Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Effects of Probiotic Fermented Fruit Juice-Based Biotransformation by Lactic Acid Bacteria and Saccharomyces boulardii CNCM I-745 on Anti-Salmonella and Antioxidative Properties

  • Laosee, Wanida (Functional Food and Nutrition Program, Faculty of Agro-Industry, Prince of Songkla University) ;
  • Kantachote, Duangporn (Department of Microbiology, Faculty of Science, Prince of Songkla University) ;
  • Chansuwan, Worrapanit (Center of Excellence in Functional Foods and Gastronomy, Prince of Songkla University) ;
  • Sirinupong, Nualpun (Center of Excellence in Functional Foods and Gastronomy, Prince of Songkla University)
  • Received : 2022.06.10
  • Accepted : 2022.09.13
  • Published : 2022.10.28
Download PDF
⟨ Previous Next ⟩

Abstract

Fermentation is an effective process for providing various beneficial effects in functional beverages. Lactic acid bacteria and yeast fermentation-based biotransformation contribute to enhancement of nutritional value and digestibility, including lactose intolerance reduction and control of infections. In this study, the probiotic fermented fruit juice (PFJ) was produced by Lactobacillus plantarum TISTR 1465, Lactobacillus salivarius TISTR 1112, and Saccharomyces boulardii CNCM I-745 while mixed fruit juice (MFJ) was used as the basic medium for microorganism growth. The potential function, the anti-salmonella activity of PFJ, was found to be effective at 250 mg/ml of MIC and 500 mg/ml of MBC. Biofilm inhibition was performed using the PFJ samples and showed at least 70% reduction in cell attachment at the MIC concentration of Salmonella Typhi DMST 22842. The antioxidant activities of PFJ were determined and the results revealed that FSB.25 exhibited 78.40 ± 0.51 mM TE/ml by FRAP assay, while FPSB.25 exhibited 3.44 ± 0.10 mM TE/ml by DPPH assay. The volatile compounds of PFJ were characterized by GC-MS, which identified alcohol, aldehyde, acid, ester, ketone, phenol, and terpene. The most abundant organic acid and alcohol detected in PFJ were acetic acid and 2-phenylethanol, and the most represented terpene was β-damascenone. The sensory attributes showed scores higher than 7 on a 9-point hedonic scale for the FPB.25, illustrating that it was well accepted by panelists. Taken together, our results showed that PFJ could meet current consumer demand regarding natural and functional, fruit-based fermented beverages.

Keywords

Acknowledgement

This work was supported by the National Research Council of Thailand (649/2563) and the scholarship fund from the Center of Excellence in Functional Foods and Gastronomy, Prince of Songkla University, Hat Yai, Songkhla 90112, Thailand. Salmonella Typhi DMST 22842 was donated from Asst. Prof. Dr. Narumol Thongwai of Chiang Mai University, Thailand.

References

  1. Ray RC and Sivakumar PS. 2009. Traditional and novel fermented foods and beverages from tropical root and tuber crops: review. Int. J. Food Sci. Technol. 44: 1073-1087. https://doi.org/10.1111/j.1365-2621.2009.01933.x
  2. Yunita D, and Dodd CER. 2018. Microbial community dynamics of a blue-veined raw milk cheese from the United Kingdom. J. Dairy Sci. 101: 4923-4935. https://doi.org/10.3168/jds.2017-14104
  3. Kakisu E, Abraham AG, Farinati CT, Ibarra C, and De Antoni GL. 2013. Lactobacillus plantarum isolated from kefir protects vero cells from cytotoxicity by type-II shiga toxin from Escherichia coli O157:H7. J. Dairy Res. 80: 64-71. https://doi.org/10.1017/S0022029912000659
  4. Marsh AJ, Hill C, Ross RP, and Cotter PD. 2014. Fermented beverages with health-promoting potential: past and future perspectives. Trends Food Sci. Technol. 38: 113-124. https://doi.org/10.1016/j.tifs.2014.05.002
  5. Van Kranenburg R, Kleerebezem M, Van Hylckama Vlieg J, Ursing BM, Boekhorst J, Smit B A, et al. 2002. Flavour formation from amino acids by lactic acid bacteria: predictions from genome sequence analysis. Int. Dairy J. 12: 111-121. https://doi.org/10.1016/S0958-6946(01)00132-7
  6. Cacho JF and Lopez R. 2005. Food and nutritional analysis alcoholic beverages. pp. 285-291., 2nd Ed. Encyclopedia of Analytical Sciences.
  7. Mugula JK, Narvhus JA, and Sorhaug T. 2003. Use of starter cultures of lactic acid bacteria and yeasts in the preparation of togwa, a Tanzanian fermented food. Int. J. Food Microbiol. 83: 307-318. https://doi.org/10.1016/S0168-1605(02)00386-0
  8. Mukisa IM, Byaruhanga YB, Muyanja CMBK, Langsrud T, and Narvhus JA. 2017. Production of organic flavor compounds by dominant lactic acid bacteria and yeasts from Obushera, a traditional sorghum malt fermented beverage. Food Sci. Nutr. 5: 702-712. https://doi.org/10.1002/fsn3.450
  9. De Albuquerque TMR, Garcia EF, De Oliveira Araujo A, Magnani M, Saarela M., and De Souza EL. 2018. In Vitro characterization of Lactobacillus strains isolated from fruit processing by-products as potential probiotics. Probiotics Antimicrob. Proteins 10: 704-716. https://doi.org/10.1007/s12602-017-9318-2
  10. Tripathi MK and Giri SK. 2014. Probiotic functional foods: survival of probiotics during processing and storage. J. Funct. Foods 9: 225-241. https://doi.org/10.1016/j.jff.2014.04.030
  11. Perricone M, Bevilacqua A, Altieri C, Sinigaglia M, Corbo MR. 2015. Challenges for the production of probiotic fruit juices. Beverages 1: 95-103. https://doi.org/10.3390/beverages1020095
  12. Laosee W, Kantachote D, Chansuwan W, Thongraung C, and Sirinupong N. 2021. Anti-salmonella potential and antioxidant activity of fermented fruit-based juice by lactic acid bacteria and its biotransformation. Funct. Foods Health Dis. 11: 368-384. https://doi.org/10.31989/ffhd.v11i8.813
  13. Roberts D, Reyes V, Bonilla F, Dzandu B, Liu C, Chouljenko A, and Sathivel S. 2018. Viability of Lactobacillus plantarum NCIMB 8826 in fermented apple juice under simulated gastric and intestinal conditions. LWT Food Sci. Technol. 97: 144-150. https://doi.org/10.1016/j.lwt.2018.06.036
  14. AOAC. 2005. Official Methods of Analysis. 18th ed. Association of Official Analytical Chemists, Washington, DC.
  15. Miller Gail Lorenz. 1959. Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal. Chem. 31: 426-428. https://doi.org/10.1021/ac60147a030
  16. Dubois M, Gilles KA, Hamilton JK, Rebers PA, and Smith F. 1956. Colorimetric method for determination of sugars and related substances. Anal. Chem. 28: 350-356. https://doi.org/10.1021/ac60111a017
  17. Li Z, Teng J, Lyu Y, Hu X, Zhao Y, and Wang M. 2019. Enhanced antioxidant activity for apple juice fermented with Lactobacillus plantarum ATCC14917. Molecules 24: 1-12.
  18. Jeong SY, Velmurugan P, Lim JM, Oh BT, Jeong DY. 2018. Photobiological (LED light)- mediated fermentation of blueberry (Vaccinium corymbosum L.) fruit with probiotic bacteria to yield bioactive compounds. LWT Food Sci. Technol. 93: 158-166. https://doi.org/10.1016/j.lwt.2018.03.038
  19. Hashemi SMB, Mousavi Khaneghah A, Barba FJ, Nemati Z, Sohrabi Shokofti S, and Alizadeh F. 2017. Fermented sweet lemon juice (Citrus limetta) using Lactobacillus plantarum LS5: chemical composition, antioxidant and antibacterial activities. J. Funct. Foods 38: 409-414. https://doi.org/10.1016/j.jff.2017.09.040
  20. Clinical and Laboratory Standards Institute (2012). Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically, approved standards (9th ed.). Wayne, PA: CLSI Document M07-A9.
  21. Schillaci D, Arizza V, Dayton T, Camarda L, Di Stefano V. 2008. In vitro anti-biofilm activity of Boswellia spp. oleogum resin essential oils. Lett. Appl. Microbiol. 47: 433-438. https://doi.org/10.1111/j.1472-765X.2008.02469.x
  22. Dall Asta C, Cirlini M., Morini E, and Galaverna G. 2011. Brand-dependent volatile fingerprinting of Italian wines from Valpolicella. J. Chromatogr. A 1218: 7557-7565. https://doi.org/10.1016/j.chroma.2011.08.042
  23. Stone H and Sidel JL. 2004. Sensory evaluation practices. Florida: Academic Press.
  24. FAO/WHO. 2002. Working group report on drafting guidelines for the evaluation of probiotics in food FAO/WHO, Ed. London, Ontario, Canada.
  25. Nout MJR and Sarkar PK. 1999. Lactic acid food fermentation in tropical climates. Antonie Van Leeuwenhoek 76: 395-401. https://doi.org/10.1023/A:1002066306013
  26. Marshall VM. 1987. Lactic acid bacteria: starters for flavour. FEMS Microbiol. Lett. 46: 327-336. https://doi.org/10.1111/j.1574-6968.1987.tb02469.x
  27. Rathore S, Salmeron I, and Pandiella SS. 2012. Production of potentially probiotic beverages using single and mixed cereal substrates fermented with lactic acid bacteria cultures. Food Microbiol. 30: 239-244. https://doi.org/10.1016/j.fm.2011.09.001
  28. Rakin M, Vukasinovic M, Siler-Marinkovic S, and Maksimovic M. 2007. Contribution of lactic acid fermentation to improved nutritive quality vegetable juices enriched with brewer's yeast autolysate. Food Chem. 100: 599-602. https://doi.org/10.1016/j.foodchem.2005.09.077
  29. Du Toit M, Engelbrecht L, Lerm E, and SKrieger-Weber, S. 2011. Lactobacillus: the next generation of malolactic fermentation starter cultures-an overview. Food Bioprocess Technol. 4: 876-906. https://doi.org/10.1007/s11947-010-0448-8
  30. Holzapfel WH, Haberer P, Geisen R, Bjorkroth J, and Schillinger U. 2001. Taxonomy and important features of probiotic microorganisms in food and nutrition. Am. J. Clin. Nutr. 73(2 suppl.): 365S-373S. https://doi.org/10.1093/ajcn/73.2.365s
  31. Siso MIG, Ramil E, Cerdan ME, and Freire-Picos M A. 1996. Respirofermentative metabolism in Kluyveromyces lactis: ethanol production and the Crabtree effect. Enzyme Microb. Technol. 18: 585-591. https://doi.org/10.1016/0141-0229(95)00151-4
  32. Ankolekar C, Johnson K, Pinto M, Johnson D, Labbe RG, Greene D, et al. 2012. Fermentation of whole apple juice using lactobacillus acidophilus for potential dietary management of hyperglycemia, hypertension, and modulation of beneficial bacterial responses. J. Food Biochem. 36: 718-738. https://doi.org/10.1111/j.1745-4514.2011.00596.x
  33. Vadivel V, Stuetz W, Scherbaum V, and Biesalski HK. 2011. Total free phenolic content and health relevant functionality of Indian wild legume grains: Effect of indigenous processing methods. J. Food Compos. Anal. 24: 935-943. https://doi.org/10.1016/j.jfca.2011.04.001
  34. Santos Filho AL dos, Freitas HV, Rodrigues S, Abreu VKG, Lemos T. de O, Gomes WF, et al. 2019. Production and stability of probiotic cocoa juice with sucralose as sugar substitute during refrigerated storage. LWT-Food Sci. Technol. 99: 371-378. https://doi.org/10.1016/j.lwt.2018.10.007
  35. Abbas CA. 2006. Production of Antioxidants, Aromas, Colours, Flavours, and Vitamins by Yeasts. pp. 285-334. In Yeasts in food and beverages. Berlin, Heidelberg: Springer.
  36. Chan MZA, Toh M, and Liu SQ. 2021. Growth, survival, and metabolic activities of probiotics Lactobacillus rhamnosus GG and Saccharomyces cerevisiae var. boulardii CNCM-I745 in fermented coffee brews. Int. J. Food Microbiol. 350: 109229. https://doi.org/10.1016/j.ijfoodmicro.2021.109229
  37. Zubaidah E, Dewantari FJ, Novitasari FR, Srianta I, and Blanc PJ. 2018. Potential of snake fruit (Salacca zalacca (Gaerth.) Voss) for the development of a beverage through fermentation with the Kombucha consortium. Biocatal. Agric. Biotechnol. 13: 198-203. https://doi.org/10.1016/j.bcab.2017.12.012
  38. Snijders JMA, Logtestijn JG Van, Mossel DAA, Smulderst FJM, Logtestijn JG Van, Mossel DAA, et al. 2011. Lactic acid as a decontaminant in slaughter and processing procedures Lactic acid as a decontaminant in slaughter and processing procedures. Vet. Q. 7: 277-283.
  39. Ge J, Sun Y, Xin X, Wang Y, and Ping W. 2016. Purification and partial characterization of a novel bacteriocin synthesized by Lactobacillus paracasei HD1-7 isolated from Chinese Sauerkraut juice. Sci. Rep. 6: 19366. https://doi.org/10.1038/srep19366
  40. Chen C, Lu Y, Yu H, Chen Z, and Tian H. 2019. Influence of 4 lactic acid bacteria on the flavor profile of fermented apple juice. Food Biosci. 27: 30-36. https://doi.org/10.1016/j.fbio.2018.11.006
  41. Fan W, Xu Y, and Han Y. 2011. Quantification of volatile compounds in Chinese ciders by stir bar sorptive extraction (SBSE) and gas chromatography-mass spectrometry (GC-MS). J. Inst. Brewing 117: 61-66. https://doi.org/10.1002/j.2050-0416.2011.tb00444.x
  42. Oliveira DR, Lopes ACA, Pereira RA, Cardoso PG, and Duarte WF. 2019. Selection of potentially probiotic Kluyveromyces lactis for the fermentation of cheese whey-based beverage. Annal. Microbiol. 69: 1361-1372. https://doi.org/10.1007/s13213-019-01518-y
  43. Derrick S, and Large PJ. 1993. Activities of the enzymes of the Ehrlich pathway and formation of branched-chain alcohols in Saccharomyces cerevisiae and Candida utilis grown in continuous culture on valine or ammonium as sole nitrogen source. J. General Microbiol. 139: 2783-2792. https://doi.org/10.1099/00221287-139-11-2783
  44. Liu SQ, and Pilone G J. 2000. An overview of formation and roles of acetaldehyde in winemaking with emphasis on microbiological implications. Int. J. Food Sci. Technol. 35: 49-61. https://doi.org/10.1046/j.1365-2621.2000.00341.x
  45. Li S, Chen C, Ji Y, Lin J, Chen X, and Qi B. 2018. Improvement of nutritional value, bioactivity and volatile constituents of quinoa seeds by fermentation with Lactobacillus casei. J. Cereal Sci. 84: 83-89. https://doi.org/10.1016/j.jcs.2018.10.008
  46. Waterhouse AL, Sacks GL, and Jeffery DW. 2016. Understanding Wine Chemistry. Understanding Wine Chemistry.
  47. Liu X, Deng J, Bi J, Wu X, and Zhang B. 2019. Cultivar classification of cloudy apple juices from substandard fruits in China based on aroma profile analyzed by HS-SPME/GC-MS. LWT-Food Sci. Technol. 102: 304-309. https://doi.org/10.1016/j.lwt.2018.12.043
  48. Melo Ramos S. de N, Danzl W, Ziegleder G, and Efraim P. 2016. Formation of volatile compounds during cupuassu fermentation: influence of pulp concentration. Food Res. Int. 87: 161-167. https://doi.org/10.1016/j.foodres.2016.06.025
  49. Ricci A, Cirlini M, Levante A, Dall'Asta C, Galaverna G and, Lazzi C. 2018. Volatile profile of elderberry juice: effect of lactic acid fermentation using L. plantarum, L. rhamnosus and L. casei strains. Food Res. Int. 105: 412-422. https://doi.org/10.1016/j.foodres.2017.11.042
  50. Gonzalez EA, Agrasar AT, Castro LMP, Fernandez IO, and Guerra NP. 2011. Solid-state fermentation of red raspberry (Rubus ideaus L.) and arbutus berry (Arbutus unedo, L.) and characterization of their distillates. Food Res. Int. 44: 1419-1426. https://doi.org/10.1016/j.foodres.2011.02.032