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Journal of Applied Phycology

, Volume 31, Issue 1, pp 741–751 | Cite as

Agar yield from R-phycoerythrin extraction by-product of the red alga Gracilaria verrucosa

  • Fethi MensiEmail author
Article

Abstract

R-phycoerythrin (RPE) extracted from the red alga Gracilaria verrucosa by enzymatic hydrolysis generates a large amount of coproduct containing agar. We developed a process for the sequential extraction of RPE and agar. A Box–Behnken design with three factors–three levels and response surface methodology were applied to study the influence of different extraction parameters (incubation temperature, incubation time, and algae-to-water ratio) on the yield, 3,6-anhydrogalatose (3,6-AG) content, and sulfated degree of agar from RPE coproduct. The extraction efficiency was maximized (28%) when the extraction process was carried out with these conditions: incubation temperature of 100 °C, time of 2.6 h, and algae-to-water ratio equal to 3 (% w/v). Optimum 3,6-AG content (30%) was maximized at 85 °C, 1.85 h, and 2.35 (% w/v). Sulfated degree varied between 6 and 12%. The results of this study indicate that fresh G. verrucosa can be subjected to a process of simultaneous extraction of R-phycoerythrin and agar.

Keywords

Gracilaria verrucosa R-phycoerythrin Coproduct Agar 3,6-anhydrogalatose Sulfate Sequential extraction 

Notes

Acknowledgments

This study was cofounded by the Ministry of Higher Education and Research of Tunisia and the project BIOVecQ (PS1.3_08) financed by the European Union through the Cross-border cooperation programme Italy–Tunisia in the frame of the European Neighborhood and Partnership Instrument IEVP-2007-2013.

References

  1. Armisen R (1995) World-wide use and importance of Gracilaria. J Appl Phycol 7:231–243CrossRefGoogle Scholar
  2. Arvizu-Higuera DL, Rodríguez-Montesinos YE, Murillo-Álvarez JI, Muñoz-Ochoa M, Hernández-Carmona G (2008) Effect of alkali treatment time and extraction time on the agar from Gracilaria vermiculophylla. J Appl Phycol 20:515–519CrossRefGoogle Scholar
  3. Ben Said R, Ksouri J (1999) La Rhodophycée Gracilaria verrucosa (Hudson) Papenfus, du lac de Bizerte (Tunisie): Variations mensuelles de la biomasse, du rendement et la qualité de l’agar. Bull Inst Natn Scien Tech Mer de Salammbô 26:127–136Google Scholar
  4. Bennamoun L, Afzal MT, Léonard A (2015) Drying of alga as a source of bioenergy feedstock and food supplement—a review. Renew Sust Energ Rev 50:1203–1212CrossRefGoogle Scholar
  5. Bird KT (1988) Agar production and quality from Gracilaria sp. strain G-16: effects of environmental factors. Bot Mar 31:33–39CrossRefGoogle Scholar
  6. Bird KT, Hinson TK (1992) Seasonal variations in agar yields and quality from North Carolina agarophytes. Bot Mar 35:291–295CrossRefGoogle Scholar
  7. Bird KT, Ryther JH (1990) Cultivation of Gracilaria verrucosa (Gracilariales, Rhodophyta) strain G-16 for agar. Hydrobiologia 204/205:347–351CrossRefGoogle Scholar
  8. Boraso de Zaixso AL (1987) Gracilaria verrucosa in Golfo Nuevo, Chubut, Argentina. Biological parameters and environmental factors. Hydrobiologia 151/152:238–244CrossRefGoogle Scholar
  9. Boxer GEP, Draper NR (2007) Response surfaces, mixtures, and ridge analyses, 2nd edn. Wiley, New YorkGoogle Scholar
  10. Christiaen D, Stadler T, Ondarza M, Verdus MC (1987) Structures and functions of the polysaccharides from the cell wall of Gracilaria verrucosa (Rhodophyceae, Gigartinales). Hydrobiologia 151/152:139–146CrossRefGoogle Scholar
  11. Costley CT, Dean JR, Newton I, Carroll J (1997) Extraction of oligomers from poly(ethyleneterephthalate) by microwave-assisted extraction. J Analyt Commun 34:89–91CrossRefGoogle Scholar
  12. Cote GL, Hanisak MD (1986) Production and properties of native agars from Gracilaria tikvahiae and other red algae. Bot Mar 24:359–366Google Scholar
  13. Craigie JS (1990) Cell walls. In: Cole KM, Sheath RG (eds) Biology of the red algae. Cambridge University Press, New York, pp 221–257Google Scholar
  14. Craigie JS, Wen ZC (1984) Effects of temperature and tissue age on gel strength and composition of agar from Gracilaria tikvahiae (Rhodophyceae). Can J Bot 62:665–1670CrossRefGoogle Scholar
  15. Craigie JS, Wen ZC, Van der Meer JP (1984) Interspecific, intraspecific and nutritionally-determined variations in the composition of agars from Gracilaria spp. Bot Mar 27:55–61CrossRefGoogle Scholar
  16. Denis C, Massé A, Fleurence J, Jaouen P (2009) Concentration and pre-purification with ultrafiltration of a R-phycoerythrin solution extracted from macro-algae Grateloupia turuturu: process definition and up-scaling. Sep Purif Technol 69:37–42CrossRefGoogle Scholar
  17. Doty MS, Santos GA, Ong KS (1983) Agar from Gracilaria cylindrica. Aquat Bot 15:299–306CrossRefGoogle Scholar
  18. Duckworth M, Hong KC, Yaphe W (1971) The agar polysaccharides of Gracilaria species. Carbohydr Res 18:1–9CrossRefGoogle Scholar
  19. Espinoza-Avalos J, Hernández-Garibay E, Zertuche-González JA, Meave del Castillo ME (2003) Agar from two coexisting species of Gracilaria (Gracilariaceae) del Caribe Mexicano. Cienc Marin 29:211–228CrossRefGoogle Scholar
  20. Falshaw R, Furneaux RH, Pickering TD, Stevenson DE (1999) Agar from three Fijian Gracilaria species. Bot Mar 42:51–59Google Scholar
  21. FAO (2010) The state of world fisheries and aquaculture 2010. Fisheries and Aquaculture Department. Food and Agriculture Organization of the United Nations, Rome, p 197Google Scholar
  22. FAO (2012) The state of world fisheries and aquaculture 2012. Fisheries and Aquaculture Department. Food and Agriculture Organization of the United Nations, Rome, p 209Google Scholar
  23. FAO (2016) The state of world fisheries and aquaculture 2016. Fisheries and Aquaculture Department. Food and Agriculture Organization of the United Nations, Rome, p 244Google Scholar
  24. Freile-Pelegrín Y (2000) Does storage time influence yield and agar properties in the tropical agarophyte Gracilaria cornea? J Appl Phycol 12:153–158CrossRefGoogle Scholar
  25. Freile-Pelegrín Y, Murano E (2005) Agars from three species of Gracilaria (Rhodophyta) from Yucatan Peninsula. Bioresour Technol 96:295–302CrossRefGoogle Scholar
  26. Freile-Pelegrín Y, Robledo D (1997) Effects of season on the agar content and chemical characteristics of Gracilaria cornea from Yucatan, Mexico. Bot Mar 40:285–290CrossRefGoogle Scholar
  27. Gan CY, Latiff AA (2011) Extraction of antioxidant pectic-polysaccharide from mangosteen (Garcinia mangostana) rind: optimization using response surface methodology. Carbohydr Polym 83:600–6007CrossRefGoogle Scholar
  28. Glazer AN (1985) Light harvesting by phycobilisomes. Annu Rev Biophys Biophys Chem 14:47–77CrossRefGoogle Scholar
  29. Glazer AJ, Stryer L (1984) Phycofluor probes. Trends Biochem Sci 9:423–427CrossRefGoogle Scholar
  30. González-Leija JA, Hernández-Garibay E, Pacheco-Ruíz I, Guardado-Puentes J, Espinoza-Avalos J, López-Vivas J, Bautista-Alcantar J (2009) Optimization of the yield and quality of agar from Gracilariopsis lemaneiformis (Gracilariales) from the Gulf of California using an alkaline treatment. J Appl Phycol 21:321–326CrossRefGoogle Scholar
  31. Izumi K (1972) Chemical heterogeneity of the agar from Gracilaria verrucosa. J Biochem 72:135–140CrossRefGoogle Scholar
  32. Jiménez-Escrig A, Sánchez-Muniz FG (2000) Dietary fibre from edible seaweeds: chemical structure, physicochemical properties and effects on cholesterol metabolism. Nutr Res 20:585–598CrossRefGoogle Scholar
  33. Kim Y-W, Shin H-J (2017) Introduction of alkali soaking and microwave drying processes to improve agar quality of Gracilaria verrucosa. Korean J Chem Eng 34:3163–3169CrossRefGoogle Scholar
  34. Kronick M (1986) The use of phycobiliproteins as fluorescent labels in immunoassay. J Immunol Methods 92:1–13CrossRefGoogle Scholar
  35. Kumar V, Fotedar R (2009) Agar extraction process for Gracilaria cliftonii (Withell, Miller and Kraft, 1994). Carbohydr Polym 78:813–819CrossRefGoogle Scholar
  36. Lahaye M, Yaphe W (1988) Effects of seasons on the chemical structure and gel strength of Gracilaria pseudoverrucosa agar (Gracilariaceae, Rhodophyta). Carbohydr Polym 8:285–301CrossRefGoogle Scholar
  37. Langston M, Maig I (1983) Acid soluble Spirulina-blue with protease and alkaline medium and acidifying. USA Patent 1983/4400400Google Scholar
  38. Li S, Zhang H, Han D, Row KH (2012) Optimization of enzymatic extraction of polysaccharides from some marine algae by response surface methodology. Korean J Chem Eng 29:650–656CrossRefGoogle Scholar
  39. Lloyd AG, Dodgson KS, Price RG, Rose FAI (1961) Infrared studies on sulphate esters. I Polysaccharide sulphates. Biochim Biophys Acta 46:108–115CrossRefGoogle Scholar
  40. Lundstedt T, Seifert E, Abramo L, Thelin B, Nystrom A, Pertensen J, Bergman R (1998) Experimental design and optimization. Chemom Intell Lab Syst 42:3–40CrossRefGoogle Scholar
  41. Marinho-Soriano E (2001) Agar polysaccharides from Gracilaria species (Rhodophyta, Gracilariaceae). J Biotechnol 89:81–84CrossRefGoogle Scholar
  42. Marinho-Soriano E, Bourret E (2003) Effects of season on the yield and quality of agar from Gracilaria species (Gracilariaceae, Rhodophyta). Bioresour Technol 90:329–333CrossRefGoogle Scholar
  43. Marinho-Soriano E, Bourret E (2005) Polysaccharides from the red seaweed Gracilaria dura (Gracilariales, Rhodophyta). Bioresour Technol 96:379–382CrossRefGoogle Scholar
  44. Marinho-Soriano E, Silva TS, Moreira WSC (2001) Seasonal variation in the biomass and agar yield from Gracilaria cervicornis and Hydropuntia cornea from Brazil. Bioresour Technol 77:115–120CrossRefGoogle Scholar
  45. McLachlan J, Bird CJ (1986) Gracilaria (Gigartinales, Rhodophyta) and productivity. Aquat Bot 26:27–49CrossRefGoogle Scholar
  46. Mensi F, Ksouri J, Seale E, Romdhane MS, Fleurence J (2012) A statistical approach for optimization of R-phycoerythrin extraction from the red algae Gracilaria verrucosa by enzymatic hydrolysis using central composite design and desirability function. J Appl Phycol 24:915–926CrossRefGoogle Scholar
  47. Myers RH, Montgomery DC (2002) Response surface methodology: product and process optimization using designed experiments, 2nd edn. Wiley, New York, p 824Google Scholar
  48. Orduña-Rojas J, García-Camacho KY, Orozco-Meyer P, Ríosmena-Rodríguez R, Pacheco-Ruiz I, Zertuche-González JA, Meling-López AE (2008) Agar properties of two species of Gracilariaceae from the Gulf of California, Mexico. J Appl Phycol 20:169–175CrossRefGoogle Scholar
  49. Porse H, Rudolph B (2017) The seaweed hydrocolloid industry: 2016 updates, requirements, and outlook. J Appl Phycol 29:2187–2200CrossRefGoogle Scholar
  50. Rodríguez MC, Matulewicz MC, Noseda MD, Ducatti DRB, Leonardi PI (2009) Agar from Gracilaria gracilis (Gracilariales, Rhodophyta) of the Patagonic coast of Argentina—content, structure and physical properties. Bioresour Technol 100:1435–1441CrossRefGoogle Scholar
  51. Santelices B, Doty MS (1989) A review of Gracilaria farming. Aquaculture 78:95–133CrossRefGoogle Scholar
  52. Santos GA, Doty MS (1983) Agar from some Hawaiian red algae. Aquat Bot 16:385–389CrossRefGoogle Scholar
  53. Sekar S, Chandramohan M (2008) Phycobiliproteins as a commodity: trends in applied research, patents and commercialization. J Appl Phycol 20:13–136CrossRefGoogle Scholar
  54. Souza BWS, Cerqueira MA, Bourbon AI, Pinheiro AC, Martins JT, Teixeira JA, Coimbra MA, Vicente AA (2012) Chemical characterization and antioxidant activity of sulfated polysaccharide from the red seaweed Gracilaria birdiae. Food Hydrocoll 27:287–292CrossRefGoogle Scholar
  55. Tako M, Higa M, Medoruma K, Nakasone Y (1999) A highly methylated agar from red seaweed Gracilaria arcuata. Bot Mar 42:513–517CrossRefGoogle Scholar
  56. Tello-Ireland C, Lemus-Mondaca R, Vega-Gálvez A, López J, Di Scala K (2011) Influence of hot-air temperature on drying kinetics, functional properties, colour, phycobiliproteins, antioxidant capacity, texture and agar yield of alga Gracilaria chilensis. LWT Food Sci Technol 44:2112–2118CrossRefGoogle Scholar
  57. Thomas PC, Krishnamurthy V (1976) Agar from cultured Gracilaria edulis (Gmel.) Silva. Bot Mar 19:115–117CrossRefGoogle Scholar
  58. Veeragurunathan V, Prasad K, Singh N, Malarvizhi J, Mandal SK, Mantri VA (2016) Growth and biochemical characterization of green and red strains of the tropical agarophytes Gracilaria debilis and Gracilaria edulis (Gracilariaceae, Rhodophyta). J Appl Phycol 28:3479–3489CrossRefGoogle Scholar
  59. Whyte JNC, Englar JR, Saunders RG, Lindsay JC (1981) Seasonal variations in the biomass, quantity and quality of agar, from the reproductive and vegetative stages of Gracilaria (verrucosa type). Bot Mar 24:493–501CrossRefGoogle Scholar
  60. Yao SS, Xia ZY, En LZ, Qing LW (1984) The yield and properties of agar extracted from different life stages of Gracilaria verrucosa. Hydrobiologia 116/117:551–553CrossRefGoogle Scholar
  61. Yaphe W (1984) Properties of Gracilaria agars. Hydrobiologia 116/117:17–186CrossRefGoogle Scholar
  62. Yaphe W, Arsenault GP (1965) Improved resocinol reagent for the the determination of fructose,and of 3,6-anhydrogalactose in polysaccharides. Anal Biochem 13:143–148CrossRefGoogle Scholar
  63. Yousefi MK, Islami HR, Filizadeh Y (2013) Effect of extraction process on agar properties of Gracilaria corticata (Rhodophyta) collected from the Persian Gulf. Phycologia 52:481–487CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Laboratoire de Biotechnologie Bleue et Bioproduits Aquatiques-B3AquaInstitut National des Sciences et Technologies de la Mer (INSTM)Le KramTunisia

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