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Characterization of Cell Wall Polysaccharides of the Coencocytic Green Seaweed Bryopsis Plumosa (Bryopsidaceae, Chlorophyta) from the Argentine Coast1

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Characterization of Cell Wall Polysaccharides of the Coencocytic Green Seaweed Bryopsis Plumosa (Bryopsidaceae, Chlorophyta) from the Argentine Coast1 J. Phycol. 48, 326–335 (2012) Ó 2012 Phycological Society of America DOI: 10.1111/j.1529-8817.2012.01131.x CHARACTERIZATION OF CELL WALL POLYSACCHARIDES OF THE COENCOCYTIC GREEN SEAWEED BRYOPSIS PLUMOSA (BRYOPSIDACEAE, CHLOROPHYTA) FROM THE ARGENTINE COAST1 Marina Ciancia 2,3 Ca´tedra de Quı´mica de Biomole´culas, Departamento de Biologı´a Aplicada y Alimentos (CIHIDECAR-CONICET), Facultad de Agronomı´a, Universidad de Buenos Aires, Av. San Martı´n 4453, C1417DSE Buenos Aires, Argentina Josefina Alberghina Departamento de Ecologı´a Gene´tica y Evolucio´n, Facultad de Ciencias Exactas y Naturales, Ciudad Universitaria-Pabello´n 2, 1428 Buenos Aires, Argentina Paula Ximena Arata Ca´tedra de Quı´mica de Biomole´culas, Departamento de Biologı´a Aplicada y Alimentos (CIHIDECAR-CONICET), Facultad de Agronomı´a, Universidad de Buenos Aires, Av. San Martı´n 4453, C1417DSE Buenos Aires, Argentina Hugo Benavides Instituto Nacional de Investigacio´n y Desarrollo Pesquero (INIDEP), Paseo Victoria Ocampo Nº 1, Escollera Norte, B7602HSA Mar del Plata, Buenos Aires, Argentina Frederik Leliaert, Heroen Verbruggen Phycology Research Group and Center for Molecular Phylogenetics and Evolution, Ghent University, Krijgslaan 281 (S8), B-9000 Gent, Belgium and Jose Manuel Estevez 3 Instituto de Fisiologı´a, Biologı´a Molecular y Neurociencias (IFIBYNE-CONICET), Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, 1428 Buenos Aires, Argentina Bryopsis sp. from a restricted area of the rocky seaweeds of the genus Codium (Bryopsidales, Chloro- shore of Mar del Plata (Argentina) on the Atlantic phyta), but some important differences were also coast was identified as Bryopsis plumosa (Hudson) found. This is the first report about the structure of C. Agardh (Bryopsidales, Chlorophyta) based on mor- the water-soluble polysaccharides biosynthesized by phological characters and rbcL and tufA DNA bar- seaweeds of the genus Bryopsis. These sulfated galac- codes. To analyze the cell wall polysaccharides of this tans and rhamnans were in situ localized mostly in seaweed, the major room temperature (B1) and 90°C two layers, one close to the plasma membrane and the (X1) water extracts were studied. By linkage analysis other close to the apoplast, leaving a middle amor- and NMR spectroscopy, the structure of a sulfated phous, unstained cell wall zone. In addition, fibrillar galactan was determined, and putative sulfated rham- polysaccharides, comprising (1 fi 3)-b-D-xylans and nan structures and furanosidic nonsulfated arabinan cellulose, were obtained by treatment of the residue structures were also found. By anion exchange from the water extractions with an LiCl ⁄ DMSO solu- chromatography of X1, a fraction (F4), comprising a tion at high temperature. These polymers were also sulfated galactan as major structure was isolated. localized in a bilayer arrangement. Structural analysis showed a linear backbone consti- Key index words: Bryopsis plumose; cell wall; green tuted of 3-linked b-D-galactose units, partially sulfated seaweed; pyruvylated galactan sulfate; sulfated on C-6 and partially substituted with pyruvic acid polysaccharides forming an acetal linked to O-4 and O-6. This galactan has common structural features with those of green Abbreviations: Ara, arabinose; CB, Coomasie Blue; CW, Calcofluor White; Fuc, focose; Gal, galactose; Glc, glucose; IEC, ion exchange chromatography; Man, mannose; Rha, rhamnose; RR, Ruthenium 1Received 1 April 2011. Accepted 29 August 2011. 2Author for correspondence: e-mail [email protected]. Red; TBO, Toluidine Blue ortho-chromatic; TFA, 3Research Member of the National Research Council of Argentina trifluoroacetic acid; Xyl, xylose (CONICET). 326 CELL WALLS IN THE GREEN SEAWEED BRYOPSIS PLUMOSA 327 Green seaweeds biosynthesize matrix sulfated and their relative amounts in relation to different polysaccharides with a great variety of chemical geographic locations and seasons has been structures. They have been classified into two main addressed recently in our group (Ferna´ndez et al. groups (Percival and McDowell 1981): (i) sulfated 2011). Briefly, samples from three different popula- glucuronoxylorhamnans and glucuronoxylorhamno- tions from the Argentine coast showed: (i) an galactans, with negative optical rotation, and (ii) sul- important variation in the relative content of sul- fated xyloarabinogalactans, which have positive fated arabinans, which increases from north to optical rotation. As example of the first group, the south, and (ii) a measurable degree of cell wall vari- major acidic polysaccharide structure of Ulva and ability in the sulfate distribution between the differ- Entoromorpha species (Ulvales) is a linear sulfated ent sulfated polysaccharides, independently of the polymer comprising alternating 4-linked b-D-glucu- amount of each polysaccharide present and of total ronic acid and a-L-rhamnose units (Lahaye and sulfate content. Overall, these results suggested that Robic 2007). On the other hand, seaweeds belong- C. vermilara has developed a mechanism to adjust ing to the Bryopsidales (Chlorophyta) are supposed the total level of cell wall sulfation by modulating to belong to the second group, and only small to the molar ratio of the individual polymers and also trace amounts of uronic acids were detected in by adjusting the sulfation level in each type of poly- some of these samples. The genus Bryopsis, as well as mer, whereas nonsulfated polymers, as the main Codium, belongs to the suborder Bryopsidineae, structural polysaccharides, did not change signifi- comprising species generally occurring in temper- cantly over the time or growing stage. ate, tropical, and subtropical marine waters (Lamb Only a recent reference has appeared concerning and Zechman 2006, Guiry and Guiry 2011). There characterization of the acidic polysaccharides from is very little information about these polysaccha- Bryopsis (Song et al. 2010). The hot water extract of rides. Moreover, only the sulfated polysaccharides Bryopsis plumosa, as well as the acidic and alkaline from some species of the genus Codium (Love and extracts were obtained from culture samples from Percival 1964a, Bilan et al. 2007, Ciancia et al. 2007, Qingdao (China). The acidic extract gave glucose as Farias et al. 2008, Estevez et al. 2009, Ohta et al. major monosaccharide component. The alkaline 2009) have been studied in detail. It has been and hot water extracts were quite similar, mainly shown that Codium species biosynthesize sulfated composed of carbohydrates, but also sulfate and galactans constituted by 3-linked b-D-galactopyranose proteins. The major sugar components were galac- (b-D-Gal) residues partially sulfated on C-4 and ⁄ or tose (Gal), followed by arabinose (Ara), also minor C-6, with ramifications on C-6 and important amounts of glucose (Glc), mannose (Man), rham- amounts of pyruvate forming mainly five-membered nose (Rha), and fucose (Fuc) were detected. The cyclic acetals (S configuration) with O-3 and O-4 of only structural feature informed was sulfation on a nonreducing terminal b-D-Gal residues. A minor primary carbon atom, inferred from the infrared part of pyruvate forms six-membered cyclic acetals spectrum. The best in vitro antioxidant activity was with O-4 and O-6 (R configuration) (Bilan et al. found for the acidic extract (Song et al. 2010). 2006). The relative amount of these structural units On the other hand, more information is available in the galactan varies with the species and also for about the fibrillar components of the cell walls of different fractions of the same species (Bilan et al. the Bryopsidales. These seaweeds lack cellulose, or 2007, Farias et al. 2008, Estevez et al. 2009). Besides, at least this polymer is not the major fibrillar com- a highly sulfated pyranosic arabinan was detected in ponent of the cell wall, and have b-(1 fi 4)-mann- C. dwarkense (Siddhanta et al. 1999) and also in ans (Love and Percival 1964b, Mackie 1969, Huizing C. fragile and C. vermilara and characterized (Ciancia and Rietema 1975, Chanzy et al. 1984, Kaihou et al. et al. 2007, Estevez et al. 2009). Its structure is now 1993, Ciancia et al. 2007) or b-(1 fi 3)-xylans under study. In addition, hydroxyproline-rich glyco- (Mackie and Percival 1959, Mackie 1969, Fukushi proteins (HRGPs) have been detected in minor et al. 1988, Maeda et al. 1990, Yamagaki et al. 1997) quantities (Estevez et al. 2009, Ferna´ndez et al. instead. In addition, it has been shown that the 2010). A small fraction from C. fragile showed a neu- major fibrillar component of the cell wall can vary tral arabinan composed of 3-linked and 5-linked in the different life stages (Huizing and Rietema a-L-arabinofuranose residues; it has been suggested 1975, Wutz and Zetsche 1976, Huizing et al. 1979). that this structure could be part of the carbohydrate Thus, gametophyte microthalli of Derbesia spp. bio- moiety of the HRGPs (Estevez et al. 2009). synthesize xylans, whereas sporophyte macrothalli of The temporal scale of cell wall variability of sev- the same genus produce mannans. Similarly, game- eral green, red, and brown seaweeds, in most of the tophyte macrothalli from the genus Bryopsis biosyn- cases, was linked to complex environmental exoge- thesize xylans, wheresas sporophyte microthalli nous factors as well as endogenous changes in the produce mannans. However, considerable amounts organisms (e.g., growth and development, morpho- of a glucan were detected in some cases (Wutz and logical change, reproduction, etc.). In addition, the Zetsche 1976, Huizing et al. 1979). Moreover, cellu- importance of the variability displayed in the struc- lose was found to comprise <10% (w ⁄ w) of the ture of cell wall polysaccharides from C. vermilara fibrillar material of the cell walls from Bryopsis 328 MARINA CIANCIA ET AL. maxima, being present in an amorphous state, extracts. The first one was treated with a-amylase (Knutsen and in contrast to the trihelical arrangement of the Grasdalen 1987) to give a purified sample, X1. The residue b-(1 fi 3)-xylan (Fukushi et al. 1988, Maeda et al. RX2 (1 g) from the water extraction was extracted with an 8.4% LiCl solution in DMSO (200 mL) at 106°C for 5 h (Flores 1990).
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