Skip to main content
SpringerLink
Log in

Techno-functionality of fisetin-enriched yoghurt fermented with Lactobacillus acidophilus bio-capsules produced via osmoporation

  • Short Communication
  • Published:
Systems Microbiology and Biomanufacturing Aims and scope Submit manuscript

Abstract

Osmoporation is a novel encapsulation approach for bioactive compounds based on the osmoresistance mechanisms of microbial cells. To the best of our knowledge, this is the first study investigating the production of fisetin-enriched yoghurt using Lactobacillus acidophilus-based bio-capsules via osmoporation as the starter culture. Results showed that the milk acidification with fisetin-loaded L. acidophilus progressed at a slower pace due to complex mechanisms induced by osmoporation and internalized fisetin. Milk fermentation using fisetin bio-capsules reached a maximum acidification rate of 0.18 pH units/h after 23 h and pH 4.6 was achieved after 32 h. Besides, the antioxidant activity of yoghurts produced with fisetin bio-capsules did not change during cold storage, while the antioxidant activity of yoghurt produced with non-encapsulated fisetin was reduced by 2.5-fold after 28 days. Overall, this study shows that fisetin osmoporation using L. acidophilus is a versatile encapsulation bioprocess that enables the delivery of preserved phytoactives into fermented foods like yoghurt. This strategy has the potential to be extended to other applications in the dairy industry using lactic acid bacteria as both the encapsulation matrix and fermentation agent.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Availability of data and materials

All data generated or analyzed during this study are included in this manuscript.

Code availability

Not applicable.

References

  1. Chen J, Hu L. Nanoscale delivery system for nutraceuticals: preparation, application, characterization, safety, and future trends. Food Eng Rev. 2020;12:14–31. https://doi.org/10.1007/s12393-019-09208-w.

    Article  CAS  Google Scholar 

  2. Delfanian M, Sahari MA. Improving functionality, bioavailability, nutraceutical and sensory attributes of fortified foods using phenolics-loaded nanocarriers as natural ingredients. Food Res Int. 2020;137: 109555. https://doi.org/10.1016/j.foodres.2020.109555.

    Article  CAS  PubMed  Google Scholar 

  3. Yadav K, Bajaj RK, Mandal S, Saha P, Mann B. Evaluation of total phenol content and antioxidant properties of encapsulated grape seed extract in yoghurt. Int J Dairy Technol. 2018;71:96–104. https://doi.org/10.1111/1471-0307.12464.

    Article  CAS  Google Scholar 

  4. Iqbal R, Mehmood Z, Baig A, Khalid N. Formulation and characterization of food grade O/W nanoemulsions encapsulating quercetin and curcumin: insights on enhancing solubility characteristics. Food Bioprod Process. 2020;123:304–11. https://doi.org/10.1016/j.fbp.2020.07.013.

    Article  CAS  Google Scholar 

  5. Akgün D, Gültekin-Özgüven M, Yücetepe A, Altin G, Gibis M, Weiss J, Özçelik B. Stirred-type yoghurt incorporated with sour cherry extract in chitosan-coated liposomes. Food Hydrocolloids. 2020;101: 105532. https://doi.org/10.1016/j.foodhyd.2019.105532.

    Article  CAS  Google Scholar 

  6. Tavakoli H, Hosseini O, Jafari SM, Katouzian I. Evaluation of physicochemical and antioxidant properties of yogurt enriched by olive leaf phenolics within nanoliposomes. J Agric Food Chem. 2018;66:9231–40. https://doi.org/10.1021/acs.jafc.8b02759.

    Article  CAS  PubMed  Google Scholar 

  7. Dadkhodazade E, Mohammadi A, Shojaee-Aliabadi S, Mortazavian AM, Mirmoghtadaie L, Hosseini SM. Yeast cell microcapsules as a novel carrier for cholecalciferol encapsulation: development, characterization and release properties. Food Biophys. 2018;13:404–11. https://doi.org/10.1007/s11483-018-9546-3.

    Article  Google Scholar 

  8. Young S, Rai R, Nitin N. Bioaccessibility of curcumin encapsulated in yeast cells and yeast cell wall particles. Food Chem. 2020;309: 125700. https://doi.org/10.1016/j.foodchem.2019.125700.

    Article  CAS  PubMed  Google Scholar 

  9. Rubio FTV, Maciel GM, da Silva MV, Corrêa VG, Peralta RM, Haminiuk CWI. Enrichment of waste yeast with bioactive compounds from grape pomace as an innovative and emerging technology: kinetics, isotherms and bioaccessibility. Innov Food Sci Emerg Technol. 2018;45:18–28. https://doi.org/10.1016/j.ifset.2017.09.004.

    Article  CAS  Google Scholar 

  10. Young S, Dea S, Nitin N. Vacuum facilitated infusion of bioactives into yeast microcarriers: evaluation of a novel encapsulation approach. Food Res Int. 2017;100:100–12. https://doi.org/10.1016/j.foodres.2017.07.067.

    Article  CAS  PubMed  Google Scholar 

  11. Dupont S, Beney L, Ritt JF, Lherminier J, Gervais P. Lateral reorganization of plasma membrane is involved in the yeast resistance to severe dehydration. Biochim Biophys Acta Biomembr. 2010;1798:975–85. https://doi.org/10.1016/j.bbamem.2010.01.015.

    Article  CAS  Google Scholar 

  12. da Silva Pedrini MR, Dupont S, de Anchieta CA, Beney L, Gervais P. Osmoporation: a simple way to internalize hydrophilic molecules into yeast. Appl Microbiol Biotechnol. 2014;98:1271–80. https://doi.org/10.1007/s00253-013-5386-8.

    Article  CAS  PubMed  Google Scholar 

  13. Medeiros FGM, Correia RTP, Dupont S, Beney L, Pedrini MRS. Curcumin and fisetin internalization into Saccharomyces cerevisiae cells via osmoporation: impact of multiple osmotic treatments on the process efficiency. Lett Appl Microbiol. 2018;67:363–9. https://doi.org/10.1111/lam.13045.

    Article  CAS  PubMed  Google Scholar 

  14. Medeiros FGM, Dupont S, Beney L, Roudaut G, Hoskin RT, da Silva Pedrini MR. Efficient stabilisation of curcumin microencapsulated into yeast cells via osmoporation. Appl Microbiol Biotechnol. 2019;103:9659–72. https://doi.org/10.1007/s00253-019-10196-4.

    Article  CAS  PubMed  Google Scholar 

  15. Câmara AA Jr, Dupont S, Beney L, Gervais P, Rosenthal A, Correia RTP, da Silva Pedrini MR. Fisetin yeast-based bio-capsules via osmoporation: effects of process variables on the encapsulation efficiency and internalized fisetin content. Appl Microbiol Biotechnol. 2016;100:5547–58. https://doi.org/10.1007/s00253-016-7425-8.

    Article  CAS  PubMed  Google Scholar 

  16. de Andrade EWV, Dupont S, Beney L, Hoskin RT, da Silva Pedrini MR. Osmoporation is a versatile technique to encapsulate fisetin using the probiotic bacteria Lactobacillus acidophilus. Appl Microbiol Biotechnol. 2022;106:1031–44. https://doi.org/10.1007/s00253-021-11735-8.

    Article  CAS  PubMed  Google Scholar 

  17. Ozogul F, Yazgan H, Ozogul Y. Lactic acid bacteria: Lactobacillus acidophilus. In: McSweeney PLH, McNamara JP, editors. Encyclopedia of Dairy sciences. 3rd ed. Amsterdam: Academic Press; 2022. p. 187–97.

    Chapter  Google Scholar 

  18. Jafarei P, Ebrahimi MT. Lactobacillus acidophilus cell structure and application. Afr J Microbiol Res. 2011;5:4033–42. https://doi.org/10.5897/AJMR11.630.

    Article  CAS  Google Scholar 

  19. Wang Y, Corrieu G, Béal C. Fermentation pH and temperature influence the cryotolerance of Lactobacillus acidophilus RD758. J Dairy Sci. 2005;88:21–9. https://doi.org/10.3168/jds.S0022-0302(05)72658-8.

    Article  CAS  PubMed  Google Scholar 

  20. Hussain T, Al-Attas OS, Alamery S, Ahmed M, Odeibat HAM, Alrokayan S. The plant flavonoid, fisetin alleviates cigarette smoke-induced oxidative stress, and inflammation in Wistar rat lungs. J Food Biochem. 2019;43: e12962. https://doi.org/10.1111/jfbc.12962.

    Article  CAS  PubMed  Google Scholar 

  21. Turkmen N, Akal C, Özer B. Probiotic dairy-based beverages: a review. J Funct Foods. 2018;2019(53):62–75. https://doi.org/10.1016/j.jff.2018.12.004.

    Article  CAS  Google Scholar 

  22. Nyanzi R, Jooste PJ, Buys EM. Invited review: probiotic yogurt quality criteria, regulatory framework, clinical evidence, and analytical aspects. J Dairy Sci. 2021;104:1–19. https://doi.org/10.3168/jds.2020-19116.

    Article  CAS  PubMed  Google Scholar 

  23. Bezerra MF, Souza DFS, Correia RTP. Acidification kinetics, physicochemical properties and sensory attributes of yoghurts prepared from mixtures of goat and buffalo milks. Int J Dairy Technol. 2012;65:437–43. https://doi.org/10.1111/j.1471-0307.2012.00845.x.

    Article  CAS  Google Scholar 

  24. Abdel-Hamid M, Romeih E, Huang Z, Enomoto T, Huang L, Li L. Bioactive properties of probiotic set-yogurt supplemented with Siraitia grosvenorii fruit extract. Food Chem. 2020;303: 125400. https://doi.org/10.1016/j.foodchem.2019.125400.

    Article  CAS  PubMed  Google Scholar 

  25. Duarte-Almeida JM, dos Santos RJ, Genovese MI, Lajolo FM. Avaliação da atividade antioxidante utilizando sistema beta-caroteno/ácido linoléico e método de seqüestro de radicais DPPH•. Ciência e Tecnol Aliment. 2006;26:446–52. https://doi.org/10.1590/S0101-20612006000200031.

    Article  CAS  Google Scholar 

  26. Meneghel J, Passot S, Dupont S, Fonseca F. Biophysical characterization of the Lactobacillus delbrueckii subsp. bulgaricus membrane during cold and osmotic stress and its relevance for cryopreservation. Appl Microbiol Biotechnol. 2017;101:1427–41. https://doi.org/10.1007/s00253-016-7935-4.

    Article  CAS  PubMed  Google Scholar 

  27. Corrieu G, Béal C. Yogurt: the product and its manufacture. In: Caballero B, Finglas PM, Toldrá F, editors. Encyclopedia of food and health. 1st ed. Amsterdam: Academic Press; 2016. p. 617–24.

    Chapter  Google Scholar 

  28. Kawabata K, Sugiyama Y, Sakano T, Ohigashi H. Flavonols enhanced production of anti-inflammatory substance(s) by Bifidobacterium adolescentis: prebiotic actions of galangin, quercetin, and fisetin. BioFactors. 2013;39:422–9. https://doi.org/10.1002/biof.1081.

    Article  CAS  PubMed  Google Scholar 

  29. Rubio FTV, Haminiuk CWI, dos Santos MM, Thomazini M, Moraes ICF, Martelli-Tosi M, Fávaro-Trindade CS. Development of natural pigments microencapsulated in waste yeast Saccharomyces cerevisiae using spray drying technology and their application in yogurt. Food Funct. 2021;12:8946–59. https://doi.org/10.1039/D1FO00708D.

    Article  CAS  PubMed  Google Scholar 

  30. Taha S, El Abd M, De Gobba C, Abdel-Hamid M, Khalil E, Hassan D. Antioxidant and antibacterial activities of bioactive peptides in buffalo’s yoghurt fermented with different starter cultures. Food Sci Biotechnol. 2017;26:1325–32. https://doi.org/10.1007/s10068-017-0160-9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Wang J, Zhao X-H. Degradation kinetics of fisetin and quercetin in solutions affected by medium pH, temperature and co-existed proteins. J Serbian Chem Soc. 2016;81:243–53. https://doi.org/10.2298/JSC150706092W.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors are grateful to the Federal University of Rio Grande do Norte (UFRN) and the Department of Chemical Engineering (DEQ/UFRN) for technical support.

Funding

E.W.V.A. was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES). E.S.S. was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).

Author information

Authors and Affiliations

  1. Bioprocess Laboratory, Chemical Engineering Department, Universidade Federal do Rio Grande do Norte, Lagoa Nova, Natal, RN, 59078-900, Brazil

    Eduardo Wagner Vasconcelos de Andrade & Márcia Regina da Silva Pedrini

  2. Laboratory of Bioactive Compounds, Chemical Engineering Department, Universidade Federal do Rio Grande do Norte, Lagoa Nova, Natal, RN, 59078-900, Brazil

    Eduardo Wagner Vasconcelos de Andrade, Edilene Souza da Silva & Roberta Targino Hoskin

  3. UMR Procédés Alimentaires et Microbiologiques (PAM, UMR A 02.102), Univ. Bourgogne Franche-Comté, AgroSup Dijon, 21000, Dijon, France

    Sebastien Dupont & Laurent Beney

Authors
  1. Eduardo Wagner Vasconcelos de Andrade
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sebastien Dupont
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Laurent Beney
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Edilene Souza da Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Roberta Targino Hoskin
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Márcia Regina da Silva Pedrini
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

EWVA: conceptualization, methodology, investigation, formal analysis, writing (draft and review), and visualization. ESS: methodology. SD and LB: writing (review). RTH and MRSP: conceptualization, methodology, resources, supervision, and writing (draft and review). All authors read and approved the manuscript.

Corresponding author

Correspondence to Márcia Regina da Silva Pedrini.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethics approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Andrade, E.W.V., Dupont, S., Beney, L. et al. Techno-functionality of fisetin-enriched yoghurt fermented with Lactobacillus acidophilus bio-capsules produced via osmoporation. Syst Microbiol and Biomanuf 2, 743–749 (2022). https://doi.org/10.1007/s43393-022-00100-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s43393-022-00100-z

Keywords

Search

Navigation