Physiological functions of phlorotannins
DOI:
https://doi.org/10.21638/spbu03.2018.108Abstract
Phlorotannins are the most abundant group of metabolites specific for brown algae. These substances contribute both to the primary and secondary metabolism of the algal cells and have practical relevance as biologically active compounds. The list of their presumable physiological functions is still not exhaustive and includes wound healing, chelation of heavy metal ions, bioadhesion, contribution to the processes of algal early embryogenesis and sporogenesis, etc. Similar to higher plant phenolics, phlorotannins also have antioxidant properties, provide chemical defense against herbivores and contribute to cell wall rigidification. The complex and diverse composition of natural phlorotannins hampers investigation of their physiological roles and leads to inconsistencies in the obtained data. Further study of the correlation between the structure of these substances and their functions is needed to take a new look at known information, thus providing better performance in the fields of both fundamental algal physiology and applied phycology.
Keywords:
phlorotannins, brown algae, phenolic compounds, cell wall, physodes, algal exudates, bioadhesion, antifouling compounds
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References
Amsler, C. D., and Fairhead, V. A. 2006. Defensive and sensory chemical ecology of brown algae. Advances in Botanical Research 43:1–91. https://doi.org/10.1016/S0065-2296(05)43001-3" target="_blank">https://doi.org/10.1016/S0065-2296(05)43001-3
Arnold, T. M., and Targett, N. M. 2000. Evidence for metabolic turnover of polyphenolics in tropical brown algae. Journal of Chemical Ecology 26:1393–1410. https://doi.org/10.1023/A:1005588023887" target="_blank">https://doi.org/10.1023/A:1005588023887
Arnold, T. M., and Targett, N. M. 2002. Marine tannins: The importance of a mechanistic framework for predicting ecological roles. Journal of Chemical Ecology 28:1919–1934. https://doi.org/10.1023/A:1020737609151" target="_blank">https://doi.org/10.1023/A:1020737609151
Arnold, T. M., and Targett, N. M. 2003. To grow and defend: lack of trade-offs for brown algal phlorotannins. Oikos 100:406–408. https://doi.org/10.1034/j.1600-0706.2003.11680.x" target="_blank">https://doi.org/10.1034/j.1600-0706.2003.11680.x
Barbehenn, R. V. C., and Constabel, P. 2011. Tannins in plantherbivore interactions. Phytochemistry 72:1551–1565. https://doi.org/10.1016/j.phytochem.2011.01.040" target="_blank">https://doi.org/10.1016/j.phytochem.2011.01.040
Barre, S., Potin, P., Leblanc, C., Delage, L. 2010. The halogenated metabolism of brown algae (Phaeophyta), its biological importance and its environmental significance. Marine Drugs 8:988–1010. https://doi.org/10.3390/md8040988" target="_blank">https://doi.org/10.3390/md8040988
Berglin, M., Delage, L., Potin, P., Vilter, H., Elwing, H. 2004. Enzymatic cross-linking of a phenolic polymer extracted from the marine alga Fucus serratus. Biomacromolecules 5(6):2376–2383. https://doi.org/10.1021/bm0496864" target="_blank">https://doi.org/10.1021/bm0496864
Bidlack, J. E., and Dashek, W. V. 2016. Plant cell walls. Plant Cells and their Organelles 9:209–238. https://doi.org/10.1002/9781118924846.ch9" target="_blank">https://doi.org/10.1002/9781118924846.ch9
Bieza, K., and Lois, R. 2001. An Arabidopsis mutant tolerant to lethal ultraviolet-B levels shows constitutively elevated accumulation of flavonoids and other phenolics. Plant Physiology 126:1105–1115. https://doi.org/10.1104/pp.126.3.1105" target="_blank">https://doi.org/10.1104/pp.126.3.1105
Bitton, R., Ben-Yehuda, M., Davidovich, M., Balazs, Y., Potin, P., Delage, L., Colin, C., Bianco-Peled, H. 2006. Structure of algal-born phenolic polymeric adhesives. Macromolecular Bioscience 6:737–746. https://doi.org/10.1002/mabi.200600073" target="_blank">https://doi.org/10.1002/mabi.200600073
Bitton, R., Berglin, M., Elwing, H., Colin, C., Delage, L., Potin, P., Bianco-Peled, H. 2007. The influence of halidemediated oxidation on algae-born adhesives. Macromolecular Bioscience 7:1280-1289. https://doi.org/10.1002/mabi.200700099" target="_blank">https://doi.org/10.1002/mabi.200700099
Boettcher, A., and Targett, N. 1993. Role of polyphenolic molecular size in reduction of assimilation efficiency in Xiphister mucosus. Ecology 74(3):891–903. https://doi.org/10.2307/1940814" target="_blank">https://doi.org/10.2307/1940814
Catarino, M. D., Silva, A. M. S., Cardoso, S. M. 2017. Fucaceae: a source of bioactive phlorotannins. International Journal of Molecular Science 18:1327. https://doi.org/10.3390/ijms18061327" target="_blank">https://doi.org/10.3390/ijms18061327
Coley, P. D., Bryant, J. P., Chapin, F. S. 1985. Resource availability and plant antiherbivory defense. Science 230:895–899. https://doi.org/10.1126/science.230.4728.895" target="_blank">https://doi.org/10.1126/science.230.4728.895
Connan, S., and Stengel, D. B. 2011. Impacts of ambient salinity and copper on brown algae: 2. Interactive effects on phenolic pool and assessment of metal binding capacity of phlorotannin. Aquatic Toxicology 104:1–13. https://doi.org/10.1016/j.aquatox.2011.03.016" target="_blank">https://doi.org/10.1016/j.aquatox.2011.03.016
Craigie, J. S., Mc Lachlan, J. 1964. Excretion of colored ultraviolet-absorbing substances by marine algae. Canadian Journal of Botany 42:23–33. https://doi.org/10.1139/b64-003" target="_blank">https://doi.org/10.1139/b64-003
Creis, E., Delage, L., Charton, S., Goulitquer, S., Leblanc, C., Potin, P., Ar Gall, E. 2015. Constitutive or inducible protective mechanisms against UV-B radiation in the brown alga Fucus vesiculosus? A Study of gene expression and phlorotannin content responses. PLoS ONE 10(6):e0128003. https://doi.org/10.1371/journal.pone.0128003" target="_blank">https://doi.org/10.1371/journal.pone.0128003
Davis, T. A., Volesky, B., Mucci, A. 2003. A review of the biochemistry of heavy metal biosorption by brown algae. Water Research 37:4311–4330. https://doi.org/10.1016/S0043-1354(03)00293-8" target="_blank">https://doi.org/10.1016/S0043-1354(03)00293-8
Ferreres, F., Lopes, G., Gil-Izquierdo, A., Andrade, P. B., Sousa, C., Mouga, T., Valentão, P. 2012. Phlorotannin extracts from Fucales characterized by HPLC-DAD-ESIMSn: approaches to hyaluronidase inhibitory capacity and antioxidant properties. Marine Drugs 10: 2766–2781. https://doi.org/10.3390/md10122766" target="_blank">https://doi.org/10.3390/md10122766
Gómez, I., and Huovinen, P. 2010. Induction of phlorotannins during UV exposure mitigates inhibition of photosynthesis and DNA damage in the kelp Lessonia nigrescens. Photochemistry and Photobiology 86:1056–1063. https://doi.org/10.1111/j.1751-1097.2010.00786.x" target="_blank">https://doi.org/10.1111/j.1751-1097.2010.00786.x
Hagerman, A. E., Riedl, K. M., Jones, G. A., Sovik, K. N., Ritchard, N. T., Hartzfeld, P. W., Riechel, T. L. 1998. High molecular weight plant polyphenolics (tannins) as biological antioxidants. Journal of Agricultural and Food Chemistry 46(5):1887–1892. https://doi.org/10.1021/jf970975b" target="_blank">https://doi.org/10.1021/jf970975b
Hammerstrom, K., Dethier, M. N., Duggins, D. O. 1998. Rapid phlorotannin induction and relaxation in five Washington kelps. Marine Ecology Progress Series 165:293–305. https://doi.org/10.3354/meps165293" target="_blank">https://doi.org/10.3354/meps165293
Heffernan, N., Nigel, P., Brunton, R. J., Fitz, G., Smyth, T. J. 2015. Profiling of the molecular weight and structural isomer abundance of macroalgae-derived phlorotannins. Marine Drugs 13:509–528. https://doi.org/10.3390/md13010509" target="_blank">https://doi.org/10.3390/md13010509
Heffernan, N., Smyth, T. J., Soler-Villa, A., Fitzgerald, R. J., Brunton, N. P. 2014. Phenolic content and antioxidant activity of fractions obtained from selected Irish macroalgae species (Laminaria digitata, Fucus serratus, Gracilaria gracilis and Codium fragile). Journal of Applied Phycology 27:519. https://doi.org/10.1007/s10811-014-0291-9" target="_blank">https://doi.org/10.1007/s10811-014-0291-9
Iken, K., Amsler, C. D., Hubbard, J. M., McClintock, J. B. and Baker, B. J. 2007. Allocation patterns of phlorotannins in Antarctic brown algae. Phycologia 46:386–395. https://doi.org/10.2216/06-67.1" target="_blank">https://doi.org/10.2216/06-67.1
Jennings, J. G., and Steinberg, P. D. 1994. In situ exudation of phlorotannins by the sublittoral kelp Ecklonia radiata. Marine Biology 121:349–354. https://doi.org/10.1007/BF00346744" target="_blank">https://doi.org/10.1007/BF00346744
Jormalainen, V., Honkanen, T., Koivikko, R., Eranen, J. 2003. Induction of phlorotannin production in a brown alga: defense or resource dynamics. Oikos 103:640–650. https://doi.org/10.1034/j.1600-0706.2003.12635.x" target="_blank">https://doi.org/10.1034/j.1600-0706.2003.12635.x
Jormalainen, V., Honkanen, T., Vesakoski, O., Koivikko, R. 2005. Polar extracts of the brown alga Fucus vesiculosus (L.) reduce assimilation efficiency but do not deter the herbivorous isopod Idotea baltica (Pallas). Journal of Experimental Marine Biology and Ecology 317:143–157. https://doi.org/10.1016/j.jembe.2004.11.021" target="_blank">https://doi.org/10.1016/j.jembe.2004.11.021
Jormalainen, V., Koivikko, R., Eränen, J. K., Loponen J. 2008. Variation of phlorotannins among three populations of Fucus vesiculosus as revealed by HPLC and colorimetric quantification. Journal of Chemical Ecology 34:57–64. https://doi.org/10.1007/s10886-007-9410-2" target="_blank">https://doi.org/10.1007/s10886-007-9410-2
Kamiya, M., Nishio, T., Yokoyama, A., Yatsuya, K., Nishigaki, T., Yoshikawa, S. Ohki, K. 2010. Seasonal variation of phlorotannin in sargassacean species from the coast of the Sea of Japan. Phycological Research 58:53–61. https://doi.org/10.1111/j.1440-1835.2009.00558.x" target="_blank">https://doi.org/10.1111/j.1440-1835.2009.00558.x
Koivikko, R., Loponen, J., Honkanen, T., Jormalainen, V. 2005. Contents of cytoplasmic, cell-wall-bound and exudes phlorotannins in the brown alga Fucus vesiculosus, with implications on their ecological functions. Journal of Chemical Ecology 31:195–209. https://doi.org/10.1007/s10886-005-0984-2" target="_blank">https://doi.org/10.1007/s10886-005-0984-2
Lau, S. C. K., and Qian, P. Y. 1997. Phlorotannins and related compounds as larval settlement inhibitors of the tubebuilding polychaete Hydroides elegans. Marine Ecology Progress Series 159:219–227. https://doi.org/10.3354/meps159219" target="_blank">https://doi.org/10.3354/meps159219
Lau, S. C. K., and Qian, P. Y. 2000. Inhibitory effect of phenolic compounds and marine bacteria on larval settlement of the barnacle Balanus amphitrite amphitrite Darwin. Biofouling 16:47–58. https://doi.org/10.1080/08927010009378429" target="_blank">https://doi.org/10.1080/08927010009378429
Lüder, U. H., and Clayton, M. N. 2004. Induction of phlorotannins in the brown macroalga Ecklonia radiata (Laminariales, Phaeophyta) in response to simulated herbivory — the first microscopic study. Planta 218(6):928–37. https://doi.org/10.1007/s00425-003-1176-3" target="_blank">https://doi.org/10.1007/s00425-003-1176-3
Martinez, J. H., and Castaneda, H. G. 2013. Preparation and chromatographic analysis of phlorotannins. Journal of Chromatographic Science 51:825–838. https://doi.org/10.1093/chromsci/bmt045" target="_blank">https://doi.org/10.1093/chromsci/bmt045
Meslet-Cladiere, L., Delage, L., Leroux, C. J., Goulitquer, S., Leblanc, C., Creis, E., Gall E. A. ; Stiger-Pouvreau, V., Czjzek, M., Potin, P. 2013. Structure/function analysis of a type III polyketide synthase in the brown alga Ectocarpus siliculosus reveals a biochemical pathway in phlorotannin monomer biosynthesis. Plant Cell 25:3089–3103. https://doi.org/10.1105/tpc.113.111336" target="_blank">https://doi.org/10.1105/tpc.113.111336
Parys, S., Kehraus, S., Krick, A., Glombitza, K. W., Carmeli, S,. Klimo, K., Gerhäuser, C., König, G. M. 2010. In vitro chemopreventive potential of fucophlorethols from the brown alga Fucus vesiculosus L. by anti-oxidant activity and inhibition of selected cytochrome P450 enzymes. Phytochemistry 71(2–3):221–9. https://doi.org/10.1016/j.phytochem.2009.10.020" target="_blank">https://doi.org/10.1016/j.phytochem.2009.10.020
Pavia, H., Cervin, G., Lindgren, A., Aberg, P. 1997. Effects of UV-B radiation and simulated herbivory on phlorotannins in the brown alga Ascophyllum nodosum. Marine Ecology Progress Series 157:139–146. https://doi.org/10.3354/meps157139" target="_blank">https://doi.org/10.3354/meps157139
Pavia, H., and Brock, E. 2000. Extrinsic factors influencing phlorotannin production in the brown alga Ascophyllum nodosum. Marine Ecology Progress Series 193:285–294. https://doi.org/10.3354/meps193285" target="_blank">https://doi.org/10.3354/meps193285
Pavia, H., and Toth, G. B. 2000. Inducible chemical resistance to herbivory in the brown seaweed Ascophyllum nodosum. Ecology 81:3212–3225. https://doi.org/10.2307/177411" target="_blank">https://doi.org/10.2307/177411
Pavia, H., Toth, G. B., Aberg, P. 2002. Optimal defense theory: Elasticity analysis as a tool to predict intraplant variation in defenses. Ecology 83:891–897. https://doi.org/10.2307/3071898" target="_blank">https://doi.org/10.2307/3071898
Peckol, P., Krane, J. M., Yates, J. L. 1996. Interactive effects of inducible defense and resource availability on phlorotannins in the North Atlantic brown alga Fucus vesiculosus. Marine Ecology Progress Series 138:209–217. https://doi.org/10.3354/meps138209" target="_blank">https://doi.org/10.3354/meps138209
Phillips, I. A., Clayton, M. N., Harvey, A. S. 1994. Comparative studies on sporangial distribution and structure in species of Zonaria, Lobophora and Homoeostrichus (Dictyotales, Phaeophyceae) from Australia. European Journal of Phycology 29:93–101. https://doi.org/10.1080/09670269400650541" target="_blank">https://doi.org/10.1080/09670269400650541
Potin, P., and Leblanc, C. L. 2006. Phenolic-based adhesives of marine brown algae. Biological Adhesives 105–124. https://doi.org/10.1007/978-3-540-31049-5_6" target="_blank">https://doi.org/10.1007/978-3-540-31049-5_6
Ragan, M. A., and Glombitza, K. W. 1986. Phlorotannins, brown algal polyphenols. Progress in Phycological Research 4:129–241.
Ragan, M. A., and Jensen, A. 1978. 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 34:245–258. https://doi.org/10.1016/S0022-0981(78)80006-9" target="_blank">https://doi.org/10.1016/S0022-0981(78)80006-9
Ragan, M. A., and Jensen, A. 1979. Quantitative studies on brown algal phenols. III. Light-mediated exudation on polyphenols from Ascophyllum nodosum (L.) Le Jol. Journal of Experimental Marine Biology and Ecology 36:91–101. https://doi.org/10.1016/0022-0981(79)90102-3" target="_blank">https://doi.org/10.1016/0022-0981(79)90102-3
Salgado, L. T., Cinelli, L. P., Viana, N. B., de Carvalho, R. T., de Souza Mourão, P. A., Teixeira, V. L., Filho, G. M. A. 2009. A vanadium bromoperoxidase catalyzes the formation of high-molecular-weight complexes between brown algal phenolic substances and alginates. Journal of Phycology 45:193–202. https://doi.org/10.1111/j.1529-8817.2008.00642.x" target="_blank">https://doi.org/10.1111/j.1529-8817.2008.00642.x
Schoenwaelder, M. E. A. 2002. The occurrence and cellular significance of physodes in brown algae. Phycologia 41(2):125–139. https://doi.org/10.2216/i0031-8884-41-2-125.1" target="_blank">https://doi.org/10.2216/i0031-8884-41-2-125.1
Schoenwaelder, M. E. A., and Clayton, M. N. 1998. Secretion of phenolic substances into the zygote wall and cell plate in embryos of Hormosira and Acrocarpia (Fucales, Phaeophyceae). Journal of Phycology 34:969–980. https://doi.org/10.1046/j.1529-8817.1998.340969.x" target="_blank">https://doi.org/10.1046/j.1529-8817.1998.340969.x
Schoenwaelder, M. E. A., and Clayton, M. N. 1999. The presence of phenolic compounds in isolated cell walls of brown algae. Phycologia 38:161–166. https://doi.org/10.2216/i0031-8884-38-3-161.1" target="_blank">https://doi.org/10.2216/i0031-8884-38-3-161.1
Schoenwaelder, M. E. A., Clayton, M. N. 2000. Physode formation in embryos of Phyllospora comosa and Hormosira banksii (Phaeopbyceae). Phycologia 39:1–9. https://doi.org/10.2216/i0031-8884-39-1-1.1" target="_blank">https://doi.org/10.2216/i0031-8884-39-1-1.1
Shibata, T., Kawaguchi, S., Hama, Y., Inagaki, M., Yamaguchi, K., Nakamura, T. 2004. Local and chemical distribution of phlorotannins in brown algae. Journal of Applied Phycology 16:291–296. https://doi.org/10.1023/B:JAPH.0000047781.24993.0a" target="_blank">https://doi.org/10.1023/B:JAPH.0000047781.24993.0a
Shibata, T., Hama, Y., Miyasaki, T., Ito, M., Nakamura, T. 2006. Extracellular secretion of phenolic substances from living brown algae. Journal of Applied Phycology 18:787-794. https://doi.org/10.1007/s10811-006-9094-y" target="_blank">https://doi.org/10.1007/s10811-006-9094-y
Sieburth, J. M., and Jensen, A. 1969. Studies on algal substances in the sea. II. The formation of Gelbstoff (humic material) by exudates of Phaeophyta. Journal of Experimental Marine Biology and Ecology 3:275–289. https://doi.org/10.1016/0022-0981(69)90051-3" target="_blank">https://doi.org/10.1016/0022-0981(69)90051-3
Steevensz, A. J., Mackinnon, S. L., Hankinson, R., Craft, C., Connan, S., Stengel, D. B., Melanson, J. E. 2012. Profiling phlorotannins in brown macroalgae by liquid chromatography-high resolution mass spectrometry. Phytochemical Analysis 23:547–553. https://doi.org/10.1002/pca.2354" target="_blank">https://doi.org/10.1002/pca.2354
Steinberg, P. D. 1995. Seasonal variation in the relationship between growth rate and phlorotannin production in the kelp Ecklonia radiata. Oecologia 102:169–173. https://doi.org/10.1007/BF00333248" target="_blank">https://doi.org/10.1007/BF00333248
Stern, J. L., Hagerman, A. E., Stainberg, P. D., Winter, F. C., Estes, J. A. 1996. A new assay for quantifying brown algal phlorotannins and comparisons to previous methods. Journal of Chemical Ecology 22:1273–1293. https://doi.org/10.1007/BF02266965" target="_blank">https://doi.org/10.1007/BF02266965
Surveswaran, S., Cai, Y., Corke, H., Sun, M. 2007. Systematic evaluation of natural phenolic antioxidants from 133 Indian medicinal plants. Food Chemistry 102:938–953. https://doi.org/10.1016/j.foodchem.2006.06.033" target="_blank">https://doi.org/10.1016/j.foodchem.2006.06.033
Swanson, A. K., and Druehl, L. D. 2002. Induction, exudation and the UV protective role of kelp phlorotannins. Aquatic Botany 73:241–253. https://doi.org/10.1016/S0304-3770(02)00035-9" target="_blank">https://doi.org/10.1016/S0304-3770(02)00035-9
Tarakhovskaya, E. R. 2014. Mechanisms of bioadhesion of macrophytic algae. Russian Journal of Plant Physiology 61: 23–30. https://doi.org/10.1134/S1021443714010154" target="_blank">https://doi.org/10.1134/S1021443714010154
Tarakhovskaya, E., Lemesheva, V., Bilova, T., Birkemeyer, C. 2017. Early embryogenesis of brown alga Fucus vesiculosus L. is characterized by significant changes in carbon and energy metabolism. Molecules 22(9): 1509. https://doi.org/10.3390/molecules22091509" target="_blank">https://doi.org/10.3390/molecules22091509
Targett, N. M., Coen, L. D., Boettcher, A. A., Tanner, C. E. 1992. Biogeographic comparisons of marine algal polyphenolics: evidence against a latitudinal trend. Oecologia 89:464–70. https://doi.org/10.1007/BF00317150" target="_blank">https://doi.org/10.1007/BF00317150
Targett, N. M., Boettcher, A. A., Targett, T. E., Vrolijk, N. H. 1995. Tropical marine herbivore assimilation of phenolicrich plants. Oecologia 103:170–9. https://doi.org/10.1007/BF00329077" target="_blank">https://doi.org/10.1007/BF00329077
Targett, N. M., and Arnold, T. M. 1998. Predicting the effects of brown algal phlorotannins on marine herbivores in tropical and temperate oceans. Journal of Phycology 34:195–205. https://doi.org/10.1046/j.1529-8817.1998.340195.x" target="_blank">https://doi.org/10.1046/j.1529-8817.1998.340195.x
Van Alstyne, K. L. 1988. Herbivore grazing increases polyphenolic defenses in the intertidal brown alga Fucus distichus. Ecology 69(3):655–663. https://doi.org/10.2307/1941014" target="_blank">https://doi.org/10.2307/1941014
Van Alstyne, K. L., Ehlig, J. M., Whitman, S. L. 1999. Feeding preferences for juvenile and adult algae depend on algal stage and herbivore species. Marine Ecology Progress Series 180:179–185. https://doi.org/10.3354/meps180179" target="_blank">https://doi.org/10.3354/meps180179
Van Alstyne, K. L., McCarthy, J. J., Hustead, C. L., Kearns, L. J. 1999. Phlorotannin allocation among tissues of northeastern Pacific kelps and rockweeds. Journal of Phycology 35:483–492. https://doi.org/10.1046/j.1529-8817.1999.3530483.x" target="_blank">https://doi.org/10.1046/j.1529-8817.1999.3530483.x
Van Alstyne, K. L., Whitman, S. L., Ehlig, J. M. 2001. Differences in herbivore preferences, phlorotannin production, and nutritional quality between juvenile and adult tissues from marine brown algae. Marine Biology 139:201–210. https://doi.org/10.1007/s002270000507" target="_blank">https://doi.org/10.1007/s002270000507
Wikström, S. A., and Pavia, H. 2004. Chemical settlement inhibition versus post-settlement mortality as an explanation for differential fouling of two congeneric seaweeds. Oecologia 138:223–230. https://doi.org/10.1007/s00442-003-1427-9" target="_blank">https://doi.org/10.1007/s00442-003-1427-9
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2018-06-08
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Lemesheva, V., & Tarakhovskaya, E. (2018). Physiological functions of phlorotannins. Biological Communications, 63(1), 70–76. https://doi.org/10.21638/spbu03.2018.108
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