Marine red algae as an inexhaustable source of biologically active substances for medicine and pharmaceutics
https://doi.org/10.36038/2307-3497-2022-188-151-165
Abstract
The aim: To study the composition and properties of biologically active substances (BAS) from marine red algae.
Result: Summary data on the composition and properties of biologically active substances in red algae (Rhodophyta) growing in the Seas of the World Ocean, as well as in the coastal zones of the White Sea of Russia, published by Foreign and Russian authors, including the authors of the article, were presented. Marine red algae are considered as sources of natural highly active substances with a variety of biological properties that have a positive effect on human health.
Novelty: Review data on a wide range of red algae biological activities from the World Ocean and new data on the antimicrobial activity of extracts from Ahnfeltia plicata, Polysiphonia fucoides, etc. are presented. It was found that alcoholic extracts from P. fucoides have antimicrobial activity against cultures of S. aureus «Viotko» and L. monocytogenes 766, and SC–CO2 extracts from P. fucoides — against L. monocytogenes.
Practical significance: The traditional use of red algae for the production of agar and carrageenans — natural gelling agents, as well as directly for food and for the production of therapeutic and prophylactic, medical products and pharmaceuticals has been shown.
Methods used: Data on the composition and properties of biologically active substances (BAS) of marine red algae are given with the involvement of a review of foreign published works and the results of our own studies of red algae from the White Sea and extracts from them. During the research, modern instrumental methods and high-precision laboratory equipment were used.
About the Authors
A. V. Podkorytova
Russian Federal Research Institute of Fisheries and Oceanography («VNIRO»)
Russian Federation
Russian Federation
Antonina V. Podkorytova
105187
19, Okruzhnoy proezd
Moscow
T. A. Ignatova
Russian Federal Research Institute of Fisheries and Oceanography («VNIRO»)
Russian Federation
Russian Federation
Tatyana A. Ignatova
105187
19, Okruzhnoy proezd
Moscow
References
1. Blinova E. I. 2007. Algae-macrophytes and grasses of the Seas of the European part of Russia (flora, distribution, biology, reserves, mariculture). Moscow: VNIRO Publish. 114 p. (In Russ.).
2. Bukeeva A. B., Kudaibergenova S. Zh. 2012. Review of modern methods for isolating bioactive substances from plants // Vestnik ENU L. N. Gumilyov. No. 2. Pp. 192–197. (In Russ.).
3. Vinogradova K. L. 1986. The genera Chaetomorpha Kutz and Rhizoclonium Kutz. (Siphonocladales) in the northern seas of the USSR // News of taxonomy of lower plants. T. 23. P. 13–25. (In Russ.).
4. Vozzhinskaya V. B. 1986. Bottom macrophytes of the White Sea. Moscow: Nauka. 192 p. (In Russ.).
5. Glubokovsky M. K., S. N. Tarasyuk, L. M. Zver’kova, L. V. Semenyak, N. N. Murzov, N. V. Petrova, S. Yu. 2012. Raw material base of Russian fisheries in 2012: Areas of Russian jurisdiction // Reference and analytical materials. Moscow: VNIRO Publish. Pp. 332–333. (In Russ.).
6. Ermak I. M., Khotimchenko S. Yu. 1997. Physical and chemical properties, application and biological activity of carrageenan — a polysaccharide of red algae // Biology of the sea. T. 23. No. 3. Pp. 129–142.
7. Zinova A. D. 1950. About some features of the flora of the White Sea // Trudy All-Union. hydrobiol. sosiety. T. 2. P. 231–252. (In Russ.).
8. Zinova A. D. 1962. On the issue of phytogeographic (zonal) zoning of the coastal strip of the World Ocean // Commission for Fishery Research of the Western Pacific: Conf. jointly research flora and fauna: Proceedings. report L.: Zool. Institute of the Academy of Sciences of the USSR. 11 p. (In Russ.).
9. Zolotukhina E. Yu., Gavrilenko E. E. 1989. Heavy metals in aquatic plants. Accumulation and toxicity // Nauch. report Higher Schools. Biol. Science. No. 9. P. 93–106. (In Russ.).
10. Ignatova T. A., Podkorytova A. V. 2021. Chemical and technological characteristics of red algae of the northern fishery basin // II Intern. scient. and pract. conf. «Innovative directions of integration of science, education and production». Kerch. pp. 227–230. (In Russ.).
11. Ignatova T. A., Podkorytova A. V., Baskakova Yu.A., Mulyanova M. P. 2021. New data on the biological activity of extracts from red algae (Rhodophyceae) and methods for their production // Proc. of the IX Intern. Baltic Sea Forum. V. 4. X Anniversary Internat. Scient. and Pract. Conf. «Food and Marine Biotechnology». Kaliningrad: BSARF Publish. pp. 40–49. (In Russ.).
12. Kizevetter I. V., Sukhoveeva M. V., Shmelkova L. P. 1981. Seaweeds and grasses of the Far Eastern seas. Moscow: Food industry. 113 p. (In Russ.).
13. Kizevetter I. V., Gruner V. S., Evtushenko V. A. 1967. Processing of seaweed and other commercial aquatic plants. Moscow: Food industry. 407 p. (In Russ.).
14. Mikhailova T. A. 2019. Vegetation of the Red Algae Belt of the White Sea (European Arctic, Russia) // News of Systematics of Lower Plants No. 53(1). Pp. 39–65. (In Russ.).
15. Nazarova I. V., Shevchenko N. M., Kovalev B. M., Khotimchenko Yu. S. 1998. Immunomodulatory properties of polysaccharides from red algae: influence on the complement system // Biology of the sea. T. 24. No. 1. P. 49–52. (In Russ.).
16. Pisareva N. A., Klochkova N. G. 2013. Brief review of modern taxonomy of red algae // Bull. of the Kamchatka STU. No. 23. P. 64–72. (In Russ.).
17. Podkorytova A. V., Vafina L. Kh. 2013. Chemical composition of brown algae of the Black Sea: the genus Cystoseira, the prospect of their use // Trudy VNIRO. V. 150. P. 100–107. (In Russ.).
18. Podkorytova A. V., Ignatova T. A., Burova N. V., Usov A. I. 2019. Promising directions for the rational use of commercial red algae of the genus Ahnfeltia, harvested in the coastal zones of the Russian seas // Trudy VNIRO. V. 176. P. 14–26. (In Russ.).
19. Sinovich A. D., Pavlov G. P. 1998. Phenols // Chemical Encyclopedia: in 5 volumes / Zefirov N. S. (chief editor). V. 5. Moscow: Great Russian Encyclopedia. 783 p. (In Russ.).
20. Khotimchenko S. V. 2003. Lipids of marine macrophytic algae and grasses. Structure, distribution, analysis. Vladivostok: Dalnauka. 230 p. (In Russ.).
21. Khristoforova N. K., Chernova E. N. 2005. Comparison of the content of heavy metals in brown algae and sea grasses // Reports of the Academy of Sciences. T. 400. No. 4. P. 571–573. (In Russ.).
22. Tsikhmeistr E. V., Gumerov F. M. 2012. Application of sub- and supercritical fluids in extraction processes // Bulletin of the Kazan Technological University. No. 10. Pp. 98–99. (In Russ.).
23. Chernova V. G., Levitsky A. L. 2019. The content of heavy metals in the coastal ecosystem of the Solovetsky Islands of the White Sea // Proc. of the II Nat. Scient. and Pract. Conf. Actual Probl. of Biodiversity and Nature Management. Simferopol: Arial. Pp. 238–244. (In Russ.).
24. Alkhalaf M. I. 2020. Chemical composition, antioxidant, antiinflammatory and cytotoxic effects of Chondrus crispus species of red algae collected from the Red Sea along the shores of Jeddah city // J. of King Saud University Science. P. 1–6. https://doi.org/10.1016/j.jksus.2020.10.007
25. Allmendinge, A., Spavieri J., Kaiser M., Casey R., Hingley-Wilson S., Lalvani A., Guiry M., Blunden G., Tasdemir D. 2010. Antiprotozoal, antimycobacterial and cytotoxicpotential of twenty-three british and irish red algae // Phytother. Res. № 24. Р. 1099–1103. DOI:10.1002/ptr.3094.
26. Alves E., Dias M., Lopes D., Almeida A., Domingues M. do R., Rey F. 2020. Antibiotics (Basel). Аntimicrobial Lipids from Plants and Marine Organisms // An Overview of the Current State-of-the-Art and Future Prospects. № 9, 441. P. 1–88. DOI:10.3390/antibiotics9080441.
27. Bansemir A., Blume M., Schröder S., Lindequist U. 2006. Screening of cultivated seaweeds for antibacterial activity against fish pathogenic bacteria // Aquaculture. № 252. Р. 79–84. https://doi.org/10.1016/j.aquaculture.2005.11.051.
28. Bansemir A., Just N., Michalik M., Lindequist U., Lalk М. 2004. Extracts and sesquiterpene derivatives from the red alga Laurencia chondrioides with antibacterial activity against fish and human pathogenic bacteria // Chem. Biodiv. 1(3). P. 463–7. DOI:10.1002/cbdv.200490039.
29. Barroso N., Rodriguez M. 1996. Action of β-phenylethylamine and related amines on nigrostriatal dopamine neurotransmission // Eur. J. pharmacol. № 297. Р. 195–203. DOI:10.1016/0014–2999(95)00757–1.
30. Chen H. M., Zheng L., Yan X. J. 2005. The Preparation and Bioactivity Research of Agaro-Oligosaccharides Agaro-Bioactivity Research of Oligosaccharides // Food Technol. Biotechnol. № 43 (1). Р. 29– 36.
31. Chen H. M., Yan X., Zhu P., Jing L. 2006. Antioxidant activity and hepatoprotective potential of agaro-oligosaccharides in vitro and in vivo // Nutrition Journal. V. 5. № 31. P. 1–12.
32. Cortés Y., Hormazábal E., Leal H., Urzúa A., Mutis A., Parra L., Quiroz A. 2014. Novel antimicrobial activity of a dichloromethane extract obtained from red seaweed Ceramium rubrum (Hudson) (Rhodophyta: Florideophyceae) against Yersinia ruckeri and Saprolegnia parasitica, agents that cause diseases in salmonids // Electronic J. of Biotechnology. № 17. Р. 126–131. https://doi.org/10.1016/j.ejbt.2014.04.005.
33. DaYong S., Feng X., Juan H., Jing L., Xiao F., Li Jun Han Shi D., Xu F., He J., Li J., Fan X., Han L. 2008. Inhibition of bromophenols against ptp1b and antihyperglycemic effect of Rhodomela confervoides extract in diabetic rats // Sci. Bull. № 53. Р. 2476–2479. DOI:10.1007/s11434–008–0353-y.
34. De Almeida C. L. F., De S. Falcao H., De M. Lima G. R., De A. Montenegro C., Lira N. S., De Athayde-Filho P. F., Rodrigues L. C., De Souza M. de F. V., Barbosa-Filho J. M., Batista L. M. 2011. Bioactivities from Marine Algae of the Genus Gracilaria // Int. J. Mol. Sci. № 12. Р. 4550–4573. DOI:10.3390/ijms12074550.
35. Dubber D., Harder T. 2008. Extracts of Ceramium rubrum, Mastocarpus stellatus and Laminaria digitata inhibit growth of marine and fish pathogenic bacteria at ecologically realistic concentrations // Aquaculture. № 274. Р. 196–200. https://doi.org/10.1016/j.aquaculture.2007.11.029.
36. Enoki T, Sagawa H., Tominaga T., Nishiyama E., Koyama N., Sakai T., Yu F. G., Ikai K., Kato I. 2003. Drugs, foods or drinks with the use of algae-derived physiologically active substances // US Patent 0105029 A1. Р. 1–5.
37. Fard S. G., Tan R., Ajwad Awad Mohammed, Goh Yong Meng, Sharifah Kharidah Syed Muhamad, Karim Alwan AL-Jashamy, Suhaila Mohamed. 2011. Wound healing properties of Eucheuma cottonii extracts in Sprague-Dawley rats // J. of Medicinal Plants Research. V. 5(27). Р. 6373–6380. DOI:10.5897/JMPR10.902.
38. Flodin C., Whitfield F. B. 2000. Brominated anisols and crecols in the red alga Polysiphonia sphaerocarpa // Photochemistry. V.53, № 1. P. 77–80. DOI:10.1016/s0031–9422(99)00429-x.
39. Gamal Ali A. El. 2010. Biological importance of marine algae // Saudi Pharmaceutical Journal. 18. Р. 1–25. https://doi.org/10.1016/j.jsps.2009.12.001
40. Güner A., Ülkü Karabay Yavaşoğlu N. 2018. Evaluation of Antioxidant, Antimicrobial and Antimutagenic Activity with Irritation Effects of Ceramium rubrum (Red Algae) Extract // International J. of Secondary Metabolite. V. 5. № 4. P. 279–287. DOI:10.21448/ijsm.432654.
41. Güven K. C., Percot A., Sezik E. 2010. Alkaloids in Marine Algae // Mar. Drugs. 8. Р. 269–284. DOI:10.3390/md8020269.
42. Guven K. C., Bora A., Sunam G. 1969. Alkaloid content of marine algae. I. Hordenine from Phyllophora nervosa // Eczacılık Bul. № 11. Р. 177–184.
43. Hapke H. J., Strathmann W. 1995. Pharmacological effects of hordenine // Deutsche tierärztliche Wochenschrift. № 102. Р. 228–232.
44. Ignatova T. A., Podkorytova A. V. 2021. Red alga Polysiphonia fucoides growing in community with Ahnfeltia plicata, its influence on the yield and quality of agar// IOP Conf. Series: Earth and Environmental Science 848. P. 1–6. doi:10.1088/1755–1315/848/1/012206.
45. Ira A. Levine, Dinabandhu Sahoo. 2010. Porphyra. Harvesting Gold from the Sea. I. K. International Publishing House. 92 p.
46. Ireland C. M., Copp B. R., Foster M. P., McDonald L.A., Radisky D. C., Swersey C. 1993. Biomedical potential of marine natural products // Pharmaceutical and Bioactive Natural Products Attaway DH, Zaborsky OR (eds). Plenum Publishing Corporation: NewYork. Р. 1–37. https://doi.org/10.1007/978–1–4899–2391–2_1
47. Islam M. R., Mikami D., Kurihara H. 2017. Two new algal bromophenols from Odonthalia corymbifera // Tetrahedron Lett. № 58. Р. 4119– 4121. DOI:10.1021/np980324p.
48. Jeyanthi R. L., Dhanalakshmi V., Shekhar C. 2012. Antibacterial activity of Sargassum Ilicifolium and Kappaphycus alvarezii // J. of Chemical and Pharmaceutical Research. № 4(1). Р. 700–705.
49. Jesus A., Correia-da-Silva M., Afonso C., Pinto M., Cidade H. 2018. Isolation and Potential Biological Applications ofHaloaryl Secondary Metabolites from Macroalgae // Mar. Drugs 2019, 17, 73; doi:10.3390/md17020073
50. Kim S. Y., Kim S. R., Oh M. J., Jung, S.J., Kang S. Y. 2011. In vitro antiviral activity of red alga, Polysiphonia morrowii extract and its bromophenols against fish pathogenic infectious hematopoietic necrosis virus and infectious pancreatic necrosis virus // J. Microbiol. № 49. Р. 102–106. DOI:10.1007/s12275–011–1035-z.
51. Kneifel H., Meinicke M., Soeder Ç. J. 1977. Analysis of amines in algae by high performance liquid chromatography // J. Phycol. Vol. 13. P. 36.
52. Kutscher G. W., Blumberg A. 1939. The use of pectin-agar mixtures in diarrhea // The American J. of Digestive Diseases. V. 6. Р. 717–720.
53. Lahaye, M., W. Yaphe, M. T. Phan Viet & C. Rochas. 1989.13C-N.M.R. spectroscopic investigation of methylated and charged agarose oligosaccharides and polysaccharides // Carbohydr. Res. 190: Р. 249–265. https://doi.org/10.1016/0008–6215(89)84129–1.
54. Lever J., CurtisG., BrkljačaR., Urban S. 2019. Bromophenolics from the Red Alga Polysiphonia decipiens // Mar Drugs.;17(9):497. DOI:10.3390/md17090497.
55. Li K., Li X.-M., Gloer J. B., Wang B. G. 2012. New nitrogen-containing bromophenols from the marine red alga Rhodomela confervoides and their radical scavenging activity // Food Chem. № 135. Р. 868–872. DOI:10.1016/j.foodchem.2012.05.117.
56. Li K., Li X. M., Gloer, J.B., Wang B. G. 2011. Isolation, characterization, and antioxidant activity of bromophenols of the marine red alga Rhodomela confervoides // J. Agric. Food Chem. № 59. Р. 9916– 9921. DOI:10.1021/jf2022447.
57. Liu M., Hansen P. E., Lin X. 2011. Bromophenols in Marine Algae and Their Bioactivities // Mar. Drugs. № 9. P. 1273–1292; doi:10.3390/md9071273.
58. Liu M., Wang G., Xiao L., Xu X., Liu X., Xu P., Lin X. 2014. Bis (2,3-di bromo-4,5-dihydroxybenzyl) ether, a marine algae derived bromophenol, inhibits the growth of botrytis cinerea and interacts with DNA molecules // Mar. Drugs. № 12. Р. 3838–3851. DOI:10.3390/md12073838.
59. Mendes M., Pereira R., Sousa Pinto I., Carvalho A. P., Gomes A. M. 2013. Antimicrobial activity and lipid profile of seaweed extracts from the NorthPortuguese Coast // International Food Research Journal. 20(6). P. 3337–3345.
60. Mikami D., Kurihara H., Kim S. M., Takahashi K. 2013. Red Algal Bromophenols as Glucose 6-Phosphate Dehydrogenase Inhibitors // Mar. Drugs. № 11. P. 4050–4057. DOI:10.3390/md11104050.
61. Mouritsen O. G., Rhatigan P., Pérez-Lloréns J.L. 2018. The rise of seaweed gastronomy: phycogastronomy // Botanica Marina. V.62. № 3. Р. 195–209. https://doi.org/10.1515/bot-2018–0041.
62. Percot A., Yalçın A., Aysel V., Erdugan H., Dural B., Güven K. C. 2009. β-Phenylethylamine content in marine algae around Turkish coasts // Bot. Mar. V. 52. P. 87–90. DOI:10.1515/BOT.2009.031.
63. Sah R., Shankhadarwar S. 2020. Evaluation of red seaweed Ahnfeltia plicata (Hudson) fries from alibaug coast for its chemical composition and antioxidant activity // Sah. et al., J Adv Sci Res. № 11 (3). Р. 134–140.
64. Salvador N., Garreta A. G., Lavelli L., Ribera M. A. 2007. Antimicrobial activity of Iberian macroalgae // Sci. Mar. № 71. Р. 101–113. DOI:10.3989/SCIMAR.2007.71N1101.
65. Sampaio A . H., Rogers D. J., Barwell C. J., Saker-Sampaio S., Nascimento K. S., Nagano C. S., Farias W. R.L. 2002. New affinity procedure for the isolation and further characterization of the blood group B specific lectin from the red marine alga Ptilota plumose // J. of Applied Phycology. № 14. P. 489–495. DOI:10.1023/A:1022327010736.
66. Shanab S. M. 2007. Antioxidant and antibiotic activities of some seaweeds (Egyptian isolates) // Int. J. Agric. Biol. Vol. 9. № 2. P. 220–225.
67. Smit A. J. 2004. Medicinal and pharmaceutical uses of seaweed natural products: A review // J. Appl. Phycol. № 16. Р. 245–262. DOI:10.1023/B:JAPH.0000047783.36600.ef.
68. Vairappan C. S. 2003. Potent antibacterial activity of galogenated metabolites from Malaysian red alga Laurencia majuscule (Rhodomelaceae, Ceramiales) // Biomol. Eng. Vol. 20. № 4–6. Р. 255–259. DOI:10.1016/s1389–0344(03)00067–4.
69. Xin Qi, Ge Liu, Lin Qiu, Xiukun Lin, Ming Liu 2015. Marine bromophenol bis(2,3-dibromo-4,5-dihydroxybenzyl) ether, represses angiogenesis in huvec cells and in zebrafish embryos via inhibiting the vegf signal systems // Biomed. Pharmacother. № 75. Р. 58–66. DOI:10.1016/j.biopha.2015.08.033.
70. Yalçın A., Percot A., Erdugan H., Coban B., Guven, K.C. 2007. Hordenine in marine alga, Gelidiumcrinale (Hare ex Turner) Gaillon // Acta. Pharm. Sci. № 49. Р.213–218.
71. Zheng W, Wise M. L., Wyrick A., Metz J. G., Yuan L., Gerwick W. H. 2002. Polyenoic fatty acid isomerise from the marine alga Pilota filicina: protein characterization and functional expression of the cloned cDNA // Arch Biochem Biophys. № 401. Р. 11–20. DOI:10.1016/S0003–9861(02)00002–4.
Review
For citations:
Podkorytova A.V., Ignatova T.A. Marine red algae as an inexhaustable source of biologically active substances for medicine and pharmaceutics. Trudy VNIRO. 2022;188:151-165. (In Russ.) https://doi.org/10.36038/2307-3497-2022-188-151-165
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