Skip to main content
Log in

Characterization of extracellular yeast peptide factors and their stress-protective effect on probiotic lactic acid bacteria

  • Experimental Articles
  • Published:
Microbiology Aims and scope Submit manuscript

Abstract

Protective effect of the extracellular peptide fraction (reactivating factors, RF) produced by yeasts of various taxonomic groups (Saccharomyces cerevisiae, Kluyveromyces lactis, Candida utilis, and Yarrowia lipolytica) on probiotic lactic acid bacteria (LAB) Lactobacillus casei, L. acidophilus, and L. reuteri under bile salt (BS)-induced stress was shown. RF of all yeasts were shown to be of peptide nature; the active component of the S. cerevisiae RF was identified as a combination of low-molecular polypeptides with molecular masses of 0.6 to 1.5 kDa. The protective and reactivating effects of the yeast factors were not species-specific and were similar to those of the Luteococcus japonicus subsp. casei RF. In BS-treated cells of the tester bacteria, a protective effect was observed after 10-min preincubation of the LAB cell suspension with yeast RF: the number of surviving cells (CFU) was 2 to 4.5 times higher than in the control. The reactivating effect was observed when RF was added to LAB cell suspensions not later than 15 min after stress treatment. It was less pronounced than the protector effect, with the CFU number 1 to 3 times that of the control. Both the protector and the reactivating effects were most pronounced in the S. cerevisiae and decreased in the row C. utilis > K. lactis > Y. lipolytica. The efficiency of protective action of yeast RF was found to depend on the properties of recipient LAB cells, with the L. casei strain being most sensitive to BS treatment. In both variants, the highest protective effect of RF (increase in the CFU number) was observed for L. acidophilus, while the least pronounced one was observed for L. casei. The reasons for application of the LAB strains combining high stress resistance and high response to stress-protecting metabolites, including RF factors, as probiotics, is discussed.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Arinbasarova, A.Yu., Biryukova, E.N., and Medentsev, A.G., Antistress systems of the yeast Yarrowia lipolytica, Appl. Biochem. Microbiol., 2015, vol. 51, no. 2, pp. 135–142.

    Article  CAS  Google Scholar 

  • Begley, M., Gaham, C.G.M., and Hill, C., The interaction between bacteria and bile, FEMS Microbiol. Rev., 2005, vol. 29, no. 4, pp. 625–651.

    Article  CAS  PubMed  Google Scholar 

  • El-Registan, G.I., Mulyukin, A.L., Nikolaev, Yu.A., Susina, N.E., Galchenko, V.F., and Duda, V.I., Adaptogenic functions of extracellular autoregulators of microorganisms, Microbiology (Moscow), 2006, vol. 75, no. 4, pp. 446–456.

    Article  CAS  Google Scholar 

  • Elkins, C.A., Moser, S.A., and Savage, D.C., Genes encoding bile salt hydrolases and conjugated bile salt transporters in Lactobacillus johnsonni 100-100 and other species, Microbiology (UK), 2001, vol. 147, no. 12, pp. 3403–3412.

    Article  CAS  Google Scholar 

  • Fagundes, C.T., Amaral, F.A., Teixeira, A.L., Souza, D.G., and Teixeira, M.M., Adapting to environmental stresses: the role of the microbiota in controlling innate immunity and behavioral responsiveness, Immunol. Rev., 2012, vol. 245, no. 1, pp. 250–264.

    Article  CAS  PubMed  Google Scholar 

  • Finegold, S.M., Gastrointestinal microbiology in the normal host, in Desk Encyclopedia of Microbiology, 2nd ed., Schaechter, M., Ed., San Diego: San Diego State Univ., 2009, pp. 552–572.

    Google Scholar 

  • Gonzales-Siso, M., Garcia-Leiro, A., Tarrio, N., and Cerdan, M., Sugar metabolism, redox balance and oxidative stress response in the respiratory yeast Kluyveromyces lactis, Microb. Cell Fact., 2009, vol. 8. publ. on-line 2009, Aug 30, p. 46.

    Article  Google Scholar 

  • Kummani, P., Satish, K.R., Yuvarai, N., Paari, K.A., Patukumar, V., and Arul, V., Probiotics and its functually valuable products—a review, Crit. Rev. Food Sci. Nutr., 2013, vol. 53, no. 6, pp. 641–658.

    Article  Google Scholar 

  • Kvasnikov, E.I. and Nesterenko, O.A., Molochnokislye bakterii i puti ikh ispol’zovaniya (Lactic Acid Bacteria and Pathways for Their Application), Moscow: Nauka, 1975.

    Google Scholar 

  • Lechner, S., Muller-Ladner, U., Schlotman, K., Jung, B., McClelland, M., Ruschoff, J., Websh, J., Scholmerich, J., and Kullmann, F., Bile acids mimic oxidative stress induced upregulation of thioredoxin reductase in colon cancer cell lines, Carcinogenesis, 2002, vol. 23, no. 8, pp. 1281–1288.

    Article  CAS  PubMed  Google Scholar 

  • Oleskin, A.V., El-Registan, G.I., and Shenderov, B.A., Intermicrobial chemical interactions and dialogue microbiota–host: role of neuromediators, Microbiology (Moscow), 2016, vol. 85, no. 1, pp. 58–64.

    Article  Google Scholar 

  • O’Mahony, S.M., Clarke, Y.E., Dianan, T.G., and Cryan, J.F., Serotonin, tryptophan metabolism and the brain-gut-microbiome axis, Behavioural Brain Res., 2014. http:dx.doi.org/10.1016/j.bbr.2014.07.027

    Google Scholar 

  • Moser, S.A. and Savage, D.C., Bile salt hydrolase activity and resistance to toxicity of conjugated bile salts are unrelated properties of Lactobacillus, Appl. Environ. Microbiol., 2001, vol. 67, no. 8, pp. 3470–3480.

    Article  Google Scholar 

  • Pennisi, E., Body’s hardworking microbes get some overdue respect, Science, 2010, vol. 330. Iss. 6011, p. 1619.

    Article  CAS  PubMed  Google Scholar 

  • Rowbury R.J., Cross-talk involving extracellular sensors and extracellular alarmones gives early warning to unstressed Escherichia coli of impeding lethal chemical stress and leads to induction of tolerance responses, J. Appl. Microbiol., 2001, vol. 90, pp. 677–695.

    Article  CAS  PubMed  Google Scholar 

  • Rowbury, R.J., UV-radiation-induced enterobacterial responses, other processes that influence UV-tolerance and likely environmental significance, Sci. Prog., 2003, vol. 86, no. 4, pp. 313–332.

    Article  PubMed  Google Scholar 

  • Saei, A.A. and Barzegari, A., The microbiome: the forgotten organ of the astronaut’s body-probiotics beyond terrestrial limits, Future Microbiol., 2012, vol. 7, pp. 1037–1046.

    Article  CAS  PubMed  Google Scholar 

  • Shenderov, B.A., Medical microbial ecology and functional nutrition, in Probiotiki i funktsional’noe pitanie (Probiotics and Functional Nutrition), Moscow: Grant, 2001, vol. 3, pp. 1–284.

    Google Scholar 

  • Shenderov, B.A., “Omic” technologies and thier role in modern preventive and restoratory medicine, Vestn. Vosstan. Med., 2012, no. 3 (490), pp. 70–78.

    Google Scholar 

  • Tkachenko, A.G., Molekulyarnye mekhanizmy stressornykh otvetov u mikroorganizmov (Molecular Mechanisms of Microbial Stress Response), Ekaterinburg: Ural. Tsentr Akadem. Issled., 2010.

    Google Scholar 

  • Vorob’eva, L.I., Khodzhaev, E.Yu., Ponomareva, G.M., and Bryukhanov, A.L., Extracellular protein metabolite of Luteococcus japonicus subsp. casei reactivates cells subjected to oxidative stress, Appl. Biochem. Microbiol., 2003, vol. 39, no. 2, pp. 178–182.

    Article  Google Scholar 

  • Vorobjeva, L.I., Khodzhaev, E.Yu., and Ponomareva, G.M., Cross-effects of extracellular factors of adaptation to stress in Luteococcus casei and Saccharomyces cerevisiae, Appl. Biochem. Microbiol., 2005, vol. 41, no. 2, pp. 150–153.

    Article  Google Scholar 

  • Vorobjeva, L.I., Khodzhaev, E.Yu., Mulyukin, A.L., and Toropygin, I.Yu., The mechanism of action of reactivating factor from Luteococcus japonicus subsp. casei, Appl. Biochem. Microbiol., 2009, vol. 45, no. 5, pp. 489–493.

    Article  Google Scholar 

  • Vorobjeva, L.I., Khodzhaev, E.Yu., and Vustin, M.M., Extracellular protein metabolite of Luteococcus japonicus subsp. casei reactivates cells subjected to oxidative stress, Appl. Biochem. Microbiol., 2011, vol. 47, no. 3, pp. 264–269.

    Article  Google Scholar 

  • Vorobjeva, L.I., Khodzhaev, E.Yu., Novikova, T.M., Mulyukin, A.L., Chudinova, E.M., Kozlova, A.N., and El’ Registan, G.I., Stress-protective and cross action of the extracellular reactivating factor of the microorganisms of the domains bacteria, archaea, and eukaryota, Microbiology (Moscow), 2013, vol. 82, no. 5, pp. 594–599.

    Article  Google Scholar 

  • Vorobjeva L.I., Khodzhaev E.Yu., Kharchenko N.V., Novikova T.M., Cherdyntseva T.A., Biological effect of extracellular peptide factor from Luteococcus japonicus subsp. casei on probiotic bacteria, Appl. Biochem. Microbiol., 2014, vol. 50, no. 4, pp. 346–352.

    Article  CAS  Google Scholar 

  • Vorobjeva, L.I., Rogozhin, E.A., Khodzhaev, E.Yu., Nikolaev, I.V., and Tourova, T.P., Reactivating factor of Luteococcus japonicus subsp. casei: isolation and characterization, Appl. Biochem. Microbiol., 2015a, vol. 51, no. 1, pp. 44–51.

    Google Scholar 

  • Vorobjeva, L.I., Khodzhaev, E.Yu., Rogozhin, E.A., Samoilenko, V.A., and Kharchenko, N.V., Structural characterization of the extracellular peptide metabolites of Luteococcus japonicus subsp. casei and their protective effect on probiotic bacteria, Microbiology (Moscow), 2015b, vol. 84, no. 4, pp. 502–511.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to L. I. Vorob’eva.

Additional information

Original Russian Text © L.I. Vorob’eva, E.Yu. Khodzhaev, E.A. Rogozhin, T.A. Cherdyntseva, A.I. Netrusov, 2016, published in Mikrobiologiya, 2016, Vol. 85, No. 4, pp. 393–402.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vorob’eva, L.I., Khodzhaev, E.Y., Rogozhin, E.A. et al. Characterization of extracellular yeast peptide factors and their stress-protective effect on probiotic lactic acid bacteria. Microbiology 85, 411–419 (2016). https://doi.org/10.1134/S0026261716040160

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026261716040160

Keywords

Navigation