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A sulfated galactan from the mucilaginous sheath of the red filamentous alga Chroodactylon ornatum (Stylonematophyceae, Rhodophyta)

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Abstract

The pseudofilamentous red alga Chroodactylon ornatum was grown in f/2 culture medium with the addition of 10, 34, and 100 μM (nominal concentration) cupric sulfate. The bioassays were terminated at two selected end points (days 4 and 12). Growth inhibition, changes in pigment composition, and oxidative stress indicators such as phenolic compounds and lipid peroxidation (dosed as thiobarbituric reactive substances) were observed in cultures with 34 and 100-μM cupric sulfate. Quinacrine (Atebrin) and chlorotetracycline fluorochromes showed abundant vacuoles of acidic content, related with mucilage secretion. Structural analyses by methylation, desulfation-methylation, alkaline treatment, and NMR spectroscopy revealed that the mucilaginous sheath of C. ornatum contains a sulfated galactan with a backbone of alternating 3-linked β-d-galactopyranose and 4-linked α-l-galactopyranose moieties, i.e., an agaran. The absence of 3,6-anhydrogalactose and of its precursor unit (α-galactose 6-sulfate) were confirmed. The highly sulfated polysaccharide contained these ester groups on the C-2 and C-4 hydroxyl groups of the 3-linked unit and on C-3 of the 4-linked units. The large proportion of sulfate esterification in this polysaccharide can be related to the extracellular biosorption of copper divalent cation (2.5 ± 0.4 mg per gram of dry weight) and to copper tolerance in bioassays.

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References

  • Andersen RA (ed) (2005) Algal culturing techniques. Elsevier Academic Press, San Diego

    Google Scholar 

  • Andrade LR, Farina M, Amado Filho GM (2004) Effects of copper on Enteromorpha flexuosa (Chlorophyta) in vitro. Ecotoxicol Environ Safety 58:117–125

    Article  CAS  PubMed  Google Scholar 

  • Areco MM, dos Santos Afonso M (2010) Copper, zinc, cadmium and lead biosorption by Gymnogongrus torulosus. Thermodyn Kinet Stud Colloids Surf B: Biointerfaces 81:620–628

    Article  CAS  Google Scholar 

  • Basson PW (1979) Marine algae of the Arabian Gulf coast of Saudi Arabia (second half). Bot Mar 22:65–82

    Google Scholar 

  • Bermejo Román R, Alvárez-Pez JM, Acién Fernández FG, Molina Grima E (2002) Recovery of pure B-phycoerythrin from the microalga Porphyridium cruentum. J Biotechnol 93:73–85

    Article  PubMed  Google Scholar 

  • Blaby Haas CE, Merchant SS (2012) The ins and outs of algal metal transport. Biochim Biophys Acta 1823:1531–1552

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bouzon ZL, Ouriques LC, Oliveira EC (2006) Spore adhesion and cell wall formation in Gelidium floridanum (Rhodophyta, Gelidiales). J Appl Phycol 18:287–294

    Article  Google Scholar 

  • Brown M, Newman JE (2003) Physiological response of Gracilariopsis longissima (Rhodophyceae) to sublethal copper concentrations. Aquat Toxicol 64:201–213

    Article  CAS  PubMed  Google Scholar 

  • Byankina Barabanova AO, Sokolova EV, Anastyuk SD, Isakov VV, Isakov VV, Glazunov VP, Volod’ko AV, Yakovleva IM, Solov’eva TF, Yermak IM (2013) Polysaccharide structure of tetrasporic red seaweed Tichocarpus crinitus. Carbohydr Polym 98:26–35

    Article  CAS  PubMed  Google Scholar 

  • Cases MR, Cerezo AS, Stortz CA (1995) Separation and quantitation of enantiomeric galactoses as their mono-O-methylethers as their diastereomeric 1-deoxy-1-(2′-hydroxypropylamino)-alditols. Carbohydr Res 269:333–341

    Article  CAS  Google Scholar 

  • Castilla JC (1996) Copper mine tailing disposal in Northern Chile rocky shores: Enteromorpha compressa (Chlorophyta) as a sentinel species. Environ Monit Assess 40:171–184

    Article  CAS  PubMed  Google Scholar 

  • Ciucanu I, Kerek F (1984) A simple and rapid method for the permethylation of carbohydrates. Carbohydr Res 131:209–217

    Article  CAS  Google Scholar 

  • Contreras L, Moenne A, Correa JA (2005) Antioxidant responses in Scytosiphon lomentaria (Phaeophyceae) inhabiting copper enriched coastal environments. J Phycol 41:1184–1195

    Article  CAS  Google Scholar 

  • Correa JA, Castilla JC, Ramirez MA, Varas M, Lagos N, Vergara S, Moenne A, Roman D, Brown MT (1999) Copper mine tailings and their effects on marine algae in Northern Chile. J Appl Phycol 11:57–67

    Article  CAS  Google Scholar 

  • Diannelidis BE, Delivopoulos SG (1997) The effects of zinc, copper and cadmium on the fine structure of Ceramium ciliatum. Mar Environ Res 44:127–134

    Article  CAS  Google Scholar 

  • Dodgson KS, Price RG (1962) A note on the determination of the ester sulphate content of sulphated polysaccharides. Biochem J 84:106–110

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Analyt Chem 28:350–356

    Article  CAS  Google Scholar 

  • Eklund BT, Kautsky L (2003) Review on toxicity testing with marine macroalgae and the need for method standardization––exemplified with copper and phenol. Mar Pollut Bull 46:171–181

    Article  CAS  PubMed  Google Scholar 

  • Farías WR, Valente A, Pereira MS, Mourao PA (2000) Structure and anticoagulant activity of sulfated galactans. J Biol Chem 275:29299–29307

    Article  PubMed  Google Scholar 

  • Gantt E (1990) Pigmentation and photoacclimation. In: Cole KM, Sheath RG (eds) Biology of the Red Algae. Cambridge University Press, Cambridge, pp 203–219

    Google Scholar 

  • Genicot-Joncour S, Poinas A, Richard O, Potin P, Rudolph B, Kloareg B, Helbert W (2009) The cyclization of the 3,6-anhydro-galactose ring of iota-carrageenan is catalyzed by two d-galactose-2,6-sulfurylases in the red alga Chondrus crispus. Plant Physiol 151:1609–1616

    Article  PubMed Central  PubMed  Google Scholar 

  • Gloaguen V, Ruiz G, Morvan H, Mouradi-Givernaud A, Maes E, Krausz P, Strecker G (2004) The extracellular polysaccharide of Porphyridium sp.: an NMR study of lithium-resistant oligosaccharidic fragments. Carbohydr Res 339:97–103

    Article  CAS  PubMed  Google Scholar 

  • Hader D, Lebert M, Sinha RP, Barbieri ES, Helbling EW (2002) Role of protective and repair mechanisms in the inhibition of photosynthesis in marine macroalgae. Photochem Photobiol Sci 1:809–814

    Article  PubMed  Google Scholar 

  • Karsten U, West JA, Zuccarello GC, Nixdorf O, Barrow KD, King RJ (1999) Low molecular weight carbohydrate patterns in the Bangiophyceae (Rhodophyta). J Phycol 35:967–976

    Article  CAS  Google Scholar 

  • Karsten U, West JA, Zuccarello GC, Engbrodt R, Yokoyama A, Hara Y, Brodie J (2003) Low molecular weight carbohydrates of the Bangiophycidae (Rhodophyta). J Phycol 39:584–589

    Article  CAS  Google Scholar 

  • Kloareg B, Quatrano RS (1988) Structure of the cell walls of marine algae and ecophysiological functions of the matrix polysaccharides. Oceanogr Mar Biol Ann Rev 26:259–315

    Google Scholar 

  • Kolender AA, Matulewicz MC (2002) Sulfated polysacchride from the red seaweed Georgiella confluens. Carbohydr Res 337:57–68

    Article  CAS  PubMed  Google Scholar 

  • Küpper H, Etlík I, Spiller M, Küpper FC, Práil O (2002) Heavy metal-induced inhibition of photosynthesis: targets of in vivo heavy metal chlorophyll formation. J Phycol 38:429–441

    Article  Google Scholar 

  • Lapidot M, Shrestha RP, Weinstein Y, Arad Malis S (2010) Red microalgae: from basic know-how to biotechnology. In: Seckbach J, Chapman D (eds) Red algae in the genomic age. Springer, Netherlands, pp 205–225

    Chapter  Google Scholar 

  • Leonardi PI, Vasquez JA (1999) Effects of copper pollution on the ultrastructure of Lessonia spp. Hydrobiologia 398(399):375–383

    Article  Google Scholar 

  • Lewin RA, Robertson JA (1971) Influence of salinity on the form of Asterocytis in pure culture. J Phycol 7:236–238

    CAS  Google Scholar 

  • Lichtenthaler H (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382

    Article  CAS  Google Scholar 

  • Lombardi AT, Vieira AH, Sartori LA (2002) Mucilaginous capsule adsorption and intracellular uptake of copper by Kirchneriella aperta (Chlorococcales). J Phycol 38:332–337

    Article  CAS  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  PubMed  Google Scholar 

  • Medcalf DG, Brannon JH, Scott JR, Allen GG, Lewis J, Norris RE (1981) Polysaccharides from microscopic red algae and diatoms. Proc Int Seaweed Symp 8:582–588

    Google Scholar 

  • Mehta SK, Gaur JP (2005) Use of algae for removing heavy metal ions from wastewater: progress and prospects. Crit Rev Biotechnol 25:113–152

    Article  CAS  PubMed  Google Scholar 

  • Miller IJ (1999) Further evaluation of the structure of the polysaccharide from Plocamium costatum with the use of set theory. Hydrobiologia 398/399:385–389

    Google Scholar 

  • Müller KM, Lynch MD, Sheath RG (2010) Bangiophytes: from one Class to six; where do we go from here? In: Seckbach J, Chapman D (eds) Red algae in the genomic age. Springer, Netherlands, pp 241–259

    Chapter  Google Scholar 

  • Navarro DA, Stortz CA (2003) Determination of the configuration of 3,6-anhydrogalactose and cyclizable α-galactose 6-sulfate units in red seaweed galactans. Carbohydr Res 338:211–218

    Article  Google Scholar 

  • Navarro DA, Flores ML, Stortz CA (2007) Microwave-assisted desulfation of sulfated polysaccharides. Carbohydr Polym 69:742–747

    Article  CAS  Google Scholar 

  • Park JT, Johnson MJ (1949) A submicrodetermination of glucose. J Biol Chem 181:149–151

    CAS  PubMed  Google Scholar 

  • Pujals C (1961) Algunas observaciones sobre Asterocytis ornata (C. Ag.) Hamel, Rodofícea nueva para Argentina. Darwiniana 12:365–377 (in Spanish)

    Google Scholar 

  • Ratkevicius N, Correa JA, Moenne A (2003) Copper accumulation, synthesis of ascorbate and activation of ascorbate peroxidase in Enteromorpha compressa (L.) Grev. (Chlorophyta) from heavy metal-enriched environments in northern Chile. Plant Cell Environ 26:1599–1608

    Article  CAS  Google Scholar 

  • Romay C, Gonzalez R, Ledon N, Remirez D, Rimbau V (2003) C-phycocyanin: a biliprotein with antioxidant, anti-inflammatory and neuroprotective effects. Curr Protein Pept Sci 4:207–216

    Article  CAS  PubMed  Google Scholar 

  • Romera E, González F, Ballester A, Blázquez ML, Muñoz JA (2007) Comparative study of biosorption of heavy metals using different types of algae. Bioresour Technol 98:3344–3353

    Article  CAS  PubMed  Google Scholar 

  • Santos JA, Mulloy B, Mourao PA (1992) Structural diversity among sulfated α-l-galactans from ascidians (tunicates). Eur J Biochem 204:669–677

    Article  CAS  PubMed  Google Scholar 

  • Singleton VL, Orthofer R, Lamuela-Raventós RM (1999) Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. In: Lester P (ed) Methods in Enzymology. Academic, London, pp 152–178

    Google Scholar 

  • Statistica 5.5 (1999) Statsoft Inc, Tulsa, Oklahoma, USA

  • Stevenson TT, Furneaux RH (1991) Chemical methods for the analysis of sulphated galactans from red algae. Carbohydr Res 210:277–298

    Article  CAS  PubMed  Google Scholar 

  • Stortz CA, Cerezo AS (2000) Novel findings in carrageenans, agaroids and ‘hybrid’ red seaweed galactans. Curr Top Phytochem 4:121–134

    CAS  Google Scholar 

  • Sztrum AA, Sabatini SE, Rodríguez MC (2012) Isocitrate lyase activity and antioxidant responses in copper stressed cultures of Chlamydomonas reinhardtii (Volvocales, Chlorophyceae). Phycologia 51:135–143

    Article  CAS  Google Scholar 

  • Usov A (2011) Polysaccharides of red algae. Adv Carbohydr Chem Biochem 65:115–217

    Article  CAS  PubMed  Google Scholar 

  • Vavilin D, Ducruet JM, Matorin DN, Venediktov PS, Rubin AB (1998) Membrane lipid peroxidation, cell viability and Photosystem II activity in the green alga Chlorella pyrenoidosa subjected to various stress conditions. J Photochem Photobiol B 42:233–239

    Article  CAS  Google Scholar 

  • Volesky B, Holan ZR (1995) Biosorption of heavy metals. Biotechnol Prog 11:235–250

    Article  CAS  PubMed  Google Scholar 

  • Xia JR, Li YJ, Lu J, Chen B (2004) Effects of copper and cadmium on growth, photosynthesis, and pigment content in Gracilaria lemaneiformis. Bull Environ Contam Toxicol 73:979–986

    Article  CAS  PubMed  Google Scholar 

  • Yoon HS, Müller KM, Sheath RG, Ott FD, Bhattacharya D (2006) Defining the major lineages of red algae (Rhodophyta). J Phycol 42:482–492

    Article  CAS  Google Scholar 

  • Yoon HS, Zuccarello GC, Bhattacharya D (2010) Evolutionary history and taxonomy of red algae. In: Seckbach J, Chapman D (eds) Red algae in the genomic age. Springer, Netherlands, pp 25–42

    Chapter  Google Scholar 

  • Zuccarello GC, West JA, Kikuchi N (2008) Phylogenetic relationships within the Stylonematales (Stylonematophyceae, Rhodophyta): Biogeographic patterns do no apply to Stylonema alsidii. J Phycol 44:384–393

    Article  CAS  Google Scholar 

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Acknowledgments

This work was funded by grants from UBA (W-759) and CONICET (PIP 0559/10). JMC is a Research Fellow of the National Research Council of Argentina (CONICET), and CAS is a Research Member of the same institution.

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  1. Juan M. Cabrera

    Present address: INIBIOMA – CRUB, Universidad del Comahue, 8400, Bariloche, Argentina

Authors and Affiliations

  1. Departamento de Química Orgánica-CIHIDECAR, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, 1428, Buenos Aires, Argentina

    Juan M. Cabrera & Carlos A. Stortz

  2. Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, 1428, Buenos Aires, Argentina

    Juan M. Cabrera & María C. Rodríguez

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  1. Juan M. Cabrera
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Correspondence to María C. Rodríguez.

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Cabrera, J.M., Stortz, C.A. & Rodríguez, M.C. A sulfated galactan from the mucilaginous sheath of the red filamentous alga Chroodactylon ornatum (Stylonematophyceae, Rhodophyta). J Appl Phycol 26, 1801–1811 (2014). https://doi.org/10.1007/s10811-014-0236-3

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