Journal of Applied Phycology

, Volume 28, Issue 1, pp 533–543

Chemical characterization and quantification of the brown algal storage compound laminarin — A new methodological approach

  • Angelika Graiff
  • Wolfgang Ruth
  • Udo Kragl
  • Ulf Karsten
Article

Abstract

The polysaccharide laminarin (β-1,3-glucan) is used as a long-term carbon storage compound in brown algae. This chemical storage form of carbon enables perennial brown algae in seasonally fluctuating ecosystems to uncouple growth from photosynthesis, i.e., most of these plants grow as seasonal anticipators in winter based on remobilization of laminarin, while in summer, growth typically ceased to fill up the storage pool. Because of this high ecological relevance, a reliable and precise method for determination and quantification of laminarin is needed. Therefore, a simple, efficient, cold water extraction method coupled to a new quantitative liquid chromatography-mass spectrometrical method (LC-MS) was developed. Laminarin was determined in 9 out of 12 brown algal species, and its expected typical molar mass distribution of 2000–7000 Da was confirmed. Furthermore, laminarin consisted of a complex mixture of different chemical forms, since 15 chemical laminarin species with distinct molecular weights were measured in 9 species of brown algae. Differences in chain length and number of laminarin species seem to be species specific and hence may indicate some chemotaxonomic value. Laminarin concentrations in the algal tissues ranged from 0.03 to 0.86 % dry weight (DW). The direct chemical characterization and quantification of laminarin by LC-MS represents a powerful method to verify the biochemical and ecological importance of laminarin for brown algae.

Keywords

Kelps LC-MS Mannitol Seasonal growth Carbon storage 

References

  1. Anderson FB, Hirst EL, Manners DJ, Ross AG (1958) 663. The constitution of laminarin. Part III. The fine structure of insoluble laminarin. J Chem Soc 3233–3243. doi:10.1039/JR9580003233
  2. Annan WD, Hirst E, Manners DJ (1965) 162. The constitution of laminarin. Part V. The location of 1,6-glucosidic linkages. J Chem Soc 885–891. doi:10.1039/JR9650000885
  3. Beattie A, Hirst EL, Percival E (1961) Studies on the metabolism of the Chrysophyceae. Comparative structural investigations on leucosin (chrysolaminarin) separated from diatoms and laminarin from the brown algae. Biochem J 79:531–537CrossRefPubMedPubMedCentralGoogle Scholar
  4. Black WAP (1948) The seasonal variation in chemical constitution of some of the sublittoral seaweeds common to Scotland. Part I. Laminaria cloustoni. J Soc Chem Ind 67:165–168CrossRefGoogle Scholar
  5. Black WAP (1949) Seasonal variation in chemical composition of some of the littoral seaweeds common to Scotland. Part II. Fucus serratus, Fucus vesiculosus, Fucus spiralis and Pelvetia canaliculata. J Soc Chem Ind 68:183–189CrossRefGoogle Scholar
  6. Black WAP (1950) The seasonal variation in weight and chemical composition of the common British Laminariaceae. J Mar Biol Assoc U K 29:45–72CrossRefGoogle Scholar
  7. Black WAP, Cornhill WJ, Dewar ET, Woodward FN (1951) Manufacture of algal chemicals. III. Laboratory-scale isolation of laminarin from brown marine algae. J Appl Chem 1:505–517CrossRefGoogle Scholar
  8. Chapman ARO, Craigie JS (1977) Seasonal growth in Laminaria longicruris: relations with dissolved inorganic nutrients and internal reserves of nitrogen. Mar Biol 40:197–205CrossRefGoogle Scholar
  9. Chapman ARO, Craigie JS (1978) Seasonal growth in Laminaria longicruris: relations with reserve carbohydrate storage and production. Mar Biol 46:209–213CrossRefGoogle Scholar
  10. Chizhov AO, Dell A, Morris HR, Reason AJ, Haslam SM, McDowell RA, Chizhov OS, Usov AI (1998) Structural analysis of laminarans by MALDI and FAB mass spectrometry. Carbohydr Res 310:203–210CrossRefGoogle Scholar
  11. Craigie JS (1974) Storage products. In: Stewart WPD (ed) Algal physiology and biochemistry. University of California Press, Berkley, pp 206–235Google Scholar
  12. Dayton PK (1985) Ecology of kelp communities. Annu Rev Ecol Syst 16:215–245CrossRefGoogle Scholar
  13. Dethier MN, Williams SL (2009) Seasonal stresses shift optimal intertidal algal habitats. Mar Biol 156:555–567CrossRefGoogle Scholar
  14. Devillé C, Damas J, Forget P, Dandrifosse G, Peulen O (2004) Laminarin in the dietary fibre concept. J Sci Food Agric 84:1030–1038CrossRefGoogle Scholar
  15. Drew EA, Hastings RM (1992) A year-round ecophysiological study of Himantothallus grandifolius (Desmarestiales, Phaeophyta) at Signy Island, Antarctica. Phycologia 31:262–277CrossRefGoogle Scholar
  16. Duggins DO, Simenstad CA, Estes JA (1989) Magnification of secondary production by kelp detritus in coastal marine ecosystems. Science 245:170–173CrossRefPubMedGoogle Scholar
  17. Dunton KH, Jodwalis CM (1988) Photosynthetic performance of Laminaria solidungula measured in situ in the Alaskan High Arctic. Mar Biol 98:277–285CrossRefGoogle Scholar
  18. Dunton KH, Schell DM (1986) Seasonal carbon budget and growth of Laminaria solidungula in the Alaskan High Arctic. Mar Ecol Prog Ser 31:57–66CrossRefGoogle Scholar
  19. Dunton KH, Schell DM (1987) Dependence of consumers on macroalgal (Laminaria solidungula) carbon in an arctic kelp community: δ13C evidence. Mar Biol 93:615–625CrossRefGoogle Scholar
  20. Fleming M, Hirst E, Manners DJ (1966) The constitution of laminarin Part VI: the fine structure of soluble laminarin. Proc Int Seaweed Symp 5:255–260Google Scholar
  21. Fredriksen S (2003) Food web studies in a Norwegian kelp forest based on stable isotope (δ13C and δ15N) analysis. Mar Ecol Prog Ser 260:71–81CrossRefGoogle Scholar
  22. Gagné JA, Mann KH, Chapman ARO (1982) Seasonal patterns of growth and storage in Laminaria longicruris in relation to differing patterns of availability of nitrogen in the water. Mar Biol 69:91–101CrossRefGoogle Scholar
  23. Gerard VA (1982) Growth and utilization of internal nitrogen reserves by the giant kelp Macrocystis pyrifera in a low-nitrogen environment. Mar Biol 35:27–35CrossRefGoogle Scholar
  24. 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
  25. 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 19:115–124CrossRefGoogle Scholar
  26. Gorham J, Lewey SA (1984) Seasonal changes in the chemical composition of Sargassum muticum. Mar Biol 80:103–107CrossRefGoogle Scholar
  27. Hatcher BG, Chapman AR, Mann KH (1977) An annual carbon budget for the kelp Laminaria longicruris. Mar Biol 44:85–96CrossRefGoogle Scholar
  28. Hurd CL (2000) Water motion, marine macroalgal physiology, and production. J Phycol 36:453–472CrossRefGoogle Scholar
  29. Jensen A, Haug A (1956) Geographical and seasonal variation in the chemical composition of Laminaria hyperborea and Laminaria digitata from the Norwegian coast. Rep Norw Inst Seaweed Res 14:1–8Google Scholar
  30. Jensen A, Indergaard M, Holt TJ (1985) Seasonal variation in the chemical composition of Saccorhiza polyschides (Laminariales, Phaeophyceae). Bot Mar 28:375–382CrossRefGoogle Scholar
  31. Johnston CS, Jones RG, Hunt RD (1977) A seasonal carbon budget for a laminarian population in a Scottish sea-loch. Helgolander Meeresun 30:527–545CrossRefGoogle Scholar
  32. Karsten U, Thomas DM, Weykam G, Daniel C, Kirst GO (1991) A simple and rapid method for extraction and separation of low molecular weight of carbohydrates from marine macroalgae using high performance liquid chromatography. Plant Physiol Biochem 29:373–378Google Scholar
  33. Kremer BP (1975) Physiologisch-chemische Charakteristik verschiedener Thallusbereiche von Fucus serratus. Helgolander Meeresun 127:115–127CrossRefGoogle Scholar
  34. Küppers U, Kremer BP (1978) Longitudinal profiles of carbon dioxide fixation capacities in marine macroalgae. Plant Physiol 62:49–53CrossRefPubMedPubMedCentralGoogle Scholar
  35. 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 44:345–350CrossRefGoogle Scholar
  36. Lloyd JB, Whelan WJ (1969) An improved method for enzymic determination of glucose in the presence of maltose. Anal Biochem 30:467–470CrossRefPubMedGoogle Scholar
  37. Lobban CS (1978) Translocation of C in Macrocystis pyrifera (Giant Kelp). Plant Physiol 61:585–589CrossRefPubMedPubMedCentralGoogle Scholar
  38. Lobban CS, Harrison PJ (1994) Seaweed ecology and physiology. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  39. Lüning K (1968) Growth of amputated and dark-exposed individuals of the brown alga Laminaria hyperborea. Mar Biol 2:218–223CrossRefGoogle Scholar
  40. Lüning K (1979) Growth strategies of three Laminaria species (Phaeophyceae) inhabiting different depth zones in the sublittoral region of Helgoland (North Sea). Mar Ecol Prog Ser 1:195–207CrossRefGoogle Scholar
  41. Lüning K, Schmitz K, Willenbrink J (1973) CO2 fixation and translocation in benthic marine algae. III. Rates and ecological significance of translocation in Laminaria hyperborea and L. saccharina. Mar Biol 23:275–281CrossRefGoogle Scholar
  42. 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 188:67–81CrossRefPubMedGoogle Scholar
  43. Peat S, Whelan WJ, Lawley HG (1958) 141. The structure of laminarin. Part I. The main polymeric linkage. J Chem Soc 724–728. doi:10.1039/JR9580000724
  44. Percival EGV, Ross AG (1951) 156. The constitution of laminarin. Part II. The soluble laminarin of Laminaria digitata. J Chem Soc 720–726. doi:10.1039/JR9510000720
  45. Pérez-Matus A, Ferry-Graham LA, Cea A, Vásquez JA (2007) Community structure of temperate reef fishes in kelp-dominated subtidal habitats of northern Chile. Mar Freshw Res 58:1069–1085CrossRefGoogle Scholar
  46. Raven JA (2003) Long-distance transport in non-vascular plants. Plant Cell Environ 26:73–85CrossRefGoogle Scholar
  47. Raven JA, Beardall J, Chudek JA, Scrimgeour CM, Clayton MN, McInroy SG (2001) Altritol synthesis by Notheia anomala. Phytochemistry 58:389–94CrossRefPubMedGoogle Scholar
  48. Read SM, Currie G, Bacic A (1996) Analysis of the structural heterogeneity of laminarin by electrospray-ionisation-mass spectrometry. Carbohydr Res 281:187–201CrossRefPubMedGoogle Scholar
  49. Rioux L-E, Turgeon SL, Beaulieu M (2009) Effect of season on the composition of bioactive polysaccharides from the brown seaweed Saccharina longicruris. Phytochemistry 70:1069–1075CrossRefPubMedGoogle Scholar
  50. Rioux L-E, Turgeon SL, Beaulieu M (2010) Structural characterization of laminaran and galactofucan extracted from the brown seaweed Saccharina longicruris. Phytochemistry 71:1586–1595CrossRefPubMedGoogle Scholar
  51. Schiener P, Black KD, Stanley MS, Green DH (2015) The seasonal variation in the chemical composition of the kelp species Laminaria digitata, Laminaria hyperborea, Saccharina latissima and Alaria esculenta. J Appl Phycol 27:363–373CrossRefGoogle Scholar
  52. Schmiedeberg W (1885) Über die Bestandteile der Laminaria. Gesellschaft deutscher Naturforscher und Ärzte, Leipzig, Tageblatt der 58. Versammlung, p. 427Google Scholar
  53. Schmitz K, Lobban CS (1976) A survey of translocation in Laminariales (Phaeophyceae). Mar Biol 36:207–216CrossRefGoogle Scholar
  54. Schmitz K, Lüning K, Willenbrink J (1972) CO2-Fixation and translocation in benthic marine algae. II. On translocation of 14C-labelled assimilates in Laminaria hyperborea and L. saccharina. Z Pflanzenphysiol 67:418–429CrossRefGoogle Scholar
  55. Stenhouse J (1844) On the occurrence of mannite in Laminaria saccharina and other seaweeds. J Chem Soc 2:136–140Google Scholar
  56. Surif MB, Raven JA (1990) Photosynthetic gas exchange under emersed conditions in eulittoral and normally submersed members of the Fucales and the Laminariales: Interpretation in relation to C isotope ratio and N and water use efficiency. Oecologia 82:68–80CrossRefPubMedGoogle Scholar
  57. Templeton DW, Quinn M, Van Wychen S, Hyman D, Laurens LML (2012) Separation and quantification of microalgal carbohydrates. J Chromatogr A 1270:225–34CrossRefPubMedGoogle Scholar
  58. Verardo DJ, Froehlich PN, McIntyre A (1990) Determination of organic carbon and nitrogen in marine sediments using Carlo Erba NA-1500 Analyzer. Deep-Sea Res 37:157–165CrossRefGoogle Scholar
  59. Wheeler PA, North WJ (1981) Nitrogen supply, tissue composition and frond growth rates for Macrocystis pyrifera off the coast of southern California. Mar Biol 64:59–69CrossRefGoogle Scholar
  60. Wiencke C, Gómez I, Dunton K (2009) Phenology and seasonal physiological performance of polar seaweeds. Bot Mar 52:585–592Google Scholar
  61. Wright PJ, Clayton MN, Chudek JA, Foster R, Reed RH (1987) The carbohydrate altritol in Bifurcariopsis capensis, Hormosira banksii, Notheia anomala and Xiphophora chondrophylla (Fucales, Phaeophyta) from the southern hemisphere. Phycologia 26:429–434CrossRefGoogle Scholar
  62. 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 7:217–229Google Scholar
  63. Yemm EW, Willis AJ (1954) The estimation of carbohydrates in plant extracts by anthrone. Biochem J 57:508–514CrossRefPubMedPubMedCentralGoogle Scholar
  64. Yvin J-C, LeVasseur F, Hud’Homme F (1999) Use of laminarin and oligosaccharides derived therefrom in cosmetics and for preparing a skin treatment drug. US Patent 5980916AGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Angelika Graiff
    • 1
  • Wolfgang Ruth
    • 2
  • Udo Kragl
    • 2
  • Ulf Karsten
    • 1
  1. 1.Institute of Biological Sciences, Applied Ecology and PhycologyUniversity of RostockRostockGermany
  2. 2.Institute of Chemistry, Analytical and Technical ChemistryUniversity of RostockRostockGermany

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