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On the Presence of Gluten-Cleaving Activity in Sodiomyces alkalinus and S. magadiensis Strains

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Abstract

Special enzymes are necessary for producing gluten-free foods, and specific proteolytic enzymes with gluten-degrading activity may be used as oral treatments for celiac disease. Enzymes of the kind were sought, identified, and preliminarily characterized in two strains of the alkaliphilic microscopic fungi Sodiomyces alkalinus and S. magadiensis. Post-glutamine cleaving activity was for the first time observed in the strains along with proline-cleaving activities of dipeptidyl peptidase 4 (DPP4) and proline aminopeptidase (PAP), allowing efficient hydrolysis of both proline/glutamine-rich gluten peptides and whole gluten. The optimal pH and pH-dependent stability were determined for the peptidases in question. All of the enzymes shown to cleave the prolyne/glutamine-containing bonds were assigned to the serine peptidase group and were found to be stable in moderately acidic and alkaline conditions. Owing to their activities, the peptidases are promising as tools to produce gluten-free foods and to design diets for gluten-intolerant patients.

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REFERENCES

  1. Basten, D.E.J.W., Moers, A.P.H.A., van Ooyen, A.J.J., et al., Characterisation of Aspergillus niger prolyl aminopeptidase, Mol. Genet. Genomics, 2005, vol. 272, no. 6, pp. 673–679.

    Article  CAS  PubMed  Google Scholar 

  2. Britton, H.T.S. and Robinson, R.A., Universal buffer solutions and the dissociation constant of veronal, J. Chem. Soc., 1931, pp. 1456–1462.

  3. Cooper, K.G. and Woods, J.P., Secreted dipeptidyl peptidase IV activity in the dimorphic fungal pathogen Histoplasma capsulatum, Infect. Immun., 2009, vol. 77, no. 6, pp. 2447–2454.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Cordain, L., Cereal grains: humanity’s double-edged sword, World Rev. Nutr. Diet, 1999, vol. 84, pp. 19–73.

    Article  CAS  PubMed  Google Scholar 

  5. Darwish, G., Helmerhorst, E.J., Schuppan, D., et al., Pharmaceutically modified subtilisins withstand acidic conditions and effectively degrade glutenin in vivo, Sci. Rep., 2019, vol. 9, p. 7505.

    Article  PubMed  PubMed Central  Google Scholar 

  6. De Angelis, M., Cassone, A., Rizzello, C., et al., Mechanism of degradation of immunogenic gluten epitopes from Triticum turgidum L. var. durum by sourdough lactobacilli and fungal proteases, Appl. Environ. Microbiol., 2010, vol. 76, pp. 508–518.

    Article  CAS  PubMed  Google Scholar 

  7. Doumas, A., van der Broek, P., Affolter, M., et al., Characterization of the prolyl dipeptidyl peptidase gene (dppIV) from the koji mold Aspergillus oryzae, Appl. Environ. Microbiol., 1998, vol. 64, no. 12, pp. 4809–4815.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Dunaevsky, Y.E., Tereshchenkova, V.F., Oppert, B., et al., Human proline specific peptidases: A comprehensive analysis, Biochim. Biophys. Acta, 2020, vol. 1864, no. 9, p. 129636.

    Article  CAS  Google Scholar 

  9. Ehren, J., Moron, B., Martin, E., et al., A food-grade enzyme preparation with modest gluten detoxification properties, PLoS One, 2009, vol. 4, no. 7, p. e6313.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Eugster, P.J., Salamin, K., Grouzmann, E., et al., Production and characterization of two major Aspergillus oryzae secreted prolyl endopeptidases able to efficiently digest proline-rich peptides of gliadin, Microbiology, 2015, vol. 161, no. 12, pp. 2277–2288.

    Article  CAS  PubMed  Google Scholar 

  11. Fujinami, S. and Fujisawa, M., Industrial applications of alkaliphiles and their enzymes—past, present and future, Environ. Technol., 2010, vol. 31, pp. 845–856.

    Article  CAS  PubMed  Google Scholar 

  12. Grum-Grzhimaylo, A.A., Falkoski, D.L., van den Heuvel, J., et al., The obligate alkalophilic soda-lake fungus Sodiomyces alkalinus has shifted to a protein diet, Mol. Ecol., 2018, vol. 27, no. 23, pp. 4808–4819.

    Article  CAS  PubMed  Google Scholar 

  13. Juntunen, K., Mäkinen, S., Isoniemi, S., et al., A new subtilase-like protease deriving from Fusarium equiseti with high potential for industrial applications, Appl. Biochem. Biotechnol., 2015, vol. 177, no. 2, pp. 407–430.

    Article  CAS  PubMed  Google Scholar 

  14. Kõiv, V. and Tenson, T., Gluten-degrading bacteria: availability and applications, Appl. Microbiol. Biotechnol., 2021, vol. 105, no. 8, pp. 1–15.

    Article  Google Scholar 

  15. Mahon, C.S., O’Donoghue, A.J., Goetz, D.H., et al., Characterization of a multimeric, eukaryotic prolyl aminopeptidase: an inducible and highly specific intracellular peptidase from the non-pathogenic fungus Talaromyces emersonii, Microbiology, 2009, vol. 155, no. 11, pp. 3673–3682.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Schulz, K., Giesler, L., Linke, D., et al., A prolyl endopeptidase from Flammulina velutipes for the possible degradation of celiac disease provoking toxic peptides in cereal proteins, Process Biochem., 2018, vol. 73, pp. 47–55.

    Article  CAS  Google Scholar 

  17. Shewry, P.R. and Tatham, A.S., The prolamin storage proteins of cereal seeds: structure and evolution, Biochem. J., 1990, vol. 267, pp. 1–12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Stepniak, D., Spaenij-Dekking, L., Mitea, C., et al., Highly efficient gluten degradation with a newly identified prolyl endoprotease: implications for celiac disease, Am. J. Physiol.: Gastrointest. Liver Physiol., 2006, vol. 291, no. 4, pp. G621–G629.

    CAS  PubMed  Google Scholar 

  19. Wei, G., Tian, N., Siezen, R., et al., Identification of food-grade subtilisins asgluten-degrading enzymes to treat celiac disease, Am. J. Physiol.: Gastrointest. Liver Physiol., 2016, vol. 311, pp. G571–G580.

    PubMed  Google Scholar 

  20. Zhuchkov, M.V. and Kotlyarov, S.N., Cutaneous manifestations of celiac disease: what a practicing gastroenterologist needs to know?, Consilium Medicum, 2017, vol. 19, pp. 45–51.

    Google Scholar 

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Funding

This work was supported by the Russian Foundation for Basic Research (project no. 19-04-00852_a).

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Correspondence to N. A. Alkin, M. A. Belozerskii or A. V. Kurakov.

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Conflict of interests. The authors declare that they have no conflicts of interest.

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

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Translated by T. Tkacheva

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Alkin, N.A., Pokrovskaya, Y.S., Belozerskii, M.A. et al. On the Presence of Gluten-Cleaving Activity in Sodiomyces alkalinus and S. magadiensis Strains. Dokl Biol Sci 508, 1–8 (2023). https://doi.org/10.1134/S0012496622700144

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  • DOI: https://doi.org/10.1134/S0012496622700144

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