Effects of lactic acid bacteria and cellulase additives on the fermentation quality, antioxidant activity, and metabolic profile of oat silage

Abstract

Oats (Avena sativa L.) are rich in nutrients and bioactive compounds, serving as a roughage source for ruminants. This study investigated the impact of lactic acid bacteria (LAB), cellulase (M), and their combinations (LM) on the fermentation quality and metabolic compounds of oat silage. Results demonstrated that all additive treatments significantly increased lactic acid content compared to the control group (P < 0.05), with the lactic acid bacteria treatment group exhibiting the lowest pH value (P < 0.05). Analysis of antioxidant activity and metabolites in oat silage over 60 days revealed 374 differential metabolites with 113 up-regulated and 261 down-regulated, and all treatment groups showing higher antioxidant activity than raw oat materials (P < 0.05). Although no significant differences in antioxidant activity were observed among the various treatment groups in this experiment, notable changes in metabolic pathways were identified. Furthermore, two metabolites (carboxylic acids and derivatives and benzene and substituted derivatives) were identified through non-targeted metabolomics technology, both of which are strongly associated with the antioxidant activity of oat silage. This finding provides a theoretical basis for the efficient use of oat silage in animal husbandry.

Graphical abstract

References

[1] Aniwaru A, Ataku K, Narasaki N, No E. Effects of addition of cell wall degrading enzyme derived from Acremonium cellulolyticus Y-94 on fermentation quality, dry matter recovery and cell wall components of grass silage. GRASSL SCI, 1998, 43(4): 406-412

[2] Bao T, Xu Y, Gowd V, Zhao JC, Xie JH, Liang WK, Chen W. Systematic study on phytochemicals and antioxidant activity of some new and common mulberry cultivars in China of the article. J FUNCT FOODS, 2016, 25: 537-547,

[3] Broderick GA, Kang JH. Automated simultaneous determination of ammonia and total amino-acids in ruminal fluid and invitro media of the article. J DAIRY SCI, 1980, 63(1): 64-75,

[4] Chen LY, Bai SQ, You MH, Xiao BX, Li P, Cai YM. Effect of a low temperature tolerant lactic acid bacteria inoculant on the fermentation quality and bacterial community of oat round bale silage of the article. Anim Feed Sci Technol, 2020, 269,

[5] Cohen-Zinder M, Weinberg Z, Leibovich H, Chen Y, Rosen M, Sagi G, Orlov A, Agmon R, Yishay M, Miron J, Shabtay A. Ensiled Moringa oleifera: an antioxidant-rich feed that improves dairy cattle performance of the article. J Agr Sci Camb, 2017, 155(7): 1174-1186,

[6] Du X, Fan H, Liu S, Zhang ZC. Selective nucleophilic α-C alkylation of phenols with alcohols via Ti=Cα intermediate on anatase TiO2 surface of the article. Nat Commun, 2023, 14(1): 4479, PMCID: 10397351

[7] Ferreira-Lazarte A, Plaza-Vinuesa L, de Las Rivas B, Villamiel M, Muñoz R, Moreno FJ. Production of α-rhamnosidases from Lactobacillus plantarum WCFS1 and their role in deglycosylation of dietary flavonoids naringin and rutin. Int J Biol Macromol, 2021, 193: 1093-1102,

[8] Floegel A, Kim DO, Chung SJ, Koo SI, Chun OK. Comparison of ABTS/DPPH assays to measure antioxidant capacity in popular antioxidant-rich US foods of the article. J Food Compos Anal, 2011, 24(7): 1043-1048,

[9] Gao Y, Zhou HZ, Wang Y, Nussio LG, Yang FY, Ni KK. Insights into fermentation with lactic acid bacteria on the flavonoids biotransformation of alfalfa silage. Chem Biol Technol Ag, 2024,

[10] Guo Q, Hao X, Li YR, Zhang Q, Wang C, Han HY. Microbial communities and metabolites of whole crop corn silage inoculated with Lentilactobacillus plantarum and Lentilactobacillus buchneri of the article. Processes, 2022, 10(11): 2369,

[11] Hasan MT AOAC. (1990). Official methods of analysis, 2015 15 Virginia Association of Official Analytical Chemists

[12] He LW, Zhou W, Wang C, Yang FY, Chen XY, Zhang Q. Effect of cellulase and Lactobacillus casei on ensiling characteristics, chemical composition, antioxidant activity, and digestibility of mulberry leaf silage of the article. J Dairy Sci, 2019, 102(11): 9919-9931,

[13] He LW, Lv HJ, Chen N, Wang C, Zhou W, Chen XY, Zhang Q. Improving fermentation, protein preservation and antioxidant activity of Moringa oleifera leaves silage with gallic acid and tannin acid of the article. Bioresource Technol, 2020, 297,

[14] Horwitz W, Allee G, Latimer G, Kenneth H Official methods of analysis of the association of official analytical chemists of the article, 1980 Rockville Association of Official Analytical Chemists

[15] Huang YC, Qiu CC, Wang YM, Zhang W, He LW. Effect of tea polyphenols on the fermentation quality, protein preservation, antioxidant capacity and bacterial community of stylo silage of the article. Front Microbiol, 2022, 13, PMCID: 9493319

[16] Jia TT, Yun Y, Yu Z. Propionic acid and sodium benzoate affected biogenic amine formation, microbial community, and quality of oat Silage of the article. Front Microbio, 2021,

[17] Kim IS, Hwang CW, Yang WS, Kim CH. Multiple antioxidative and bioactive molecules of oats (Avena sativa L.) in human health of the article. Antioxid Basel, 2021, 10(9): 10091454,

[18] Liu Y, Zi X, Chen T, Li M. Research progress and countermeasure on microbial diversity of forage silage of the article. Anim Nutr, 2021, 33(11): 6084-6092,

[19] Lozicki A, Koziorzebska A, Halik G, Dymnicka M, Arkuszewska E, Niemiec T, Bogdan J. Effect of ensiling pumpkin (Cucurbita maxima D.) with dried sugar beet pulp on the content of bioactive compounds in silage and its antioxidant potential of the article. Anim Feed Sci Tech, 2015, 206: 108-113,

[20] Meeske R, van der Merwe GD, Greyling JF, Cruywagen CW. The effect of adding an enzyme containing lactic acid bacterial inoculant to big round bale oat silage on intake, milk production and milk composition of jersey cows of the article. Anim Feed Sci Tech, 2002, 97(3–4): 159-167,

[21] Min-Jie J, Han-Lu W, Wei L, Jian-Min Z. Quantum chemistry study on the reaction mechanism of ozone oxidation of benzothiophene and its derivatives of the article. Adv New Renew Energy, 2016, 4(2): 139-145.

[22] Ni KK, Wang FF, Zhu BG, Yang JX, Zhou GA, Pan Y, Tao Y, Zhong J. Effects of lactic acid bacteria and molasses additives on the microbial community and fermentation quality of soybean silage. Bioresource Technol, 2017, 238: 706-715,

[23] Okoye CO, Wang YL, Gao L, Wu YF, Li X, Sun JZ, Jiang JX. The performance of lactic acid bacteria in silage production: a review of modern biotechnology for silage improvement of the article. Microbiol Res, 2023, 266,

[24] Ponnampalam EN, Kiani A, Santhiravel S, Holman BWB, Lauridsen C, Dunshea FR. The importance of dietary antioxidants on oxidative stress, meat and milk production, and their preservative aspects in farm animals: antioxidant action, animal health, and product quality-invited review of the article. Animals Basel, 2022, 12(23): 12233279,

[25] Sinaga DP, Tampubolon DKA, Kembaren RF, Martgrita MM. Fermentation process effect to enhance antioxidant and antibacterial activity of phenolic compounds and its possible application to galactomannan polysaccharides: a review. Earth Env Sci T R So, 2022,

[26] Su RA, Ke WC, Bai J, Wang MS, Usman S, Xie DM, Xu DM, Chen MY, Guo XS. Comprehensive profiling of the metabolome in corn silage inoculated with or without Lactiplantibacillus plantarum using different untargeted metabolomics analyses of the article. Arch Anim Nutr, 2023, 77(5): 323-341,

[27] Suttie JM, Reynolds SG Fodder oats: a world overview of the book, 2004 Rome Food\& Agriculture Org

[28] Tedeschi LO, Muir JP, Naumann HD, Norris AB, Ramírez-Restrepo A, Mertens-Talcott SU (2021) Nutritional Aspects of Ecologically Relevant Phytochemicals in Ruminant Production of the article. ‌Front Vet Sci. 8(5): 628445. https://doi.org/10.3389/fvets.2021.628445

[29] Vansoest PJ, Robertson JB, Lewis BA. Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition of the article. J Dairy SCI, 1991, 74(10): 3583-3597,

[30] Vasilev N, Boccard J, Lang G, Gromping U, Fischer R, Goepfert S, Rudaz S, Schillberg S. Structured plant metabolomics for the simultaneous exploration of multiple factors of the article. SCI REP-UK, 2016, 6: 37390,

[31] Wang B, Luo HL. Effects of mulberry leaf silage on antioxidant and immunomodulatory activity and rumen bacterial community of lambs of the article. BMC MICROBIOL, 2021, 21(1): 250, PMCID: 8454139

[32] Wang LC, Guan LH, Fang JC, Cai YM, Cao Y. Fermentation characteristics and in vitro ruminal digestion of yacon residue silage with lactic acid bacteria inoculant or beet pulp of the article. Rev Bras Zootecn, 2019, 48,

[33] Want EJ, Masson P, Michopoulos F, Wilson ID, Theodoridis G, Plumb RS, Shockcor J, Loftus N, Holmes E, Nicholson JK. Global metabolic profiling of animal and human tissues via UPLC-MS of the article. NAT PROTOC, 2013, 8(1): 17-32,

[34] Weinberg ZG, Akiri B, Potoyevski E, Kanner J. Enhancement of polyphenol recovery from rosemary (Rosmarinus officinalis) and sage (Salvia officinalis) by enzyme-assisted ensiling (ENLAC) of the article. J Agric Food Chem, 1999, 47(7): 2959-2962,

[35] Xiong H, Zhu Y, Wen Z, Liu G, Guo Y, Sun B. Effects of cellulase, lactobacillus plantarum, and sucrose on fermentation parameters, chemical composition, and bacterial community of hybrid pennisetum silage of the article. Fermentation (basel), 2022, 8(8): 356,

[36] Xiong Y, Xu JJ, Guo LN, Chen F, Jiang DD, Lin YL, Guo CZ, Li XM, Chen YR, Ni KK, Yang FY. Exploring the effects of different bacteria additives on fermentation quality, microbial community and in vitro gas production of forage oat silage. Animals (Basel), 2022, PMCID: 9515223

[37] Yi Q, Wang P. Research progress of biological additives in silage of the article. Anim Nutr, 2023, 35(3): 1475-1488,

[38] Zelena E, Dunn W B, Broadhurst D, Francis-McIntyre S, Carroll K M, Begley P, O'Hagan S, Knowles J D, Halsall A, Wilson I D, Kell D B, Consortium H. Development of a robust and repeatable UPLC-MS method for the long-term metabolomic study of human serum of the article. Anal Chem, 2009, 81(4): 1357-1364,

[39] Zhang YX, Ke WC, Vyas D, Adesogan AT, Franco M, Li FH, Bai J, Guo XS. Antioxidant status, chemical composition and fermentation profile of alfalfa silage ensiled at two dry matter contents with a novel Lactobacillus plantarum strain with high-antioxidant activity of the article. Anim Feed Sci Tech, 2021, 272,

[40] Zhang X, Guo X, Li F, Usman S, Zhang Y, Ding Z. Antioxidant, flavonoid, α-tocopherol, β-carotene, fatty acids, and fermentation profiles of alfalfa silage inoculated with novel Lactiplantibacillus Plantarum and Pediococcus acidilactici strains with high-antioxidant activity of the article. Anim Feed Sci Tech, 2022, 288,

Funding

Modern Agro-industry Technology Research System of China,(No. CARS-07-E-3)