Daily dynamics of polyphenol accumulation in cells of Fucus vesiculosus L. and Ascophyllum nodosum (L.) Le Jolis during the polar day on the Barents Sea coast
Main
Google Scholar
Details
Abstract
Polyphenols are a group of secondary metabolites that protect the organism from ultraviolet radiation, participate in plant metabolism, and also have therapeutic properties. Studying the dynamics of polyphenol accumulation in brown algae (Phaeophyceae: Fucales) is of considerable interest for understanding the mechanisms of their adaptation to changing environment. The aim of the work is to reveal daily changes in polyphenol content in cells of Fucus vesiculosus Linnaeus and Ascophyllum nodosum (Linnaeus) Le Jolis inhabiting the Barents Sea coast, to analyze the dependence of their accumulation on light and temperature, and to determine the role of endogenous rhythms and external factors in the regulation of polyphenol metabolism in cells. The study was carried out in July 2022 and 2023 on the Barents Sea coast (both in the natural environment and in a laboratory). The Folin–Ciocalteu spectrophotometric method was used to analyze polyphenol content. The significant daily dynamics of polyphenols was shown. The key changes in their content occur in the natural environment: during the daytime and during low tide, when thalli dry out. During high tide, when thalli are submerged, the concentration of polyphenols does not change. Polyphenol content depends on a combination of light level, temperature, and cycles of drying and rewettering. In a laboratory, the daily rhythm of changes in polyphenol concentration is not preserved, which may indicate a reduced role of endogenous rhythms and the predominant role of environmental factors in the regulation of polyphenol synthesis. The data obtained expand information on Fucales physiological and biochemical features in the Arctic zone, as well as on mechanisms of algal adaptation to the tidal zone of seas. The results can be used in the development of algae aquaculture technology to obtain raw materials with desired properties.
Authors
References
Боголицын К. Г., Дружинина А. С., Овчинников Д. В., Каплицин П. А., Шульгина Е. В., Паршина А. Э. Полифенолы бурых водорослей // Химия растительного сырья. 2018. № 3. С. 5–21. [Bogolitsyn K. G., Druzhinina A. S., Ovchinnikov D. V., Kaplitsin P. A., Shulgin E. V., Parshina A. E. Polyphenols of brown algae. Khimiya rastitel’nogo syr’ya, 2018, no. 3, pp. 5–21. (in Russ.)]. https://doi.org/10.14258/jcprm.2018031898
Растения и лишайники мурманского побережья Баренцева моря : полевой атлас. Петрозаводск : Изд-во ПетрГУ, 2016. 191 с. [Rasteniya i lishainiki murmanskogo poberezh’ya Barentseva morya : field atlas. Petrozavodsk : Izd-vo PetrGU, 2016, 191 p. (in Russ.)]
Рыжик И. В., Фисак Е. М. Годовая динамика содержания растворимых флоротаннинов в клетках Fucus vesiculosus L. и возможное их участие в процессах репарации тканей // Вопросы современной альгологии. 2018. № 1 (16). [Ryzhik I. V., Fisak E. M. The annual dynamics of the content of soluble phlorotannins in the cells of Fucus vesiculosus L. and their possible role in the repair processes of damaged tissue. Voprosy sovremennoi al’gologii, 2018, no. 1 (16). (in Russ.)]. URL: http://algology.ru/1248 [accessed: 29.09.2024].
Ткач А. В., Облучинская Е. Д. Стерины и полифенолы фукоидов мурманского побережья Баренцева моря // Вестник МГТУ. Труды Мурманского государственного технического университета. 2017. Т. 20, № 2. С. 326–335. [Tkach A. V., Obluchinskaya E. D. Sterols and polyphenols of fucoids from the Murmansk coast of the Barents Sea. Vestnik MGTU. Trudy Murmanskogo gosudarstvennogo tekhnicheskogo universiteta, 2017, vol. 20, no. 2, pp. 326–335. (in Russ.)]. https://elibrary.ru/zchvlx
Abdala-Díaz R. T., Cabello-Pasini A., Pérez-Rodríguez E., Conde Álvarez R. M., Figueroa F. L. Daily and seasonal variations of optimum quantum yield and phenolic compounds in Cystoseira tamariscifolia (Phaeophyta). Marine Biology, 2006, vol. 148, iss. 3, pp. 459–465. https://doi.org/10.1007/s00227-005-0102-6
Aminina N. M., Vishnevskaya T. I., Karaulova E. P., Epur N. V., Yakush E. V. Prospects for the use of commercial and potentially commercial brown algae of the Far Eastern seas as a source of polyphenols. Russian Journal of Marine Biology, 2020, vol. 46, iss. 1, pp. 34–41. https://doi.org/10.1134/s1063074020010022
Arnold T. M., Targett N. M. Evidence for metabolic turnover of polyphenolics in tropical brown algae. Journal of Chemical Ecology, 2000, vol. 26, iss. 6, pp. 1393–1410. https://doi.org/10.1023/a:1005588023887
Arnold T. M., Targett N. M. Quantifying in situ rates of phlorotannin synthesis and polymerization in marine brown algae. Journal of Chemical Ecology, 1998, vol. 24, iss. 3, pp. 577–595. https://doi.org/10.1023/a:1022373121596
Connan S. Etude de la diversité spécifique des macroalgues de la Pointe de Bretagne et analyse des composés phénoliques des Phéophycées dominantes. PhD thesis. Brest, 2004.
Connan S., Delisle F., Deslandes E., Ar Gall E. Intra-thallus phlorotannin content and antioxidant activity in Phaeophyceae of temperate waters. Botanica Marina, 2006, vol. 49, iss. 1, pp. 39–46. https://doi.org/10.1515/bot.2006.005
Connan E., Deslandes E., Ar Gall E. Influence of day–night and tidal cycles on phenol content and antioxidant capacity in three temperate intertidal brown seaweeds. Journal of Experimental Marine Biology and Ecology, 2007, vol. 349, iss. 2, pp. 360–365. https://doi.org/10.1016/j.jembe.2007.05.028
Connan S., Goulard F., Stiger V., Deslandes E., Ar Gall E. Interspecific and temporal variation in phlorotannin levels in an assemblage of brown algae. Botanica Marina, 2004, vol. 47, iss. 5, pp. 410–416. https://doi.org/10.1515/bot.2004.057
Dubois A., Iken K. Seasonal variation in kelp phlorotannins in relation to grazer abundance and environmental variables in the Alaskan sublittoral zone. Algae, 2012, vol. 27, no. 1, pp. 9–19. https://doi.org/10.4490/algae.2012.27.1.009
Gómez I., Huovinen P. Induction of phlorotannins during UV exposure mitigates inhibition of photosynthesis and DNA damage in the kelp Lessonia nigrescens. Photochemistry and Photobiology, 2010, vol. 86, iss. 5, pp. 1056–1063. https://doi.org/10.1111/j.1751-1097.2010.00786.x
Ilvessalo H., Tuomi J. Nutrient availability and accumulation of phenolic compounds in the brown alga Fucus vesiculosus. Marine Biology, 1989, vol. 101, iss. 1, pp. 115–119. https://doi.org/10.1007/bf00393484
Jennings J. G., Steinberg P. D. Phlorotannins versus other factors affecting epiphyte abundance on the kelp Ecklonia radiata. Oecologia, 1997, vol. 109, iss. 3, pp. 461–473. https://doi.org/10.1007/s004420050106
Jormalainen V., Honkanen T., Koivikko R., Eränen J. Induction of phlorotannin production in a brown alga: Defense or resource dynamics? Oikos, 2003, vol. 103, no. 3, pp. 640–650. https://doi.org/10.1034/j.1600-0706.2003.12635.x
Kamiya M., Nishio T., Yokoyama A., Yatsuya K., Nishigaki T., Shinya Y., Ohki K. Seasonal variation of phlorotannin in sargassacean species from the coast of the Sea of Japan. Phycological Research, 2010, vol. 58, iss. 1, pp. 53–61. https://doi.org/10.1111/j.1440-1835.2009.00558.x
Karapetyan S., Dong X. Redox and the circadian clock in plant immunity: A balancing act. Free Radical Biology and Medicine, 2018, vol. 119, pp. 56–61. https://doi.org/10.1016/j.freeradbiomed.2017.12.024
Klindukh M. P., Ryzhik I. V., Makarov M. V. Influence of environmental factors on the contents of free amino acids in Fucus vesiculosus in the Barents Sea during the day. E3S Web of Conferences, 2023, vol. 390, iss. 2, art. 05008 (6 p.). https://doi.org/10.1051/e3sconf/202339005008
Koivikko R., Loponen J., Honkanen T., Jormalainen V. Contents of soluble, cell-wall-bound and exuded phlorotannins in the brown alga Fucus vesiculosus, with implications on their ecological functions. Journal of Chemical Ecology, 2005, vol. 31, iss. 1, pp. 195–212. https://doi.org/10.1007/s10886-005-0984-2
Makarov M. V., Ryzhik I. V., Voskoboinikov G. M. The effect of Fucus vesiculosus L. (Phaeophyceae) depth of vegetation in the Barents Sea (Russia) on its morphophysiological parameters. International Journal on Algae, 2013, vol. 15, iss. 1, pp. 77–90. https://doi.org/10.1615/interjalgae.v15.i1.60
Mannino A. M., Vaglica V., Oddo E. Seasonal variation in total phenolic content of Dictyopteris polypodioides (Dictyotaceae) and Cystoseira amentacea (Sargassaceae) from the Sicilian coast. Flora Mediterranea, 2014, vol. 24, pp. 39–50. https://doi.org/10.7320/flmedit24.039
Mezghani S., Dezső C., Bourguiba I., Hohmann J., Mohamed A., Bouaziz M. Characterization of phenolic compounds of Ulva rigida (Chlorophycae) and its antioxidant activity. European Journal of Medicinal Plants, 2016, vol. 12, iss. 1, art. ejmp.22935 (9 p.). https://doi.org/10.9734/ejmp/2016/22935
Parys S., Kehraus S., Pete R., Küpper F. C., Glombitza K.-W., König G. M. Seasonal variation of polyphenolics in Ascophyllum nodosum (Phaeophyceae). European Journal of Phycology, 2009, vol. 44, iss. 3, pp. 331–338. https://doi.org/10.1080/09670260802578542
Pavia H., Brock E. Extrinsic factors influencing phlorotannin production in the brown alga Ascophyllum nodosum. Marine Ecology Progress Series, 2000, vol. 193, pp. 285–294. https://doi.org/10.3354/meps193285
Pavia H., Cervin G., Lindgren A., Åberg P. Effects of UV-B radiation and simulated herbivory on phlorotannins in the brown alga Ascophyllum nodosum. Marine Ecology Progress Series, 1997, vol. 157, pp. 139–146. https://doi.org/10.3354/meps157139
Pavia H., Toth G. B. Influence of light and nitrogen on the phlorotannin content of the brown seaweeds Ascophyllum nodosum and Fucus vesiculosus. Hydrobiologia, 2000, vol. 440, iss. 1–3, pp. 299–305. https://doi.org/10.1023/a:1004152001370
Peckol P., Krane J. M., Yates J. L. Interactive effects of inducible defense and resource availability on phlorotannins in the North Atlantic brown alga Fucus vesiculosus. Marine Ecology Progress Series, 1996, vol. 138, pp. 209–217. https://doi.org/10.3354/meps138209
Pedersen A. Studies on phenol content and heavy metal uptake in fucoids. Hydrobiologia, 1984, vol. 116, iss. 1–3, pp. 498–504. https://doi.org/10.1007/bf00027732
Ragan M. A., Jensen A. Quantitative studies on brown algal phenols. II. Seasonal variation in polyphenol content of Ascophyllum nodosum (L.) Le Jol. and Fucus vesiculosus (L.). Journal of Experimental Marine Biology and Ecology, 1978, vol. 34, iss. 3, pp. 245–258. https://doi.org/10.1016/s0022-0981(78)80006-9
Ragan M. A., Glombitza K. W. Phlorotannins, brown algal polyphenols. In: Progress in Phycological Research / F. E. Round, D. J. Chapman (Eds). Bristol, UK : Biopress, 1986, vol. 4, pp. 129–241.
Reboleira J., Silva S., Chatzifragkou A., Niranjan K., Lemos M. F. L. Seaweed fermentation within the fields of food and natural products. Trends in Food Science & Technology, 2021, vol. 116, pp. 1056–1073. https://doi.org/10.1016/j.tifs.2021.08.018
Rönnberg O., Ruokolahti C. Seasonal variation of algal epiphytes and phenolic content of Fucus vesiculosus in a northern Baltic archipelago. Annales Botanici Fennici, 1986, vol. 23, no. 4, pp. 317–323.
Ryzhik I. V. Seasonal variations in the metabolic activity of cells of Fucus vesiculosus Linnaeus, 1753 (Phaeophyta: Fucales) from the Barents Sea. Russian Journal of Marine Biology, 2016, vol. 42, iss. 5, pp. 433–436. https://doi.org/10.1134/s1063074016050102
Schoenwaelder M. E. A. The occurrence and cellular significance of physodes in brown algae. Phycologia, 2002, vol. 41, iss. 2, pp. 125–139. https://doi.org/10.2216/i0031-8884-41-2-125.1
Schoenwaelder M. E. A., Clayton M. N. The presence of phenolic compounds in isolated cell walls of brown algae. Phycologia, 1999, vol. 38, iss. 3, pp. 161–166. https://doi.org/10.2216/i0031-8884-38-3-161.1
Steinberg P. D. Effects of quantitative and qualitative variation in phenolic compounds on feeding in three species of marine invertebrate herbivores. Journal of Experimental Marine Biology and Ecology, 1988, vol. 120, iss. 3, pp. 221–237. https://doi.org/10.1016/0022-0981(88)90003-2
Steinberg P. D. Seasonal variation in the relationship between growth rate and phlorotannin production in the kelp Ecklonia radiata. Oecologia, 1995, vol. 102, iss. 2, pp. 169–173. https://doi.org/10.1007/bf00333248
Van Alstyne K. L., McCarthy III J. J., Hustead C. L., Duggins D. O. Geographic variation in polyphenolic levels of Northeastern Pacific kelps and rockweeds. Marine Biology, 1999, vol. 133, iss. 2, pp. 371–379. https://doi.org/10.1007/s002270050476
Van Alstyne K. L., Whitman S. L., Ehlig J. M. Differences in herbivore preferences, phlorotannin production, and nutritional quality between juvenile and adult tissues from marine brown algae. Marine Biology, 2001, vol. 139, iss. 1, pp. 201–210. https://doi.org/10.1007/s002270000507
