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Characterization of Polyphenolic Content in the Aquatic Plants Ruppia Cirrhosa and Ruppia Maritima —A Source of Nutritional Natural Products

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Characterization of Polyphenolic Content in the Aquatic Plants Ruppia Cirrhosa and Ruppia Maritima —A Source of Nutritional Natural Products molecules Article Characterization of Polyphenolic Content in the Aquatic Plants Ruppia cirrhosa and Ruppia maritima —A Source of Nutritional Natural Products Kjersti Hasle Enerstvedt 1, Anders Lundberg 2 and Monica Jordheim 1,* ID 1 Department of Chemistry, University of Bergen, Allégt. 41, N-5007 Bergen, Norway; [email protected] 2 Department of Geography, University of Bergen, Fosswinckelsft. 6, N-5020 Bergen, Norway; [email protected] * Correspondence: [email protected]; Tel.: +47-55-58-35-48 Received: 10 November 2017; Accepted: 20 December 2017; Published: 22 December 2017 Abstract: Herein, the polyphenolic content in extracts of Ruppia cirrhosa (Petagna) Grande and Ruppia maritima L.was fully characterized for the first time. High amounts of the main compound chicoric acid (CA)(≤30.2 ± 4.3 mg/g) were found in both Ruppia species. In addition, eight flavonoids, namely the 3-O-glucopyranosides and 3-O-galactopyranosides, as well as malonylated 3-O-glycosides of quercetin and isorhamnetin, were isolated and identified. The antioxidant activity of Ruppia cirrhosa extracts and isolated compounds was investigated spectrophotometrically by a 1,1-diphenyl-2-picrylhydrazyl (DPPH·) radical scavenging assay. IC50 values were 31.8–175.7 µg/mL for Ruppia cirrhosa extracts and 12.1–88.4 µg/mL for isolated flavonoids. Both individual and total phenolic and flavonoid content were quantified in crude extracts using analytical HPLC. The relative high amount of total flavonoids ranged from 5.9 to 14.7 mg/g in both species, with concentrations of individual flavonoids ranging from 0.4 to 2.9 mg/g dry weight. The content of chicoric acid was twofold more in Ruppia maritima than in Ruppia cirrhosa. Seasonal variation of the quantitative content in Ruppia cirrhosa was examined. Total flavonoid content ranged from 8.4 mg/g in October to 14.7 mg/g in August, whereas the highest concentration of chicoric acid was observed in March (29.2 mg/g). Keywords: Ruppiaceae; chicoric acid; flavonoids; NMR characterization; quantification; antioxidant assay 1. Introduction The marine environment is a potential source for a wide variety of nutritional natural products. Seaweeds are used as human food or as raw materials for the production of compounds of nutritional interest [1]. On the other hand, marine angiosperms, such as seagrasses, are known for their content of secondary metabolites [2,3]; however, these are very little exploited to find commercially valuable natural products. A few seagrass species, especially of the genus Zostera, Halophila, Posidonia, Thalassia and Syringodium, have been investigated for their content of phenolics and flavonoids [3–13]. The widgeon grass family (Ruppiaceae) is a submersed aquatic angiosperm widely distributed in temperate and tropical regions all over the world. Ruppia species usually occur in brackish or saline waters, but can also be found in diluted fresh water or fresh water with high salinity, and only rarely under marine conditions [14–16]. In Norwegian coastal waters, two Ruppia species have been found, namely Ruppia maritima L. and Ruppia cirrhosa (Petagna) Grande, the latter occasionally synonymized under R. spiralis L. ex Dumort. Both species can be found in single populations with no other vascular plants present, and they are hardly ever found together. R. maritima can sometimes Molecules 2018, 23, 16; doi:10.3390/molecules23010016 www.mdpi.com/journal/molecules Molecules 2018, 23, 16 2 of 15 Molecules 2018, 23, 16 2 of 14 beproximity found inof proximityZostera noltii of Zosterapopulations, noltii populations,while R. cirrhosa while canR. be cirrhosa found withcan be or foundclose to with Zostera or close marina to ZosteraL. populations. marina L. populations. The numbernumber ofof studiesstudies investigating investigating secondary secondary metabolites metabolites in inRuppia Ruppiaspecies species are are limited, limited, and and a full a analysisfull analysis of polyphenolic of polyphenolic content content is lacking is lacking [7,10,17 [7,10,17].]. In 1973 In Boutard 1973 Boutard et al. [7] analyzedet al. [7] andanalyzed identified and twoidentified flavonoids two flavonoids in R. maritima in R.based maritima on chrysoeriolbased on chrysoeriol and possibly and luteolin. possibly Harborneluteolin. Harborne and Williams and reportedWilliams inreported 1976 an in unidentified 1976 an unidentified glycosylflavone, glycosyl asflavone, well as as three well caffeoyl as three conjugates caffeoyl conjugates in R. maritima in R., whereasmaritima, no whereas phenolic no derivatives phenolic werederivatives foundin wereR. cirrhosa found[ 10in]. R Haynes. cirrhosa and [10]. Roberts Haynes indicated and laterRoberts the presenceindicated of later flavonols the presen in oneceRuppia of flavonolsspecies [17 in], yetone these Ruppia results species remain [17], unpublished, yet these andresults no accurateremain identificationunpublished, ofand the no flavonols accurate has id beenentification concluded. of the The flavonols previous has identification been concluded. work is basedThe previous on TLC retentionidentification times work and is electrophoretic based on TLC surveys retentio [n7 ,times10]. and electrophoretic surveys [7,10]. The aim of this work was to characterizecharacterize the phenolic content of R. cirrhosa and R. maritima collected from Norwegian coastal waters with the aims of findingfinding a new source of nutritional natural products. To our knowledge, this is the firstfirst reportreport onon completecomplete structuralstructural characterization of both flavonoidsflavonoids and one phenolic acid in these two species and ourour quantitativequantitative studies revealed high amounts of the potent chicoric acid ((CA)CA)[ [18].18]. 2. Results and Discussion 2.1. Characterization of PolyphenolicPolyphenolic Compounds in Ruppia cirrhosa The HPLC profileprofile (Figure1 1)) ofof the the crude crude extract extract of of R.R. cirrhosacirrhosa detecteddetected atat 360360± ± 10 nm revealed one phenolic acid and eight flavonoidsflavonoids (Figure2 2).). AfterAfter purificationpurification ofof thethe concentratedconcentrated extractextract byby Amberlite XAD-7XAD-7 (Sigma-Aldrich, (Sigma-Aldrich, St. St. Louis, Louis, MO, MO USA), USA) chromatography, chromatography, the compounds the compounds were isolated were byisolated preparative by preparative HPLC and HPLC analyzed and usinganalyzed high using resolution high LC-MSresolution and LC 1D‒ andMS 2Dand NMR 1D and spectroscopy. 2D NMR Theirspectroscopy. physiochemical Their physiochemical and spectral data and werespectral compared data were to previouslycompared to reported previously values reported in literature, values andin literature, the compounds and the compounds were identified were as identified quercetin as 3- quercetinO-b-D-galactopyranoside 3-O-β-D-galactopyranoside (1)[19–21], (1 quercetin) [19–21], 00 3-quercetinO-b-D-glucopyranoside 3-O-β-D-glucopyranoside (2)[19,21,22], quercetin(2) [19,21,22], 3-O-b-D-(6 -Oquercetin-malonyl)galactopyranoside 3-O-β-D-(6″-O-malonyl) (4)[23], isorhamnetingalactopyranoside 3-O- (4b)- D[23],-galactopyranoside isorhamnetin 3-O- (5β)[-D-galactopyranoside24,25], isorhamnetin (5) [24,25], 3-O-b isorhamnetin-D-glucopyranoside 3-O-β- 00 (D6-)[glucopyranoside22,25,26], isorhamnetin (6) [22,25,26], 3-O- isorhamnetinb-D-(6 -O-malonyl)galactopyranoside 3-O-β-D-(6″-O-malonyl)galactopyranoside (7)[23,27], isorhamnetin (7) [23,27], 00 3-isorhamnetinO-b-D-(6 -O 3--malonyl)-glucopyranosideO-β-D-(6″-O-malonyl)-glucopyranoside (8)[27] and ( chicoric8) [27] and acid chicoric (CA)[ acid28]. ( QuercetinCA) [28]. Quercetin 3-O-b-D- 00 (63-O--Oβ-malonyl)-glucopyranoside-D-(6″-O-malonyl)-glucopyranoside (3) was identified (3) was byidentified comparison by withcomparison an analytical with standard an analytical (≥85% (HPLC),standard Sigma-Aldrich). (≥85% (HPLC), Sigma-Aldrich. Figure 1. (a(–ac–)c )HPLC HPLC chromatogram chromatogram of ofRuppiaRuppia cirrhosa cirrhosa (a) and(a) andRuppiaRuppia maritima maritima (b) recorded(b) recorded at 360 at ± 36010 nm;± 10 (c nm;) UV-Vis (c) UV-Vis spectrum spectrum of isorhamnetin of isorhamnetin 3-O-β- 3-DO--galactopyranosideb-D-galactopyranoside (5) and (5 chicoric) and chicoric acid (CA acid). (SeeCA Figure). See Figure 2 for structures,2 for structures, 1‒8 and1– 8CAand. * CAunidentified. * unidentified caffeoyl caffeoyl unit. unit. The mainmain phenolic phenolic acid acid in bothin bothRuppia Ruppiaspecies species was chicoric was chicoric acid (CA acid), which (CA), has which been foundhas been previously found inpreviously the seagrasses in theCymodocea seagrasses nodosa CymodoceaU. [29 nodosa], Syringodium U. [29], filiformeSyringodiumK[12 ],filiformePosidionia K [12], oceanica PosidioniaL. [30– oceanica32] and L. [30–32] and Thalassia hemprichii (Ehrenb.) Ash. [33]. This is the first time flavonoids 1‒8 and chicoric acid have been identified in R. cirrhosa and R. maritima. The flavonoids quercetin 3-O-β-D- Molecules 2018, 23, 16 3 of 15 Molecules 2018, 23, 16 3 of 14 Thalassia hemprichii (Ehrenb.) Ash. [33]. This is the first time flavonoids 1–8 and chicoric acid have glucopyranosidebeen identified in andR. cirrhosaisorhamnetinand R. 3- maritimaO-β-D-.glucopyranoside The flavonoids quercetinhave previously 3-O-b-D been-glucopyranoside identified in andthe seagrassisorhamnetin C. nodosa 3-O- b[29].-D-glucopyranoside As far as we know, have previouslythis is the beenfirst report identified of 3- inO the-galactopyranosides seagrass C. nodosa and[29]. malonylatedAs far as we glycosides
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