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

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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.

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References

  • 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

  • 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

  • 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 79:531–537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 67:165–168

    Article  CAS  Google Scholar 

  • 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 68:183–189

    Article  CAS  Google Scholar 

  • Black WAP (1950) The seasonal variation in weight and chemical composition of the common British Laminariaceae. J Mar Biol Assoc U K 29:45–72

    Article  CAS  Google Scholar 

  • 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 1:505–517

    Article  CAS  Google Scholar 

  • Chapman ARO, Craigie JS (1977) Seasonal growth in Laminaria longicruris: relations with dissolved inorganic nutrients and internal reserves of nitrogen. Mar Biol 40:197–205

    Article  CAS  Google Scholar 

  • Chapman ARO, Craigie JS (1978) Seasonal growth in Laminaria longicruris: relations with reserve carbohydrate storage and production. Mar Biol 46:209–213

    Article  CAS  Google Scholar 

  • 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 310:203–210

    Article  CAS  Google Scholar 

  • Craigie JS (1974) Storage products. In: Stewart WPD (ed) Algal physiology and biochemistry. University of California Press, Berkley, pp 206–235

    Google Scholar 

  • Dayton PK (1985) Ecology of kelp communities. Annu Rev Ecol Syst 16:215–245

    Article  Google Scholar 

  • Dethier MN, Williams SL (2009) Seasonal stresses shift optimal intertidal algal habitats. Mar Biol 156:555–567

    Article  Google Scholar 

  • Devillé C, Damas J, Forget P, Dandrifosse G, Peulen O (2004) Laminarin in the dietary fibre concept. J Sci Food Agric 84:1030–1038

    Article  Google Scholar 

  • Drew EA, Hastings RM (1992) A year-round ecophysiological study of Himantothallus grandifolius (Desmarestiales, Phaeophyta) at Signy Island, Antarctica. Phycologia 31:262–277

    Article  Google Scholar 

  • Duggins DO, Simenstad CA, Estes JA (1989) Magnification of secondary production by kelp detritus in coastal marine ecosystems. Science 245:170–173

    Article  CAS  PubMed  Google Scholar 

  • Dunton KH, Jodwalis CM (1988) Photosynthetic performance of Laminaria solidungula measured in situ in the Alaskan High Arctic. Mar Biol 98:277–285

    Article  Google Scholar 

  • Dunton KH, Schell DM (1986) Seasonal carbon budget and growth of Laminaria solidungula in the Alaskan High Arctic. Mar Ecol Prog Ser 31:57–66

    Article  Google Scholar 

  • Dunton KH, Schell DM (1987) Dependence of consumers on macroalgal (Laminaria solidungula) carbon in an arctic kelp community: δ13C evidence. Mar Biol 93:615–625

    Article  CAS  Google Scholar 

  • Fleming M, Hirst E, Manners DJ (1966) The constitution of laminarin Part VI: the fine structure of soluble laminarin. Proc Int Seaweed Symp 5:255–260

    Google Scholar 

  • Fredriksen S (2003) Food web studies in a Norwegian kelp forest based on stable isotope (δ13C and δ15N) analysis. Mar Ecol Prog Ser 260:71–81

    Article  CAS  Google Scholar 

  • 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 69:91–101

    Article  Google Scholar 

  • Gerard VA (1982) Growth and utilization of internal nitrogen reserves by the giant kelp Macrocystis pyrifera in a low-nitrogen environment. Mar Biol 35:27–35

    Article  Google Scholar 

  • 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 25–46

    Chapter  Google Scholar 

  • 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

    Article  Google Scholar 

  • Gorham J, Lewey SA (1984) Seasonal changes in the chemical composition of Sargassum muticum. Mar Biol 80:103–107

    Article  CAS  Google Scholar 

  • Hatcher BG, Chapman AR, Mann KH (1977) An annual carbon budget for the kelp Laminaria longicruris. Mar Biol 44:85–96

    Article  CAS  Google Scholar 

  • Hurd CL (2000) Water motion, marine macroalgal physiology, and production. J Phycol 36:453–472

    Article  CAS  Google Scholar 

  • 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 14:1–8

    CAS  Google Scholar 

  • Jensen A, Indergaard M, Holt TJ (1985) Seasonal variation in the chemical composition of Saccorhiza polyschides (Laminariales, Phaeophyceae). Bot Mar 28:375–382

    Article  CAS  Google Scholar 

  • Johnston CS, Jones RG, Hunt RD (1977) A seasonal carbon budget for a laminarian population in a Scottish sea-loch. Helgolander Meeresun 30:527–545

    Article  CAS  Google Scholar 

  • 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 29:373–378

    CAS  Google Scholar 

  • Kremer BP (1975) Physiologisch-chemische Charakteristik verschiedener Thallusbereiche von Fucus serratus. Helgolander Meeresun 127:115–127

    Article  Google Scholar 

  • Küppers U, Kremer BP (1978) Longitudinal profiles of carbon dioxide fixation capacities in marine macroalgae. Plant Physiol 62:49–53

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • Lloyd JB, Whelan WJ (1969) An improved method for enzymic determination of glucose in the presence of maltose. Anal Biochem 30:467–470

    Article  CAS  PubMed  Google Scholar 

  • Lobban CS (1978) Translocation of C in Macrocystis pyrifera (Giant Kelp). Plant Physiol 61:585–589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lobban CS, Harrison PJ (1994) Seaweed ecology and physiology. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Lüning K (1968) Growth of amputated and dark-exposed individuals of the brown alga Laminaria hyperborea. Mar Biol 2:218–223

    Article  Google Scholar 

  • 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 1:195–207

    Article  Google Scholar 

  • 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 23:275–281

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

  • 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

  • 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 58:1069–1085

    Article  Google Scholar 

  • Raven JA (2003) Long-distance transport in non-vascular plants. Plant Cell Environ 26:73–85

    Article  Google Scholar 

  • Raven JA, Beardall J, Chudek JA, Scrimgeour CM, Clayton MN, McInroy SG (2001) Altritol synthesis by Notheia anomala. Phytochemistry 58:389–94

    Article  CAS  PubMed  Google Scholar 

  • Read SM, Currie G, Bacic A (1996) Analysis of the structural heterogeneity of laminarin by electrospray-ionisation-mass spectrometry. Carbohydr Res 281:187–201

    Article  CAS  PubMed  Google Scholar 

  • Rioux L-E, Turgeon SL, Beaulieu M (2009) Effect of season on the composition of bioactive polysaccharides from the brown seaweed Saccharina longicruris. Phytochemistry 70:1069–1075

    Article  CAS  PubMed  Google Scholar 

  • Rioux L-E, Turgeon SL, Beaulieu M (2010) Structural characterization of laminaran and galactofucan extracted from the brown seaweed Saccharina longicruris. Phytochemistry 71:1586–1595

    Article  CAS  PubMed  Google Scholar 

  • 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 27:363–373

    Article  CAS  Google Scholar 

  • Schmiedeberg W (1885) Über die Bestandteile der Laminaria. Gesellschaft deutscher Naturforscher und Ärzte, Leipzig, Tageblatt der 58. Versammlung, p. 427

  • Schmitz K, Lobban CS (1976) A survey of translocation in Laminariales (Phaeophyceae). Mar Biol 36:207–216

    Article  Google Scholar 

  • 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 67:418–429

    Article  CAS  Google Scholar 

  • Stenhouse J (1844) On the occurrence of mannite in Laminaria saccharina and other seaweeds. J Chem Soc 2:136–140

    Google Scholar 

  • 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 82:68–80

    Article  PubMed  Google Scholar 

  • Templeton DW, Quinn M, Van Wychen S, Hyman D, Laurens LML (2012) Separation and quantification of microalgal carbohydrates. J Chromatogr A 1270:225–34

    Article  CAS  PubMed  Google Scholar 

  • 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 37:157–165

    Article  CAS  Google Scholar 

  • Wheeler PA, North WJ (1981) Nitrogen supply, tissue composition and frond growth rates for Macrocystis pyrifera off the coast of southern California. Mar Biol 64:59–69

    Article  CAS  Google Scholar 

  • Wiencke C, Gómez I, Dunton K (2009) Phenology and seasonal physiological performance of polar seaweeds. Bot Mar 52:585–592

    CAS  Google Scholar 

  • 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 26:429–434

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Yemm EW, Willis AJ (1954) The estimation of carbohydrates in plant extracts by anthrone. Biochem J 57:508–514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 5980916A

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Acknowledgments

We gratefully thank Udo Nitschke and Andreas Wagner for collection and provision of the algal material, and Juliane Müller and Henrike Pfefferkorn for their invaluable help in the lab. This research was funded by the Project BIOACID Phase II of the German Federal Ministry of Education and Research (BMBF; FKZ 03F0655L).

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Authors and Affiliations

  1. Institute of Biological Sciences, Applied Ecology and Phycology, University of Rostock, Albert-Einstein-Straße 3b, 18059, Rostock, Germany

    Angelika Graiff & Ulf Karsten

  2. Institute of Chemistry, Analytical and Technical Chemistry, University of Rostock, Albert-Einstein-Straße 3a, 18059, Rostock, Germany

    Wolfgang Ruth & Udo Kragl

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  1. Angelika Graiff
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  2. Wolfgang Ruth
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  3. Udo Kragl
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Correspondence to Angelika Graiff.

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Graiff, A., Ruth, W., Kragl, U. et al. Chemical characterization and quantification of the brown algal storage compound laminarin — A new methodological approach. J Appl Phycol 28, 533–543 (2016). https://doi.org/10.1007/s10811-015-0563-z

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  • DOI: https://doi.org/10.1007/s10811-015-0563-z

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