Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Valorization of the filamentous seaweed Chaetomorpha gracilis (Cladophoraceae, Chlorophyta) from an IMTA system

Abstract

The filamentous green seaweed Chaetomorpha can grow in a wide range of salinities and temperatures, and it is often reported as nuisance in other cultures due to its proliferation capacity and ordinarily discarded. However, Chaetomorpha can represent a promising feedstock for different purposes due to their potential valuable compounds. In the present study, Chaetomorpha gracilis grown as an opportunistic species in Solieria filiformis cultivated under an integrated multitrophic aquaculture (IMTA) in tanks was valorized through three sequential extractions. The sequential extraction process implemented was successful and managed to recover three valuable products: a lipid fraction with interesting saturated fatty acids (SFAs), a water-soluble sulfated polysaccharide (SP) with gelling capacity and antioxidant activity, and a highly crystalline cellulose. We discuss on the promising uses and applications for this C. gracilis compounds valuable to obtain biofuel and other pharmacological uses and industrial applications (composites and/or as pulp in paper making).

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  1. Ajjabi LC, Chouba L (2009) Biosorption of Cu2+ and Zn2+ from aqueous solutions by dried marine green macroalga Chaetomorpha linum. J Environ Manag 90:3485–3489

  2. Aknin M, Moellet-Nzaou R, Cisse E, Kornprobst JM, Gaydou EM, Samb A, Miralles J (1992) Fatty acid composition of 12 species of Chlorophyceae from the Senegalese coast. Phytochemistry 31:2739–2741

  3. Alves A, Caridade SG, Mano JF, Sousa RA, Reis RL (2010) Extraction and physico-chemical characterization of a versatile biodegradable polysaccharide obtained from green algae. Carbohydr Res 345:2194–2200

  4. Alves A, Sousa RA, Reis RL (2013) A practical perspective on ulvan extracted from green algae. J Appl Phycol 25:407–424

  5. Arata PX, Quintana I, Raffo MP, Ciancia M (2016) Novel sulfated xylogalactoarabinans from green seaweed Cladophora falklandica: chemical structure and action on the fibrin network. Carbohydr Polym 154:139–150

  6. Atkinson MJ, Smith SV (1983) C:N:P ratios of benthic marine plants. Limnol Oceanogr 28:568–574

  7. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

  8. Blumenkrantz N, Asboe-Hansen G (1973) New method for quantitative determination of uronic acids. Anal Biochem 54:484–489

  9. Chen YW, Lee HW, Juan JC (2016) Production of new cellulose nanomaterial from red algae marine biomass Gelidium elegans. Carbohydr Polym 151:1210–1219

  10. Chiellini F, Morelli A (2011) Ulvan: a versatile platform of biomaterials from renewable resources. In: Pignatello R (ed) Biomaterials-physics and chemistry. IntechOpen, Riejeka pp 75–98

  11. Chollet L, Saboural P, Chauvierre C, Villemin JN, Letourneur D, Chaubet F (2016) Fucoidans in nanomedicine. Mar Drugs 14:145

  12. Costa LS, Fidelis GP, Cordeiro SL, Oliveira RM, Sabry DA, Câmara RB, Nobre LT, Costa MS, Almeida-Lima J, Farias EHC, El L, Rocha HAO (2010) Biological activities of sulfated polysaccharides from tropical seaweeds. Biomed Pharmacother 64:21–28

  13. Cunha L, Grenha A (2016) Sulfated seaweed polysaccharides as multifunctional in drug delivery applications. Mar Drugs 14:42

  14. De Souza Lima MM, Borsali R (2004) Rodlike cellulose microcrystals: structure, properties, and applications. Macromol Rapid Commun 25:771–787

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

  16. Dunn EK, Shoue DA, Huang X, Kline RE, MacKay AL, Carpita NC, Taylor IE, Mandoli DF (2007) Spectroscopic and biochemical analysis of regions of the cell wall of the unicellular ‘mannan weed’, Acetabularia acetabulum. Plant Cell Physiol 48:122–133

  17. El Maghraby DM, Fakhry EM (2015) Lipid content and fatty acid composition of Mediterranean macro-algae as dynamic factors for biodiesel production. Oceanologia 57:86–92

  18. Fernández PV, Estevez JM, Cerezo AS, Ciancia M (2012) Sulfated β-D-mannan from green seaweed Codium vermilara. Carbohydr Polym 87:916–919

  19. Filisetti-Cozzi TM, Carpita NC (1991) Measurement of uronic acids without interference from neutral sugars. Anal Biochem 197:157–162

  20. Ganesh EA, Das S, Arun G, Balamurugan S, Ruban Raj R (2009) Heparin like compound from green alga Chaetomorpha antennina as potential anticoagulant agent. Asian J Med Sci 1:114–116

  21. Ge S, Champagne P (2017) Cultivation of the marine macroalgae Chaetomorpha linum in municipal wastewater for nutrient recovery and biomass production. Environ Sci Technol 51:3558–3566

  22. George J, Sabapathi SN (2015) Cellulose nanocrystals: synthesis, functional properties, and applications. Nanotechnol Sci Appl 8:45–54

  23. Gilbert RD, Kadla JF (1998) Polysaccharides—cellulose. In: Kaplan DL (ed) Biopolymers from renewable resources. Springer, Berlin, pp 47–95

  24. Heiba HI, Al-Easa HS, Rizk AM (1997) Fatty acid composition of twelve algae from the coastal zones of Qatar. Plant Foods Hum Nutr 51:27–34

  25. Huang SQ, Ding SD, Fan LP (2012) Antioxidant activities of five polysaccharides from Inonotus obliquus. Int J Biol Macromol 50:1183–1187

  26. Jackson SG, McCandless EL (1978) Simple, rapid, turbidometric determination of inorganic sulfate and/or protein. Anal Biochem 90:802–808

  27. Kesava Rao C, Induskhar VK (1987) Carbon, nitrogen and phosphorus ratios is seaweater and seaweeds of Saurashtra, north west coast of India. Indian J Mar Sci 16:117–121

  28. Khotimchenko SV (1993) Fatty acids of green macrophytic algae from the sea of Japan. Phytochemistry 32:1203–1207

  29. Khotimchenko SV, Vaskovsky VE, Titlyanova TV (2002) Fatty acids of marine algae from the Pacific Coast of North California. Bot Mar 45:17–22

  30. Knoshaug P, Shi B, Shannon TG, Mleziva MM, Pienkos PT (2013) The potential of photosynthetic aquatic species as sources of useful cellulose fibers-a review. J Appl Phycol 25:1123–1134

  31. Knothe G, Matheaus AC, Ryan TW (2003) Cetane numbers of branched and straight-chain fatty esters determined in an ignition quality tester. Fuel 82:971–990

  32. Kumari P, Reddy CRK, Jha B (2011) Comparative evaluation and selection of a method for lipid and fatty acid extraction from macroalgae. Anal Biochem 415:134–144

  33. Kumari P, Bijo AJ, Mantri VA, Reddy CRK, Jha B (2013) Fatty acid profiling of tropical marine macroalgae: an analysis from chemotaxonomic and nutritional perspectives. Phytochemistry 86:44–56

  34. Lahaye M, Robic A (2007) Structure and functional properties of ulvan, a polysaccharide from green seaweeds. Biomacromolecules 8:1765–1774

  35. Lakshmi DS, Trivedi N, Reddy CRK (2017) Synthesis and characterization of seaweed cellulose derived carboxymethyl cellulose. Carbohydr Polym 157:1604–1610

  36. Leal GF, Ramos LA, Barrett DH, Curvelo AAS, Rodella CB (2015) A thermogravimetric analysis (TGA) method to determine the catalytic conversion of cellulose from carbon supported hydrogenolysis process. Thermochim Acta 616:9–13

  37. Li Q, Luo J, Wang C, Tai W, Wang H, Zhang X, Liu K, Jia Y, Lyv X, Wang L, He H (2018) Ulvan extracted from green seaweeds as new natural additives in diets for laying hens. J Appl Phycol 30:2017–2027

  38. Littler DS, Littler MM (2000) Caribbean reef plants. An identification guide to the reef plants of the Caribbean, Bahamas, Florida and Gulf of Mexico. Offshore Graphics, Washington DC

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

  40. Martins JT, Cerqueira MA, Bourbon AI, Pinheiro AC, Souza BWS, Vicente AA (2012) Synergistic effects between k-carrageenan and locust bean gum on physicochemical properties of edible films made thereof. Food Hydrocoll 29:280–289

  41. Martone PT, Estevez JM, Lu F, Ruel K, Denny MW, Somerville C, Ralph J (2009) Discovery of lignin in seaweed reveals convergent evolution of cell-wall architecture. Curr Biol 19:169–175

  42. Matshuhiro B, Zanlungo AB (1983) Colorimetric determination of 3,6 anhydrogalactose in polysaccharides from red seaweed. Carbohydr Res 118:4–7

  43. McGlathery KJ, Pedersen MF (1999) The effect of growth irradiance on the coupling of carbon and nitrogen metabolism in Chaetomorpha linum (Chlorophyta). J Phycol 35:721–731

  44. Messyasz B, Michalak I, Łęska B, Schroeder B, Górka B, Korzeniowska K, Lipok J, Wieczorek P, Rój E, Wilk R, Dobrzyńska-Inger A, Górecki H, Chojnacka K (2018) Valuable natural products from marine and freshwater macroalgae obtained from supercritical fluid extracts. J Appl Phycol 30:591–603

  45. Mihranyan A (2011) Cellulose from Cladophorales green algae: from environmental problem to high-tech composite materials. J Appl Polym Sci 119:2449–2460

  46. Murugaiyan K, Narasimman S (2013) Biochemical and mineral contents of selected green seaweeds from Gulf of Mannar Coastal region, TamilNadu, India. Int J Plant Sci 3:96–100

  47. Neifar M, Chatter R, Chouchane H, Genouiz R, Jaouani A, Masmoudi AS, Cherif A (2016) Optimization of enzymatic saccharification of Chaetomorpha linum biomass for the production of macroalgae-based third generation bioethanol. AIMS Bioeng 3:400–411

  48. Nicolai E, Preston RD (1952) Cell-wall studies in the Chlorophyceae. I. A general survey of submicroscopic structure in filamentous species. Proc Roy Soc Lond B 140:245–274

  49. Ogawa K, Yui T, Mizuno T (1991) X-ray diffraction study of glucomanns and their acetates. Agric Biol Chem 55:21052111

  50. Oksman K, Aitomäki Y, Mathew AP, Siqueira G, Zhou Q, Butylina S, Tanpichai S, Zhou X, Hooshmand S (2016) Review of the recent developments in cellulose nanocomposite processing. Composites Part A 83:2–18

  51. Parekh RG, Chauhan V (1987) Lipid content of some Indian seaweeds. Indian J Mar Sci 16:272–273

  52. Patarra RF, Leite J, Pereira R, Baptista J, Neto AI (2013) Fatty acid composition of selected macrophytes. Nat Prod Res 27:665–669

  53. Patel S (2012) Therapeutic importance of sulfated polysaccharides from seaweeds: updating the recent findings. 3 Biotech 2:171–185

  54. Pereira H, Barreira L, Figueiredo F, Custódio L, Vizetto-Duarte C, Polo C, Rešek E, Engelen A, Varela J (2012) Polyunsaturated fatty acids of marine macroalgae: potential for nutritional and pharmaceutical applications. Mar Drugs 10:1920–1935

  55. Pierre G, Sopena V, Juin C, Mastouri A, Graber M, Maugard T (2011) Antibacterial activity of a sulfated galactan extracted from the marine alga Chaetomorpha aerea against Staphylococcus aureus. Biotechnol Bioprocess Eng 16:937–945

  56. Poletto M, Pistor V, Zeni M, Zattera AJ (2011) Crystalline properties and decomposition kinetics of cellulose fibers in wood pulp obtained by two pulping processes. Polym Degrad Stab 96:679–685

  57. Poletto M, Zattera AJ, Forte AMC, Santana RMC (2012) Thermal decomposition of wood: influence of wood components and cellulose crystallite size. Bioresour Technol 109:148–153

  58. Qi H, Sun Y (2015) Antioxidant activity of high sulfate content derivative of ulvan in hyperlipidemic rats. Int J Biol Macromol 76:326–329

  59. Qi H, Zhang Q, Zhao T, Chen R, Zhang H, Niu X, Li Z (2005) Antioxidant activity of different sulfate content derivatives of polysaccharide extracted from Ulva pertusa (Chlorophyta) in vitro. Int J Biol Macromol 4:15–37

  60. Ramos MJ, Fernández CM, Casas A, Rodríguez L, Pérez Á (2009) Influence of fatty acid composition of raw materials on biodiesel properties. Bioresour Technol 100:261–268

  61. Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C (1999) Antioxidant activity applying an improved ABT radical cation decolorization assay. Free Radic Biol Med 26:1231–1237

  62. Romera E, González F, Ballester A, Blázquez ML, Muñoz JA (2006) Biosorption with algae: a statistical review. Crit Rev Biotechnol 26:223–235

  63. Rosaline XD, Sakthivelkumar S, Chitra S, Janarthanan S (2017) Antibacterial activity of the seaweeds Chaetomorpha linum and Padina gymnospora on human bacterial pathogens. J Environ Biotechnol Res 6:43–52

  64. Sánchez-Borroto Y, Lapuerta M, Melo-Espinosa EA, Bolonio D, Tobío-Perez I, Piloto-Rodríguez R (2018) Green-filamentous macroalgae Chaetomorpha cf. gracilis from Cuban wetlands as a feedstock to produce alternative fuel: a physicochemical characterization. Energ Source Part A 40:1279–1289

  65. Segal L, Creely JJ, Martin AE Jr, Conrad CM (1959) An empirical method for estimating the degree of crystallinity of native cellulose using X-ray diffractometer. Tex Res J 29:786–794

  66. Shameel M, Khan R (1991) Fatty acid composition of nine green seaweeds. Bot Mar 34:501–504

  67. Shao P, Chen XX, Sun PL (2013) In vitro antioxidant and antitumor activities of different sulfated polysaccharides isolated from three algae. Int J Biol Macromol 62:155–161

  68. Sharmila S, Jeyanthi Rebecca L, Das MP (2012) Production of biodiesel from Chaetomorpha antennina and Gracilaria corticata. J Chem Pharm Res 4:4870–4874

  69. Siddhanta AK, Prasad K, Meena R, Prasad G, Mehta GK, Chhatbar MU, Oza MD, Kumar S, Sanandiya N (2009) Profiling of cellulose content in Indian seaweed species. Bioresour Technol 100:6669–6673

  70. Siddhanta AK, Mahesh U, Chhatbar MU, Mehta GK, Sanandiya ND, Kumar S, Oza MD, Prasad K, Meena R (2011) The cellulose content in Indian seaweed species. J Appl Phycol 23:919–923

  71. Torres MD, Kraan S, Domínguez H (2019) Seaweed biorefinery. Rev Environ Sci Biotechnol 18:335–388

  72. Trivedi N, Baghel RS, Bothwell J, Gupta V, Reddy CRK, Lali AM, Jha B (2016) An integrated process for the extraction of fuel and chemicals from marine macroalgal biomass. Sci Rep 6:30728

  73. Tsutsui I, Kanjanaworakul P, Srisapoome P, Aue-umneoy D, Hamano K (2010) Growth of giant tiger prawn, Penaeus monodon Fabricius, under co-culture with a discarded filamentous seaweed, Chaetomorpha ligustica (Kützing) Kützing, at an aquarium-scale. Aquacult Int 18:545–553

  74. Tsutsui I, Miyoshi T, Aue-umneoy D, Songphatkaew J, Meeanan C, Klomkling S, Sukchai H, Pinphoo P, Yamaguchi I, Ganmanee M, Maeno Y, Hamano K (2015) High tolerance of Chaetomorpha sp. to salinity and water temperature enables survival and growth in stagnant waters of central Thailand. Int Aquat Res 7:47–62

  75. van Ginneken VJT, Helsper JPFG, de Visser W, van Keulen H, Brandenburg WA (2011) Polyunsaturated fatty acids in various macroalgal species from North Atlantic and tropical seas. Lipids Health Dis 10:104

  76. Vázquez-Delfín E, Robledo D, Freile-Pelegrín Y (2014) Microwave-assisted extraction of the carrageenan from Hypnea musciformis (Cystocloniaceae, Rhodophyta). J Appl Phycol 26:901–907

  77. Venkata Rao E, Sri Ramana K (1991) Structural studies of a polysaccharide isolated from the green seaweed Chaetomorpha anteninna. Carbohydr Res 217:163–170

  78. Vincekovic M, Pustak A, Tusek-Bozic L, Liu F, Ungar G, Bujan M, Smit I, Filipovic-Vincekovic N (2010) Structural and thermal study of mesomorphic dodecylammonium carrageenates. J Colloid Interf Sci 341:117–123

  79. Wada M, Okano T (2001) Localization of Iα and Iβ phases in algal cellulose revealed by acid treatments. Cellulose 8:183–188

  80. Wang X, Zhang Z, Yao Q, Zhao M, Qi H (2013) Phosphorylation of low-molecular-weight polysaccharide from Enteromorpha linza with antioxidant activity. Carbohydr Polym 96:371–375

  81. Whistler RL (1963) Methods in carbohydrate chemistry, vol 3. Cellulose. Academic Press, New York

  82. Yahmed NB, Jmel MA, Alaya MB, Bouallagui H, Marzouki MN, Smaali I (2016) A biorefinery concept using the green macroalgae Chaetomorpha linum for the coproduction of bioethanol and biogas. Energ Convers Manage 119:257–265

  83. Ye SH, Liu F, Wang JH, Wang H, Zhang MP (2012) Antioxidant activities of an exopolysaccharide isolated and purified from marine Pseudomonas PF-6. Carbohydr Polym 87:764–770

Download references

Funding

The authors received financial support from the National Council for Science and Technology (CONACYT) for the PN-CONACYT 2015-01-118 project.

Author information

Correspondence to Yolanda Freile-Pelegrín.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Freile-Pelegrín, Y., Chávez-Quintal, C., Caamal-Fuentes, E. et al. Valorization of the filamentous seaweed Chaetomorpha gracilis (Cladophoraceae, Chlorophyta) from an IMTA system. J Appl Phycol (2020). https://doi.org/10.1007/s10811-020-02066-8

Download citation

Keywords

  • Chaetomorpha gracilis
  • Chlorophyceae
  • Fatty acids
  • Sulfated polysaccharides
  • Cellulose