Optimization and Characterization of Spirulina and Chlorella Hydrolysates for Industrial Application.
Acid
Autoclave
Cellulase
Chlorella sp
Hydrolysis efficiency
Liquid food
Spirulina sp
Ultrasound
Journal
Applied biochemistry and biotechnology
ISSN: 1559-0291
Titre abrégé: Appl Biochem Biotechnol
Pays: United States
ID NLM: 8208561
Informations de publication
Date de publication:
29 Jun 2023
29 Jun 2023
Historique:
accepted:
19
06
2023
medline:
29
6
2023
pubmed:
29
6
2023
entrez:
29
6
2023
Statut:
aheadofprint
Résumé
Chlorella and Spirulina are the most used microalgae mainly as powder, tablets, or capsules. However, the recent change in lifestyle of modern society encouraged the emergence of liquid food supplements. The current work evaluated the efficiency of several hydrolysis methods (ultrasound-assisted hydrolysis UAH, acid hydrolysis AH, autoclave-assisted hydrolysis AAH, and enzymatic hydrolysis EH) in order to develop liquid dietary supplements from Chlorella and Spirulina biomasses. Results showed that, EH gave the highest proteins content (78% and 31% for Spirulina and Chlorella, respectively) and also increased pigments content (4.5 mg/mL of phycocyanin and 12 µg/mL of carotenoids). Hydrolysates obtained with EH showed the highest scavenging activity (95-91%), allowing us, with the other above features, to propose this method as convenient for liquid food supplements development. Nevertheless, it has been shown that the choice of hydrolysis method depended on the vocation of the product to be prepared.
Identifiants
pubmed: 37382791
doi: 10.1007/s12010-023-04596-6
pii: 10.1007/s12010-023-04596-6
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Wells, M. L., Potin, P., Craigie, J. S., et al. (2017). Algae as nutritional and functional food sources: Revisiting our understanding. Journal of Applied Phycology, 29, 949–982. https://doi.org/10.1007/s10811-016-0974-5
doi: 10.1007/s10811-016-0974-5
pubmed: 28458464
Monteverde, D. R., Gómez-Consarnau, L., Suffridge, C., & Sañudo-Wilhelmy, S. A. (2017). Life’s utilization of B vitamins on early Earth. Geobiology, 15, 3–18. https://doi.org/10.1111/gbi.12202
doi: 10.1111/gbi.12202
pubmed: 27477998
Edelmann, M., Aalto, S., Chamlagain, B., et al. (2019). Riboflavin, niacin, folate and vitamin B12 in commercial microalgae powders. Journal of Food Composition and Analysis, 82, 103226. https://doi.org/10.1016/j.jfca.2019.05.009
doi: 10.1016/j.jfca.2019.05.009
Soni, R. A., Sudhakar, K., & Rana, R. S. (2017). Spirulina – From growth to nutritional product: A review. Trends in Food Science & Technology, 69:. https://doi.org/10.1016/j.tifs.2017.09.010
Coelho, D., Lopes, P. A., Cardoso, V., et al. (2020). A two-enzyme constituted mixture to improve the degradation of Arthrospira platensis microalga cell wall for monogastric diets. Journal of Animal Physiololgy & Animal Nutrition, 104, 310–321. https://doi.org/10.1111/jpn.13239
doi: 10.1111/jpn.13239
Cha, K. H., Lee, H. J., Koo, S. Y., et al. (2010). Optimization of pressurized liquid extraction of carotenoids and chlorophylls from Chlorella vulgaris. Journal of Agriculture and Food Chemistry, 58, 793–797. https://doi.org/10.1021/jf902628j
doi: 10.1021/jf902628j
Agustina, S., Aidha, N. N., & Oktarina, E. (2020). The extraction of antioxidants from Chlorella vulgaris for cosmetics In IOP Conference Series: Materials Science and Engineering, 10 (suite?).
Herrero, M., del Pilar Sánchez-Camargo, A., Cifuentes, A., & Ibáñez, E. (2015). Plants, seaweeds, microalgae and food by-products as natural sources of functional ingredients obtained using pressurized liquid extraction and supercritical fluid extraction. TrAC Trends in Analytical Chemistry, 71, 26–38. https://doi.org/10.1016/j.trac.2015.01.018
doi: 10.1016/j.trac.2015.01.018
Machado, L., Carvalho, G., & Pereira, R. N. (2022). Effects of innovative processing methods on microalgae cell wall: Prospects towards digestibility of protein-rich biomass. Biomass, 2, 80–102. https://doi.org/10.3390/biomass2020006
doi: 10.3390/biomass2020006
Patel, A., Arora, N., Pruthi, V., & Pruthi, P. A. (2019). A novel rapid ultrasonication-microwave treatment for total lipid extraction from wet oleaginous yeast biomass for sustainable biodiesel production. Ultrasonics Sonochemistry, 51, 504–516. https://doi.org/10.1016/j.ultsonch.2018.05.002
doi: 10.1016/j.ultsonch.2018.05.002
pubmed: 30082251
Timira, V., Meki, K., & Li, Z., et al. (2021) A comprehensive review on the application of novel disruption techniques for proteins release from microalgae. Critical Reviews in Food Science and Nutrition, 1–17. https://doi.org/10.1080/10408398.2021.1873734
de Farias Silva, C. E., Meneghello, D., de Souza Abud, A. K., & Bertucco, A. (2020). Pretreatment of microalgal biomass to improve the enzymatic hydrolysis of carbohydrates by ultrasonication: Yield vs energy consumption. Journal of King Saud University - Science, 32, 606–613. https://doi.org/10.1016/j.jksus.2018.09.007
doi: 10.1016/j.jksus.2018.09.007
Günerken, E., D’Hondt, E., Eppink, M. H. M., et al. (2015). Cell disruption for microalgae biorefineries. Biotechnology Advances, 33, 243–260. https://doi.org/10.1016/j.biotechadv.2015.01.008
doi: 10.1016/j.biotechadv.2015.01.008
pubmed: 25656098
Kapoore, R. V., Wood, E. E., & Llewellyn, C. A. (2021). Algae biostimulants: A critical look at microalgal biostimulants for sustainable agricultural practices. Biotechnology Advances, 49, 107754. https://doi.org/10.1016/j.biotechadv.2021.107754
doi: 10.1016/j.biotechadv.2021.107754
pubmed: 33892124
Miranda, J. R., Passarinho, P. C., & Gouveia, L. (2012). Pre-treatment optimization of Scenedesmus obliquus microalga for bioethanol production. Bioresource Technology, 104, 342–348. https://doi.org/10.1016/j.biortech.2011.10.059
doi: 10.1016/j.biortech.2011.10.059
pubmed: 22093974
Demuez, M., Mahdy, A., Tomás-Pejó, E., et al. (2015). Enzymatic cell disruption of microalgae biomass in biorefinery processes. Biotechnology and Bioengineering, 112, 1955–1966. https://doi.org/10.1002/bit.25644
doi: 10.1002/bit.25644
pubmed: 25976593
Al-Zuhair, S., Ashraf, S., Hisaindee, S., et al. (2017). Enzymatic pre-treatment of microalgae cells for enhanced extraction of proteins. Engineering in Life Sciences, 17, 175–185. https://doi.org/10.1002/elsc.201600127
doi: 10.1002/elsc.201600127
pubmed: 32624765
Alavijeh, R. S., Karimi, K., Wijffels, R. H., et al. (2020). Combined bead milling and enzymatic hydrolysis for efficient fractionation of lipids, proteins, and carbohydrates of Chlorella vulgaris microalgae. Bioresource Technology, 309, 123321. https://doi.org/10.1016/j.biortech.2020.123321
doi: 10.1016/j.biortech.2020.123321
pubmed: 32305840
Rokicka, M., Zieliński, M., Dudek, M., & Dębowski, M. (2021). Effects of ultrasonic and microwave pretreatment on lipid extraction of microalgae and methane production from the residual extracted biomass. BioEnergy Research, 14, 752–760. https://doi.org/10.1007/s12155-020-10202-y
doi: 10.1007/s12155-020-10202-y
Zhao, W., Duan, M., Zhang, X., & Tan, T. (2018). A mild extraction and separation procedure of polysaccharide, lipid, chlorophyll and protein from Chlorella spp. Renewable Energy, 118, 701–708. https://doi.org/10.1016/j.renene.2017.11.046
doi: 10.1016/j.renene.2017.11.046
Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. 7.
DuBois, M., Gilles, K. A., & Hamilton, J. K., et al (2002) Colorimetric method for determination of sugars and related substances. In: ACS Publ. https://pubs.acs.org/doi/pdf/10.1021/ac60111a017 . Accessed 5 Jan 2022
Bligh, E. G., & Dyer, W. J. (1959). A rapid method of total lipid extraction and purification. Canadian journal of biochemistry and physiology, 37(8), 911–917.
doi: 10.1139/o59-099
pubmed: 13671378
Bennett, A., & Bogorad, L. (1973). Complementary chromatic adaptation in a filamentous blue-green alga. Journal of Cell Biology, 58, 419–435.
doi: 10.1083/jcb.58.2.419
pubmed: 4199659
pmcid: 2109051
Yang, C. M., Chang, K. W., Yin, M. H., & Huang, H. M. (1998). Methods for the determination of the chlorophylls and their derivatives. Taiwania, 43(2), 116–122.
Kang, M.-Y., Lee, Y.-R., Koh, H.-J., & Nam, S.-H. (2004). Antioxidative and antimutagenic activity of ethanolic extracts from giant embroynic rices. Applied Biological Chemistry, 47, 61–66.
Velioglu, Y. S., Mazza, G., Gao, L., & Oomah, B. D. (1998). Antioxidant activity and total phenolics in selected fruits, vegetables, and grain products. Journal of Agriculture and Food Chemistry, 46, 4113–4117. https://doi.org/10.1021/jf9801973
doi: 10.1021/jf9801973
He, X. F., & Lv, X. G. (2021). From the color composition to the color psychology: Soft drink packaging in warm colors, and spirits packaging in dark colors. Color Research & Application. https://doi.org/10.1002/col.22748
doi: 10.1002/col.22748
Carvalho, F. R., Moors, P., Wagemans, J., & Spence, C. (2017). The influence of color on the consumer’s experience of beer. Frontiers in Psychology, 8, 2205. https://doi.org/10.3389/fpsyg.2017.02205
doi: 10.3389/fpsyg.2017.02205
pubmed: 29312065
pmcid: 5742240
Balbinot-Alfaro, E., Craveiro, D. V., Lima, K. O., et al. (2019). Intelligent packaging with pH indicator potential. Food Engineering Reviews, 11, 235–244. https://doi.org/10.1007/s12393-019-09198-9
doi: 10.1007/s12393-019-09198-9
Seow, W. K., & Thong, K. M. (2005) Erosive effects of common beverages on extracted premolar teeth. Australian Dental Journal, 50:173–178; quiz 211. https://doi.org/10.1111/j.1834-7819.2005.tb00357.x
Talley, K., & Alexov, E. (2010). On the pH-optimum of activity and stability of proteins. Proteins, 78, 2699–2706. https://doi.org/10.1002/prot.22786
doi: 10.1002/prot.22786
pubmed: 20589630
pmcid: 2911520
Waghmare, A. G., Salve, M. K., LeBlanc, J. G., & Arya, S. S. (2016). Concentration and characterization of microalgae proteins from Chlorella pyrenoidosa. Biores Bioprocess, 3, 16. https://doi.org/10.1186/s40643-016-0094-8
doi: 10.1186/s40643-016-0094-8
Walke, S. (2019). Protein extraction from Spirulina Platensis. International Journal of Innovative Technology and Exploring Engineering, 8, 1524–1530. https://doi.org/10.35940/ijitee.L3110.1081219
doi: 10.35940/ijitee.L3110.1081219
Cristiane, R. L., Aline, M. P., & Jorge, A. V. C. (2016). Biopeptides with antioxidant activity extracted from the biomass of Spirulina sp. LEB 18. African Journal of Microbiology Research, 10, 79–86. https://doi.org/10.5897/AJMR2015.7760
doi: 10.5897/AJMR2015.7760
Coelho, D., Lopes, P. A., Cardoso, V., et al. (2019). Novel combination of feed enzymes to improve the degradation of Chlorella vulgaris recalcitrant cell wall. Science and Reports, 9, 5382. https://doi.org/10.1038/s41598-019-41775-0
doi: 10.1038/s41598-019-41775-0
Kusmiyati, K., Heratri, A., & Kubikazari, S (2020) Hydrolysis of microalgae Spirulina platensis, chlorella sp., and macroalgae Ulva lactuca for Bioethanol Production. 4:7 suite?
Martin Juárez, J., Martínez-Páramo, S., Maté-González, M., et al. (2021). Evaluation of pretreatments for solubilisation of components and recovery of fermentable monosaccharides from microalgae biomass grown in piggery wastewater. Chemosphere, 268, 129330. https://doi.org/10.1016/j.chemosphere.2020.129330
doi: 10.1016/j.chemosphere.2020.129330
pubmed: 33359992
Becker, E. W. (2007). Micro-algae as a source of protein. Biotechnology Advances, 25, 207–210. https://doi.org/10.1016/j.biotechadv.2006.11.002
doi: 10.1016/j.biotechadv.2006.11.002
pubmed: 17196357
Nakamura, Y., Takahashi, J., Sakurai, A., et al. (2005). Some cyanobacteria synthesize semi-amylopectin type α-polyglucans instead of glycogen. Plant and Cell Physiology, 46, 539–545. https://doi.org/10.1093/pcp/pci045
doi: 10.1093/pcp/pci045
pubmed: 15695453
Markou, G., Angelidaki, I., & Georgakakis, D. (2012). Microalgal carbohydrates: An overview of the factors influencing carbohydrates production, and of main bioconversion technologies for production of biofuels. Applied Microbiology and Biotechnology, 96, 631–645. https://doi.org/10.1007/s00253-012-4398-0
doi: 10.1007/s00253-012-4398-0
pubmed: 22996277
Chen, C.-Y., Zhao, X.-Q., Yen, H.-W., et al. (2013). Microalgae-based carbohydrates for biofuel production. Biochemical Engineering Journal, 78, 1–10. https://doi.org/10.1016/j.bej.2013.03.006
doi: 10.1016/j.bej.2013.03.006
Markou, G., Angelidaki, I., Nerantzis, E., & Georgakakis, D. (2013). Bioethanol production by carbohydrate-enriched biomass of Arthrospira (Spirulina) platensis. Energies, 6, 3937–3950. https://doi.org/10.3390/en6083937
doi: 10.3390/en6083937
Hernández, D., Riaño, B., Coca, M., & García-González, M. C. (2015). Saccharification of carbohydrates in microalgal biomass by physical, chemical and enzymatic pre-treatments as a previous step for bioethanol production. Chemical Engineering Journal, 262, 939–945. https://doi.org/10.1016/j.cej.2014.10.049
doi: 10.1016/j.cej.2014.10.049
Park, C., Lee, J. H., Yang, X., et al. (2016). Enhancement of hydrolysis of Chlorella vulgaris by hydrochloric acid. Bioprocess and Biosystems Engineering, 39, 1015–1021. https://doi.org/10.1007/s00449-016-1570-4
doi: 10.1007/s00449-016-1570-4
pubmed: 26899601
John, R. P., Anisha, G. S., Nampoothiri, K. M., & Pandey, A. (2011). Micro and macroalgal biomass: A renewable source for bioethanol. Bioresource Technology, 102, 186–193. https://doi.org/10.1016/j.biortech.2010.06.139
doi: 10.1016/j.biortech.2010.06.139
pubmed: 20663661
del Campo, I., Alegría, I., Zazpe, M., et al. (2006). Diluted acid hydrolysis pretreatment of agri-food wastes for bioethanol production. Industrial Crops and Products, 24, 214–221. https://doi.org/10.1016/j.indcrop.2006.06.014
doi: 10.1016/j.indcrop.2006.06.014
Rehman, Z. U., & Anal, A. K. (2018). Enhanced lipid and starch productivity of microalga (Chlorococcum sp. TISTR 8583) with nitrogen limitation following effective pretreatments for biofuel production. Biotechnology Reports, 21, e00298. https://doi.org/10.1016/j.btre.2018.e00298
doi: 10.1016/j.btre.2018.e00298
pubmed: 30619730
pmcid: 6308246
Duongbia, N., Chaiwongsar, S., Chaichana, C., & Chaiklangmuang, S. (2019). Acidic hydrolysis performance and hydrolyzed lipid characterizations of wet Spirulina platensis. Biomass Conversion and Biorefinery, 9, 305–319. https://doi.org/10.1007/s13399-018-0350-6
doi: 10.1007/s13399-018-0350-6
Hoseini, S. M., Khosravi-Darani, K., & Mozafari, M. R. (2013). Nutritional and medical applications of Spirulina Microalgae. Mini-Reviews in Medicinal Chemistry., 13, 1231–1237.
doi: 10.2174/1389557511313080009
Khan, Z., Bhadouria, P., & Bisen, P. S. (2005). Nutritional and therapeutic potential of Spirulina. Current Pharmaceutical Biotechnology, 6, 373–379. https://doi.org/10.2174/138920105774370607
doi: 10.2174/138920105774370607
pubmed: 16248810
Pohndorf, R. S., Camara, Á. S., Larrosa, A. P. Q., et al. (2016). Production of lipids from microalgae Spirulina sp.: Influence of drying, cell disruption and extraction methods. Biomass and Bioenergy, 93, 25–32. https://doi.org/10.1016/j.biombioe.2016.06.020
doi: 10.1016/j.biombioe.2016.06.020
Wang, M., Yuan, W., Jiang, X., et al. (2014). Disruption of microalgal cells using high-frequency focused ultrasound. Bioresource Technology, 153, 315–321. https://doi.org/10.1016/j.biortech.2013.11.054
doi: 10.1016/j.biortech.2013.11.054
pubmed: 24374364
Chaiklahan, R., Chirasuwan, N., Loha, V., & Bunnag, B. (2008). Lipid and fatty acids extraction from the cyanobacterium Spirulina. ScienceAsia, 34, 299. https://doi.org/10.2306/scienceasia1513-1874.2008.34.299
doi: 10.2306/scienceasia1513-1874.2008.34.299
Hadiyanto, H., & Adetya, N. P. (2018). Response surface optimization of lipid and protein extractions from Spirulina platensis using ultrasound assisted osmotic shock method. Food Science and Biotechnology, 27, 1361–1368. https://doi.org/10.1007/s10068-018-0389-y
doi: 10.1007/s10068-018-0389-y
pubmed: 30319845
pmcid: 6170260
Safi, C., Zebib, B., Merah, O., et al. (2014). Morphology, composition, production, processing and applications of Chlorella vulgaris: A review. Renewable and Sustainable Energy Reviews, 35, 265–278. https://doi.org/10.1016/j.rser.2014.04.007
doi: 10.1016/j.rser.2014.04.007
Izadi, M., & Fazilati, M. (2018). Extraction and purification of phycocyanin from Spirulina platensis and evaluating its antioxidant and anti- inflammatory activity. Asian Journal of Green Chemistry, 2:. https://doi.org/10.22034/ajgc.2018.63597
Fratelli, C., Burck, M., Amarante, M. C. A., & Braga, A. R. C. (2021). Antioxidant potential of nature’s “something blue”: Something new in the marriage of biological activity and extraction methods applied to C-phycocyanin. Trends in Food Science & Technology, 107, 309–323. https://doi.org/10.1016/j.tifs.2020.10.043
doi: 10.1016/j.tifs.2020.10.043
Vali Aftari, R., Rezaei, K., Mortazavi, A., & Bandani, A. R. (2015). The optimized concentration and purity of Spirulina platensis C-phycocyanin: A comparative study on microwave-assisted and ultrasound-assisted extraction methods: Extraction modeling to optimize the phycocyanin. Journal of Food Processing and Preservation, 39, 3080–3091. https://doi.org/10.1111/jfpp.12573
doi: 10.1111/jfpp.12573
Schipper, K., Fortunati, F., Oostlander, P. C., et al. (2020). Production of phycocyanin by Leptolyngbya sp. in desert environments. Algal Research, 47, 101875. https://doi.org/10.1016/j.algal.2020.101875
doi: 10.1016/j.algal.2020.101875
Gong, M., & Bassi, A. (2016). Carotenoids from microalgae: A review of recent developments. Biotechnology Advances, 34, 1396–1412. https://doi.org/10.1016/j.biotechadv.2016.10.005
doi: 10.1016/j.biotechadv.2016.10.005
pubmed: 27816618
Damergi, E., Schwitzguébel, J.-P., Refardt, D., et al. (2017). Extraction of carotenoids from Chlorella vulgaris using green solvents and syngas production from residual biomass. Algal Research, 25, 488–495. https://doi.org/10.1016/j.algal.2017.05.003
doi: 10.1016/j.algal.2017.05.003
Adadi, P., Barakova, N. V., & Krivoshapkina, E. F. (2018). Selected methods of extracting carotenoids, characterization, and health concerns: A review. Journal of Agriculture and Food Chemistry, 66, 5925–5947. https://doi.org/10.1021/acs.jafc.8b01407
doi: 10.1021/acs.jafc.8b01407
Mary Leema, J. T., Persia Jothy, T., Magesh Peter, D., et al. (2021). A critical look into different salt removal treatments for the production of high value pigments and fatty acids from marine microalgae Chlorella vulgaris (NIOT-74). Biotechnology Reports, 30, e00627. https://doi.org/10.1016/j.btre.2021.e00627
doi: 10.1016/j.btre.2021.e00627
Yadav, S., & Prabha, R. (2014). Effect of Ph and temperature on carotenoid pigments produced from Rhodotorula minuta. International Journal of Fermented Foods, 3, 105. https://doi.org/10.5958/2321-712X.2014.01312.X
doi: 10.5958/2321-712X.2014.01312.X
Lian, H., Wen, C., Zhang, J., et al. (2021). Effects of simultaneous dual-frequency divergent ultrasound-assisted extraction on the structure, thermal and antioxidant properties of protein from Chlorella pyrenoidosa. Algal Research, 56, 102294. https://doi.org/10.1016/j.algal.2021.102294
doi: 10.1016/j.algal.2021.102294
Ferreira-Santos, P., Miranda, S. M., Belo, I., et al. (2021). Sequential multi-stage extraction of biocompounds from Spirulina platensis: Combined effect of ohmic heating and enzymatic treatment. Innovative Food Science & Emerging Technologies, 71, 102707. https://doi.org/10.1016/j.ifset.2021.102707
doi: 10.1016/j.ifset.2021.102707
Xu, G., Ye, X., Chen, J., & Liu, D. (2007). Effect of heat treatment on the phenolic compounds and antioxidant capacity of citrus peel extract. Journal of Agricultural and Food chemistry, 55(2), 330–335.
doi: 10.1021/jf062517l
pubmed: 17227062
Ghafoor, K., Ahmed, I. A. M., & Doğu, S., et al. (2019). The effect of heating temperature on total phenolic content, antioxidant activity, and phenolic compounds of plum and Mahaleb fruits. International Journal of Food Engineering, 15:. https://doi.org/10.1515/ijfe-2017-0302
Kurd, F., & Samavati, V. (2015). Water soluble polysaccharides from Spirulina platensis: Extraction and in vitro anti-cancer activity. International Journal of Biological Macromolecules, 74, 498–506. https://doi.org/10.1016/j.ijbiomac.2015.01.005
doi: 10.1016/j.ijbiomac.2015.01.005
pubmed: 25583023
Ramos-Romero, S., Torrella, J. R., Pagès, T., et al. (2021). Edible microalgae and their bioactive compounds in the prevention and treatment of metabolic alterations. Nutrients, 13, 563. https://doi.org/10.3390/nu13020563
doi: 10.3390/nu13020563
pubmed: 33572056
pmcid: 7916042