Journal of Chemical Ecology

, Volume 22, Issue 10, pp 1877–1899

Phlorotannin-protein interactions

  • J. Lewis Stern
  • Ann E. Hagerman
  • Peter D. Steinberg
  • Pamela K. Mason
Article

Abstract

Tannins are one of the most broadly distributed types of plant secondary compounds, and have been the focal point for many studies of plant/herbivore interactions. Tannins interact strongly with proteins, so that the fate and effects of ingested tannins are in part dependent on the mode of interaction of the tannin with dietary and endogenous proteins in an herbivore's gut. We investigated the factors affecting the precipitation of proteins by phlorotannins from three species of marine brown algae:Carpophyllum maschalocarpum, Ecklonia radiata, andLobophora variegata. Phlorotannins were precipitated by proteins in a pH-dependent and concentration-dependent fashion. Precipitation also varied as a function of the presence of reducing agent, the type of phlorotannin or protein used, and the presence of organic solvents such as hydrogen bond inhibitors. Of particular significance was the ability of some phlorotannins to oxidize and form covalent bonds with some proteins. In contrast, under similar experimental conditions three types of terrestrial tannins (procyanidins, profisetinidins, and gallotannins) apparently did not form covalent complexes with proteins. Our results suggest several ways in which the biological activity of phlorotannins may vary as a function of the properties of the gut environment of marine herbivores. Moreover, we identify specific structural characteristics of phlorotannins which affect their tendency to oxidize, and thus, their potential effects on marine herbivores.

Key Words

Tannin-protein interaction tannins hydrogen bonding protein precipitation marine brown algae phlorotannins Carpophyllum maschalocarpum Ecklonia radiata Lobophora variegata 

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References

  1. Appel, H. M. 1993. Phenolics in ecological interactions: The importance of oxidation.J. Chem. Ecol. 19:1521–1552.Google Scholar
  2. Asquith, T. N., andButler, L. G. 1985. Use of dye-labeled protein as spectrophotometric assay for protein precipitants such as tannin.J. Chem. Ecol. 11:1535–1544.Google Scholar
  3. Bernays, E. A., Chamberlain, D., andMcCarthy, P. 1980. The differential effects of ingested tannic acid on different species of Acridoidea.Ent. Exp. Appl. 28:158–166.Google Scholar
  4. Bernays, E. A., Cooper-Driver, G., andBilgener, M. 1989. Herbivores and plant tannins.Adv. Ecol. Res. 19:263–302.Google Scholar
  5. Boettcher, A. A., andTargett, N. M. 1993. Role of polyphenolic molecular size in reduction of assimilation efficiency inXiphister mucosus.Ecology 74:891–903.Google Scholar
  6. Clausen, T. P., Provenza, F. D., Burritt, E. A., Reichardt, P. B., andBryant, J. P. 1990. Ecological implication of condensed tannin structure: A case study.J. Chem. Ecol. 16:2381–2392.Google Scholar
  7. Felton, G. W., Donato, K. K., Broadway, R. M., andDuffey, S. S. 1992. Impact of oxidized plant phenolics on the nutritional quality of dietary protein to a Noctuid herbivoreSpodoptera exigua.J. Insect Physiol. 38:277–285.Google Scholar
  8. Glombitza, K. W., andLi, S. M. 1991a. Hydroxyphlorethols from the brown algaCarpophyllum maschalocarpum.Phytochemistry 30:2741–2745.Google Scholar
  9. Glombitza, K. W., andLi, S. M. 1991b. Fucophlorethols from the brown algaCarpophyllum maschalocarpum.Phytochemistry 30:3423–3427.Google Scholar
  10. Hagerman, A. E. 1992. Tannin-protein interactions, pp. 236–247,in C. T. Ho, C. Y. Lee, and M. T. Huang (eds.). Phenolic Compounds in Food and Their Effects on Health I. Analysis, Occurrence, and Chemistry. ACS Symposium Series 506. American Chemical Society, Washington, DC.Google Scholar
  11. Hagerman, A. E., andButler, L. G. 1978. Protein precipitation method for the quantitative determination of tannins.J. Agric. Food Chem. 26:809–812.Google Scholar
  12. Hagerman, A. E., andButler, L. G. 1980a. Determination of protein in tannin-protein precipitates.J. Agric. Food Chem. 28:944–947.PubMedGoogle Scholar
  13. Hagerman, A. E., andButler, L. G. 1980b. Condensed tannin purification and characterization of tannin-associated proteins.J. Agric. Food Chem. 28:947–952.PubMedGoogle Scholar
  14. Hagerman, A. E., andButler, L. G. 1981. Specificity of proanthocyanidin-protein interactions.J. Biol. Chem. 256:4494–4497.PubMedGoogle Scholar
  15. Hagerman, A. E., andKlucher, K. M. 1996. Tannin-protein interactions, pp. 67–76,in V. Cody, E. Middleton, and J. Harborne (eds.). Plant Flavonoids in Biology and Medicine: Biochemical, Pharmacological and Structure Activity Relationships. Alan R. Liss, Inc., New York, New York.Google Scholar
  16. Hagerman, A. E., andRobbins, C. T. 1987. Implications of soluble tannin-protein complexes for tannin analysis and plant defense mechanisms.J. Chem. Ecol. 13:1243–1259.Google Scholar
  17. Hagerman, A. E., andRobbins, C. T. 1993. Specificity of tannin-binding salivary proteins relative to diet selection by mammals.Can. J. Zool. 71:628–633.Google Scholar
  18. Harborne, J. B. 1991. The chemical basis of plant defense, pp. 45–60,in R. T. Palo and C. T. Robbins (eds.). Plant Defenses against Mammalian Herbivory. CRC Press, Boca Raton, Florida.Google Scholar
  19. Haslam, E. 1989.Plant Polyphenols. Vegetable Tannins Revisited. Cambridge, U.K.: Cambridge University Press.Google Scholar
  20. Horn, M. H. 1989. Biology of marine herbivorous fishes.Oceanography and Marine Biology Annual Review 27:167–272.Google Scholar
  21. Kennedy, R. M. 1990. Hydrophobic chromatography.Method. Enzymol. 182:339–343.Google Scholar
  22. Leatham, G. F., King, V., andStahmann, M. A. 1980. In vitro protein polymerization by quinones or free radicals generated by plant or fungal oxidative enzymes.Phytopathology 70:1134–1140.Google Scholar
  23. Li, S. M., andGlombitza, K. W. 1991. Carmalols and phlorethofuhalols from the brown algaCarpophyllum maschalocarpum.Phytochemistry 30:3417–3421.Google Scholar
  24. Mahler, H. R., andCordes, E. H. 1971. Biological Chemistry. Harper and Row, New York, New York.Google Scholar
  25. Malamud, D., andDrysdale, J. W. 1978. Isoelectric point of proteins: A table.Anal. Biochem. 86:620–647.PubMedGoogle Scholar
  26. Martin, J. S., andMartin, M. M. 1983. Tannin assays in ecological studies. Precipitation or ribulose-1,5-bisphosphate carboxylase/oxygenase by tannic acid, quebracho, and oak leaf foliage extracts.J. Chem. Ecol. 9:285–294.Google Scholar
  27. Martin, M. M., andMartin, J. S. 1984. Surfactants: Their role in preventing the precipitation of proteins by tannins in insect guts.Oecologia (Berlin) 61:342–345.Google Scholar
  28. McArthur, C., Hagerman, A. E., andRobbins, C. T. 1991. Physiological strategies of mammalian herbivores against plant defenses, pp. 103–114,in R. T. Palo and C. T. Robbins (eds.). Plant Defenses Against Mammalian Herbivory. CRC Press, Boca Raton, Florida.Google Scholar
  29. Meites, L., andZuman, P. 1974 Electrochemical Data. John Wiley & Sons, New York, New York.Google Scholar
  30. Paech, C. 1985. The major protein of chloroplast stroma, ribulosebisphosphate carboxylase. pp. 199–230,in H. F. Linskens and J. F. Jackson (eds.). Modern Methods of Plant Analysis New Series Volume I. Cell Components. Springer-Verlag, Berlin.Google Scholar
  31. Peters Jr., T. 1975. Serum albumin, pp. 133–181,in F. W. Putnam (ed.). The Plasma Proteins, Academic Press, New York, New York.Google Scholar
  32. Pierpoint, W. S. 1969a. O-quinones formed in plant extracts.Biochem. J. 112:609–618.PubMedGoogle Scholar
  33. Pierpoint, W. S. 1969b. O-quinones formed in plant extracts. Their reactions with bovine serum albumin.Biochem. J. 112:619–629.PubMedGoogle Scholar
  34. Ragan, M. A., andGlombitza, K. 1986. Phlorotannins, brown algal polyphenols.Prog. Phycol. Res. 4:177–241.Google Scholar
  35. Robbins, C. T., Hanley, T. A., Hagerman, A. E., Hjeljord, O., Baker, D. L., Schwartz, C. C., andMautz, W. W. 1987. Role of tannins in defending plants against ruminants: Reduction in protein availability.Ecology 68:98–107.Google Scholar
  36. Ronlan, A. 1978. Phenols, pp. 242–275,in A. J. Bard and H. Lund (eds.). Encyclopedia of Electrochemistry of the Elements. Marcel Dekker Inc., New York, New York.Google Scholar
  37. Steinberg, P. D. 1988. The effects of quantitative and qualitative variation in phenolic compounds on feeding in three species of marine invertebrate herbivores.J. Exp. Marine Biol. Ecol. 120:221–237.Google Scholar
  38. Steinberg, P. D. 1993. Geographical variation in the interaction between marine herbivores and brown algal secondary metabolites, pp. 51–92,in V. J. Paul (ed.). Ecological Roles for Marine Secondary Metabolites. Comstock Publishing, Ithaca, New York.Google Scholar
  39. Steinberg, P. D., andVan Altena, I. A. 1992. Tolerance of Australasian marine herbivores to brown algal phlorotannins in temperate Australasia.Ecol. Mono. 62:189–222.Google Scholar
  40. Steinberg, P. D., Estes, J. A., andWinter, F. C. 1995. Trophic cascades in kelp communities.Proc. Nat. Acad. Sci. (USA), in press.Google Scholar
  41. Stern, J. L., Hagerman, A. E., Steinberg, P. D., Winter, F. C., andEstes, J. A. 1996 A new assay for quantifying brown algal phlorotannins and comparisons to previous methods.J. Chem. Ecol. in press.Google Scholar
  42. Suatoni, J. C., Snyder, R. E., andClark, R. O. 1961. Voltammetric studies of phenol and aniline ring substitution.Anal. Chem. 33:1894–1897.Google Scholar
  43. Sugiyama, T., Nakayama, N., Ogawa, M., andAkazawa, T. 1968. Structure and function of chloroplast proteins. II. Effect of p-chloromercuribenzoate treatment on the ribulose 1,5-diphosphate carboxylase activity of spinach leaf fraction I protein.Arch. Biochem. Biophy. 125:98–106.Google Scholar
  44. Tugwell, S., andBranch, G. M. 1992. Effects of herbivore gut surfactants on kelp polyphenol defenses.Ecology 73:205–215.Google Scholar
  45. Van Alsytne, K. L., andPaul, V. J. 1990. The evolution and biogeography of antiherbivore compounds in marine macroalgae: Why don't tropical brown algae use temperate defenses against herbivorous fishes?Oecologia (Berlin) 84:158–163.Google Scholar
  46. Van Altena, I. A., andSteinberg, P. D. 1992. Are differences in the responses between North American and Australasian marine herbivores to phlorotannins due to differences in phlorotannin structure?Biochem. Syst. Ecol. 20:493–499.Google Scholar
  47. Zucker, W. V. 1983. Tannins: Does structure determine function? An ecological perspective.Am. Nat. 121:335–365.Google Scholar

Copyright information

© Plenum Publishing Corporation 1996

Authors and Affiliations

  • J. Lewis Stern
    • 1
  • Ann E. Hagerman
    • 2
  • Peter D. Steinberg
    • 3
  • Pamela K. Mason
    • 4
  1. 1.Department of BiologyUniversity of New South WalesKensingtonAustralia
  2. 2.Department of ChemistryMiami UniversityOxford
  3. 3.Department of BiologyUniversity of New South WalesKensingtonAustralia
  4. 4.Department of ChemistryMiami UniversityOxford

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