Non-antibiotic feed additives production by Acremonium terricola solid-fermented Camellia oleifera meal

Abstract

The Camellia oleifera meal (COM), a primary byproduct of oil-tea processing, often being discarded or used as a low-grade fertilizer due to its low value. The underutilization has become a significant bottleneck hindering the high-quality development of the oil-tea industry. In this study, the production of antibiotic-free feed additives through the solid-state fermentation of COM by Acremonium terricola was investigated. Our findings revealed that a saponin concentration of 5 mg/mL significantly enhanced the production of cordycepic acid (70.4 mg/g), ergosterol (3.32 mg/g), and chitin (110 mg/g) by A. terricola. This concentration also promoted chitin production and the activities of peroxidase (POD) and Na⁺/K⁺-ATPase, thereby maintaining cellular homeostasis and energy balance in A. terricola. Solid-state fermented rice bran (RB), wheat bran (WB), and desaponificated COM (containing 2.6 mg/100 g of tea saponin) were all found to be beneficial for increasing the production of cordycepic acid and ergosterol. The blend of COM, RB, and WB in the ratio of 15:65:20 was particularly advantageous for the production and accumulation of cordycepic acid and ergosterol, yielding 1.54 and 1.43 times, 1.27 and 1.37 times, and 1.98 and 5.52 times more than those produced by WB, RB, and COM alone, respectively.Meantime, the difference in contents of sugar and protein in A. terricola cultures (ATCs) using combination were not significant compared to RB and WB. These results indicated that COM can partially replace foodstuffs or food by-products to prepare antibiotic-free feed additives by A. terricola.

Graphical Abstract

References

[1] BiZ, ZhaoY, MorrellJJ, et al. . The antifungal mechanism of Konjac flying powder extract and its active compounds against wood decay fungi. Ind Crop Prod, 2021, 164: 113406

[2] ChenJ, GuoY, LuY, et al. . Effects of Acremonium terricola culture on the growth, slaughter yield, immune organ, serum biochemical indexes, and antioxidant indexes of geese. Animals, 2022, 12: 1164

[3] ChiX, BiS, XuW, et al. . Oral administration of tea saponins to relive oxidative stress and immune suppression in chickens. Poult Sci, 2017, 96: 3058-3067

[4] Costa-de‐OliveiraS, SilvaAP, MirandaIM, et al. . Determination of chitin content in fungal cell wall: an alternative flow cytometric method. Cytometry Pt A, 2013, 83A: 324-328

[5] DiT, YangS, DuF, et al. . Cytotoxic and hypoglycemic activity of triterpenoid saponins from Camellia Oleifera Abel. Seed pomace. Molecules, 2017, 22: 1562

[6] FanM, HuangB, LiC, LiZ. A new record species of the genus Acremonium from China. Mycosystema, 1999, 18: 449

[7] Guajardo-FloresD, Serna-SaldívarSO, Gutiérrez-UribeJA. Evaluation of the antioxidant and antiproliferative activities of extracted saponins and flavonols from germinated black beans (Phaseolus vulgaris L). Food Chem, 2013, 141: 1497-1503

[8] HeJ, WuZ, ZhangS, et al. . Optimization of microwave-assisted extraction of tea saponin and its application on cleaning of historic silks. J Surfact Deterg, 2014, 17: 919-928

[9] HelanderIM, Mattila-SandholmT. Permeability barrier of the Gram-negative bacterial outer membrane with special reference to nisin. Int J Food Microbiol, 2000, 60: 153-161

[10] HuW, LiuJ, YeJ, et al. . Effect of tea saponin on rumen fermentation in vitro. Anim Feed Sci Tech, 2005, 120: 333-339

[11] IsmailM, SrivastavaV, MarimaniM, AhmadA. Carvacrol modulates the expression and activity of antioxidant enzymes in Candida Auris. Res Microbiol, 2022, 173: 103916

[12] KimJD, KhanMI, ShinJH, et al. . HPLC fractionation and pharmacological assessment of green tea seed saponins for antimicrobial, anti-angiogenic and hemolytic activities. Biotechnol Bioproc E, 2015, 20: 1035-1043

[13] Le BotM, ThibaultJ, PottierQ, et al. . An accurate, cost-effective and simple colorimetric method for the quantification of total triterpenoid and steroidal saponins from plant materials. Food Chem, 2022, 383: 132597

[14] LiB, XuY, JinY, et al. . Response surface optimization of supercritical fluid extraction of kaempferol glycosides from tea seed cake. Ind Crop Prod, 2010, 32: 123-128

[15] LiQ, BaiZ, O’DonnellA, et al. . Oxidative stress in fungal fermentation processes: the roles of alternative respiration. Biotechnol Lett, 2011, 33: 457-467

[16] LiT, ZhangH, WuC. Screening of antioxidant and antitumor activities of major ingredients from defatted Camellia oleifera seeds. Food Sci Biotechnol, 2014, 23: 873-880

[17] LiY, WangY, DingX, et al. . Effects of Acremonium terricola culture on growth performance, antioxidant status and immune functions in weaned calves. Livest Sci, 2016, 193: 66-70

[18] LiY, WangY, ZhangG, et al. . Effects of Acremonium terricola culture supplementation on apparent digestibility, rumen fermentation, and blood parameters in dairy cows. Anim Feed Sci Tech, 2017, 230: 13-22

[19] LiY, SunY, LiX, et al. . Effects of Acremonium terricola culture on performance, milk composition, rumen fermentation and immune functions in dairy cows. Anim Feed Sci Tech, 2018, 240: 40-51

[20] Li Y, Jiang X, Xu H et al (2020) Acremonium terricola culture plays anti-inflammatory and antioxidant roles by modulating MAPK signaling pathways in rats with lipopolysaccharide-induced mastitis. Food Nutr Res 64. https://doi.org/10.29219/fnr.v64.3649

[21] LinS, LiuZ, XueY, et al. . Biosynthetic pathway analysis for improving the cordycepin and cordycepic acid production in Hirsutella Sinensis. Appl Biochem Biotechnol, 2016, 179: 633-649

[22] LiuY, RenL, ZhaoJ, et al. . Ergosterol production at elevated temperatures by Upc2-overexpressing Kluyveromyces marxianus using Jerusalem artichoke tubers as feedstock. Bioresour Technol, 2022, 362: 127878

[23] LuanF, ZengJ, YangY, et al. . Recent advances in Camellia Oleifera Abel: a review of nutritional constituents, biofunctional properties, and potential industrial applications. J Funct Foods, 2020, 75: 104242

[24] MenezesRT, PereiraTC, JunqueiraJC, et al. . Synergistic combination of duloxetine hydrochloride and fluconazole reduces the cell growth and capsule size of Cryptococcus neoformans. Acad Bras Ciênc, 2022, 94: e20211021

[25] MissallTA, LodgeJK, McEwenJE. Mechanisms of resistance to oxidative and nitrosative stress: implications for fungal survival in mammalian hosts. Eukaryot Cell, 2004, 3: 835-846

[26] National Research Council (U.S.). Nutrient requirements of poultry, 9th revised Edition, 1994Washington, D.CNational Academy

[27] PatraAK, SaxenaJ. The effect and mode of action of saponins on the microbial populations and fermentation in the rumen and ruminant production. Nutr Res Rev, 2009, 22: 204-219

[28] RamdaniD, YuniartiE, JayanegaraA, ChaudhryAS. Roles of essential oils, polyphenols, and saponins of medicinal plants as natural additives and anthelmintics in ruminant diets: a systematic review. Animals, 2023, 13: 767

[29] RiccardiC, NicolettiI. Analysis of apoptosis by propidium iodide staining and flow cytometry. Nat Protoc, 2006, 1: 1458-1461

[30] SharmaK, KaurR, KumarS, et al. . Saponins: a concise review on food related aspects, applications and health implications. Food Chem Adv, 2023, 2: 100191

[31] WangY, LiY, XuQ, et al. . Effects of Acremonium terricola culture on production performance, antioxidant status, and blood biochemistry in transition dairy cows. Anim Feed Sci Tech, 2019, 256: 114261

[32] WangW, PengY, NieY, et al. . Dietary supplementation with Acremonium terricola culture alters the gut microbial structure and improves the growth performance, antioxidant status, and immune function of weaning piglets. BMC Vet Res, 2023, 19: 258

[33] WeiJ, BiY, XueH, et al. . Antifungal activity of cinnamaldehyde against Fusarium sambucinum involves inhibition of ergosterol biosynthesis. J Appl Microbiol, 2020, 129: 256-265

[34] XiaoY, XiangY, ZhouW, et al. . Microbial community mapping in intestinal tract of broiler chicken. Poult Sci, 2017, 96: 1387-1393

[35] YangWS, KoJ, KimE, et al. . 21-O-Angeloyltheasapogenol E3, a novel triterpenoid saponin from the seeds of tea plants, inhibits macrophage-mediated inflammatory responses in a NF-κB-dependent manner. Mediat Inflamm, 2014, 2014: 1-9

[36] YuX, HeY. Tea saponins: effective natural surfactants beneficial for soil remediation, from preparation to application. RSC Adv, 2018, 8: 24312-24321

[37] YuZ, WuX, HeJ. Study on the antifungal activity and mechanism of tea saponin from Camellia oleifera cake. Eur Food Res Technol, 2022, 248: 783-795

[38] YuW, ZhongH, FangX, DuM. Physicochemical properties and antioxidant potential of protein isolate from camellia cake (Camellia Oleifera Abel.): effect of different processing techniques on industrial scale. LWT, 2023, 184: 114993

[39] ZhangX, St. LegerRJ, FangW. Stress-induced pyruvate accumulation contributes to cross protection in a fungus. Environ Microbiol, 2018, 20: 1158-1169

[40] ZhaoW, LiN, ZhangX, et al. . Cancer chemopreventive theasaponin derivatives from the total tea seed saponin of Camellia sinensis. J Funct Foods, 2015, 12: 192-198

[41] ZhaoY, SuR, ZhangW, et al. . Antibacterial activity of tea saponin from Camellia Oleifera shell by novel extraction method. Ind Crop Prod, 2020, 153: 112604

[42] ZhengM, MaoP, TianX, et al. . Effects of dietary supplementation of alfalfa meal on growth performance, carcass characteristics, meat and egg quality, and intestinal microbiota in Beijing-you chicken. Poult Sci, 2019, 98: 2250-2259

Funding

Key Research and Development Program of Hunan Province of China(2023NK2034)

Hunan Province Forestry Science and Technology Innovation Foundation(XLK202445)

Program for Science & Technology Innovation Talents of Hunan Province(2019TP1029)