Skip to main content
SpringerLink
Log in

Mechanisms of bioadhesion of macrophytic algae

  • Reviews
  • Published:
Russian Journal of Plant Physiology Aims and scope Submit manuscript

Abstract

During the evolution the benthic macrophytic algae developed effective mechanisms of bioadhesion enabling their attachment to almost any surface in the aqueous medium. The attachment of algal spores and zygotes includes two successive stages: the primary and the secondary (final) adhesion. Analysis of information on the composition of adhesive materials and attachment mechanisms in brown, green, and red marine macrophytes indicates that synthesis and release of adhesive substances by algal cells can be considered as a temporary intensification of cell wall synthesis. The structure of the primary adhesive material comprises a gel phase (alginate, ulvan, and agar gels) and a structuring component, i.e., a flexible network based on branched chains and/or rings of phenolic compounds, polysaccharides, or glycoproteins. Irreversible hardening of the primary adhesive material arises from phenol polymerization catalyzed by different peroxidases (brown algae) or from polymerization of glycoproteins comprising amino acids with phenolic residues (red algae). In parallel with these processes, covalent cross-links are being formed between the adhesive structural components and the gel phase polysaccharides. This results in the formation of the secondary adhesive and in eventual attachment of the organism to the substrate. The attachment mechanisms of benthic algae appear to have some features in common with the mechanisms of bioadhesion of marine invertebrates.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Vreeland, V., Waite, J.H., and Epstein, L., Polyphenols and oxidases in substratum adhesion by marine algae and mussels, J. Phycol., 1998, vol. 34, pp. 1–8.

    Article  CAS  Google Scholar 

  2. Fletcher, R.L. and Callow, M.E., The settlement, attachment and establishment of marine algal spores, British Phycol. J., 1992, vol. 27, pp. 303–329.

    Google Scholar 

  3. Apple, M.E. and Harlin, M.M., Inhibition of tetraspore adhesion in Champia parvula (Rhodophyta), Phycologia, 1995, vol. 34, pp. 417–423.

    Article  Google Scholar 

  4. Bitton, R., Ben-Yehuda, M., Davidovich, M., Balazs, Y., Potin, P., Delage, L., Colin, C., and Bianco-Peled, H., Structure of algal-born phenolic polymeric adhesives, Macromol. BioSci., 2006, vol. 6, pp. 737–746.

    Article  CAS  PubMed  Google Scholar 

  5. Higgins, M.J., Crawford, S.A., Mulvaney, P., and Wetherbee, R., Characterization of the adhesive mucilages secreted by live diatom cells using atomic force microscopy, Protist, 2002, vol. 153, pp. 25–38.

    Article  PubMed  Google Scholar 

  6. Knox, J.P., Cell adhesion, cell separation and plant morphogenesis, Plant J., 1992, vol. 2, pp. 137–141.

    Article  CAS  Google Scholar 

  7. Wojtaszek, P., Genes and plant cell walls: a difficult relationship, Biol. Rev., 2000, vol. 75, pp. 437–475.

    Article  CAS  PubMed  Google Scholar 

  8. Callow, J.A., Stanley, M.S., Wetherbee, R., and Callow, M.E., Cellular and molecular approaches to understanding primary adhesion in Enteromorpha: An overview, Biofouling, 2000, vol. 16, pp. 141–150.

    Article  CAS  Google Scholar 

  9. Potin, P. and Leblanc, C., Phenolic-based adhesives of marine brown algae, Biological Adhesives, Smith, A.M. and Callow, J.A., Eds., Berlin: Springer-Verlag, 2006, pp. 105–124.

    Chapter  Google Scholar 

  10. Gurvan, M., Tonon, T., Scornet, D., Cock, J.M., and Kloareg, B., The cell wall polysaccharide metabolism of the brown alga Ectocarpus siliculosus. Insights into the evolution of extracellular matrix polysaccharides in eukaryotes, New Phytol., 2010, vol. 188, pp. 82–97.

    Article  Google Scholar 

  11. Sharova, E.I., Kletochnaya stenka rastenii (Plant Cell Wall), St. Petersburg: St. Petersburg Gos. Univ., 2004.

    Google Scholar 

  12. Popper, Z.A., Michel, G., Hervé, C., Domozych, D.S., Willats, W.G.T., Tuohy, M.G., Kloareg, B., and Stengel, D.B., Evolution and diversity of plant cell walls: from algae to flowering plants, Annu. Rev. Plant Biol., 2011, vol. 62, pp. 567–590.

    Article  CAS  PubMed  Google Scholar 

  13. Vreeland, V., Grotkopp, E., Espinosa, S., Quiroz, D., Laetsch, W.M., and West, J., The pattern of cell wall adhesive formation by Fucus zygotes, Hydrobiologia, 1993, vol. 260/261, pp. 485–491.

    Article  Google Scholar 

  14. Quatrano, R.S. and Stevens, P.T., Cell wall assembly in Fucus zygotes: 1. Characterization of the polysaccharide components, Plant Physiol., 1976, vol. 58, pp. 224–231.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  15. Schoenwaelder, M.E.A. and Clayton, M.N., Secretion of phenolic substances into the zygote wall and cell plate in embryos of Hormosira and Acrocarpia (Fucales, Phaeophyceae), J. Phycol., 1998, vol. 34, pp. 969–980.

    Article  CAS  Google Scholar 

  16. Bisgrove, S.R. and Kropf, D.L., Cell wall deposition during morphogenesis in fucoid algae, Planta, 2001, vol. 212, pp. 648–658.

    Article  CAS  PubMed  Google Scholar 

  17. Rinaudo, M., Seaweed polysaccharides, Comprehensive Glycoscience. From Chemistry to Systems Biology, vol. 2, Kamerling, J.P., Ed., New York: Elsevier, 2007, pp. 691–735.

    Google Scholar 

  18. Usov, A.I. and Bilan, M.I., Fucoidans sulfated polysaccharides in brown algae, Usp. Khim., 2009, vol. 78, pp. 846–862.

    Article  Google Scholar 

  19. Vishchuk, O., Tarbeeva, D., Ermakova, S., and Zvyagintseva, T., Structural characteristics and biological activity of fucoidans from brown algae Alaria sp. and Saccharina japonica of different reproductive status, Chem. Biodiversity, 2012, vol. 9, pp. 817–828.

    Article  CAS  Google Scholar 

  20. Tsekos, I., The sites of cellulose synthesis in algae: diversity and evolution of cellulose-synthesizing enzyme complexes, J. Phycol., 1999, vol. 35, pp. 635–655.

    Article  CAS  Google Scholar 

  21. Hallmann, A., The pherophorins: common, versatile building blocks in the evolution of extracellular matrix architecture in Volvocales, Plant J., 2006, vol. 45, pp. 292–307.

    Article  CAS  PubMed  Google Scholar 

  22. Lahaye, M. and Robic, A., Structure and functional properties of ulvan, a polysaccharide from green seaweeds, Biomacromolecules, 2007, vol. 8, pp. 1765–1774.

    Article  CAS  PubMed  Google Scholar 

  23. Domozych, D.S., Sørensen, I., and Willats, W.G.T., The distribution of cell wall polymers during antheridium development and spermatogenesis in the charophycean green alga, Chara coralline, Ann. Bot., 2009, vol. 104, pp. 1045–1056.

    Article  CAS  Google Scholar 

  24. Sørensen, I., Pettolino, F.A., Bacic, A., Ralph, J., Lu, F., O’Neill, M.A., Fei, Z., Rose, J.K., Domozych, D.S., and Willats, W.G., The charophycean green algae provide insights into the early origins of plant cell walls, Plant J., 2011, vol. 68, pp. 201–211.

    Article  PubMed  Google Scholar 

  25. Kloareg, B. and Quatrano, R.S., Structure of the cell walls of marine algae and ecophysiological functions of the matrix polysaccharides, Oceanogr. Mar. Biol. Annu. Rev., 1988, vol. 26, pp. 259–315.

    Google Scholar 

  26. Tsekos, I., The supramolecular organization of red algal cell membranes and their participation in the biosynthesis and secretion of extracellular polysaccharides: a review, Protoplasma, 1996, vol. 193, pp. 10–32.

    Article  CAS  Google Scholar 

  27. Lechat, H., Amat, M., Mazoyer, J., Buleon, A., and Lahaye, M., Structure and distribution of glucomannan and sulfated glucan in the cell walls of the red alga Kappaphycus alvarezii (Gigartinales, Rhodophyta), J. Phycol., 2000, vol. 36, pp. 891–902.

    Article  CAS  Google Scholar 

  28. Usov, A.I., Problems and achievements of the structural analysis of sulfated polysaccharides of red algae, Khimiya Rastit. Syr’ya, 2001, no. 2, pp. 7–20.

    Google Scholar 

  29. Martone, P.T., Estevez, J.M., Lu, F., Ruel, K., Denny, M.W., Somerville, C., and Ralph, J., Discovery of lignin in seaweed reveals convergent evolution of cell-wall architecture, Curr. Biol., 2009, vol. 19, pp. 169–175.

    Article  CAS  PubMed  Google Scholar 

  30. Domozych, D.S., Algal Cell Walls, Publ. Online: 15 Sept. 2011, doi 10.1002/9780470015902.a0000315.pub3

    Google Scholar 

  31. Quatrano, R.S., Developmental biology: development in marine organisms, Experimental Marine Biology, Mariscal, R.N., Ed., New York: Academic, 1974, pp. 303–346.

    Google Scholar 

  32. Hable, W.E. and Kropf, D.L., Roles of secretion and cytoskeleton in cell adhesion and polarity establishment in Pelvetia compressa zygotes, Dev. Biol., 1998, vol. 198, pp. 45–65.

    CAS  PubMed  Google Scholar 

  33. Kropf, D.L., Bisgrove, S.R., and Hable, W.E., Establishing a growth axis in fucoid algae, Trends Plant Sci., 1999, vol. 4, pp. 490–494.

    Article  PubMed  Google Scholar 

  34. Tarakhovskaya, E.R., Maslov, Yu.I., and Railkin, A.I., Effect of hydrodynamic conditions and some physiologically active substances on growth and attachment of Fucus vesiculosus L. and Fucus edentatus De la Pyl. (Phaeophyta) embryos to the substrate, Tez. dokl. XI nauch. sessii Morskoi biologicheskoi stantsii SPbGU (Abst. XI Scientific Session of the Marine Biological Station, St. Petersburg Gos. Univ.), St. Petersburg: St. Petersburg Gos. Univ., 2010, pp. 54–56.

    Google Scholar 

  35. Bitton, R., Berglin, M., Elwing, H., Colin, C., Delage, L., Potin, P., and Bianco-Peled, H., The influence of halide-mediated oxidation on algae-born adhesives, Macromol. BioSci., 2007, vol. 7, pp. 1280–1289.

    Article  CAS  PubMed  Google Scholar 

  36. Ragan, M.A. and Glombitza, K.W., Phlorotannins, brown algal polyphenols, Prog. Phycol. Res, 1986, vol. 4, pp. 129–241.

    CAS  Google Scholar 

  37. Mehrtens, G., Haloperoxidase activities in arctic macroalgae, Polar Biol., 1994, vol. 14, pp. 351–354.

    Article  Google Scholar 

  38. Butler, A. and Walker, J.V., Marine haloperoxidases, Chem. Rev., 1998, vol. 93, pp. 1937–1944.

    Article  Google Scholar 

  39. Van Schijndel, J.W.P.M., Vollenbroek, E.G.M., and Wever, R., The chloroperoxidase from the fungus Curvularia inaequalis: a novel vanadium enzyme, Biochim. Biophys. Acta, 1993, vol. 1161, pp. 249–256.

    Article  PubMed  Google Scholar 

  40. Wever, R., Structure and function of vanadium haloperoxidases, Vanadium: Biochemical and Molecular Biological Approaches, Michibata, H., Ed., Dordrecht: Springer-Verlag, 2012, pp. 95–125.

    Chapter  Google Scholar 

  41. Eickhoff, H., Jung, G., and Rieker, A., Oxidative phenol coupling tyrosine dimers and libraries containing tyrosyl peptide dimers, Tetrahedron, 2001, vol. 57, pp. 353–364.

    Article  CAS  Google Scholar 

  42. Colin, C., Leblanc, C., Wagner, E., Delage, L., Leize-Wagner, E., van Dorsselaer, A., Kloareg, B., and Potin, P., The brown algal kelp Laminaria digitata features distinct bromoperoxidase and iodoperoxidase activities, J. Biol. Chem., 2003, vol. 278, pp. 23545–23552.

    Article  CAS  PubMed  Google Scholar 

  43. Berglin, M., Delage, L., Potin, P., Vilter, H., and Elwing, H., Enzymatic cross-linking of a phenolic polymer extracted from the marine alga Fucus serratus, Biomacromolecules, 2004, vol. 5, pp. 2376–2383.

    Article  CAS  PubMed  Google Scholar 

  44. Callow, J.A. and Callow, M.E., The Ulva spore adhesive system, Biological Adhesives, Smith, A.M. and Callow, J.A., Eds., Berlin: Springer-Verlag, 2006, pp. 63–78.

    Chapter  Google Scholar 

  45. Haug, A., The influence of borate and calcium on the gel formation of a sulfated polysaccharide from Ulva lactuca, Acta Chem. Scand., 1976, vol. 30, pp. 562–566.

    Article  CAS  Google Scholar 

  46. Stanley, M.S., Callow, M.E., and Callow, J.A., Monoclonal antibodies to adhesive cell coat glycoproteins secreted by zoospores of the green alga Enteromorpha, Planta, 1999, vol. 210, pp. 61–71.

    Article  CAS  PubMed  Google Scholar 

  47. Kieslisewski, M.J. and Lamport, D.T.A., Extensin: repetitive motifs, functional sites, posttranslational codes and phylogeny, Plant J., 1994, vol. 5, pp. 157–172.

    Article  Google Scholar 

  48. Pettitt, M.E., Henry, S.L., Callow, M.E., Callow, J.A., and Clare, A.S., Activity of commercial enzymes on settlement and adhesion of cypris larvae of the barnacle Balanus amphitrite, spores of the green alga Ulva linza, and the diatom Navicula perminuta, Biofouling, 2004, vol. 20, pp. 299–311.

    Article  CAS  PubMed  Google Scholar 

  49. Humphrey, A.J., Finlay, J.A., Pettitt, M.E., Stanley, M.S., and Callow, J.A., Effect of Ellman’s reagent and dithiothreitol on the curing of the spore adhesive glycoprotein of the green alga Ulva, J. Adhesion, 2005, vol. 81, pp. 791–803.

    Article  CAS  Google Scholar 

  50. Chamberlain, A.H.L. and Evans, L.V., Aspects of spore production in the red alga Ceramium, Protoplasma, 1973, vol. 76, pp. 139–159.

    Article  Google Scholar 

  51. Bouzon, Z.L., Ouriques, L.C., and Oliveira, E.C., Spore adhesion and cell wall formation in Gelidium floridanum (Rhodophyta, Gelidiales), J. Appl. Phycol., 2006, vol. 18, pp. 287–294.

    Article  Google Scholar 

  52. Ouriques, L.C., Schmidt, E.C., and Bouzon, Z.L., The mechanism of adhesion and germination in the carpospores of Porphyra spiralis var. amplifolia (Rhodophyta, Bangiales), Micron, 2012, vol. 43, pp. 269–277.

    Article  CAS  PubMed  Google Scholar 

  53. Tsekos, I., Growth and differentiation of the Golgi apparatus and wall formation during carposporogenesis in the red alga, Gigartina teedii (Roth.) Lamour., J. Cell Sci., 1981, vol. 52, pp. 71–84.

    CAS  PubMed  Google Scholar 

  54. Railkin, A.I., Kolonizatsiya tverdykh tel bentosnymi organizmami (Colonization of Solids by Benthic Organisms), St. Petersburg: St. Petersburg Gos. Univ., 2008.

    Google Scholar 

  55. Bitton, R. and Bianco-Peled, H., Novel biometric adhesives based on algae glue, Macromol. BioSci., 2008, vol. 8, pp. 393–400.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Plant Physiology and Biochemistry, Faculty of Biology and Soil Science, St. Petersburg State University, Universitetskaya nab. 7/9, St. Petersburg, 199034, Russia

    E. R. Tarakhovskaya

Authors
  1. E. R. Tarakhovskaya
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. R. Tarakhovskaya.

Additional information

Original Russian Text © E.R. Tarakhovskaya, 2014, published in Fiziologiya Rastenii, 2014, Vol. 61, No. 1, pp. 23–30.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tarakhovskaya, E.R. Mechanisms of bioadhesion of macrophytic algae. Russ J Plant Physiol 61, 19–25 (2014). https://doi.org/10.1134/S1021443714010154

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1021443714010154

Keywords

Search

Navigation