.J., Capper, B.S. and Matty, A.J. (1982). Evaluation of some plant proteins in complete diets for the tilapia Sarotherodon mossambicus. Aquaculture. 27(2): 97-109.

  27. Jacqueline, E.W. and Broerse, B.V. (1996). Assessing the Potential: In Biotechnology Building on Farmer’s Knowledge. Edited by Joske Bunders Bertus Haverkort, WIM Hiermstra Published by Macmillian Education Ltd., London and Basingstoke.

  28. Joye, I. (2019). Protein digestibility of cereal products. Foods. 8(6): 199. doi: 10.3390/foods8060199.

  29. Khalaf, M.A. and Meleigy, S.A. (2008). Reduction of free gossypol levels in cottonseed meal by microbial treatment. International  Journal of Agriculture and Biology. 10(2): 185-190.

  30. Krogdahl, A. (1989). Alternative Protein Sources From Plants Contain Antinutrients Affecting Digestion In Salmonids. Proc. III. Proc. III. Feeding and Nutrition in Fish. Toba, Japan, 253-261.

  31. Kumar, M., Tomar, M., Punia, S. and Grasso, S. (2021). Cottonseed: A sustainable contributor to global protein requirements. Trends in Food Science and Technology. 111: 100-13.

  32. Liener, I.E. and Kakade, M.L. (1980). Protease inhibitors. Toxic Constituents Of Plant Foodstuffs. 6: 7.

  33. Liu, H., Dong, X., Tan, B., Du, T., Zhang, S. et al. (2020). Effects of fish meal replacement by low gossypol cottonseed meal on growth performance, digestive enzyme activity, intestine histology and inflammatory gene expression of silver sillago (Sillago sihama Forsskál) (1775).  Aquaculture Nutrition. 26(5): 1724-1735.

  34. Mahmood, F., Khan, M.Z., Khan, A., Muhammad, G. and Javed, I. (2011). Lysine induced modulation of toxico-pathological effects of cottonseed meal in broiler breeder males. Pakistan Journal of Zoology. 43(2): 357-365.

  35. Malik, C.P. and Srivastava, A.K. (1979). Text Book of Plant Physiology.

  36. Manzanares, P., Ballesteros, I., Negro, M.J. et al. (2012). Biological conversion of forage sorghum biomass to ethanol by steam explosion pretreatment and simultaneous hydrolysis and fermentation at high solid content. Biomass Conversion and Biorefinery. 2(2): 123-132.

  37. Meghavarnam, A.K. and Janakiraman, S. (2017). Solid state fermentation: An effective fermentation strategy for the production of L-asparaginase by Fusarium culmorum (ASP-87). Biocatalysis and Agricultural Biotechnology.  11: 124-130.

  38. Meshram, S., Deo, A.D., Kumar, S., Aklakur, M. and Sahu, N.P. (2018). Replacement of de oiled rice bran by soaked and fermented sweet potato leaf meal: Effect on growth performance, body composition and expression of insulin like growth factor 1 in Labeo rohita (Hamilton), fingerlings.  Aquaculture Research. 49(8): 2741-2750.

  39. Mohamed, S., Lajis, S.M.M. and Hamid, N.A. (1995). Effects of protein from different sources on the characteristics of sponge cakes, rice cakes (apam), doughnuts and frying batters. Journal of the Science of Food and Agriculture.  68(3): 271-277.

  40. Mukhopadhyay, N.A. (1999). Effect of fermentation on the nutritive value of sesame seed meal in the diets for rohu, Labeo rohita (Hamilton), fingerlings. Aquaculture Nutrition. 5: 229-236.

  41. Munro, J.M. and Munro, J.M. (1987). Cotton (2nd Edn.) (Tropical Agriculture Series). Longman.

  42. National Research Council (1993). Nutrient Requirements of Fish. National Academies Press.

  43. Obioha, F.C. (1992). A Guide to Poultry Production in the Tropics. Acena.

  44. Olukomaiya, O., Fernando, C., Mereddy, R., Li, X. and Sultanbawa, Y. (2019). Solid-state fermented plant protein sources in the diets of broiler chickens: A review. Animal Nutrition. 5(4):  319-330.

  45. Onyimba, I.A., Ogbonna, A.I., Egbere, J.O. et al. (2015). Bioconversion of sweet potato leaves to animal feed. Annual Research and Review in Biology. 1-6.

  46. Paiano, D., Moreira, I., da Silva, M.A.A., Sartori, Y.M. et al. (2006). Farelos de algodão com diferentes níveis de proteína na alimentação de suínos na fase inicial: Digestibilidade e desempenho. Acta Scientiarum. Animal Sciences. 28(4): 415-422.

  47. Pandey, A. (2003). Solid-state fermentation. Biochemical Engineering Journal. 13(2-3): 81-84.

  48. Pandey, A., Ashakumary, L. and Selvakumar, P. (1995). Copra waste- A novel substrate for solid-state fermentation. Bioresource  Technology. 51(2-3): 217-220.

  49. Pandey, A., Soccol, C.R., Nigam, P. and Soccol, V.T. (2000). Biotechnological potential of agro-industrial residues. I: Sugarcane bagasse. Bioresource Technology. 74(1): 69-80.

  50. Ramachandran, S. and Ray, A.K. (2007). Nutritional evaluation of fermented black gram (Phaseolus mungo) seed meal in compound diets for rohu, Labeo rohita (Hamilton), fingerlings. Journal of Applied Ichthyology. 23(1): 74-79.

  51. Reddy, N.R. and Pierson, M.D. (1994). Reduction in anti-nutritional and toxic components in plant foods by fermentation. Food Research International. 27(3): 281-290.

  52. Romano, G.B. and Scheffler, J.A. (2008). Lowering seed gossypol content in glanded cotton (Gossypium hirsutum L.) lines. Plant Breeding. 127(6): 619-624.

  53. Sarker, A.K., Saha, D., Begum, H., Zaman, A. and Rahman, M.M. (2015). Comparison of cake compositions, pepsin digestibility and amino acids concentration of proteins isolated from black mustard and yellow mustard cakes. AMB Express. 5(1): 1-6.

  54. Schanderi, S.H. (1970). Methods in Food Analysis. New York: Academic, 709.

  55. ShuangQi, T., Yue, S., ZhiCheng, C., YingQi, Y. and YanBo, W. (2019). Functional properties of polyphenols in grains and effects of physicochemical processing on polyphenols. Journal of Food Quality. 2793973.

  56. Singhania, R.R., Patel, A.K., Soccol, C.R. and Pandey, A. (2009). Recent advances in solid-state fermentation. Biochemical Engineering Journal. 44(1): 13-18.

  57. Smith, C.R., Shekleton, M.C., Wolff, I.A. and Jones, Q. (1959). Seed protein sources-Amino acid composition and total protein content of various plant seeds. Economic Botany.  13(2): 132-150.

  58. Smith, F.H. (1972). Effect of gossypol bound to cottonseed protein on growth of weanling rats. Journal of Agricultural and Food Chemistry. 20(4): 803-804.

  59. Tacon, A.G. (1990). Standard Methods for the Nutrition and Feeding of Farmed Fish and Shrimp. Redmond, Washington, USA: Argent Laboratories Press. 3, 454.

  60. Tajoddin, M., Manohar, S. and Lalitha, J. (2014). Effect of soaking and germination on polyphenol content and polyphenol oxidase activity of mung bean (Phaseolus aureus L.) cultivars differing in seed color. International Journal of Food Properties. 17(4): 782-790.

  61. Tang, J.W., Sun, H., Yao, X.H., Wu, Y.F., Wang, X. and Feng, J. (2012). Effects of replacement of soybean meal by fermented cottonseed meal on growth performance, serum biochemical parameters and immune function of yellow-feathered broilers. Asian-Australasian Journal of Animal Sciences. 25(3): 393-400.

  62. Tanksley, Jr. T.D. (1990). Cottonseed Meal. In: Nontraditional Feed Sources for use in swine Production [edited by Thacker, P.A. and Kirkwood, R.N.]. Boston, Butterworth. Pp. 139-51. 

  63. Tekeli, A. (2014). Nutritional value of black cumin (Nigella sativa) meal as an alternative protein source in poultry nutritýon.  Journal of Animal Advances. 4: 479-806.

  64. Viesturs, U.E., Strikauska, S.V., Leite, M.P. et al. (1987). Combined submerged and solid substrate fermentation for the bioconversion of lignocellulose. Biotechnology and Bioengineering. 30(2): 282-288.

  65. Wan, M., Yin, P., Fang, W., Xie, S., Chen, S.J., Tian, L.X. and Niu, J.  (2018). The effect of replacement of fishmeal by concentrated dephenolization cottonseed protein on the growth, body composition, haemolymph indexes and haematological enzyme activities of the Pacific white shrimp (Litopenaeus vannamei). Aquaculture Nutrition. 24(6): 1845-1854.

  66. Withers, W.A. and Carruth, F.E. (1915). Gossypol, the toxic substance in cottonseed meal. Journal of Agricultural Research. 5: 261-288.

  67. Xiong, J.L., Wang, Z.J., Miao, L.H., Meng, F.T. and Wu, L.Y. (2016). Growth performance and toxic response of broilers fed diets containing fermented or unfermented cottonseed meal. Journal of Animal and Feed Sciences. 25: 348-53.

  68. Zhang, W.J., Xu, Z.R., Zhao, S.H., Sun, J.Y. and Yang, X. (2007). Development of a microbial fermentation process for detoxification of gossypol in cottonseed meal. Animal Feed Science and Technology. 135(1-2): 176-186.

  69. Zhang, Z., Yang, D., Liu, L., Chang, Z. and Peng, N. (2022). Effective gossypol removal from cottonseed meal through optimized solid-state fermentation by Bacillus coagulans. Microbial Cell Factories. 21(1): 252. https://doi.org/10.1186/s12934- 022-01976-1.

  70. Zhao, Z.X., Song, C.Y., Xie, J., Ge, X.P., Liu, B., Xia, S.L., Yang, S., Wang, Q. and Zhu, S.H. (2016). Effects of fish meal replacement by soybean peptide on growth performance, digestive enzyme activities and immune responses of yellow catfish Pelteobagrus fulvidraco. Fisheries Science. 82(4): 665-673. 

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