Revista Mexicana de Ingeniería Química, Vol. 23, No. 1 (2024), Alim24140

Improving Xanthophyllomyces dendrorhous astaxanthin stability by encapsulation using a fructan matrix

A. Torres-Haro, J.C. Mateos-Díaz, H. Espinosa-Andrews, G.A. Castillo-Herrera, M. Arellano-Plaza

https://doi.org/10.24275/rmiq/Alim24140

 

Abstract

Astaxanthin is a pigment and powerful antioxidant that has gained a high interest as a bioactive food constituent, compared to other carotenoids. Xanthophyllomyces dendrorhous is one of the main producers of non-esterified (3R, 3´R)-astaxanthin, which is highly assimilable, however, its stability is low (half-life of 19 h at 30 °C). Microencapsulation has emerged as an interesting technique to increase astaxanthin stability, maintain its bioactivity and preserve interesting characteristics. In the present study, a bio-based food constituent fructan (inulin and/or agave fructans) containing microencapsulated non-esterified (3R, 3´R)-astaxanthin produced by X. dendrorhous and extracted using supercritical CO2 was obtained and characterized. Using this technique, astaxanthin stability increased 26-fold compared to the free molecule. In addition, it was also demonstrated that microencapsulated astaxanthin using inulin as a matrix (91.3 ± 0.56 encapsulation efficiency), the capsules resulted well defined (size 2.66 ± 1.08 µm) and maintained their color tone (>70%) for at least 240 h under oxidation conditions. This work obtained a new bio-based stable fructan-astaxanthin microencapsulated food constituent with presumably increased solubility (82.00 ± 5.01 water solubility; size: 2.66 ± 1.08 µm) and bioavailability.

Keywords: Carotenoids, stability, prebiotic matrix, encapsulation, Xanthophyllomyces dendrorhous.

 

References

  • Amado, I. R. and Vázquez, J. A. (2015). Mussel processing wastewater: A low-cost substrate for the production of astaxanthin by Xanthophyllomyces dendrorhous. Microbial Cell Factories. BioMed Central 14(1), 1–11. https://doi.org/10.1186/s12934-015-0375-5
  • Andrewes, A. G., Phaff, H. J. and Starr, M. P. (1976). Carotenoids of Phaffia rhodozyma, a red-pigmented fermenting yeast. Phytochemistry 15(6), 1003–1007. https://doi.org/10.1016/S0031-9422(00)84390-3
  • Avalos, J. and Carmen Limón, M. (2015). Biological roles of fungal carotenoids, Current Genetics. Springer Berlin Heidelberg 61(3), 309–324. https://doi.org/10.1007/s00294-014-0454-x
  • Barajas-Álvarez, P. Castillo-Herrera, G. A., Guatemala-Morales, G. M., Corona-González, R. I., Arriola-Guevara, E. and Espinosa-Andrews, H. (2021). Supercritical CO2-ethanol extraction of oil from green coffee beans: optimization conditions and bioactive compound identification. International Journal of Food Science and Technology 58(12), 4514–4523. https://doi.org/10.1007/s13197-020-04933-1
  • Bernhart, K. (1990). Synthetic Astaxanthin. The Route of a Carotenoid from Research to Commercialisation. Carotenoids: Chemistry and Biology 337–363. https://doi.org/10.1007/978-1-4613-0849-2_24.
  • Bhosale, P. (2004). Environmental and cultural stimulants in the production of carotenoids from microorganisms. Applied Microbiology and Biotechnology 63(4), 351–361. https://doi.org/10.1007/s00253-003-1441-1
  • Boussiba, S. (2000.) Procedure for large-scale production of astaxanthin from Haematococcus. United States. Available at: https://patents.google.com/patent/US6022701A/en.
  • Domínguez-Bocanegra, A. R., Ponce-Noyola, T. and Torres-Muñoz, J. A. (2007). Astaxanthin production by Phaffia rhodozyma and Haematococcus pluvialis: a comparative study. Applied Microbiology and Biotechnology 783–791. https://doi.org/10.1007/s00253-007-0889-9
  • Farías, L. J., Gschaedler, A., Sanchez, A., Cervantes, J., Arellano, M., Zamora, C., Amillastre, E. and Herrera, E.J. (2018). Xanthophyllomyces dendrorhous physiological stages determination using combined measurements from dielectric and Raman spectroscopies, a cell counter system and fluorescence flow cytometry. Biochemical Engineering Journal 136, 1–8. https://doi.org/10.1016/j.bej.2018.04.016
  • García-Curbelo, Y., Mercedes G., Bocourt, R., Collado, E., Nereyda, A. and Nuñez, O. (2015). Structural characterization of fructans from Agave fourcroydes (Lem.) with potential as prebiotic. Cuban Journal of Agricultural Science 49(1), 75–80. https://cjascience.com/index.php/CJAS/article/view/551
  • Gio-Bin, L., Sang-Yun, L., Eun-Kyu, L., Seung-Joo, H. and Woo-Sik, K. (2002). Separation of Astaxanthin from Red Yeast Phaffia Rhodozyma by Supercritical Carbon Dioxide Extraction. Biochemical Engineering Journal 11(2–3), 181–187. https://doi.org/10.1016/S1369-703X(02)00023-2.
  • Gómez-Estaca, J., Comunian, T. A., Montero, P., Ferro-Furtado, R. and Favaro-Trindade, C. S. (2016). Encapsulation of an astaxanthin-containing lipid extract from shrimp waste by complex coacervation using a novel gelatin-cashew gum complex. Food Hydrocolloids 61: 155–162. https://doi.org/10.1016/j.foodhyd.2016.05.005
  • Hasan., A. S., Socha, M., Lamprecht, A., Ghazouani, F., Sapin, A., Hoffman, M., Maincent, P. and Ubrich, N. (2007). Effect of the microencapsulation of nanoparticles on the reduction of burst release. International Journal of Pharmaceutics 344(1–2), 53–61. https://doi.org/10.1016/j.ijpharm.2007.05.066
  • Higuera-Ciapara, I., Félix-Valenzuela, L. and Goycoolea, F. M. (2006). Astaxanthin: A review of its chemistry and applications. Critical Reviews in Food Science and Nutrition 46(2), 185–196. https://doi.org/10.1080/10408690590957188.
  • Honda, M., Kageyama, H., Hibino, T., Osawa, Y., Kawashima, Y., Hirasawa, K. and Kuroda, I. (2021). Evaluation and improvement of storage stability of astaxanthin isomers in oils and fats. Food Chemistry 352, 129371. https://doi.org/10.1016/j.foodchem.2021.129371
  • Kittikaiwan, P., Powthongsook, S., Pavasant, P. and Shotipruk, A. (2007). Encapsulation of Haematococcus pluvialis using chitosan for astaxanthin stability enhancement. Carbohydrate Polymers 70(4), 378–385. https://doi.org/10.1016/j.carbpol.2007.04.021
  • Lee, J. S., Park, S. A., Chung, D. and Lee, H. G. (2011). Encapsulation of astaxanthin-rich Xanthophyllomyces dendrorhous for antioxidant delivery. International Journal of Biology and Macromolecules 49(3), 268–273. https://doi.org/10.1016/j.ijbiomac.2011.04.021
  • Li, R., Chen, R., Liu, W., Qin, C. and Han, J. (2016). Preparation of enteric-coated microcapsules of astaxanthin oleoresin by complex coacervation. Pharmaceutical Development and Technology 23(7), 674–681. https://doi.org/10.1080/10837450.2016.1238483
  • Shen-Fu, L., Ying-Chen, C., Ray-Neng, C., Ling-Chun, C., Hsiu-O, H., Yu-Han, T., Ming-Thau, S. and Der-Zen, L. (2016). Improving the stability of astaxanthin by microencapsulation in calcium alginate beads. PLoS ONE 11(4), 1–10. https://doi.org/10.1371/journal.pone.0153685
  • Machado, F. R. S., Reis, D. F., Boschetto, D. L., Burkert, J. F. M., Ferreira, S. R. S. and Oliveira, J. V. (2014). Encapsulation of astaxanthin from Haematococcus pluvialis in PHBV by means of SEDS technique using supercritical CO2. Industrial Crops and Products 54, 17–21. https://doi.org/10.1016/j.indcrop.2014.01.007
  • Machado, F. R. S., Trevisol, T. C., Boschetto, D. L., Burkert, J. F. M., Ferreira, S. R. S., Oliveira, J. V. and André, C. (2016). Technological process for cell disruption, extraction and encapsulation of astaxanthin from Haematococcus pluvialis. Journal of Biotechnology 218, 108–114. https://doi.org/10.1016/j.jbiotec.2015.12.004
  • Macías-Sánchez, M. D., Serrano, C. M., Rodríguez, M. R. and de la Ossa, E.M. (2008). Extraction of carotenoids and chlorophyll from microalgae with supercritical carbon dioxide and ethanol as cosolvent. Journal of Separation Science 31, 1352–1362. https://doi.org/10.1002/jssc.200700503
  • Martínez-Álvarez, Ó., Calvo, M. M. and Gómez-Estaca, J. (2020). Recent advances in astaxanthin micro/nanoencapsulation to improve its stability and functionality as a food ingredient. Marine Drugs 18(8), 1–25. https://doi.org/10.3390/md18080406
  • Martínez-Preciado, A. H., Silva-Jara, J. M., Flores-Nuño, B. A., Michel, C. R., Castellanos-Haro, M. E. and Macías-Rodríguez, M. E. (2021). Microencapsulation by spray-drying of Manilkara zapota pulp and probiotics (Lactobacillus fermentum A15): Assessment of shelf-life in a food matrix. Revista Mexicana de Ingeniería Química 20(2), 635-648. https://doi.org/10.24275/rmiq/Alim2166
  • Mata-Gómez, L., Montañez, J. C., Méndez-Zavala, A. and Aguilar, C. N. (2014). Biotechnological production of carotenoids by yeasts: an overview. Microbial Cell Factories 13(1), 12. https://doi.org/10.1186/1475-2859-13-12.
  • Mezzomo, N., Paz, E. D., Maraschin, M., Martín, Á., Cocero, M. J. and Ferreira, S. R. S. (2012). Supercritical anti-solvent precipitation of carotenoid fraction from pink shrimp residue: Effect of operational conditions on encapsulation efficiency. Journal of Supercritical Fluids 66, 342–349. https://doi.org/10.1016/j.supflu.2011.08.006
  • Mortensen, A., Skibsted, L. H. and Truscott T.G. (2001). The interaction of dietary carotenoids with radical species. Archives of Biochemistry and Biophysics 385(1), 13–19. https://doi.org/10.1006/abbi.2000.2172
  • Muñoz, J., Alfaro, M. D. C. and Zapata, I. (2007). Avances en la formulación de emulsiones. Grasas y Aceites 58(1), 64–73. http://hdl.handle.net/11441/17634
  • Naguib, Y. M. A. (2000). Antioxidant activities of astaxanthin and related carotenoids. Journal of Agricultural and Food Chemistry 48(4), 1150–1154. https://doi.org/10.1021/jf991106k
  • Østerlie, M., Bjerkeng, B. and Liaaen-Jensen, S. (2000). Plasma appearance and distribution of astaxanthin E/Z and R/S isomers in plasma lipoproteins of men after single dose administration of astaxanthin. Journal of Nutritional Biochemistry 11(10), 482–490. https://doi.org/10.1016/S0955-2863(00)00104-2
  • Pan, L., Zhang, S., Gu, K. and Zhang, N. (2018). Preparation Of astaxanthin-loaded liposomes: Characterization, storage stability and antioxidant activity. CyTA–Journal of Food 16(1), 607–618. https://doi.org/10.1080/19476337.2018.1437080
  • Pérez-Alonso, C., Campos-Montiel, R. G., Morales-Luna, E., Reyes-Munguía, A., Aguirre-Álvarez, D. J. and Pimentel-González, D. J. (2015). Stabilization of phenolic compounds from Opuntia oligacantha Först by microencapsulation with agave sap (aguamiel). Revista Mexicana de Ingeniería Química 14(2), 579-588. 
  • Sedmak, J. J., Weerasinghe, D. K. and Jolly, S. O. (1990). Extraction and quantitation of astaxanthin from Phaffia rhodozyma. Biotechnology Techniques 4(2), 107–112. https://doi.org/10.1007/BF00163282.
  • Storebakken, T., Foss, P., Schiedt, K., Austreng, E., Liaaen-Jensen, S. and Manz, U. (1987). Carotenoids in diets for salmonids. IV. Pigmentation of Atlantic salmon with astaxanthin, astaxanthin dipalmitate and canthaxanthin. Aquaculture 65(3–4), 279–292. https://doi.org/10.1016/0044-8486(87)90241-9.
  • Tachaprutinun, A., Udomsup, T., Luadthong, C. and Wanichwecharungruang, S. (2009). Preventing the thermal degradation of astaxanthin through nanoencapsulation. International Journal of Pharmaceutics 374(1-2), 119–124. https://doi.org/10.1016/j.ijpharm.2009.03.001
  • Tibayrenc, P., Preziosi-Belloy, L., Jean-Michel, R. and Ghommidh, C. (2010). Assessing yeast viability from cell size measurements? Journal of Biotechnology 149(1–2), 74–80. https://doi.org/10.1016/j.jbiotec.2010.06.019.
  • Tirado, D.F., Palazzo, I., Scognamiglio, M., Calvo, L., Della Porta G. and Reverchon, E. (2019). Astaxanthin encapsulation in ethyl cellulose carriers by continuous supercritical emulsions extraction: A study on particle size, encapsulation efficiency, release profile and antioxidant activity. Journal of Supercritical Fluids 150, 128–136. https://doi.org/10.1016/j.supflu.2019.04.017
  • Torres‐Haro, A., Arellano‐Plaza, M., Mateos‐Díaz, J. C., Espinosa‐Andrews, H. and Castillo‐Herrera, G. A. (2022). Non‐conventional high‐pressure extraction process: A comparative study for astaxanthin recovery from Xanthophyllomyces dendrorhous. International Journal of Food Science and Technology 57, 1–10. https://doi.org/10.1111/ijfs.15466
  • Torres-Haro, A., Verdín, J., Kirchmayr, M. R. and Arellano-Plaza, M. (2021a). Metabolic engineering for high yield synthesis of astaxanthin in Xanthophyllomyces dendrorhous. Microbial Cell Factories. BioMed Central, 20(1), 1–17. https://doi.org/10.1186/s12934-021-01664-6
  • Torres-Haro, A., Gschaedler, A., Mateos-Díaz, J. C., Herrera-López, E. J., Camacho-Ruíz, R. M. and Arellano-Plaza, M. (2021b). Improvement of a specific culture medium based on industrial glucose for carotenoid production by Xanthophyllomyces dendrorhous. Processes 9(3), 1–16. https://doi.org/10.3390/pr9030429
  • Wang, H. D. Chen, C. C., Huynh, P. and Chang, J. S. (2015). Exploring the potential of using algae in cosmetics. Bioresource Technology 184, 355–362. https://doi.org/10.1016/j.biortech.2014.12.001
  • Wang, L., Yang, B., Yan, B. and Yao, X. (2012). Supercritical fluid extraction of astaxanthin from Haematococcus pluvialis and its antioxidant potential in sunflower oil. Innovative Food Science and Emerging Technologies 13, 120–127. https://doi.org/10.1016/j.ifset.2011.09.004
  • Zapata-Luna, R. L., Davidov-Pardo, G., Pacheco, N., Ayora-Talavera, T., Espinosa-Andrews, H., García-Márquez, E. and Cuevas-Bernardino, J. C. (2023). Structural and physicochemical properties of bio-chemical chitosan and its performing in an active film with quercetin and Phaseolus polyanthus starch. Revista Mexicana de Ingeniería Química 22(2). https://doi.org/10.24275/rmiq/Alim2315
  • Zhang, C., Chen, X. and Too, H. P. (2020). Microbial astaxanthin biosynthesis: recent achievements, challenges, and commercialization outlook. Applied Microbiology and Biotechnology 104(13), 5725–5737. https://doi.org/10.1007/s00253-020-10648-2
  • Zhou, T., Wang, X., Ju, Y., Shi, C. and Kan, G. (2018). Stability application and research of astaxanthin integrated into food. Materials Science and Engineering 394(2). https://doi.org/10.1088/1757-899X/394/2/022007