tatpipТехника и технология пищевых производствFood Processing: Techniques and Technology2074-94142313-1748Кемеровский государственный университет10.21603/2074-9414-2024-2-2501EFYVTBtatpip-118Research ArticleСтатьиСкрининг и характеристика антиоксидантных свойств психрофильных микроводорослей и цианобактерий Балтийского моряScreening and Profiling the Antioxidant Properties of Psychrophilic Microalgae and Cyanobacteria from the Baltic Seahttps://orcid.org/0000-0003-0603-7456ДолганюкВ. Ф.DolganyukV. F.

Калининград

Vyacheslav F. Dolganyuk

Kaliningrad

https://orcid.org/0000-0001-7910-8388СухихС. А.SukhikhS. A.

Калининград

Stanislav A. Sukhikh

Kaliningrad

stas-asp@mail.ruhttps://orcid.org/0000-0003-0442-5471КаширскихЕ. В.KashirskihE. V.

Калининград

Egor V. Kashirskih

Kaliningrad

https://orcid.org/0000-0003-4107-7277УльрихЕ. В.UlrikhE. V.

Калининград

Elena V. Ulrikh

Kaliningrad

КремлеваО. Е.KremlevaO. E.

Гродно

Olga E. Kremleva

Grodno

https://orcid.org/0000-0002-4921-8997БабичО. О.BabichO. O.

Калининград

Olga O. Babich

Kaliningrad

Балтийский федеральный университет имени Иммануила КантаРоссияImmanuel Kant Baltic Federal UniversityRussian FederationКалининградский государственный технический университетРоссияKaliningrad State Technical UniversityRussian FederationГродненский государственный университет имени Янки КупалыБеларусьYanka Kupala State University of GrodnoBelarus202420082026542212221Copyright © Долганюк В.Ф., Сухих С.А., Каширских Е.В., Ульрих Е.В., Кремлева О.Е., Бабич О.О., 20262026Долганюк В.Ф., Сухих С.А., Каширских Е.В., Ульрих Е.В., Кремлева О.Е., Бабич О.О.Dolganyuk V.F., Sukhikh S.A., Kashirskih E.V., Ulrikh E.V., Kremleva O.E., Babich O.O.Данная работа распространяется под лицензией Creative Commons Attribution 4.0.This work is licensed under a Creative Commons Attribution 4.0 License.https://www.fptt.ru/jour/article/view/118

Получение комплекса биологически активных веществ с антиоксидантной активностью из психрофильных микроводорослей и цианобактерий вызывает научный интерес, расширяет область их промышленного применения и открывает новые перспективы их использования. Целью работы являлся сбор и идентификация психрофильных микроводорослей и цианобактерий Балтийского моря, а также изучение их соединений, которые проявляют антиоксидантные свойства.

Объекты исследования – образцы психрофильных микроводорослей (Skeletonema pseudocostatum, Thalassiosira pseudonana и Fragilariopsis kerguelensis) и цианобактерий (Aphanizomenon gracile и Anabaena cylindrica). Образцы отобрали из природных источников в акватории Балтийского моря в Калининградской области (Куршский залив и Балтийский залив) в период с марта по май 2022 г. Анализ выделенных чистых культур осуществляли методами Пастера и проточной цитофлуориметрии. Антиоксидантную активность психрофильных микроводорослей и цианобактерий определяли путем анализа активности поглощения радикалов, восстанавливающей способности и хелатной активности с помощью спектрофотометрии.

Наибольшей антиоксидантной активностью по трем методам анализа обладала психрофильная микроводоросль S. pseudocostatum, которая по методу ABTS составила 17,62 мкмоль/г эквивалентов тролокса, по методу DPPH 58,16 мкмоль/г эквивалентов тролокса, по методу FRAP 3,91 мкмоль/г эквивалентов тролокса. Антиоксидантная активность T. pseudonana равна 12,08, 12,42 и 3,13 мкмоль/г эквивалентов тролокса. Для психрофильной микроводоросли F. kerguelensis этот показатель составил 13,53, 11,84 и 1,09 мкмоль/г эквивалентов тролокса. Антиоксидантная активность психрофильной цианобактерии A. gracile равна 15,73, 19,89 и 2,47 мкмоль/г эквивалентов тролокса. Значения антиоксидантной активности психрофильной цианобактерии A. cylindrica составили 12,62, 13,16 и 2,16 мкмоль/г эквивалентов тролокса.

Отобрали образцы психрофильных микроводорослей и цианобактерий из природных источников в акватории Балтийского моря (Калининградская область), которые продуцируют компоненты с высокой антиоксидантной активностью. Полученные результаты могут стать основой для разработки новой фармацевтической субстанции.

 

At present, the issue of obtaining a complex of biologically active substances with antioxidant activity from psychrophilic Psychrophilic microalgae and cyanobacteria are a prospective source of biologically active antioxidant substances. New antioxidant complexes could expand the scope of their industrial application. The research objective was to identify psychrophilic microalgae and cyanobacteria from the Baltic Sea in order to study their antioxidant properties.

The research featured psychrophilic microalgae and cyanobacteria obtained from the Curonian Lagoon and the Baltic Bay in the Baltic Sea, Kaliningrad Region, Russia, in March – May 2022. The authors used the Pasteur method and the flow cytometry method to isolate pure cultures of psychrophilic microalgae and cyanobacteria. The method of spectrophotometry made it possible to study the antioxidant activity by analyzing radical scavenging, reducing ability, and chelating.

The psychrophilic microalga Skeletonema pseudocostatum demonstrated the highest antioxidant activity in all three methods: 17.62 μmol/g trolox equivalents according to the ABTS method, 58.16 μmol/g trolox equivalents according to the DPPH method, and 3.91 μmol/g trolox equivalents according to the FRAP method. The psychrophilic microalga Thalassiosira pseudonana exhibited the following values of antioxidant activity: 12.08, 12.42, and 3.13 μmol/g trolox equivalents, respectively. The antioxidant activity of the psychrophilic microalgae Fragilariopsis kerguelensis was 13.53, 11.84, and 1.09 μmol/g trolox equivalents, respectively. The antioxidant activity of the psychrophilic cyanobacterium Aphanizomenon gracile was 15.73, 19.89, and 2.47 μmol/g trolox equivalents, respectively. The antioxidant activity of the psychrophilic cyanobacterium Anabaena cylindrica was 12.62, 13.16, and 2.16 μmol/g trolox equivalents, respectively.

The samples of psychrophilic microalgae and cyanobacteria obtained from natural environment in the Russian Baltic Sea demonstrated good antioxidant properties, which makes them a potential raw material for new pharmaceutical substances.

Skeletonema pseudocostatumThalassiosira pseudonanaFragilariopsis kerguelensisAphanizomenon gracileAnabaena cylindricaмикроводорослибиологически активные веществаскринингидентификацияантиоксидантная активностьSkeletonema pseudocostatumThalassiosira pseudonanaFragilariopsis kerguelensisAphanizomenon gracileAnabaena cylindricamicroalgaebiologically active substancesscreeningidentificationantioxidant activityРабота выполнена при финансовой поддержке Министерства науки и высшего образования Российской Федерации (Минобрнауки России) (грант Президента Российской Федерации), проект № МК-484.2022.1.4 (соглашение № 075-15-2022-393)The research was supported by the Presidential Grant from the Ministry of Science and Higher Education of the Russian Federation (Minobrnauki) , project no. MK-484.2022.1.4, agreement no. 075-15-2022-393ReferencesСобакарь М. С., Ших Е. В. Антиоксидантная терапия и метаболические подходы к лечению заболеваний сердечно-сосудистой системы // Биомедицина. 2010. № 3. С. 10–21. https://www.elibrary.ru/NUJCKZSobakar’ MS, Shih EV. Antioxidant therapy and metabolic approaches to treatment of cardio-vascular system diseases. Journal Biomed. 2010;(3):10–21. (In Russ.). https://www.elibrary.ru/NUJCKZFaskhutdinova ER, Sukhikh AS, Le VM, Minina VI, Khelef MEA, Loseva AI. Effects of bioactive substances isolated from Siberian medicinal plants on the lifespan of Caenorhabditis elegans. Foods and Raw Materials. 2022;10(2):340–352. https://doi.org/10.21603/2308-4057-2022-2-544Faskhutdinova ER, Sukhikh AS, Le VM, Minina VI, Khelef MEA, Loseva AI. Effects of bioactive substances isolated from Siberian medicinal plants on the lifespan of Caenorhabditis elegans. Foods and Raw Materials. 2022;10(2):340–352. https://doi.org/10.21603/2308-4057-2022-2-544Prosekov AYu, Dyshlyuk LS, Milentyeva IS, Sykhikh SA, Babich OO, Ivanova SA, et al. Antioxidant and antimicrobial activity of bacteriocin-producing strains of lactic acid bacteria isolated from the human gastrointestinal tract. Progress in Nutrition. 2017;19(1):67–80. https://doi.org/10.23751/pn.v19i1.5147Prosekov AYu, Dyshlyuk LS, Milentyeva IS, Sykhikh SA, Babich OO, Ivanova SA, et al. Antioxidant and antimicrobial activity of bacteriocin-producing strains of lactic acid bacteria isolated from the human gastrointestinal tract. Progress in Nutrition. 2017;19(1):67–80. https://doi.org/10.23751/pn.v19i1.5147Nikitina OA, Darenskaya MA, Semenova NV, Kolesnikova LI. Antioxidant defense system: Regulation of metabolic processes, genetic determinants, methods of determination. The Siberian Scientific Medical Journal. 2022;42(3):4–17. (In Russ.). https://doi.org/10.18699/SSMJ20220301Nikitina OA, Darenskaya MA, Semenova NV, Kolesnikova LI. Antioxidant defense system: Regulation of metabolic processes, genetic determinants, methods of determination. The Siberian Scientific Medical Journal. 2022;42(3):4–17. (In Russ.). https://doi.org/10.18699/SSMJ20220301Coulombier N, Nicolau E, le Déan L, Antheaume C, Jauffrais T, Lebouvier N. Impact of light intensity on antioxidant activity of tropical microalgae. Marine Drugs. 2020;18(2):122. https://doi.org/10.3390/md18020122Coulombier N, Nicolau E, le Déan L, Antheaume C, Jauffrais T, Lebouvier N. Impact of light intensity on antioxidant activity of tropical microalgae. Marine Drugs. 2020;18(2):122. https://doi.org/10.3390/md18020122Coulombier N, Blanchier P, le Dean L, Barthelemy V, Lebouvier N, Jauffrais T. The effects of CO2 -induced acidification on Tetraselmis biomass production, photophysiology and antioxidant activity: A comparison using batch and continuous culture. Journal of Biotechnology. 2021;325:312–324. https://doi.org/10.1016/j.jbiotec.2020.10.005Coulombier N, Blanchier P, le Dean L, Barthelemy V, Lebouvier N, Jauffrais T. The effects of CO2 -induced acidification on Tetraselmis biomass production, photophysiology and antioxidant activity: A comparison using batch and continuous culture. Journal of Biotechnology. 2021;325:312–324. https://doi.org/10.1016/j.jbiotec.2020.10.005Coulombier N, Nicolau E, le Déan L, Barthelemy V, Schreiber N, Brun P, et al. Effects of nitrogen availability on the antioxidant activity and carotenoid content of the microalgae Nephroselmis sp. Marine Drugs. 2020;18(9):453. https://doi.org/10.3390/md18090453Coulombier N, Nicolau E, le Déan L, Barthelemy V, Schreiber N, Brun P, et al. Effects of nitrogen availability on the antioxidant activity and carotenoid content of the microalgae Nephroselmis sp. Marine Drugs. 2020;18(9):453. https://doi.org/10.3390/md18090453Paliwal C, Mitra M, Bhayani K, Bharadwaj VSV, Ghosh T, Dubey S, et al. Abiotic stresses as tools for metabolites in microalgae. Bioresource Technology. 2017;244:1216–1226. https://doi.org/10.1016/j.biortech.2017.05.058Paliwal C, Mitra M, Bhayani K, Bharadwaj VSV, Ghosh T, Dubey S, et al. Abiotic stresses as tools for metabolites in microalgae. Bioresource Technology. 2017;244:1216–1226. https://doi.org/10.1016/j.biortech.2017.05.058Alloyarova YuV, Kolotova DS, Derkach SR. Nutritional and therapeutic potential of functional components of brown seaweed: A review. Foods and Raw Materials. 2024;12(2):398–419. https://doi.org/10.21603/2308-4057-2024-2-616Alloyarova YuV, Kolotova DS, Derkach SR. Nutritional and therapeutic potential of functional components of brown seaweed: A review. Foods and Raw Materials. 2024;12(2):398–419. https://doi.org/10.21603/2308-4057-2024-2-616Sathasivam R, Ki J-S. A review of the biological activities of microalgal carotenoids and their potential use in healthcare and cosmetic industries. Marine Drugs. 2018;16(1):26. https://doi.org/10.3390/md16010026Sathasivam R, Ki J-S. A review of the biological activities of microalgal carotenoids and their potential use in healthcare and cosmetic industries. Marine Drugs. 2018;16(1):26. https://doi.org/10.3390/md16010026Gill SS, Tuteja N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry. 2010;48(12):909–930. https://doi.org/10.1016/j.plaphy.2010.08.016Gill SS, Tuteja N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry. 2010;48(12):909–930. https://doi.org/10.1016/j.plaphy.2010.08.016Dolganyuk V, Belova D, Babich O, Katserov D, Patyukov N, Sukhikh S, et al. Microalgae: A promising source of valuable bioproducts. Biomolecules. 2020;10(8):1153. https://doi.org/10.3390/biom10081153Dolganyuk V, Belova D, Babich O, Katserov D, Patyukov N, Sukhikh S, et al. Microalgae: A promising source of valuable bioproducts. Biomolecules. 2020;10(8):1153. https://doi.org/10.3390/biom10081153Gulcin İ. Antioxidants and antioxidant methods: An updated overview. Archives of Toxicology. 2020;94:651–715. https://doi.org/10.1007/s00204-020-02689-3Gulcin İ. Antioxidants and antioxidant methods: An updated overview. Archives of Toxicology. 2020;94:651–715. https://doi.org/10.1007/s00204-020-02689-3Huang JJ, Lin S, Xu W, Cheung PCK. Occurrence and biosynthesis of carotenoids in phytoplankton. Biotechnology Advances. 2017;35(5):597–618. https://doi.org/10.1016/j.biotechadv.2017.05.001Huang JJ, Lin S, Xu W, Cheung PCK. Occurrence and biosynthesis of carotenoids in phytoplankton. Biotechnology Advances. 2017;35(5):597–618. https://doi.org/10.1016/j.biotechadv.2017.05.001Ribeiro D, Freitas M, Silva AMS, Carvalho F, Fernandes E. Antioxidant and pro-oxidant activities of carotenoids and their oxidation products. Food and Chemical Toxicology. 2018;120:681–699. https://doi.org/10.1016/j.fct.2018.07.060Ribeiro D, Freitas M, Silva AMS, Carvalho F, Fernandes E. Antioxidant and pro-oxidant activities of carotenoids and their oxidation products. Food and Chemical Toxicology. 2018;120:681–699. https://doi.org/10.1016/j.fct.2018.07.060Yu M, Chen M, Gui J, Huang S, Liu Y, Shentu H, et al. Preparation of Chlorella vulgaris polysaccharides and their antioxidant activity in vitro and in vivo. International Journal of Biological Macromolecules. 2019;137:139–150. https://doi.org/10.1016/j.ijbiomac.2019.06.222Yu M, Chen M, Gui J, Huang S, Liu Y, Shentu H, et al. Preparation of Chlorella vulgaris polysaccharides and their antioxidant activity in vitro and in vivo. International Journal of Biological Macromolecules. 2019;137:139–150. https://doi.org/10.1016/j.ijbiomac.2019.06.222Sukhikh SA, Budenkova EA, Boychenko Yu-DS, Anokhova VD, Dolganyuk VF, Kashirskih EV. Optimizing the production of polysaccharides from Cyanobacterium sp. IPPAS B-1200. Food Processing: Techniques and Technology. 2023; 53(3):630–641. (In Russ.). https://doi.org/10.21603/2074-9414-2023-3-2463Sukhikh SA, Budenkova EA, Boychenko Yu-DS, Anokhova VD, Dolganyuk VF, Kashirskih EV. Optimizing the production of polysaccharides from Cyanobacterium sp. IPPAS B-1200. Food Processing: Techniques and Technology. 2023; 53(3):630–641. (In Russ.). https://doi.org/10.21603/2074-9414-2023-3-2463Gürlek C, Yarkent Ç, Köse A, Tuğcu B, Gebeloğlu IK, Öncel SŞ, et al. Screening of antioxidant and cytotoxic activities of several microalgal extracts with pharmaceutical potential. Health and Technology. 2020;10:111–117. https://doi.org/10.1007/s12553-019-00388-3Gürlek C, Yarkent Ç, Köse A, Tuğcu B, Gebeloğlu IK, Öncel SŞ, et al. Screening of antioxidant and cytotoxic activities of several microalgal extracts with pharmaceutical potential. Health and Technology. 2020;10:111–117. https://doi.org/10.1007/s12553-019-00388-3Allen KM, Habte-Tsion H-M, Thompson KR, Filer K, Tidwell JH, Kumar V. Freshwater microalgae (Schizochytrium sp.) as a substitute to fish oil for shrimp feed. Scientific Reports. 2019;9:6178. https://doi.org/10.1038/s41598-019-41020-8Allen KM, Habte-Tsion H-M, Thompson KR, Filer K, Tidwell JH, Kumar V. Freshwater microalgae (Schizochytrium sp.) as a substitute to fish oil for shrimp feed. Scientific Reports. 2019;9:6178. https://doi.org/10.1038/s41598-019-41020-8Laroche C. Exopolysaccharides from microalgae and cyanobacteria: Diversity of strains, production strategies, and applications. Marine Drugs. 2022;20(5):336. https://doi.org/10.3390/md20050336Laroche C. Exopolysaccharides from microalgae and cyanobacteria: Diversity of strains, production strategies, and applications. Marine Drugs. 2022;20(5):336. https://doi.org/10.3390/md20050336Nacer W, Baba Ahmed FZ, Merzouk H, Benyagoub O, Bouanane S. Evaluation of the anti-inflammatory and antioxidant effects of the microalgae Nannochloropsis gaditana in streptozotocin-induced diabetic rats. Journal of Diabetes and Metabolic Disorders. 2020;19:1483–1490. https://doi.org/10.1007/s40200-020-00681-3Nacer W, Baba Ahmed FZ, Merzouk H, Benyagoub O, Bouanane S. Evaluation of the anti-inflammatory and antioxidant effects of the microalgae Nannochloropsis gaditana in streptozotocin-induced diabetic rats. Journal of Diabetes and Metabolic Disorders. 2020;19:1483–1490. https://doi.org/10.1007/s40200-020-00681-3Qiao H, Hu D, Ma J, Wang X, Wu H, Wang J. Feeding effects of the microalga Nannochloropsis sp. on juvenile turbot (Scophthalmus maximus L.). Algal Research. 2019;41:101540. https://doi.org/10.1016/j.algal.2019.101540Qiao H, Hu D, Ma J, Wang X, Wu H, Wang J. Feeding effects of the microalga Nannochloropsis sp. on juvenile turbot (Scophthalmus maximus L.). Algal Research. 2019;41:101540. https://doi.org/10.1016/j.algal.2019.101540Каширских Е. В., Асякина Л. К., Надцонов Д. Д. Исследование физико-химических свойств микроводорослей Балтийского моря // Вестник Балтийского федерального университета им. И. Канта. Серия: Естественные и медицинские науки. 2022. № 1. С. 88–97. https://www.elibrary.ru/DPEBHTKashirskikh EV, Asyakina LK, Nadtsonov DD. On physicochemical properties of microalgae of the Baltic Sea. Vestnik IKBFU. Natural and Medical Sciences. 2022;(1):88–97. (In Russ.). https://www.elibrary.ru/DPEBHTPereira H, Barreira L, Mozes A, Florindo C, Polo C, Duarte CV, et al. Microplate-based high throughput screening procedure for the isolation of lipid-rich marine microalgae. Biotechnology for Biofuels and Bioproducts. 2011;4:61. https://doi.org/10.1186/1754-6834-4-61Pereira H, Barreira L, Mozes A, Florindo C, Polo C, Duarte CV, et al. Microplate-based high throughput screening procedure for the isolation of lipid-rich marine microalgae. Biotechnology for Biofuels and Bioproducts. 2011;4:61. https://doi.org/10.1186/1754-6834-4-61López-Hernández J-F, Kean-Meng T, Asencio-Alcudia G-G, Asyraf-Kassim M, Alvarez-González C-A, Márquez-Rocha F-J. Sustainable microalgae and cyanobacteria biotechnology. Applied Sciences. 2022;12(14):6887. https://doi.org/10.3390/app12146887López-Hernández J-F, Kean-Meng T, Asencio-Alcudia G-G, Asyraf-Kassim M, Alvarez-González C-A, Márquez-Rocha F-J. Sustainable microalgae and cyanobacteria biotechnology. Applied Sciences. 2022;12(14):6887. https://doi.org/10.3390/app12146887Temraleeva AD, Dronova SA, Moskalenko SV, Didovich SV. Modern methods for isolation, purification, and cultivation of soil cyanobacteria. Microbiology. 2016;85:389–399. https://doi.org/10.1134/S0026261716040159Temraleeva AD, Dronova SA, Moskalenko SV, Didovich SV. Modern methods for isolation, purification, and cultivation of soil cyanobacteria. Microbiology. 2016;85:389–399. https://doi.org/10.1134/S0026261716040159Gao S, Kong Y, Yu J, Miao L, Ji L, Song L, et al. Isolation of axenic cyanobacterium and the promoting effect of associated bacterium on axenic cyanobacterium. BMC Biotechnology. 2020;20:61. https://doi.org/10.1186/s12896-020-00656-5Gao S, Kong Y, Yu J, Miao L, Ji L, Song L, et al. Isolation of axenic cyanobacterium and the promoting effect of associated bacterium on axenic cyanobacterium. BMC Biotechnology. 2020;20:61. https://doi.org/10.1186/s12896-020-00656-5Takahashi T. Routine management of microalgae using autofluorescence from chlorophyll. Molecules. 2019;24(24): 4441. https://doi.org/10.3390/molecules24244441Takahashi T. Routine management of microalgae using autofluorescence from chlorophyll. Molecules. 2019;24(24): 4441. https://doi.org/10.3390/molecules24244441Dolganyuk VF, Kashirskikh EV, Budenkova EA, Andreeva AP, Sukhikh SA. Study of morphological features and growth parameters of psychrophilic microalgae and cyanobacteria. Food Systems. 2022;5(4):289–297. (In Russ.). https://doi.org/10.21323/2618-9771-2022-5-4-289-297Dolganyuk VF, Kashirskikh EV, Budenkova EA, Andreeva AP, Sukhikh SA. Study of morphological features and growth parameters of psychrophilic microalgae and cyanobacteria. Food Systems. 2022;5(4):289–297. (In Russ.). https://doi.org/10.21323/2618-9771-2022-5-4-289-297Chaves N, Santiago A, Alías JC. Quantification of the antioxidant activity of plant extracts: Analysis of sensitivity and hierarchization based on the method used. Antioxidants. 2020;9(1):76. http://doi.org/10.3390/antiox9010076Chaves N, Santiago A, Alías JC. Quantification of the antioxidant activity of plant extracts: Analysis of sensitivity and hierarchization based on the method used. Antioxidants. 2020;9(1):76. http://doi.org/10.3390/antiox9010076Oleinik G, Dario PP, de Morais Gasperin K, Benvegnú DM, Lima FO, Soares LC, et al. In vitro antioxidant extracts evaluation from the residue of the Hevea brasiliensis seed. Scientific Reports. 2022;12:480. http://doi.org/10.1038/s41598-021-04017-wOleinik G, Dario PP, de Morais Gasperin K, Benvegnú DM, Lima FO, Soares LC, et al. In vitro antioxidant extracts evaluation from the residue of the Hevea brasiliensis seed. Scientific Reports. 2022;12:480. http://doi.org/10.1038/s41598-021-04017-wCoulombier N, Jauffrais T. Lebouvier N. Antioxidant compounds from microalgae: A review. Marine Drugs. 2021; 19(10):549. https://doi.org/10.3390/md19100549Coulombier N, Jauffrais T. Lebouvier N. Antioxidant compounds from microalgae: A review. Marine Drugs. 2021; 19(10):549. https://doi.org/10.3390/md19100549Duarte TL, Lunec J. Review: When is an antioxidant not an antioxidant? A review of novel actions and reactions of vitamin C. Free Radical Research. 2005;39(7):671–686. https://doi.org/10.1080/10715760500104025Duarte TL, Lunec J. Review: When is an antioxidant not an antioxidant? A review of novel actions and reactions of vitamin C. Free Radical Research. 2005;39(7):671–686. https://doi.org/10.1080/10715760500104025Sharma P, Jha AB, Dubey RS, Pessarakli M. Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. Journal of Botany. 2012;2012:21703. https://doi.org/10.1155/2012/217037Sharma P, Jha AB, Dubey RS, Pessarakli M. Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. Journal of Botany. 2012;2012:21703. https://doi.org/10.1155/2012/217037Richards SL, Wilkins KA, Swarbreck SM, Anderson AA, Habib N, Smith AG, et al. The hydroxyl radical in plants: From seed to seed. Journal of Experimental Botany. 2015;66(1):37–46. https://doi.org/10.1093/jxb/eru398Richards SL, Wilkins KA, Swarbreck SM, Anderson AA, Habib N, Smith AG, et al. The hydroxyl radical in plants: From seed to seed. Journal of Experimental Botany. 2015;66(1):37–46. https://doi.org/10.1093/jxb/eru398Дружинина А. С. Флоротаннины арктических бурых водорослей: дис. … канд. хим. наук. Архангельск, 2019. 120 с.Druzhinina AS. Phlorotannins in Arctic brown algae. Cand. Sci. Chem. diss. Arkhangelsk: Northern (Arctic) Federal University named after M.V. Lomonosov; 2019. 120 p. (In Russ.). [Дружинина А. С. Флоротаннины арктических бурых водорослей: дис. … канд. хим. наук. Архангельск, 2019. 120 с.Перспектива развития технологии производства микроводорослей / С. М. Шинкарев [и др.] // Вестник технологического университета. 2017. Т. 20. № 14. С. 146–149. https://www.elibrary.ru/WQMOEQShinkarev CM, Samujlenko AI, Grin SA, Neminuschiy LA, Skotnikova TA, Pavlenko IV, et al. Prospects for the development of microalgae production technology. Bulletin of the Technological University. 2017;20(14):146–149. (In Russ.). https://www.elibrary.ru/WQMOEQСравнительное изучение антиоксидантной активности растительных сборов / С. Р. Хасанова [и др.] // Вестник Воронежского государственного университета. Серия: Химия. Биология. Фармация. 2007. № 1. С. 163–166. https://www.elibrary.ru/KWHQXLHasanova SR, Plehanova TI, Gashimova DT, Galiahmetova EH, Klysh EA. Comparative reseach of antioxydant activity vegetative gathering. Proceedings of Voronezh State University. Series: Chemistry. Biology. Pharmacy. 2007;(1):163– 166. (In Russ.). https://www.elibrary.ru/KWHQXLMarques AEML, Balen RE, da Silva Pereira Fernandes L, Motta CM, de Assis HCS, Taher DM, et al. Diets containing residual microalgae biomass protect fishes against oxidative stress and DNA damage. Journal of Applied Phycology. 2019;31:2933–2940. https://doi.org/10.1007/s10811-019-01825-6Marques AEML, Balen RE, da Silva Pereira Fernandes L, Motta CM, de Assis HCS, Taher DM, et al. Diets containing residual microalgae biomass protect fishes against oxidative stress and DNA damage. Journal of Applied Phycology. 2019;31:2933–2940. https://doi.org/10.1007/s10811-019-01825-6Ranga Rao A, Raghunath Reddy RL, Baskaran V, Sarada R, Ravishankar GA. Characterization of microalgal carotenoids by mass spectrometry and their bioavailability and antioxidant properties elucidated in rat model. Journal of Agricultural and Food Chemistry. 2010;58(15):8553–8559. https://doi.org/10.1021/jf101187kRanga Rao A, Raghunath Reddy RL, Baskaran V, Sarada R, Ravishankar GA. Characterization of microalgal carotenoids by mass spectrometry and their bioavailability and antioxidant properties elucidated in rat model. Journal of Agricultural and Food Chemistry. 2010;58(15):8553–8559. https://doi.org/10.1021/jf101187kRahman NA, Khatoon H, Yusuf N, Banerjee S, Haris NA, Lananan F, et al. Tetraselmis chuii biomass as a potential feed additive to improve survival and oxidative stress status of Pacific white-leg shrimp Litopenaeus vannamei postlarvae. International Aquatic Research. 2017;9:235–247. https://doi.org/10.1007/s40071-017-0173-2Rahman NA, Khatoon H, Yusuf N, Banerjee S, Haris NA, Lananan F, et al. Tetraselmis chuii biomass as a potential feed additive to improve survival and oxidative stress status of Pacific white-leg shrimp Litopenaeus vannamei postlarvae. International Aquatic Research. 2017;9:235–247. https://doi.org/10.1007/s40071-017-0173-2McKenzie CH, Bates SS, Martin JL, Haigh N, Howland KL, Lewis NI, et al. Three decades of Canadian marine harmful algal events: Phytoplankton and phycotoxins of concern to human and ecosystem health. Harmful Algae. 2021;102:101852. https://doi.org/10.1016/j.hal.2020.101852McKenzie CH, Bates SS, Martin JL, Haigh N, Howland KL, Lewis NI, et al. Three decades of Canadian marine harmful algal events: Phytoplankton and phycotoxins of concern to human and ecosystem health. Harmful Algae. 2021;102:101852. https://doi.org/10.1016/j.hal.2020.101852

The authors declare that there are no conflicts of interest present.