Skip to main content
Log in

Lipid content and fatty acid consumption in zoospores/developing gametophytes of Saccharina latissima (Laminariales, Phaeophyceae) as potential precursors for secondary metabolites as phlorotannins

  • Original Paper
  • Published:
Polar Biology Aims and scope Submit manuscript

Abstract

Phlorotannins are considered inter alia to act protective to a variety of stressors, while lipids in spores are known to fuel various metabolic processes during spore release and settlement. Here, phlorotannin production in zoospores/juvenile gametophytes in relation to lipid metabolism was investigated for the first time in order to study-related metabolic costs. The experiment was carried out in Ny-Ålesund (Svalbard, Arctic) within the development from spores to juvenile gametophytes of the brown alga Saccharina latissima over 20 days. In the release stage, the total phlorotannin content of single zoospores was 1.5 × 10−7 μg and 1.9 × 10−7 μg in the surrounding medium. Upon release, the total amount of lipids was 1.76 × 10−5 μg lipid zoospore−1 containing the major fatty acids 16:0 and 18:0, 18:1(n-9), 18:2 (n-6), 18:3(n-3), 20:4(n-6), and 20:5(n-3). During development from spores to gametophytes, a decrease in fatty acids was observed via electron microscopy and a decrease in the fatty acid 18:1(n-9) from 45 to 30% was measured by gas chromatography in particular. While phlorotannin content within the spores remained stable, phlorotannins accumulated in the surrounding medium of gametophytes to 4.0 × 10−7 μg phlorotannins spore−1 indicating exudation processes. Results obtained support the key and multifunctional role of lipids in zoospore/gametophyte metabolism and may indicate that gametophytes of S. latissima need approximately 10 days to switch to photo-autotrophic strategies, becoming independent of storage lipids. In addition, fatty acids might represent an essential energy source to fuel adaptive responses.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abdala-Díaz RT, Cabello-Pasini A, Pérez-Rodríguez E, Conde Álvarez RM, Figueroa FL (2005) Daily and seasonal variations of optimum quantum yield and phenolic compounds in Cystoseira tamariscifolia (Phaeophyta). Mar Biol 148:459–465

    Article  Google Scholar 

  • Amsler CD, Neushul M (1991) Photosynthetic physiology and chemical composition of spores of the kelps Macrocystis pyrifera, Nereocystis luetkeana, Laminaria farlowii, and Pterygophora californica (Phaeophyceae). J Phycol 27:26–34

    Article  CAS  Google Scholar 

  • Araki S, Sakurai T, Kawaguchi A, Murata N (1987) Positional distribution of fatty acids in glycerolipids of the marine red alga Porphyra yezoensis. Plant Cell Physiol 28:761–766

    CAS  Google Scholar 

  • Arnold TM, Targett NM (1998) Quantifying in situ rates of phlorotannin synthesis and polymerization in marine brown algae. J Chem Ecol 24:577–595

    Article  CAS  Google Scholar 

  • Banaimoon SA (1992) Fatty acids in marine macroalgae from southern Yemen (Hadramout) including occurrence of eicosatetraenoic (20:4) and eicosapentaenoic (20:5) acids. Bot Mar 35:165–168

    Article  CAS  Google Scholar 

  • Bartsch I, Wiencke C, Bischof K, Buchholz CM, Buck BH, Eggert A, Feuerpfeil P, Hanelt D, Jacobsen S, Karez R, Karsten U, Molis M, Roleda MY, Schumann R, Schubert H, Valentin K, Weinberger F, Wiese J (2008) The genus Laminaria sensu lato: recent insights and developments. Eur J Phycol 43:1–86

    Article  Google Scholar 

  • Brzezinski MA, Reed DC, Amsler CD (1993) Neutral lipids as major storage products in zoospores of the giant kelp Macrocystis pyrifera (Phaeophyceae). J Phycol 29:16–23

    Article  CAS  Google Scholar 

  • Fairhead VA, Amsler CD, McClintock JB (2006) Lack of defense or phlorotannin induction by UV radiation or mesograzers in Desmarestia anceps and D. menziesii (Phaeophyceae). J Phycol 42:1174–1183

    Article  CAS  Google Scholar 

  • Fleurence J, Gutbier G, Mabeau S, Estes IA (1994) Fatty acids from 11 marine macroalgae of the french Brittany coast. J Appl Phycol 6:527–532

    Article  CAS  Google Scholar 

  • Folch J, Lees M, Stanley GHS (1957) A simple method for the purification of total lipids from animal tissues. J Biol Chem 226:497–509

    PubMed  CAS  Google Scholar 

  • Gerwick WH, Proteau PJ, Nagle DG, Wise ML, Jiang ZD, Bernart MW, Hamberg M (1993) Biologically active oxylipins from seaweeds. Hydrobiologia 260(261):653–665

    Article  Google Scholar 

  • Graeve M, Kattner G, Wiencke C, Karsten U (2002) Fatty acid composition of Arctic and Antarctic macroalgae: indicator of phylogenic and trophic relationships. Mar Ecol Prog Ser 231:67–74

    Article  CAS  Google Scholar 

  • Hammerstrom K, Dethier MN, Duggins DO (1998) Rapid phlorotannin induction and relaxation in five Washington kelps. Mar Ecol Prog Ser 165:293–305

    Article  CAS  Google Scholar 

  • Harwood JL (1984) Effects of the environment on the acyl lipids of algae and higher plants. In: Siegenthaler PA, Eichenberger W (eds) Structure function and metabolism of plant lipids. Elsevier Science, New York, pp 543–550

    Google Scholar 

  • Harwood JL (1988) Fatty acid metabolism. Ann Rev Plant Physio 3:101–138

    Article  Google Scholar 

  • Harwood JL (1998) Membrane lipids in algae. In: Siegenthaler PA, Murata N (eds) Lipids in photosynthesis. Kluwer Academic Publishers, Dordrecht, pp 53–64

    Google Scholar 

  • Henry EC, Cole KM (1982a) Ultrastructure of swarmers in the Laminariales (Phaeophyceae). I. Zoospores. J Phycol 18:550–569

    Article  Google Scholar 

  • Henry EC, Cole KM (1982b) Ultrastructure of swarmers in the Laminariales (Phaeophyceae). II. Sperm. J Phycol 18:570–579

    Article  Google Scholar 

  • Henry BE, Van Alstyne KL (2004) Effects of UV radiation on growth and phlorotannins in Fucus gardneri (Phaeophyceae) juveniles and embryos. J Phycol 40:527–533

    Article  CAS  Google Scholar 

  • Hitchcock C, Nichols BW (1971) Plant lipid biochemistry. Academic press, London

    Google Scholar 

  • Jamieson GR, Reid EH (1972) The component fatty acids of some marine algal lipids. Phytochemistry 11:1423–1432

    Article  CAS  Google Scholar 

  • Jennings JG, Steinberg PD (1997) Phlorotannins versus other factors affecting epiphyte abundance on the kelp Ecklonia radiata. Oecologia 109:461–473

    Article  Google Scholar 

  • Jones AL, Harwood JL (1992) Lipid composition of the brown algae Fucus vesiculosus and Ascophyllum nodosum. Phytochemistry 31:3397–3403

    Article  CAS  Google Scholar 

  • Kattner G, Fricke HSG (1986) Simple gas-liquid chromatographic method for the simultaneous determination of fatty acids and alcohols in wax esters of marine organisms. J Chromatogr 361:263–268

    Article  CAS  Google Scholar 

  • Khotimchenko SV, Vaskowsky VE (1990) Distribution of C20 polyenoic fatty acids in red macrophytic algae. Bot Mar 33:525–528

    Article  CAS  Google Scholar 

  • Koivikko R, Loponen J, Honkanen T, Jormalainen V (2005) Contents of soluble, cell-wall-bound and exuded phlorotannins in the brown alga Fucus vesicolosus, with implications on their ecological functions. J Chem Ecol 31:195–210

    Article  PubMed  CAS  Google Scholar 

  • Loiseaux S (1973) Ultrastructure of zoidogenesis in unilocular zoidocysts of several brown algae. J Phycol 9:277–289

    Google Scholar 

  • Napolitano GE (1994) The relationship of lipids with light and chlorophyll measurement in fresh water algae and periphyton. J Phycol 30:943–950

    Article  CAS  Google Scholar 

  • Pavia H, Cervin G, Lindgren A, Åberg P (1997) Effects of UV-B radiation and simulated herbivory on phlorotannins in the brown alga Ascophyllum nodosum. Mar Ecol Progr Ser 157:139–146

    Article  CAS  Google Scholar 

  • Pohl P, Zurheide F (1979) Fatty acid and lipids of marine algae and the control of their biosynthesis by environmental factors. In: Hoppe HA, Levring T, Tanaka Y (eds) Marine algae in pharmaceutical science. Walter de Gruyter, Berlin, pp 473–523

    Google Scholar 

  • Ragan MA, Glombitza KW (1986) Phlorotannins, brown algal polyphenols. In: Round, Chapman (eds.) Progress in phycological research 4, Biopress LTD, Bristol, pp 129–241

  • Reed DC, Amsler CD, Ebeling AW (1992) Dispersal in kelps: factors affecting spore swimming and competency. Ecology 73:1577–1585

    Article  Google Scholar 

  • Reed DC, Brzezinski MA, Coury DA, Graham WH, Petty RL (1999) Neutral lipids in macroalgal spores and their role in swimming. Mar Biol 133:737–744

    Article  CAS  Google Scholar 

  • Roughan PG, Slack CR (1982) Cellular organization of glycerolipid mechanism. Ann Rev Plant Physiol 33:97–132

    Article  CAS  Google Scholar 

  • Schlapfer P, Eichenberger W (1983) Evidence for the involvement of DGTS in the desaturation of oleic and linoleic acids in Chlamydomonas reinhardii (Chlorophyceae). Plant Sci Lett 32:243–252

    Article  CAS  Google Scholar 

  • Schoenwaelder MEA, Clayton MN (1998) Secretion of phenolic substances into zygote wall and cell plate in embryos of Hormosira and Acrocarpia (Fucales, Phaeophyceae). J Phycol 34:969–980

    Article  CAS  Google Scholar 

  • Smith KL, Harwood JL (1984) Lipids and lipid metabolism in the brown alga Fucus serratus. Phytochemistry 23:2469–2473

    Article  CAS  Google Scholar 

  • Sokal R, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research. Freeman, New York

    Google Scholar 

  • Somerville C (1995) Direct tests of the role of membrane lipid composition in low-temperature-induced photoinhibition and chilling sensitivity in plants and cyanobacteria. Proc Natl Acad Sci USA 92:6215–6218

    Article  PubMed  CAS  Google Scholar 

  • Steinberg PD (1985) Feeding preferences of Tegula funebralis and chemical defences of marine brown algae. Ecol Monogr 55:333–349

    Article  Google Scholar 

  • Steinberg PD, van Altena I (1992) Tolerance of marine invertebrate herbivores to brown algal phlorotannins in temperate Australasia. Ecol Monogr 62:189–222

    Article  Google Scholar 

  • Steinhoff FS, Wiencke C, Müller R, Bischof K (2008) Effects of ultraviolet radiation and temperature on the ultrastructure of zoospores of the brown macroalga Laminaria hyperborea. Plant Biol 10:388–397

    Article  PubMed  CAS  Google Scholar 

  • Sukenik A, Carmeli Y (1990) Lipid synthesis and fatty acid composition in Nannochloropsis sp. (Eustigmatophyceae) grown in a light-dark cycle. J Phycol 26:463–469

    Article  CAS  Google Scholar 

  • Swanson AK, Druehl LD (2002) Induction, exudation and the protective role of kelp phlorotannins. Aquat Bot 73:241–253

    Article  CAS  Google Scholar 

  • Targett NM, Arnold AM (1998) Predicting the effects of brown algal phlorotannins on marine herbivores in tropical and temperate oceans. J Phycol 34:195–205

    Article  CAS  Google Scholar 

  • Thompson GA Jr (1996) Lipids and membrane functions in green algae. Biochim Biophys Acta 1302:17–45

    PubMed  Google Scholar 

  • Van Alstyne KL, Ehlig JM, Whitman SL (2001) Differences in herbivore preferences, phlorotannin production, and nutritional quality between adult and juvenile tissues from marine brown algae. Mar Biol 139:201–210

    Article  Google Scholar 

  • Waterman PG, Mole S (1994) Analysis of phenolic plant metabolites. Blackwell Scientific, Oxford, pp 1–237

    Google Scholar 

  • Wiencke C, Roleda MY, Gruber A, Clayton MN, Bischof K (2006) Susceptibility of zoospores to UV radiation determines upper depth distribution limit of Arctic kelps: evidence through field experiments. J Ecol 94:455–463

    Article  Google Scholar 

Download references

Acknowledgments

The authors would like to express their gratitude to the two anonymous reviewers who helped to improve the manuscript substantially. We thank Max Schwanitz and the AWI diving group for collecting algae in Kongsfjorden, Dr. Riitta Koivikko for kind advice regarding phlorotannin extraction, Dr. Michael Y. Roleda and Sandra Heinrich for laboratory support and Dr. Bánk Beszteri for statistical help. This study was supported by the Bremen International Graduate School for Marine Sciences (GLOMAR) that is funded by the German Research Foundation (DFG) within the frame of the Excellence Initiative by the German federal and state governments to promote science and research at German universities, the Alfred-Wegener- Institute for Polar- and Marine Research, the University of Bremen, and the University of Gothenburg.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Franciska S. Steinhoff.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Steinhoff, F.S., Graeve, M., Wiencke, C. et al. Lipid content and fatty acid consumption in zoospores/developing gametophytes of Saccharina latissima (Laminariales, Phaeophyceae) as potential precursors for secondary metabolites as phlorotannins. Polar Biol 34, 1011–1018 (2011). https://doi.org/10.1007/s00300-011-0960-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00300-011-0960-y

Keywords

Navigation