, Volume 249, Issue 2, pp 377–391 | Cite as

Distribution of natural ingredients suggests a complex network of metabolic transport between source and sink tissues in the brown alga Fucus vesiculosus

  • Claudia Birkemeyer
  • Natalia Osmolovskaya
  • Ludmila Kuchaeva
  • Elena TarakhovskayaEmail author
Original Article


Main conclusion

Tight regulation of intra-thallus metabolite distribution in Fucus vesiculosus in late summer reveals the complex biochemical processes complying with reproduction and the preparation to the dark season.

We used inductively coupled plasma atomic emission spectroscopy to study the tissue-specific elemental composition, and gas chromatography coupled to mass spectrometry to study the distribution of small-molecular weight primary and secondary metabolites of the brown alga Fucus vesiculosus thalli in the reproductive phase. Beyond general physiological requirements, the observed distribution of the analysed nutrients was also found to depend on characteristics related to the season of harvesting, i.e., the reproductive period. However, a particular curious result was the high metabolic activity found in the stipe of the plant. In conclusion, our data not only provide valuable information for industrial use of fucoids targeting specific algal ingredients, but also give highly interesting insights in the multifaceted system of intra-thallus biochemical interactions during reproduction of the brown algae.


Elemental composition Fucoid algae Intra-thallus profiling Long-distance transport Metabolomics Reproduction 



Principal component


Retention index


Total ion current



This project has been supported by the Russian Foundation for Basic Research (project no. 17-04-01331), Deutscher Akademischer Austauschdienst (“Dmitry Mendeleev program”, Grant ID 57203217) and the universities of Leipzig (CB) and St. Petersburg (ET, NO and LK). We thank Marine biological station “UNB Belomorskaya” and Chemistry educational centre of St. Petersburg State University for providing facilities. We also sincerely thank Jeevan Sharma, Aleksandra Kushnareva, Dr. Susan Billig, Dr. Tatiana Bilova and Dr. Elena Stepchenkova for technical assistance.

Compliance with ethical standards

Conflicts of interest

The authors declare no conflict of interest.

Supplementary material

425_2018_3009_MOESM1_ESM.pdf (643 kb)
Supplementary material 1 (PDF 643 kb)


  1. Abbasi A, Hajirezaei M, Hofius D, Sonnewald U, Voll LM (2007) Specific roles of α- and γ tocopherol in abiotic stress responses of transgenic tobacco. Plant Physiol 143:1720–1738. CrossRefGoogle Scholar
  2. Amat MA, Srivastava LM (1985) Translocation of iodine in Laminaria saccharina (Phaeophyta). J Phycol 21:330–333. CrossRefGoogle Scholar
  3. Andrade PB, Barbosa M, Matos RP, Lopes G, Vinholes J, Mouga T, Valentão P (2013) Valuable compounds in macroalgae extracts. Food Chem 138:1819–1828. CrossRefGoogle Scholar
  4. Benveniste P (2004) Biosynthesis and accumulation of sterols. Annu Rev Plant Biol 55:429–457. CrossRefGoogle Scholar
  5. Berteau O, Mulloy B (2003) Sulfated fucans, fresh perspectives: structures, functions, and biological properties of sulfated fucans and an overview of enzymes active toward this class of polysaccharide. Glycobiology 13:29R–40R. CrossRefGoogle Scholar
  6. Bieleski RL (1973) Phosphate pools, phosphate transport, and phosphate availability. Ann Rev Plant Physiol 24:225–252. CrossRefGoogle Scholar
  7. Catarino MD, Silva AMS, Cardoso SM (2017) Fucaceae: a source of bioactive phlorotannins. Int J Mol Sci 18:1327. CrossRefGoogle Scholar
  8. Chong J, Soufan O, Li C, Caraus I, Li S, Bourque G, Wishart DS, Xia J (2018) MetaboAnalyst 4.0: towards more transparent and integrative metabolomics analysis. Nucl Acids Res 46:W486–W494. CrossRefGoogle Scholar
  9. Cock JM, Sterck L, Rouze P et al (2010) The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature 465:617–621. CrossRefGoogle Scholar
  10. Connan S, Delisle F, Deslandes E, Gall EA (2006) Intra-thallus phlorotannin content and antioxidant activity in Phaeophyceae of temperate waters. Bot Mar 49:39–46. CrossRefGoogle Scholar
  11. DeBoer JA, Whoriskey FG (1983) Production and role of hyaline hairs in Ceramium rubrum. Mar Biol 77:229–234. CrossRefGoogle Scholar
  12. DellaPenna D, Pogson BJ (2006) Vitamin synthesis in plants: tocopherols and carotenoids. Annu Rev Plant Biol 57:711–738. CrossRefGoogle Scholar
  13. Diouris M (1989) Long-distance transport of 14C-labelled assimilates in the Fucales: nature of translocated substances in Fucus serratus. Phycologia 28:504–511. CrossRefGoogle Scholar
  14. Dittami SM, Gravot A, Renault D, Goulitquer S, Eggert A, Bouchereau A, Boyen C, Tonon T (2011) Integrative analysis of metabolite and transcript abundance during the short-term response to saline and oxidative stress in the brown alga Ectocarpus siliculosus. Plant, Cell Environ 34:629–642. CrossRefGoogle Scholar
  15. Falk J, Munné-Bosch S (2010) Tocochromanol functions in plants: antioxidation and beyond. J Exp Bot 61:1549–1566. CrossRefGoogle Scholar
  16. Farias DR, Hurd CL, Eriksen RS, Macleod CK (2018) Macrophytes as bioindicators of heavy metal pollution in estuarine and coastal environments. Mar Pollut Bull 128:175–184. CrossRefGoogle Scholar
  17. Ferreres F, Lopes G, Gil-Izquierdo A, Andrade PB, Sousa C, Mouga T, Valentão P (2012) Phlorotannin extracts from Fucales characterized by HPLC-DAD-ESI-MSn: approaches to hyaluronidase inhibitory capacity and antioxidant properties. Mar Drugs 10:2766–2781. CrossRefGoogle Scholar
  18. Fielding AH, Carter PL, Smith CA (1987) Sieve plates in Fucus: a reappraisal of size and pore distribution. Phycologia 26:501–504. CrossRefGoogle Scholar
  19. Fletcher HR, Biller P, Ross AB, Adams JMM (2017) The seasonal variation of fucoidan within three species of brown macroalgae. Algal Res 22:79–86. CrossRefGoogle Scholar
  20. Floc’h JY, Penot M (1980) Variation de la composition minerale et transport a longue distance au cours de la croissance de la lame chez Laminaria hyperborea (Gunn) Fosl. Z Pflanzenphysiol 96:377–385. CrossRefGoogle Scholar
  21. Gilroy S, Bethke PC, Jones RL (1993) Calcium homeostasis in plants. J Cell Sci 106:453–462. Google Scholar
  22. Gómez I, Huovinen P (2010) Induction of phlorotannins during UV exposure mitigates inhibition of photosynthesis and DNA damage in the kelp Lessonia nigrescens. Photochem Photobiol 86:1056–1063. CrossRefGoogle Scholar
  23. Gómez I, Huovinen P (2012) Morpho-functionality of carbon metabolism in seaweeds. In: Wiencke C, Bischof K (eds) Seaweed biology: novel insights into ecophysiology, ecology and utilization. Springer, Berlin, pp 25–46CrossRefGoogle Scholar
  24. Gómez I, Wiencke C (1998) Seasonal changes in C, N and major organic compounds and their significance to morpho-functional processes in the endemic Antarctic brown alga Ascoseira mirabilis. Polar Biol 19:115–124. CrossRefGoogle Scholar
  25. Gómez I, Ulloa N, Orostegui M (2005) Morpho-functional patterns of photosynthesis and UV sensitivity in the kelp Lessonia nigrescens (Laminariales, Phaeophyta). Mar Biol 148:231–240. CrossRefGoogle Scholar
  26. Graiff A, Ruth W, Kragl U, Karsten U (2016) Chemical characterization and quantification of the brown algal storage compound laminarin—a new methodological approach. J Appl Phycol 28:533–543. CrossRefGoogle Scholar
  27. Gravot A, Dittami SM, Rousvoal S, Lugan R, Eggert A, Collén J, Boyen C, Bouchereau A, Tonon T (2010) Diurnal oscillations of metabolite abundances and gene analysis provide new insights into central metabolic processes of the brown alga Ectocarpus siliculosus. New Phytol 188:98–110. CrossRefGoogle Scholar
  28. Harnedy PA, FitzGerald RJ (2011) Bioactive proteins, peptides, and amino acids from macroalgae. J Phycol 47:218–232. CrossRefGoogle Scholar
  29. Harrison PJ, Hurd CL (2001) Nutrient physiology of seaweeds: application of concepts to aquaculture. Biol Mar 42:71–82Google Scholar
  30. Heffernan N, Smyth TJ, Soler-Villa A, Fitzgerald RJ, Brunton NP (2014) Phenolic content and antioxidant activity of fractions obtained from selected Irish macroalgae species (Laminaria digitata, Fucus serratus, Gracilaria gracilis and Codium fragile). J Appl Phycol 27:519–530. CrossRefGoogle Scholar
  31. Hill J (1980) The remobilization of nutrients from leaves. J Plant Nutrition 2:407–444. CrossRefGoogle Scholar
  32. Holligan PM, Drew EA (1971) Routine analysis by gas-liquid chromatography of soluble carbohydrates in extracts of plant tissues. II. Quantitative analysis of standard carbohydrates, and the separation and estimation of soluble sugars and polyols from a variety of plant tissues. New Phytol 70:271–297. CrossRefGoogle Scholar
  33. Honkanen T, Jormalainen V (2002) Within-alga integration and compensation: effects of simulated herbivory on growth and reproduction of the brown alga, Fucus vesiculosus. Int J Plant Sci 163:815–823. CrossRefGoogle Scholar
  34. Hurd CL, Galvin RS, Norton TA, Dring MJ (1993) Production of hyaline hairs by intertidal species of Fucus (Fucales) and their role in phosphate uptake. J Phycol 29:160–165. CrossRefGoogle Scholar
  35. Hutschenreuther A, Kiontke A, Birkenmeier G, Birkemeyer C (2012) Comparison of extraction conditions and normalization approaches for cellular metabolomics of adherent growing cells with GCMS. Anal Methods 4:1959–1963. CrossRefGoogle Scholar
  36. Jones AL, Harwood JL (1993) Lipid metabolism in the brown marine algae Fucus vesiculosus and Ascophyllum nodosum. J Exp Bot 44:1203–1210. CrossRefGoogle Scholar
  37. Khotimchenko SV, Vaskovsky VE, Titlyanova TV (2002) Fatty acids of marine algae from the pacific coast of North California. Bot Mar 45:17–22. CrossRefGoogle Scholar
  38. Klindukh MP, Obluchinskaya ED (2018) A comparative study of free amino acids of the brown alga Fucus vesiculosus Linnaeus 1753 from the intertidal zone of the Murman shore, Barents Sea. Russ J Mar Biol 44:232–239. CrossRefGoogle Scholar
  39. Knoblauch J, Peters WS, Knoblauch M (2016) The gelatinous extracellular matrix facilitates transport studies in kelp: visualization of pressure-induced flow reversal across sieve plates. Ann Bot 117:599–606. CrossRefGoogle Scholar
  40. Kopka J, Schauer N, Krueger S, Birkemeyer C, Usadel B, Bergmüller E, Dörmann P, Weckwerth W, Gibon Y, Willmitzer MSL, Fernie AR, Steinhauser D (2005) GMD@CSB.DB: the Golm metabolome database. Bioinformatics 21:1635–1638. CrossRefGoogle Scholar
  41. Kovàts E (1958) Characterization of organic compounds by gas chromatography. Part 1. Retention indices of aliphatic halides, alcohols, aldehydes and ketones. Helv Chim Acta 41:1915–1932. CrossRefGoogle Scholar
  42. Küppers U, Kremer BP (1978) Longitudinal profiles of carbon dioxide fixation capacities in marine macroalgae. Plant Physiol 62:49-53.
  43. Lee RE (2008) Phycology, 4th edn. Cambridge University Press, New YorkCrossRefGoogle Scholar
  44. Lehvo A, Bäck S, Kiirikki M (2001) Growth of Fucus vesiculosus L. (Phaeophyta) in the Northern Baltic proper: energy and nitrogen storage in seasonal environment. Bot Mar 44:345–350. CrossRefGoogle Scholar
  45. Lemesheva V, Tarakhovskaya E (2018) Physiological functions of phlorotannins. Biol Commun 63:70–76. CrossRefGoogle Scholar
  46. Macaya EC, Rothausler E, Thiel M, Molis M, Wahl M (2005) Induction of defenses and within-alga variation of palatability in two brown algae from the northern-central coast of Chile: effects of mesograzers and UV radiation. J Exp Mar Biol Ecol 325:214–227. CrossRefGoogle Scholar
  47. Mackie W, Preston RD (1974) Cell wall and intercellular region polysaccharides. In: Stewart WDP (ed) Algal physiology and biochemistry. Los Angeles, Berkeley, pp 40–85Google Scholar
  48. Masclaux C, Valadier M-H, Brugière N, Morot-Gaudry J-F, Hirel B (2000) Characterization of the sink/source transition in tobacco (Nicotiana tabacum L.) in relation to nitrogen management and leaf senescence. Planta 211:510–518. CrossRefGoogle Scholar
  49. Michel G, Tonon T, Scornet D, Cock JM, Kloareg B (2010) Central and storage carbon metabolism of the brown alga Ectocarpus siliculosus: insights into the origin and evolution of storage carbohydrates in Eukaryotes. New Phytol 188:67–81. CrossRefGoogle Scholar
  50. Milledge JJ, Nielsen BV, Bailey D (2016) High-value products from macroalgae: the potential uses of the invasive brown seaweed, Sargassum muticum. Rev Environ Sci Biotechnol 15:67–88. CrossRefGoogle Scholar
  51. Moss BL (1967) The apical meristem of Fucus. New Phytol 66:67–74. CrossRefGoogle Scholar
  52. Moss BL (1983) Sieve elements in the Fucales. New Phytol 93:433–437. CrossRefGoogle Scholar
  53. Moulin M, Deleua C, Larher F, Bouchereau A (2006) The lysine-ketoglutarate reductase–saccharopine dehydrogenase is involved in the osmo-induced synthesis of pipecolic acid in rapeseed leaf tissues. Plant Physiol Biochem 44:474–482. CrossRefGoogle Scholar
  54. Nishitsuji K, Arimoto A, Iwai K, Sudo Y, Hisata K, Fujie M, Arakaki N, Kushiro T, Konishi T, Shinzato C (2016) A draft genome of the brown alga, Cladosiphon okamuranus, S-strain: a platform for future studies of ‘mozuku’ biology. DNA Res 23:561–570. CrossRefGoogle Scholar
  55. Parker BC (1966) Translocation in Macrocystis. III. Composition of sieve tube exudate and identification of the major C14-labeled products. J Phycol 2:38–41. CrossRefGoogle Scholar
  56. Patterson GW (1971) The distribution of sterols in algae. Lipids 6:120–127. CrossRefGoogle Scholar
  57. Pedersen M, Borum J, Fotel F (2010) Phosphorus dynamics and limitation of fast- and slow-growing temperate seaweeds in Oslofjord, Norway. Mar Ecol Prog Ser 399:103–115. CrossRefGoogle Scholar
  58. Penot M, Penot M (1977) Quelques aspects originaux des transports à longue distance dans le thalle de Ascophyllum nodosum (L.) Le Jolis (Phaeophyceae, Fucales). Phycologia 16:339–347. CrossRefGoogle Scholar
  59. Penot M, Floc’h JY, Penot M (1976) Physiologie comparee des transports it longue distance chez les vegetaux superieurs et chez les algues marines. Phycologia 15:299–308. CrossRefGoogle Scholar
  60. Ragan MA, Glombitza KW (1986) Phlorotannins, brown algal polyphenols. In: Round FE, Chapman DJ (eds) Progress in phycological research, 4th edn. Biopress Ltd., Amsterdam, pp 130–241Google Scholar
  61. Raven JA (2003) Long-distance transport in non-vascular plants. Plant, Cell Environ 26:73–76. CrossRefGoogle Scholar
  62. Ravindran G, Ravindran V (1988) Changes in the nutritional composition of cassava (Manihot esculenta Crantz) leaves during maturity. Food Chem 27:299–309. CrossRefGoogle Scholar
  63. Rickert E, Wahl M, Link H, Richter H, Pohnert G (2016) Seasonal variations in surface metabolite composition of Fucus vesiculosus and Fucus serratus from the Baltic Sea. PLoS One 11(12):e0168196. CrossRefGoogle Scholar
  64. Sáez CA, Lobos MG, Macaya EC, Oliva D, Quiroz W, Brown MT (2012) Variation in patterns of metal accumulation in thallus parts of Lessonia trabeculata (Laminariales; Phaeophyceae): implications for biomonitoring. PLoS One 7:e50170. CrossRefGoogle Scholar
  65. Schmid M, Stengel DB (2015) Intra-thallus differentiation of fatty acid and pigment profiles in some temperate Fucales and Laminariales. J Phycol 51:25–36. CrossRefGoogle Scholar
  66. Schmitz K, Srivastava LM (1974) The enzymatic incorporation of 32P into ATP and other organic compounds by sieve-tube sap of Macrocystis integrifolia Bory. Planta 116:85–89. CrossRefGoogle Scholar
  67. Schmitz K, Srivastava LM (1975) On the fine structure of sieve tubes and the physiology of assimilate transport in Alaria marginata. Can J Bot 53:861–876. CrossRefGoogle Scholar
  68. Seca AML, Gouveia VLM, Barreto MC, Silva AMS, Pinto DCGA (2018) Comparative study by GC-MS and chemometrics on the chemical and nutritional profile of Fucus spiralis L. juvenile and mature life-cycle phases. J Appl Phycol 30:2539–2548. CrossRefGoogle Scholar
  69. Silberfeld T, Leigh JW, Verbruggen H, Cruaud C, de Reviers B, Rousseau F (2010) A multi-locus time-calibrated phylogeny of the brown algae (Heterokonta, Ochrophyta, Phaeophyceae): investigating the evolutionary nature of the ‘‘brown algal crown radiation”. Mol Phylogenet Evol 56:659–674. CrossRefGoogle Scholar
  70. Stein SE (1999) An integrated method for spectrum extraction and compound identification from gas chromatography/mass spectrometry data. J Am Soc Mass Spectrom 10:770–781. CrossRefGoogle Scholar
  71. Stengel DB, McGrath H, Morrison LJ (2005) Tissue Cu, Fe and Mn concentrations in different-aged and different functional thallus regions of three brown algae from western Ireland. Estuar Coast Shelf Sci 65:687–696. CrossRefGoogle Scholar
  72. Tarakhovskaya ER, Maslov YI (2007) The dynamics of photosynthetic pigments content in ontogenesis of Fucus vesiculosus L. Vestnik Sankt-Peterburgskogo Gosudarstvennogo Universiteta, Seriya 3. Biologiya 4:111–118 In Russian Google Scholar
  73. Tarakhovskaya ER, Bilova TE, Maslov YI (2015) Hydrogen peroxide content and vanadium-dependent haloperoxidase activity in thalli of six species of Fucales (Phaeophyceae). Phycologia 54:417–424. CrossRefGoogle Scholar
  74. 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 22:1509. CrossRefGoogle Scholar
  75. Terauchi M, Nagasato C, Motomura T (2015) Plasmodesmata of brown algae. J Plant Res 128:7–15. CrossRefGoogle Scholar
  76. Turgeon R (1989) The sink-source transition in leaves. Annu Rev Plant Physiol Plant Mol Biol 40:119–138. CrossRefGoogle Scholar
  77. Van Alstyn KL, Whitman SL, Ehlig JM (2001) Differences in herbivore preferences, phlorotannin production, and nutritional quality between juvenile and adult tissues from marine brown algae. Mar Biol 139:201–210. CrossRefGoogle Scholar
  78. Wells ML, Potin P, Craigie JS, Raven JA, Merchant SS, Helliwell KE, Smith AG, Camire ME, Brawley SH (2017) Algae as nutritional and functional food sources: revisiting our understanding. J Appl Phycol 29:949–982. CrossRefGoogle Scholar
  79. Yamaguchi T, Ikawa T, Nisizawa K (1966) Incorporation of radioactive carbon from H14CO3- into sugar constituents by a brown alga, Eisenia bicyclis, during photosynthesis and its fate in the dark. Plant Cell Physiol 7:217–229. Google Scholar
  80. Ye N, Zhang X, Miao M, Fan X, Zheng Y, Xu D, Wang J, Zhou L, Wang D, Gao Y, Wang Y, Shi W, Ji P, Li D, Guan Z, Shao C, Zhuang Z, Gao Z, Qi J, Zhao F (2015) Saccharina genomes provide novel insight into kelp biology. Nat Commun 6:6986. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Faculty of Chemistry and MineralogyLeipzig UniversityLeipzigGermany
  2. 2.Department of Plant Physiology and Biochemistry, Faculty of BiologySt.-Petersburg State UniversitySt.-PetersburgRussia
  3. 3.Department of Scientific InformationRussian Academy of Sciences LibrarySt.-PetersburgRussia

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