Abstract
Microbial treatment can reduce the antinutritional factors and allergenic proteins in corn-soybean meal mixture (CSMM), but the role of the microbial community in hypoallergenicity and digestibility during the fermentation process remains unclear. Therefore, the fermentation strains of Bacillus and LAB were determined, and the compatibility and fermentation process of two-stage solid fermentation composite bacteria were optimized, and the dynamic changes in physicochemical property and microbial community during two-stage fermentation were investigated. Results showed that Bacillus subtilis NCUBSL003 and Lactobacillus acidophilus NCUA065016 were the best fermentation combinations. The optimal fermentation conditions were inoculum 7.14%, solid–liquid ratio of 1:0.88 and fermentation time of 74.30 h. The contents of TI, β-conglycinin and glycinin decreased significantly after fermentation. Besides, TCA-SP, small peptides and FAA increased. Bacillus and Lactobacillus were the main genera. Pathogenic bacteria genera were inhibited effectively. This study suggests the feasibility of two-stage fermentation in improving the nutrient values and safety of the CSMM.
Similar content being viewed by others
References
Álvarez-Estrada Á, Martínez-Martínez S, Martín C-BG, García-Iglesias M-J, Pérez-Martínez C, Yubero-Delgado S, Guizzo JA, Frandoloso R, Rodríguez-Ferri E-F. Immunogenic characterization of vaccines based on Haemophilus parasuis Nagasaki strain, OmpP2, OmpP5 and OmpD15, in colostrum-deprived pigs experimentally challenged with the same strain. Research in Veterinary Science. 119: 292-301 (2018)
AOAC. Official methods of analysis of AOAC International. Arlington: AOAC (1990)
Barros L, Carvalho AM, Morais JS, Ferreira ICFR. Strawberry-tree, blackthorn and rose fruits: detailed characterisation in nutrients and phytochemicals with antioxidant properties. Food Chemistry. 120: 247-254 (2010)
Beshiru A, Igbinosa IH, Omeje FI, Ogofure AG, Eyong MM, Igbinosa EO. Multi-antibiotic resistant and putative virulence gene signatures in Enterococcus species isolated from pig farms environment. Microbial Pathogenesis. 104: 90-96 (2017)
Canibe N, Jensen BB. Fermented liquid feed—microbial and nutritional aspects and impact on enteric diseases in pigs. Animal Feed Science and Technology. 173: 17-40 (2012)
Chi CH, Cho SJ. Improvement of bioactivity of soybean meal by solid-state fermentation with Bacillus amyloliquefaciens versus Lactobacillus spp. and Saccharomyces cerevisiae. LWT- Food Science and Technology. 68: 619-625 (2016)
Cutting SM. Bacillus probiotics. Food Microbiology. 28: 214-220 (2011)
Dai C, Ma H, He R, Huang L, Zhu S, Ding Q, Luo L. Improvement of nutritional value and bioactivity of soybean meal by solid-state fermentation with Bacillus subtilis. LWT. 86: 1-7 (2017)
Drew MD, Borgeson TL, Thiessen DL. A review of processing of feed ingredients to enhance diet digestibility in finfish. Animal Feed Science and Technology. 138: 118-136 (2007)
Goebel KP, Stein HH. Ileal digestibility of amino acids in conventional and low-Kunitz soybean products fed to weanling pigs. Asian-Australas. Asian-Australasian Journal of Animal Sciences. 24: 88-95 (2010)
Goodarzi Boroojeni F, Kozłowski K, Jankowski J, Senz M, Wiśniewska M, Boros D, Drażbo A, Zentek J. Fermentation and enzymatic treatment of pea for turkey nutrition. Animal Feed Science and Technology. 237: 78-88 (2018)
Guan Q, Zheng W, Huang T, Xiao Y, Liu Z, Peng Z, Gong D, Xie M, Xiong T. Comparison of microbial communities and physiochemical characteristics of two traditionally fermented vegetables. Food Research International. 128: 108755 (2020)
Hou X, Dai C, Tang Y, Xing Z, Mintah BK, Dabbour M, Ding Q, He R, Ma H. Thermophilic solid-state fermentation of rapeseed meal and analysis of microbial community diversity. LWT. 116: 108520 (2019)
Hu J, Lu W, Wang C, Zhu R, Qiao J. Characteristics of solid-state fermented feed and its effects on performance and nutrient digestibility in growing-finishing pigs. Asian-Australas. Asian-Australasian Journal of Animal Sciences. 21: 1635-1641 (2008)
Huang J, Zhang W, Fan R, Liu Z, Huang T, Li J, Du T, Xiong T. Composition and functional diversity of fecal bacterial community of wild boar, commercial pig and domestic native pig as revealed by 16S rRNA gene sequencing. Archives of Microbiology. 202: 843-857 (2020)
Koo B, Kim JW, Nyachoti CM. Nutrient and energy digestibility, and microbial metabolites in weaned pigs fed diets containing Lactobacillus-fermented wheat. Animal Feed Science and Technology. 241: 27-37 (2018)
Lan RX, Koo JM, Kim IH. Effects of Lactobacillus acidophilus supplementation in different energy and nutrient density diets on growth performance, nutrient digestibility, blood characteristics, fecal microbiota shedding, and fecal noxious gas emission in weaning pigs. Animal Feed Science and Technology. 219: 181-188 (2016)
Li DF, Nelssen JL, Reddy PG, Blecha F, Klemm R, Goodband RD. Interrelationship between hypersensitivity to soybean proteins and growth performance in early-weaned pigs. Journal of Animal Science. 69: 4062-4069 (1991)
Li J, Meng Q, Xing J, Wang C, Song C, Ma D, Shan A. Citric acid enhances clean recycling of Chinese cabbage waste by anaerobic fermentation. Journal of Cleaner Production. 348: 131366 (2022)
Li J, Zhou R, Ren Z, Fan Y, Hu S, Zhuo C, Deng Z. Improvement of protein quality and degradation of allergen in soybean meal fermented by Neurospora crassa. LWT. 101: 220-228 (2019)
Ling N, Jiang X, Forsythe S, Zhang D, Shen Y, Ding Y, Wang J, Zhang J, Wu Q, Ye Y. Food safety risks and contributing factors of Cronobacter spp. Engineering. 12: 128-138 (2022)
Lyberg K, Lundh T, Pedersen C, Lindberg E. Influence of soaking, fermentation and phytase supplementation on nutrient digestibility in pigs offered a grower diet based on wheat and barley. Animal Science. 82(6): 853-858 (2007)
Medeiros S, Xie J, Dyce PW, Cai HY, DeLange K, Zhang H, Li J. Isolation of bacteria from fermented food and grass carp intestine and their efficiencies in improving nutrient value of soybean meal in solid state fermentation. Journal of Animal Science and Biotechnology. 9: 29 (2018)
Missotten JAM, Goris J, Michiels J, Van Coillie E, Herman L, De Smet S, Dierick NA, Heyndrickx M. Screening of isolated lactic acid bacteria as potential beneficial strains for fermented liquid pig feed production.Animal Feed Science and Technology. 150: 122-138 (2009)
Moktan B, Saha J, Sarkar PK. Antioxidant activities of soybean as affected by Bacillus-fermentation to kinema. Food Research International. 41: 586-593 (2008)
Pi X, Fu G, Yang Y, Wan Y, Xie M. Changes in IgE binding capacity, structure, physicochemical properties of peanuts through fermentation with Bacillus natto and Lactobacillus plantarum along with autoclave pretreatment. Food Chemistry. 392: 133208 (2022)
Pi X, Sun Y, Fu G, Wu Z, Cheng J. Effect of processing on soybean allergens and their allergenicity. Trends in Food Science & Technology. 118: 316-327 (2021)
Pi X, Wan Y, Yang Y, Li R, Wu X, Xie M, Li X, Fu G. Research progress in peanut allergens and their allergenicity reduction. Trends in Food Science & Technology. 93: 212-220 (2019)
Qu Y, Jiang W, Yin G, Wei C, Bao J. Effects of feeding corn-lablab bean mixture silages on nutrient apparent digestibility and performance of dairy cows. Asian-Australas. Asian-Australasian Journal of Animal Sciences. 26: 509-516 (2013)
Reddy LVA, Wee Y-J, Yun J-S, Ryu H-W. Optimization of alkaline protease production by batch culture of Bacillus sp. RKY3 through Plackett–Burman and response surface methodological approaches. Bioresource Technology. 99: 2242-2249 (2008)
Riebroy S, Benjakul S, Visessanguan W, Kijrongrojana K, Tanaka M. Some characteristics of commercial Som-fug produced in Thailand. Food Chemistry. 88: 527-535 (2004)
Seo S-H, Cho S-J. Changes in allergenic and antinutritional protein profiles of soybean meal during solid-state fermentation with Bacillus subtilis. LWT. 70: 208-212 (2016)
Shi C, He J, Yu J, Yu B, Mao X, Zheng P, Huang Z, Chen D. Amino acid, phosphorus, and energy digestibility of Aspergillus niger fermented rapeseed meal fed to growing pigs. Journal of Animal Science. 93: 2916-2925 (2015)
Shi C, Zhang Y, Lu Z, Wang Y. Solid-state fermentation of corn-soybean meal mixed feed with Bacillus subtilis and Enterococcus faecium for degrading antinutritional factors and enhancing nutritional value. Journal of Animal Science and Biotechnology. 8: 50 (2017)
Smith C, van Megen W, Twaalfhoven L, Hitchcock C. The determination of trypsin inhibitor levels in foodstuffs. Journal of the Science of Food and Agriculture. 31: 341-350 (1980)
Van Soest PJ, Robertson JB, Lewis BA. Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. Journal of Dairy Science. 74:3583-3597 (1991)
Song YS, Pérez VG, Pettigrew JE, Martinez-Villaluenga C, de Mejia EG. Fermentation of soybean meal and its inclusion in diets for newly weaned pigs reduced diarrhea and measures of immunoreactivity in the plasma. Animal Feed Science and Technology. 159: 41-49 (2010)
Sun P, Li D, Dong B, Qiao S, Ma X. Effects of soybean glycinin on performance and immune function in early weaned pigs. Archives of Animal Nutrition. 62: 313-321 (2008).
Wang C, Shi CY, Su W, Jin ML, Xu BC, Hao LH, Zhang Y, Lu ZQ, Wang FQ, Wang YZ, Du HH. Dynamics of the physicochemical characteristics, microbiota, and metabolic functions of soybean meal and corn mixed substrates during two-stage solid-state fermentation. Applied and Environmental Science. 5(1): e00501-19 (2020)
Wang J, Liu Z, Xia J, Chen Y. Effect of microbial inoculation on physicochemical properties and bacterial community structure of citrus peel composting. Bioresource Technology. 291: 121843 (2019)
Wang R, Dong P, Zhu Y, Yan M, Liu W, Zhao Y, Huang L, Zhang D, Guo H. Bacterial community dynamics reveal its key bacterium, Bacillus amyloliquefaciens ZB, involved in soybean meal fermentation for efficient water-soluble protein production. LWT. 135: 110068 (2021)
Yeh RH, Hsieh CW, Chen KL. Screening lactic acid bacteria to manufacture two-stage fermented feed and pelleting to investigate the feeding effect on broilers. Poultry Science. 97: 236-246 (2018)
Yin H, Zhong Y, Xia S, Hu J, Nie S, Xiong T, Xie M. Effects of fermentation with Lactobacillus plantarum NCU137 on nutritional, sensory and stability properties of Coix (Coix lachryma-jobi L.) seed. Food Chemistry. 314: 126037 (2020)
Zeng T, Li X, Guan H, Yang W, Liu W, Liu J, Du Z, Li X, Xiao Q, Wang X, Zhang X, Huang L, Xiang Q, Peng Q, Yan Y. Dynamic microbial diversity and fermentation quality of the mixed silage of corn and soybean grown in strip intercropping system. Bioresource Technology. 313: 123655 (2020)
Zentek J, Goodarzi Boroojeni F. (Bio)technological processing of poultry and pig feed: impact on the composition, digestibility, anti-nutritional factors and hygiene. Animal Feed Science and Technology. 268: 114576 (2020)
Acknowledgements
This work was supported by the Basic Research and Talent Cultivation Project of Jiangxi Academy of Agricultural Sciences (No. JXSNKYJCRC202321), Open Project Program of the State Key Laboratory of Food Science and Technology, Nanchang University (No. SKLF-KF-202206), Key Research and Development Program of Jiangxi Province (20223BBF61024), Central Guidance for Local Scientific and Technological Development Funds (20221ZDF03018), Ten Main Directions of Agricultural Science and Technology Innovation of the “14th Five-Year Plan” Guangdong Province (Project No. 2022SDZG04), and Vegetable Industry Technology System Post Expert Project of Jiangxi Province (Project No. JXARS-06).
Author information
Authors and Affiliations
Contributions
TD: conceiving and designing research, conducting experiments and writing original draft. SX: investigation, methodology, validation. LW: methodology, visualization, software. QG: methodology, software, formal analysis. MX, TX: supervision, conceptualization, project administration. JH, GL: resources, supervision, project administration, funding acquisition.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that none of them have a conflict of interest regarding this manuscript.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Du, T., Xiong, S., Wang, L. et al. Two-stage fermentation of corn and soybean meal mixture by Bacillus subtilis and Lactobacillus acidophilus to improve feeding value: optimization, physicochemical property, and microbial community. Food Sci Biotechnol 33, 1207–1219 (2024). https://doi.org/10.1007/s10068-023-01426-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10068-023-01426-7