Journal of Applied Phycology

, Volume 31, Issue 5, pp 3163–3173 | Cite as

Brazilian native species of Gracilaria (Gracilariales, Rhodophyta) as a source of valuable compounds and as nutritional supplements

  • Priscila TorresEmail author
  • Alice Nagai
  • Dárlio Inácio Alves Teixeira
  • Eliane Marinho-Soriano
  • Fungyi Chow
  • Deborah Y. A. C. dos Santos


In Brazil species of Gracilaria play a social and economic role in some poor communities of the northeastern coast. Considering that these algae are typically consumed after depigmentation and drying, little is known about the chemical composition and nutritional value after processing. In the present study dried and depigmented samples of Gracilaria birdiae (GB), Gracilaria caudata (GC), Gracilaria domingensis (GD), and a commercially available sample of G. birdiae (C-GB), provided by a local community, were studied as a source of valuable compounds and as nutritional supplements. In nutritional terms, the dietary fiber and mineral contents of the studied algae were higher than those of the traditional foods in the standard Brazilian diet. The results suggest that these algae have functional properties and consequently may be used as a source of nutraceutical. GB and GC showed a high antioxidant potential, similar to that of some staple foods (e.g., cereals and legumes), but lower than that of rich-antioxidant foods (e.g., berries and nuts). The polysaccharides from both G. birdiae samples (GB and C-GB) showed a low sulfation degree and higher yields, suggesting that they are a good source of agar. GB was also rich in mycosporine-like amino acids (MAAs), mainly porphyra-334. In contrast, C-GB contained the lowest values of MAAs and antioxidants. The reduction in these compounds may compromise the use of C-GB for other purposes such as cosmetic production. However, the sample of C-GB showed the highest potential as a source of dietary fiber and agar. In general, the analyzed species are alternatives to traditional foods and a source of valuable compounds.


Antioxidant Gracilaria Mycosporine-like amino acids Proximate composition Polysaccharides 


Funding information

The authors thank CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) (140073/2013-2) and FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo) (2013/07543-0 and 2013/50731-1) for financial support. FC thanks CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) for the productivity fellowship (303937/2015-7).

Supplementary material

10811_2019_1804_MOESM1_ESM.docx (39 kb)
ESM 1 (DOCX 39 kb)


  1. Anderson JW, Baird P, Davis RH, Ferreri S, Knudtson M, Koraym A, Waters V, Williams CL (2009) Health benefits of dietary fiber. Nutr Rev 67:188–205CrossRefPubMedGoogle Scholar
  2. Armisen R (1997) Agar. In: Imeson AP (ed) Thickening and gelling agents for food, 2nd edn. Springer, Boston, pp 1–21Google Scholar
  3. Armisen R, Galatas F (1987) Production, properties and uses of agar. In: McHugh DJ (ed) Production and utilization of products from commercial seaweeds, FAO Fisheries Technical Paper, vol 288, pp 1–57Google Scholar
  4. Baghel RS, Kumari P, Reddy CRK, Jha B (2014) Growth, pigments, and biochemical composition of marine red alga Gracilaria crassa. J Appl Phycol 26:2143–2150Google Scholar
  5. Barros FCN, Silva DC, Sombra VG, Maciel JS, Feitosa JPA, Freitas ALP, Paula RCM (2013) Structural characterization of polysaccharide obtained from red seaweed Gracilaria caudata (J Agardh). Carbohydr Polym 92:598–603CrossRefPubMedGoogle Scholar
  6. Becker K, Hartmann A, Ganzera M, Fuchs D, Gostner JM (2016) Immunomodulatory effects of the mycosporine-like amino acids shinorine and porphyra-334. Mar Drugs 14:1–12CrossRefGoogle Scholar
  7. Benjama O, Masniyom P (2012) Biochemical composition and physicochemical properties of two red seaweeds (Gracilaria fisheri and G. tenuistipitata) from the Pattani Bay in Southern Thailand. Songklanakarin J Sci Technol 34:223–230Google Scholar
  8. Benzie IFF, Strain JJ (1996) The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem 239:70–76CrossRefPubMedGoogle Scholar
  9. Briani B, Sissini MN, Lucena LA, Batista MB, Costa IO, Nunes JMC, Schmitz C, Ramlov F, Maraschin M, Korbee N, Rörig L, Horta PA, Figueroa FL, Barufi JB (2018) The influence of environmental features in the content of mycosporine-like amino acids in red marine algae along the Brazilian coast. J Phycol 54:380–390Google Scholar
  10. Cardozo KHM, Marques LG, Carvalho VM, Carignan MO, Pinto E, Marinho-Soriano E, Colepicolo P (2011) Analyses of photoprotective compounds in red algae from the Brazilian coast. Braz J Pharmacogn 21:202–208CrossRefGoogle Scholar
  11. Carlsen MH, Halvorsen BL, Holte K, Bøhn SK, Dragland S, Sampson L, Willey C, Senoo H, Umezono Y, Sanada C, Barikmo I, Berhe N, Willett WC, Phillips KM, Jacobs DR Jr, Blomhoff R (2010) The total antioxidant content of more than 3100 foods, beverages, spices, herbs and supplements used worldwide. Nutr J 9:3CrossRefPubMedPubMedCentralGoogle Scholar
  12. Chan PT, Matanjun P (2017) Chemical composition and physicochemical properties of tropical red seaweed, Gracilaria changii. Food Chem 221:302–310CrossRefPubMedGoogle Scholar
  13. Coura CO, de Araújo IWF, Vanderlei ESO, Rodrigues JA, Quinderé AL, Fontes BP, de Queiroz IN, de Menezes DB, Bezerra MM, e Silva AA, Chaves HV, Jorge RJ, Evangelista JS, Benevides NM (2012) Antinociceptive and anti-inflammatory activities of sulphated polysaccharides from the red seaweed Gracilaria cornea. Basic Clin Pharmacol Toxicol 110:335–341CrossRefPubMedGoogle Scholar
  14. De la Coba F, Aguilera J, de Gálvez MV, Alvarez M, Gallego E, Figueroa FL, Herrera E (2009) Prevention of the ultraviolet effects on clinical and histopathological changes, as well as the heat shock protein-70 expression in mouse skin by topical application of algal UV-absorbing compounds. J Dermatol Sci 55:161–169CrossRefPubMedGoogle Scholar
  15. Debbarma J, Rao BM, Murthy LN, Mathew S, Venkateshwarlu G, Ravishankar CN (2016) Nutritional profiling of the edible seaweeds Gracilaria edulis, Ulva lactuca and Sargassum sp. Indian J Fish 63:81–87CrossRefGoogle Scholar
  16. FAO – Food and Agriculture Organization of the United Nations (2016) The state of world fisheries and aquaculture 2016: contributing to food security and nutrition for all. Rome. 200 ppGoogle Scholar
  17. FAO – Food and Agriculture Organization of the United Nations (2018) FAO yearbook. Fishery and aquaculture statistics 2016. Accessed 07 May 2018
  18. Fernandes SC, Alonso-Varona A, Palomares T, Zubillaga V, Labidi J, Bulone V (2015) Exploiting mycosporines as natural molecular sunscreens for the fabrication of UV-absorbing green materials. ACS Appl Mater Interfaces 7:16558–16564CrossRefPubMedGoogle Scholar
  19. Firuzi O, Miri R, Tavakkoli M, Saso L (2011) Antioxidant therapy: current status and future prospects. Curr Med Chem 18:3871–3888CrossRefPubMedGoogle Scholar
  20. Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226:497–507PubMedGoogle Scholar
  21. Gillespie KM, Chae JM, Ainsworth EA (2007) Rapid measurement of total antioxidant capacity in plants. Nat Protoc 2:867–870CrossRefPubMedGoogle Scholar
  22. Guimarães M, Viana AG, Duarte MER, Ascêncio SD, Plastino EM, Noseda MD (2007) Low-molecular-mass carbohydrates and soluble polysaccharides of green and red morphs of Gracilaria domingensis (Gracilariales, Rhodophyta). Bot Mar 50:314–317CrossRefGoogle Scholar
  23. Harb TB, Torres PB, Pires JS, Santos DYAC, Chow F (2016) Ensaio em microplaca do potencial antioxidante através do sistema quelante de metais para extratos de algas. Instituto de Biociências, Universidade de São Paulo, São Paulo. Accessed 06 May 2018
  24. Hartmann A, Becker K, Karsten U, Remias D, Ganzera M (2015a) Analysis of mycosporine-like amino acids in selected algae and cyanobacteria by hydrophilic interaction liquid chromatography and a novel MAA from the red alga Catenella repens. Mar Drugs 13:6291–6305CrossRefPubMedPubMedCentralGoogle Scholar
  25. Hartmann A, Gostner J, Fuchs JE, Chaita E, Aligiannis N, Skaltsounis L, Ganzera M (2015b) Inhibition of collagenase by mycosporine-like amino acids from marine sources. Planta Med 81:813–820CrossRefPubMedPubMedCentralGoogle Scholar
  26. Haytowitz D, Bhagwat S (2010) USDA database for the oxygen radical absorbance capacity (ORAC) of selected foods, release 2. US Department of Agriculture, Beltsville, 48 ppGoogle Scholar
  27. Huang D, Ou B, Prior RL (2005) The chemistry behind antioxidant capacity assays. J Agric Food Chem 53:1841–1856CrossRefPubMedGoogle Scholar
  28. Kailas AP, Nair SM (2015) Comparison of nutrient compositions and calorific values of eight tropical seaweeds. Phykos 45:62–74Google Scholar
  29. Lawrence KP, Long PF, Young AR (2018) Mycosporine-like amino acids for skin photoprotection. Curr Med Chem 25:5512–5527CrossRefPubMedPubMedCentralGoogle Scholar
  30. Maciel JS, Chaves LS, Souza BWS, Teixeira DIA, Freitas ALP, Feitosa JPA, Paula RCM (2008) Structural characterization of cold extracted fraction of soluble sulfated polysaccharide from red seaweed Gracilaria birdiae. Carbohydr Polym 71:559–565CrossRefGoogle Scholar
  31. Marinho-Soriano E (2017) Historical context of commercial exploitation of seaweeds in Brazil. J Appl Phycol 29:665–671CrossRefGoogle Scholar
  32. Mazumder S, Ghosal PK, Pujol CA, Carlucci MJ, Damonte EB, Ray B (2002) Isolation, chemical investigation and antiviral activity of polysaccharides from Gracilaria corticata (Gracilariaceae, Rhodophyta). Int J Biol Macromol 31:87–95CrossRefPubMedGoogle Scholar
  33. McDermid KJ, Stuercke B (2003) Nutritional composition of edible Hawaiian seaweeds. J Appl Phycol 15:513–524CrossRefGoogle Scholar
  34. Mehta GK, Meena R, Prasad K, Ganesan M, Siddhanta AK (2010) Preparation of galactans from Gracilaria debilis and Gracilaria salicornia (Gracilariales, Rhodophyta) of Indian waters. J Appl Phycol 22:623–627CrossRefGoogle Scholar
  35. Melo MRS, Feitosa JPA, Freitas ALP, De Paula RCM (2002) Isolation and characterization of soluble sulfated polysaccharide from the red seaweed Gracilaria cornea. Carbohydr Polym 49:491–498CrossRefGoogle Scholar
  36. MEXT - Ministry of Education, Culture, Sports, Science and Technology (2015) The standard tables of food composition in Japan (Seventh Revised Edition). Accessed 07 may 2017
  37. Min B, McClung AM, Chen M-H (2011) Phytochemicals and antioxidant capacities in rice brans of different color. J Food Sci 76:C117–C126CrossRefPubMedGoogle Scholar
  38. Navarro NP (2015) Sunscreens of red algae from Patagonia: a biotechnological perspective. Pure Appl Chem 87:953–960CrossRefGoogle Scholar
  39. NEPA - Núcleo de Estudos e Pesquisas em Alimentação (2011) Tabela brasileira de composição de alimentos - TACO, 4th ed. Nepa-Unicamp, Campinas. Accessed 07 may 2017
  40. Pellegrini N, Serafini M, Salvatore S, Del Rio D, Bianchi M, Brighenti F (2006) Total antioxidant capacity of spices, dried fruits, nuts, pulses, cereals and sweets consumed in Italy assessed by three different in vitro assays. Mol Nutr Food Res 50:1030–1038CrossRefPubMedGoogle Scholar
  41. Pires JS, Torres PB, Santos DYAC, Chow F (2017) Ensaio em microplaca de substâncias redutoras pelo método do Folin-Ciocalteu para extratos de algas. Instituto de Biociências, Universidade de São Paulo, São Paulo. raw&Itemid=98. Accessed 06 May 2018
  42. Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med 26:1231–1237CrossRefPubMedGoogle Scholar
  43. Rioux LE, Beaulieu L, Turgeon SL (2017) Seaweeds: a traditional ingredients for new gastronomic sensation. Food Hydrocoll 68:255–265CrossRefGoogle Scholar
  44. Robledo D, Freile-Pelegrin Y (1997) Chemical and mineral composition of six potentially edible seaweed species of Yucatán. Bot Mar 40:301–306CrossRefGoogle Scholar
  45. Ryu J, Park SJ, Kim IH, Choi YH, Nam TJ (2014) Protective effect of porphyra-334 on UVA-induced photoaging in human skin fibroblasts. Int J Mol Med 34:796–803CrossRefPubMedPubMedCentralGoogle Scholar
  46. Sardinha AN, Canella DS, Martins AP, Claro RM, Levy RB (2014) Dietary sources of fiber intake in Brazil. Appetite 79:134–138CrossRefPubMedGoogle Scholar
  47. Seedevi P, Moovendhan M, Viramani S, Shanmugam A (2017) Bioactive potential and structural chracterization of sulfated polysaccharide from seaweed (Gracilaria corticata). Carbohydr Polym 155:516–524CrossRefPubMedGoogle Scholar
  48. Seeram NP, Aviram M, Zhang Y, Henning SM, Feng L, Dreher M, Heber D (2008) Comparison of antioxidant potency of commonly consumed polyphenol-rich beverages in the United States comparison of antioxidant potency of commonly consumed polyphenol-rich beverages in the United States. J Agric Food Chem 56:1415–1422CrossRefPubMedGoogle Scholar
  49. Setthamongkol P, Tunkijjanukij S, Satapornvanit K, Salaenoi J (2015) Growth and nutrients analysis in marine macroalgae. Kasetsart J Nat Sci 49:211–218Google Scholar
  50. 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
  51. Sudharsan S, Subhapradha N, Seedevi P, Shanmugam V, Madeswaran P, Shanmugam A, Srinivasan A (2015) Antioxidant and anticoagulant activity of sulfated polysaccharide from Gracilaria debilis (Forsskal). Int J Biol Macromol 81:1031–1038CrossRefPubMedGoogle Scholar
  52. Torres A, Hochberg M, Pergament I, Smoum R, Niddam V, Dembitsky VM, Temina M, Dor I, Lev O, Srebnik M, Enk CD (2004) A new UV-B absorbing mycosporine with photo protective activity from the lichenized ascomycete Collema cristatum. Eur J Biochem 271:780–784CrossRefPubMedGoogle Scholar
  53. Torres PB, Pires JS, Santos DYAC, Chow F (2017) Ensaio do potencial antioxidante de extratos de algas através do sequestro do ABTS•+ em microplaca. Instituto de Biociências, Universidade de São Paulo, São Paulo. component&format=raw&Itemid=98. Accessed 06 May 2018
  54. Torres P, Novaes P, Ferreira LG, Santos JP, Mazepa E, Duarte MER, Noseda MD, Chow F, Santos DYAC (2018a) Effects of extracts and isolated molecules of two species of Gracilaria (Gracilariales, Rhodophyta) on early growth of lettuce. Algal Res 32:142–149CrossRefGoogle Scholar
  55. Torres P, Pires J, Chow F, Pena MJ, Santos DYAC (2018b) Comparative analysis of in vitro antioxidant capacities of mycosporine-like amino acids (MAAs). Algal Res 34:57–67CrossRefGoogle Scholar
  56. Torres P, Pires J, Chow F, Santos DYAC (2019) A comprehensive review of traditional uses, bioactivity potential, and chemical diversity of the genus Gracilaria (Gracilariales, Rhodophyta). Algal Res 37:288–306CrossRefGoogle Scholar
  57. Urrea-Victoria V, Pires J, Torres PB, Santos DYAC, Chow F (2016) Ensaio antioxidante em microplaca do poder de redução do ferro (FRAP) para extratos de algas. Instituto de Biociências, Universidade de São Paulo, São Paulo. Accessed 06 May 2018
  58. Wada N, Sakamoto T, Matsugo S (2015) Mycosporine-like amino acids and their derivatives as natural antioxidants. Antioxidants 4:603–646CrossRefPubMedPubMedCentralGoogle Scholar
  59. Waterman PG, Mole S (1994) Analysis of phenolic plant metabolites. Wiley-Blackwell. 248 ppGoogle Scholar
  60. Wells ML, Potin P, Craigie JS, Raven JA, Merchant SS, Helliwell KE, Smith AG, Camire ME, Brawley SH (2017) Algae as nutritional and functional food sources: revisiting our understanding. J Appl Phycol 29:949–982CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Botany, Institute of BiosciencesUniversity of São PauloSão PauloBrazil
  2. 2.Agricultural School of JundiaíFederal University of Rio Grande do NorteMacaíbaBrazil
  3. 3.Department of Oceanography and LimnologyFederal University of Rio Grande do NorteNatalBrazil

Personalised recommendations