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A New Assay for Quantifying Brown Algal Phlorotannins and Comparisons to Previous Methods

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A New Assay for Quantifying Brown Algal Phlorotannins and Comparisons to Previous Methods Journal of Chemical Ecology, Vol. 22, No. 7, 1996 A NEW ASSAY FOR QUANTIFYING BROWN ALGAL PHLOROTANNINS AND COMPARISONS TO PREVIOUS METHODS J. LEWIS STERN, I'* ANN E. HAGERMAN, 2 PETER D. STEINBERG, I FRANK C. WINTER, 3 and JAMES A. ESTES 4 ~School of Biological Science, University of New South Wales Sydney, N.S. W. 2052 Australia ZDepartment of Chemistry, Miami University Oxford, Ohio 45056 ~University of Auckland, l_x,igh Marine Laboratories RD5 Warkworth, New Zealand 4National Biological Survey, University of California Santa Cruz, California 95064 (Received May 30, 1995; accepted March 4, 1996) Abstract--Quantitative measurement of phlorotannins (polyphenolics) in brown algae (Phaeophyta) by colorimetric assays can be confounded because: (1) most such assays also react to nonphlorotannin substances (interferences) and (2) the appropriate reference compound for such assays is not always clear, although phloroglucinol is typically used. We developed a new assay in which 2,4-dimethoxybenzaldehyde (DMBA) reacts specifically with 1,3- and 1,3,5-substituted phenols (e.g., phlorotannins) to form a colored product, This new assay, as well as eliminating the problem of measuring interferences, is inexpensive, rapid, and can be used with small sample volumes. We rec- ommend it for all assays of phlorotannins from one or a set of closely related species where the structural types of phlorotannins present are likely to be similar among samples. It is also appropriate for broader surveys of phloro- tannin levels across many species, but in this case a reference must be chosen with care. We also compared the DMBA assay to existing assays, including the Folin-Denis Iboth before and after the samples were mixed with poly- vinylpolypyrrolidone (PVPP)] and the Prussian blue assays. PVPP was not 100% efficient (and often much less) at removing phlorotannins from solution, and its effectiveness varied among different phlorotannins. Thus, in contrast to previous studies, measuring phenolic levels in extracts before and after *To whom correspondence should be addressed. 1273 (g}98-0331/96/0700 1273509.50/0 rc~ 1996 Plenum Publishing Coz3~oration 1274 J.L. STERN ET AL. treatment with PVPP will not necessarilyresult in an interference-freemeasure of phlorotannins. Based on an analysis of reactive substances in red and green algae (which do not contain phlorotannins) in the Folin-Denis and Prussian blue assays, we estimate that the average level of interferences (nonphloro- tannins) in brown algae measured in these two assays is on the order of 0.5 % by dry weight. Key Words--Phlomtannins, DMBA, Folin-Denis assay, brown algae, sea- weeds, phenolics, PVPP. INTRODUCTION Polyphenolics are one of the most common classes of secondary metabolites in terrestrial plants (Harborne, 1991; Haslam, 1989; Swain, 1979), marine angio- sperms (McMillan, 1984), and macroalgae (Ragan and Glombitza, 1986; Stein- berg and van Altena, 1992). They are ecologically important in both terrestrial and marine systems, deterring or inhibiting herbivores, epiphytes, pathogens, or competitors (e.g., allelopathy) (Beress et al., 1993; Bernays et al., 1989; Hay and Fenical, 1988). In particular, there is a substantial empirical and the- oretical literature on the effects of polyphenolics against herbivores (Coley et al., 1985; Feeny, 1976; Steinberg, 1992; Swain, 1979). Polyphenolics can also significantly affect broad-scale ecosystem properties in both terrestrial (Schles- inger, 1991) and marine (Carlson and Mayer, 1983) systems. Although terrestrial and marine plant polyphenolics are similar in some respects, there are some fundamental differences among the compounds. Ter- restrial polyphenolics, or tannins, are polymers based on flavonoids or gallic acid (Haslam, 1989). Algal polyphenolics, or "phlorotannins" (Ragan and Glombitza 1986), which are only known from the brown algae (Phaeophyta), are restricted to polymers of phloroglucinol (1,3,5-trihydroxybenzene). Phlo- rotannins and terrestrial tannins vary in their linkages between monomeric units, in their size (dimers to 600,000 amu), and to some extent in the types of substitutions present (i.e., halogenation, sulfated groups) (Ragan and Glombitza, 1986). While the abundance and ecological importance of polyphenolics in natural systems has long been recognized, the ability to quantitatively measure these compounds in plant tissue remains a complex issue (Mole and Waterman, 1987a,b; Ragan and Glombitza, 1986; Ragan and Jensen, 1977; Van Alstyne, 1995). Because the compounds are typically large, polar, and water soluble, they are difficult to measure by the standard analytical techniques used to analyze smaller nonpolar metabolites such as terpenes and acetogenins. Analysis of algal polyphenolics is further complicated by the difficulty of separating the individual compounds from the polymeric mixtures which occur naturally in vivo. Consequently, polyphenolics have typically been analyzed in one of two QUANTIFYING BROWN ALGAL PHLOROTANNINS 1275 ways. The first is via various spectrophotometric procedures based on the reac- tion of a colored reagent with the easily oxidized phenolic functional group. The best known of these procedures is the Folin-Denis test, or variations thereof, such as the micro-Folin Denis (Arnold et al., 1995; Targett et al., 1995; Van Alstyne, 1995) or Folin-Ciocalteau (1927) tests. This assay and its variations have been used extensively in the analysis of phenolics from both marine and terrestrial plants (Ragan and Jensen, 1977; Mole and Waterman, 1987a,b; Stein- berg, 1989). The second set of methods uses the ability of polyphenolics to bind to macromolecules such as proteins, thus generating a measure of "relative tanning ability" (Hagerman and Butler, 1989). Such techniques have been very useful, but they are subject to a number of sources of error, of which two are perhaps the most significant for phloro- tannins (Ragan and Glombitza, 1986; Steinberg, 1989; Van AIstyne, 1995). Firstly, because specific molecules are not analyzed, but rather total phenols or tanning ability, variation in the reactivity of structurally different polyphenolics (due to variation in size, structure, etc.) is not separable from variation in reactivity due to different amounts of compounds. Secondly, nonpolyphenolic interferences can react with the reagents used in some colorimetric assays, result- ing in an overestimate of phenolic levels. In this paper we compared three spectrophotometric assays in an attempt to assess the variation in the three assays resulting from different types of phlo- rotannins from marine brown algae and to determine the effect of interferences in these assays. We compared the Folin-Denis technique, used with and without polyvinylpolypyrrolidone (PVPP), a resin which binds to, and removes poly- phenols in solution; the Prussian blue assay, which has been suggested to be less sensitive than the Folin-Denis assay to interfering compounds; and a new assay, which is based on the ability of 2,4-dimethoxybenzaldehyde (DMBA) to react specifically with 1,3- and 1,3,5-substituted phenols (i.e., phlorotannins), and which does not react with tannic acid containing only ortho- and parahy- droxyl-substituted phenolics). We compared the color yield of these three tech- niques for both purified phlorotannin fractions and crude extracts from a number of brown algae. The effect of interferences on the measurement of phlorotannins was examined by measuring phenolic levels in our extracts before and after the addition of PVPP and by measuring the reactivity of extracts from red and green algae, which lack phlorotannins. METHODS AND MATERIALS Chemical Assays Phenolic levels in crude extracts of brown algae and in "purified" phlo- rotannin fractions (see Preparation of Pure Phlorotannin Fractions, below) were 1276 J.L. STERN ET AL. quantified by three methods. The first, the Folin-Denis procedure for measuring total phenolic content (Ragan and Jensen, 1977; Swain and Hillis, 1959), has been used extensively for measuring phlorotannins in brown algae (Ragan and Glombitza, 1986; Steinberg, 1989; Targett et al., 1992; Van Alstyne, 1995). The second, the Prussian blue assay (Price and Butler, 1977), is also well described in the literature but has not been used as extensively as the Folin- Denis procedure. Our new technique, the DMBA assay, is based on the vanillin- H2SO4 reaction (Butler, 1982; Butler et al., 1982; Putnam and Butler, 1985). Folin-Denis Assay. Folin-Denis reagent was prepared by dissolving 25 g of sodium tungstate (Na2WO4"2HeO) and 5 g of dodecamolybdophosphoric acid (12MoO3.H3PO4-H20) in 175 ml distilled water, adding 12.5 ml phosphoric acid to the solution, boiling under reflux for 2 hr, and then making up to 250.0 ml. The sample (1.0 ml) was mixed with 4.0 ml of this reagent and 8.0 ml of a saturated sodium carbonate solution and then made up to a reaction volume of 25.0 ml with distilled water. Color was allowed to develop for 5-6 hr, which allowed the precipitate that formed to settle before the absorbance was read at 725 nm. Prussian Blue Assay. Samples were comprised of 100 /xl of extract or diluted extract in 50.0 ml of distilled water in a 125 ml flask. Three milliliters of ferric ammonium sulfate (0.1 M FeNH4(SO4)2 in 0.1 M HC1) was then added to successive samples at intervals of 1.0 minute. Exactly 20 min after the addi- tion of ferric ammonium sulfate to each sample, 3.0 ml of potassium ferricyanide [0.008 M K3Fe(CN)6] was added. Exactly 20 min after the addition of potassium ferricyanide, the absorbance at 720 nm was read. Solvent-only blanks were included and subtracted from sample absorbances. Like Folin-Denis, Prussian blue reacts with reducing compounds such as phenols, but the phenolic group is not directly incorporated into the colored product. DMBA Assay. Stock solutions of 2,4-dimethoxybenzaldehyde (2 g/100 ml solution) (Sigma D-3269) and of hydrochloric acid (16.0 ml concentrated hydro- chloric acid per 100.0 ml solution) were prepared in glacial acetic acid. The working reagent, prepared by mixing equal volumes of these two solutions just prior to use, was kept at room temperature before starting the assay.
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