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Impact of a novel probiotic Lactobacillus strain isolated from the bee gut on GABA content, antioxidant activity, and potential cytotoxic activity against HT-29 cell line of rice bran

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Abstract

Rice bran was fermented with Lactobacillus apis, isolated from the bee gut as a novel probiotic strain, and Saccharomyces cerevisiae to investigate the relationship between its metabolites and antioxidant activity, nutraceutical value, and cytotoxic activity against the HT-29 cell line. The findings showed that L. apis improved the antioxidant activity (DPPH of 37.73%) and antioxidant capacity (ABTS of 37.62 mg Trolox/g,), as well as, hydroxyl radical-scavenging activity (91.55%) of rice bran compared to S. cerevisiae. The metabolic analysis of volatile compounds revealed an increase of alcohols and lactones in the samples fermented with S. cerevisiae. While the samples fermented with L. apis displayed an increase of ketones, esters, and thiazoles. On the other hand, L. apis and S. cerevisiae exhibited a significant ability to increase γ-aminobutyric acid during different fermentation times. Compared with non-fermented samples (18.54%), L. apis increased the cytotoxic activity of rice bran against the HT-29 cell line to 34.17%, and S. cerevisiae to 31.34%. These results suggest that the fermentation of rice bran with S. cerevisiae and L. apis provides a promising strategy to improve the antioxidant activity and nutraceuticals of rice bran, and a potential source for plant-based pharmaceutical products.

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Abbreviations

ABTS:

2,2'-Azino-bis(3-ethylbenzothiazoline-6-sulfonate)

DPPH:

2,2-Diphenyl-1-picrylhydrazyl; di(phenyl)-(2,4,6-trinitrophenyl) iminoazanium)

Trolox:

6-Hydroxy-2,5,7,8-tetramethylchroman-2-carboxylic acid

TPC:

Total phenolic content

HPLC:

High performance liquid chromatography

LC–MS:

Liquid chromatography–mass spectrometry

SPME/GC–MS:

Solid-phase microextraction/ gas chromatography-mass spectrometry

HT-29:

Human colorectal adenocarcinoma cell line with epithelial morphology

PCA:

Principal component analysis

VC:

L-ascorbic acid

VB2:

Vitamin B2 (Riboflavin)

VB6:

Vitamin B6 (Pyridoxine)

References

  • Adnan M, Siddiqui AJ, Hamadou WS, Ashraf SA, Hassan MI, Snoussi M, Badraoui R, Jamal A, Bardakci F, Awadelkareem AM (2021) Functional and structural characterization of Pediococcus pentosaceus-derived biosurfactant and its biomedical potential against bacterial adhesion, quorum sensing, and biofilm formation. Antibiotics 10(11):1371

    Article  CAS  Google Scholar 

  • Al-Maqtari QA, Mahdi AA, Al-Ansi W, Mohammed JK, Wei M, Yao W (2021) Evaluation of bioactive compounds and antibacterial activity of Pulicaria jaubertii extract obtained by supercritical and conventional methods. J Food Meas Charact 15(1):449–456

    Article  Google Scholar 

  • Aoki N, Yanli Z, Kanda S, Kurokawa Y, Sultana H, Itabashi H (2021) Effect of Saccharomyces cerevisiae fermentation product on ruminal fermentation, blood metabolites, and milk production in dairy cows. Jpn Agric Res Quart JARQ 55(3):265–271

    Article  CAS  Google Scholar 

  • Ashraf SA, Elkhalifa AEO, Ahmad MF, Patel M, Adnan M and Sulieman AME (2022) Probiotic fermented foods and health promotion, african fermented food products-new trends. pp 59–88. Springer

  • Bhosale S, Vijayalakshmi D (2015) Processing and nutritional composition of rice bran. Curr Res Nutr Food Sci 3(1):74–80

    Article  Google Scholar 

  • Chaiyasut C, Pengkumsri N, Sirilun S, Peerajan S, Khongtan S, Sivamaruthi BS (2017) Assessment of changes in the content of anthocyanins, phenolic acids, and antioxidant property of Saccharomyces cerevisiae mediated fermented black rice bran. AMB Express 7(1):1–11

    Article  CAS  Google Scholar 

  • Costa SL, Silva VDA, dos Santos SC, Santos CC, Paris I, Muñoz P, Segura-Aguilar J (2016) Impact of plant-derived flavonoids on neurodegenerative diseases. Neurotox Res 30(1):41–52

    Article  CAS  Google Scholar 

  • Cho S-J (2020) Changes in the antioxidant properties of rice bran protein isolate upon simulated gastrointestinal digestion. LWT 126:109206

    Article  CAS  Google Scholar 

  • Christ-Ribeiro A, Chiattoni LM, Mafaldo CRF, Badiale-Furlong E, de Souza-Soares LA (2021) Fermented rice-bran by Saccharomyces cerevisiae: Nutritious ingredient in the formulation of gluten-free cookies. Food Biosci 40:100859

    Article  CAS  Google Scholar 

  • Cui Y, Miao K, Niyaphorn S, Qu X (2020) Production of gamma-aminobutyric acid from lactic acid bacteria: a systematic review. Int J Mol Sci 21(3):995

    Article  CAS  Google Scholar 

  • Fairbairn S, McKinnon A, Musarurwa HT, Ferreira AC, Bauer FF (2017) The impact of single amino acids on growth and volatile aroma production by Saccharomyces cerevisiae strains. Front Microbiol 8:2554

    Article  Google Scholar 

  • Folashade BI, Gani H-SM, Kharidah M (2019) Optimisation of important processing conditions for rice bran sourdough fermentation using Lactobacillus plantarum. Foods Raw Mater 7(1):131–142

    Google Scholar 

  • Garofalo C, Sabbatini R, Zamporlini F, Minazzato G, Ferrocino I, Aquilanti L, Raffaelli N, Osimani A (2021) Exploratory study on the occurrence and dynamics of yeast-mediated nicotinamide riboside production in craft beers. LWT 147:111605

    Article  CAS  Google Scholar 

  • Ghamry M, Li L and Zhao W (2021) A metabolomics comparison of Lactobacillus communities isolated from breast milk and camel milk and Lactobacillus apis isolated from bee gut during cereals-based fermentation vs. Lactobacillus plantarum as a reference. LWT, p 111400

  • Ju EM, Lee SE, Hwang HJ, Kim JH (2004) Antioxidant and anticancer activity of extract from Betula platyphylla var japonica. Life Sci 74(8):1013–1026

    Article  CAS  Google Scholar 

  • Kang C-H, Kim J-S, Park HM, Kim S, Paek N-S (2021) Antioxidant activity and short-chain fatty acid production of lactic acid bacteria isolated from Korean individuals and fermented foods. Biotech 11(5):1–8

    Google Scholar 

  • Kim B, Cho BR, Hahn JS (2014) Metabolic engineering of Saccharomyces cerevisiae for the production of 2-phenylethanol via Ehrlich pathway. Biotechnol Bioeng 111(1):115–124

    Article  CAS  Google Scholar 

  • Lai L-R, Hsieh S-C, Huang H-Y, Chou C-C (2013) Effect of lactic fermentation on the total phenolic, saponin and phytic acid contents as well as anti-colon cancer cell proliferation activity of soymilk. J Biosci Bioeng 115:552–556

    Article  CAS  Google Scholar 

  • Lee SK, Kim HJ, Chi SG, Jang JY, Nam KD, Kim NH, Joo KR, Dong SH, Kim BH, Chang YW (2005) Saccharomyces boulardii activates expression of peroxisome proliferator-activated receptor-gamma in HT-29 cells. Korean J Gastroenterol= Taehan Sohwagi Hakhoe Chi 45(5):328–334

    PubMed  Google Scholar 

  • Li Y, Wang T, Li S, Yin P, Sheng H, Wang T, Zhang Y, Zhang K, Wang Q, Lu S (2021) Influence of GABA-producing yeasts on cheese quality, GABA content, and the volatilome. LWT 154:112766

    Article  Google Scholar 

  • Liu N, Qin L, Lu X, Zhao Y, Miao S (2021) Physicochemical components and flavor properties of acid rice soup (rice-acid) fermented with Lactobacillus paracasei and/or Kluyveromyces marxianus. Food Biosci 43:101278

    Article  CAS  Google Scholar 

  • Nisa K, Rosyida V, Nurhayati S, Indrianingsih A, Darsih C and Apriyana W (2019) Total phenolic contents and antioxidant activity of rice bran fermented with lactic acid bacteria, In: IOP Conference Series: Earth and Environmental Science (Vol 251, No. 1, p 012020). IOP Publishing.

  • Plessas S, Nouska C, Karapetsas A, Kazakos S, Alexopoulos A, Mantzourani I, Chondrou P, Fournomiti M, Galanis A, Bezirtzoglou E (2017) Isolation, characterization and evaluation of the probiotic potential of a novel Lactobacillus strain isolated from Feta-type cheese. Food Chem 226:102–108

    Article  CAS  Google Scholar 

  • Punia S, Sandhu KS, Grasso S, Singh Purewal S, Kaur M, Kumar Siroha A, Kumar K, Kumar V, Kumar M (2021) Aspergillus oryzae Fermented rice bran: a byproduct with enhanced bioactive compounds and antioxidant potential. Foods 10(1):70

    Article  CAS  Google Scholar 

  • Rui-Peng Y, Li-Ping W, Chen-Kai Z, Sheng-Fang W, Qi-Jun S (2020) Determination of volatile metabolites in Microcystis Aeruginosa using headspace-solid phase microextraction arrow combined with gas chromatography-mass spectrometry. Chin J Anal Chem 48(6):750–756

    Article  Google Scholar 

  • Tiptiri-Kourpeti A, Spyridopoulou K, Santarmaki V, Aindelis G, Tompoulidou E, Lamprianidou EE, Saxami G, Ypsilantis P, Lampri ES, Simopoulos C (2016) Lactobacillus casei exerts anti-proliferative effects accompanied by apoptotic cell death and up-regulation of TRAIL in colon carcinoma cells. PLoS ONE 11(2):e0147960

    Article  Google Scholar 

  • Vaitkeviciene R, Zadeike D, Gaizauskaite Z, Valentaviciute K, Marksa M, Mazdzieriene R, Bartkiene E, Lele V, Juodeikiene G, Jakstas V (2021) Functionalisation of rice bran assisted by ultrasonication and fermentation for the production of rice bran–lingonberry pulp-based probiotic nutraceutical. Int J Food Sci Technol 57(3):1462–1472

    Article  Google Scholar 

  • Wang M, Lei M, Samina N, Chen L, Liu C, Yin T, Yan X, Wu C, He H, Yi C (2020) Impact of Lactobacillus plantarum 423 fermentation on the antioxidant activity and flavor properties of rice bran and wheat bran. Food Chem 330:127156

    Article  CAS  Google Scholar 

  • Xu Y, Jin Y, Su J, Yang N, Xu X, Jin Z, Cui B, Wu F (2021) Changes in the nutritional value, flavor, and antioxidant activity of brown glutinous rice during fermentation. Food Biosci 43:101273

    Article  CAS  Google Scholar 

  • Yang X, Hu W, Xiu Z, Jiang A, Yang X, Ji Y, Guan Y, Feng K (2020) Microbial dynamics and volatilome profiles during the fermentation of Chinese northeast sauerkraut by Leuconostoc mesenteroides ORC 2 and Lactobacillus plantarum HBUAS 51041 under different salt concentrations. Food Res Int 130:108926

    Article  CAS  Google Scholar 

  • Yoon HJ, Lee KA, Lee JH, Jin HJ, Kim HJ, Kim KT, Paik HD (2015) Effect of fermentation by Bacillus subtilis on antioxidant and cytotoxic activities of black rice bran. Int J Food Sci Technol 50(3):612–618

    Article  CAS  Google Scholar 

  • Yu Y, Zhang J, Wang J, Sun B (2019) The anti-cancer activity and potential clinical application of rice bran extracts and fermentation products. RSC Adv 9(31):18060–18069

    Article  CAS  Google Scholar 

  • Zafra-Gómez A, Garballo A, Morales JC, García-Ayuso LE (2006) Simultaneous determination of eight water-soluble vitamins in supplemented foods by liquid chromatography. J Agric Food Chem 54(13):4531–4536

    Article  Google Scholar 

  • Zhu Y-Y, Thakur K, Feng J-Y, Cai J-S, Zhang J-G, Hu F, Wei Z-J (2020) B-vitamin enriched fermented soymilk: A novel strategy for soy-based functional foods development. Trends Food Sci Technol 105:43–55

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Key Research and Development Program of China (No. 2017YFC1601704), the National Natural Science Foundation of China (No. 1522044, 31671909 and 31772034), the Program of the Jiangsu Key Laboratory of Advanced Food Manufacturing Equipment & Technology (No. FMZ201904), the National First-Class Discipline Program of Food Science and Technology (No. JUFSTR20180205) to W.Z.

Funding

This work was supported by the National Key Research and Development Program of China (No. 2017YFC1601704), the National Natural Science Foundation of China (No. 1522044, 31671909 and 31772034), the Program of the Jiangsu Key Laboratory of Advanced Food Manufacturing Equipment and Technology (No. FMZ201904), the National First-Class Discipline Program of Food Science and Technology (No. JUFSTR20180205) to W.Z.

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Authors and Affiliations

  1. State Key Laboratory of Food Science and Technology, School of Food Science and Technology, Jiangnan University, Wuxi, 214122, Jiangsu, China

    Mohamed Ghamry, Ahmed Fathy Ghazal, Qais Ali Al-Maqtqri, Li Li & Wei Zhao

  2. Food Technology Department, Faculty of Agriculture, Benha University, Moshtohor, 13736, Egypt

    Mohamed Ghamry

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  1. Mohamed Ghamry
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  2. Ahmed Fathy Ghazal
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  3. Qais Ali Al-Maqtqri
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  4. Li Li
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  5. Wei Zhao
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Contributions

Conception and design of study: MG, LL, WZ. Acquisition of data: MG, LL, AFG, QAA-M. Analysis and/or interpretation of data: MG, LL. Drafting the manuscript: MG, LL. Revising the manuscript critically for important intellectual content: LL, WZ. Approval of the version of the manuscript to be published: MG, LL, WZ, AFG, QAA-M. The supervision: WZ.

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Correspondence to Li Li or Wei Zhao.

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Ghamry, M., Ghazal, A.F., Al-Maqtqri, Q.A. et al. Impact of a novel probiotic Lactobacillus strain isolated from the bee gut on GABA content, antioxidant activity, and potential cytotoxic activity against HT-29 cell line of rice bran. J Food Sci Technol 59, 3031–3042 (2022). https://doi.org/10.1007/s13197-022-05512-2

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