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Effects of drying processes on antioxidant properties and chemical constituents of four tropical macroalgae suitable as functional bioproducts

Abstract

Seaweeds are a source of antioxidants and pigments, which can be used as functional ingredients for food, cosmetic, pharmaceutical, and industrial applications. As fresh seaweed has a large amount of water, it usually goes through a drying process in order to be commercialized, which facilitates transportation and storage and also increases shelf time. However, the drying procedures can change the chemical composition and antioxidant properties of seaweeds. Thus, the aim of this study was to evaluate the antioxidant properties and pigment and protein content of four Brazilian macroalgae (Gracilariopsis tenuifrons, Pterocladiella capillacea, Sargassum stenophyllum, and Ulva fasciata) suitable for use as functional bioproducts after processing with three different drying procedures (freeze-drying, oven-drying and silica-drying), using a fresh frozen treatment as control. Among the studied species, S. stenophyllum presented the highest antioxidant activity. For this species, freeze-drying was the procedure with the highest activity in the Folin-Ciocalteu and metal chelating assays, while for the ABTS, DPPH, and FRAP assays, no significant differences were observed between freeze-drying and silica-drying. Freeze-drying also showed low reduction of photosynthetic pigments in G. tenuifrons, P. capillacea, and U. fasciata and was the method that best-preserved protein content in the four species. In general, the antioxidant potential and pigment and protein content for the studied algae decreased in the following order: fresh frozen (control) > freeze-dried > silica-dried > oven-dried. Freeze-drying was the procedure that presented the lowest alteration in functional properties, as the low temperature prevents the degradation of heat-sensitive compounds. In addition, freeze-drying is a vacuum process and the absence of oxygen prevents oxidation reactions of functional ingredients.

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References

  1. Badmus UO, Taggart MA, Boyd KG (2019) The effect of different drying methods on certain nutritionally important chemical constituents in edible brown seaweeds. J Appl Phycol 31:3883–3897

  2. Barsanti L, Gualtieri P (2014) Algae: anatomy, biochemistry, and biotechnology. CRC Press, Boca Raton, pp 267–308

  3. Beer S, Eshel A (1985) Determining phycoerythrin and phycocyanin concentrations in aqueous crude extracts of red algae. Mar Freshw Res 36:785–792

  4. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

  5. Brito LL, Silva S (2005) Fenología y ciclo de vida del alga Gracilariopsis tenuifrons (Gracilariaceae) en Sucre, Venezuela. J Trop Biol 53:67–73

  6. Cardoso SM, Carvalho LG, Silva PJ, Rodrigues MS, Pereira OR, Pereira L (2014) Bioproducts from seaweeds: a review with special focus on the Iberian Peninsula. Curr Org Chem 18:896–917

  7. Chen Z, Bertin R, Froldi G (2013) EC50 estimation of antioxidant activity in DPPH assay using several statistical programs. Food Chemistry 138:414–420

  8. Chenlo F, Arufe S, Díaz D, Torres MD, Sineiro J, Moreira R (2018) Air-drying and rehydration characteristics of the brown seaweeds, Ascophylum nodosum and Undaria pinnatifida. J Appl Phycol 30:1259–1270

  9. Costa ES, Plastino EM, Petti R, Oliveira EC, Mariana MC (2012) The Gracilariaceae Germplasm bank of the University of São Paulo, Brazil - a DNA barcoding approach. J Appl Phycol 24:1643–1653

  10. Cruces E, Rojas-Lillo Y, Ramirez-Kushel E, Atala E, López-Alarcón C, Lissi E, Gómez I (2016) Comparison of different techniques for the preservation and extraction of phlorotannins in the kelp Lessonia spicata (Phaeophyceae): assays of DPPH, ORAC-PGR, and ORAC-FL as testing methods. J Appl Phycol 28:573–580

  11. Edwards P (1970) Illustrated guide to the seaweeds and sea grasses in the vicinity of Port Aransas. University of Texas Marine Science Institute, Port Aransas

  12. Fernando IPS, Kim M, Son KT, Jeong Y, Jeon YJ (2016) Antioxidant activity of marine algal polyphenolic compounds: a mechanistic approach. J Med Food 19:1–14

  13. Fleurence J (2016) Seaweeds as food. In: Fleurence J, Levine I (eds) Seaweed in health and disease prevention. Elsevier, Amsterdam, pp 149–167

  14. Frankel EN, Meyer AS (2000) The problems of using one-dimensional methods to evaluate multifunctional food and biological antioxidants. J Sci Food Ag 80:1925–1941

  15. Gordon MH (1990) The mechanism of antioxidant action in vitro. In: Hudson BJF (ed) Food antioxidants. Springer, Dordrecht pp 1-18

  16. Gupta S, Cox S, Abu-Ghannam N (2011) Effect of different drying temperatures on the moisture and phytochemical constituents of edible Irish brown seaweed. LWT Food Sci Technol 44:1266–1272

  17. 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. Universidade de São Paulo, Instituto de Biociências

  18. Harb TB, Nardelli A, Chow F (2018) Physiological responses of Pterocladiella capillacea (Rhodophyta, Gelidiales) under two light intensities. Photosynthetica 56:1093–1106

  19. Holdt SL, Kraan S (2011) Bioactive compounds in seaweed: functional food applications and legislation. J Appl Phycol 23:543–597

  20. Huang D, Ou B, Prior RL (2005) The chemistry behind antioxidant capacity assays. J Agric Food Chem 53:1841–1856

  21. Humphrey A (2004) Chlorophyll as a color and functional ingredient. J Food Sci 69:C422–C425

  22. Jairaj KS, Singh SP, Srikant K (2009) A review of solar dryers developed for grape drying. Sol Energy 83:1698–1712

  23. Jiménez-Escrig A, Jiménez-Jiménez I, Pulido R, Saura-Calixto F (2001) Antioxidant activity of fresh and processed edible seaweeds. J Sci Food Agric 81:530–534

  24. Kruger CL, Mann SW (2003) Safety evaluation of functional ingredients. Food Chem Toxicol 41:793–805

  25. Kursar TA, Van der Meer J, Alberte RS (1983) Light-harvesting system of the red alga Gracilaria tikvahiae. Plant Physiol 73:361–369

  26. Le Lann K, Jégou C, Stiger-Pouvreau V (2008) Effect of different conditioning treatments on total phenolic content and antioxidant activities in two Sargassacean species: comparison of the frondose Sargassum muticum (Yendo) Fensholt and the cylindrical Bifurcaria bifurcata R. Ross. Phycol Res 56:238–245

  27. Li B, Smith B, Hossain M (2006) Extraction of phenolics from citrus peels: I. solvent extraction method. Sep Purif Technol 48:182–188

  28. Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV-VIS. Curr Protocols Food Analyt Chem 1:F4.3.1–F4.3.8

  29. Lim YY, Murtijaya J (2007) Antioxidant properties of Phyllanthus amarus extracts as affected by different drying methods. LWT Food Sci Technol 40:1664–1669

  30. Ling ALM, Yasir S, Matanjun P, Abu Bakar MF (2015) Effect of different drying techniques on the phytochemical content and antioxidant activity of Kappaphycus alvarezii. J Appl Phycol 27:1717–1723

  31. Mahanom H, Azizah A, Dzulkifly M (1999) Effect of different drying methods on concentrations of several phytochemicals in herbal preparation of 8 medicinal plants leaves. Malays J Nutr 5:47–54

  32. Maillard MN, Berset C (1995) Evolution of antioxidant activity during kilning: role of insoluble bound phenolic acids of barley and malt. J Agric Food Chem 43:1789–1793

  33. Martín-Cabrejas MA, Aguilera Y, Pedrosa M, Cuadrado C, Hernández T, Díaz S, Esteban RM (2009) The impact of dehydration process on antinutrients and protein digestibility of some legume flours. Food Chem 114:1063–1068

  34. McDermid KJ, Stuercke B (2003) Nutritional composition of edible Hawaiian seaweeds. J Appl Phycol 15:513–524

  35. Moreira R, Chenlo F, Sineiro J, Arufe S, Sexto S (2016) Drying temperature effect on powder physical properties and aqueous extract characteristics of Fucus vesiculosus. J Appl Phycol 28:2485–2494

  36. Mudau FN, Ngezimana W (2014) Effect of different drying methods on chemical composition and antimicrobial activity of bush tea (Athrixia phylicoides). Int J Agric Biol 16:1560–8530

  37. Murgatroyd K (1997) The freeze drying process. In: Cameron P (ed.) Good Pharmaceutical Freeze-Drying Practice. Interpharm Press, pp. 1–57

  38. Pangestuti R, Kim SK (2011) Biological activities and health benefit effects of natural pigments derived from marine algae. J Funct Foods 3:255–266

  39. Pires J, Torres PB, Santos DYAC, Chow F (2017a) Ensaio em microplaca do potencial antioxidante através do método de sequestro do radical livre DPPH para extratos de algas. Instituto de Biociências, Universidade de São Paulo, São Paulo

  40. Pires J, Torres PB, Santos DYAC, Chow F (2017b) Ensaio em microplaca de substâncias redutoras pelo método do Folin-Ciocalteu para extratos de algas. Instituto de Biociências, Universidade de São Paulo, São Paulo.

  41. Rioux LE, Beaulieu L, Turgeon SL (2017) Seaweeds: a traditional ingredient for new gastronomic sensation. Food Hydrocoll 68:255–265

  42. Ritchie RJ (2008) Universal chlorophyll equations for estimating chlorophylls a, b, c, and d and total chlorophylls in natural assemblages of photosynthetic organisms using acetone, methanol, or ethanol solvents. Photosynthetica 46:115–126

  43. Rubinskienė M, Viškelis P, Dambrauskienė E, Viškelis J, Karklelienė R (2015) Effect of drying methods on the chemical composition and colour of peppermint (Mentha × piperita L .) leaves. Zemdirbyste-Agriculture 102:223–228

  44. Santos JP, Torres PB, Santos DYAC, Motta LB, Chow F, (2019) Seasonal effects on antioxidant and anti-HIV activities of Brazilian seaweeds. J Appl Phycol 31:1333–1341

  45. Sappati PK, Nayak B, VanWalsum PV, Mulrey OT (2019) Combined effects of seasonal variation and drying methods on the physicochemical properties and antioxidant activity of sugar kelp (Saccharina latissima). J Appl Phycol 31:1311–1332

  46. Silva AFR, Abreu H, Silva MAS, Cardoso SM (2019) Effect of oven-drying on the recovery of valuable compounds from Ulva rigida, Gracilaria sp. and Fucus vesiculosus. Mar Drugs 17:90

  47. Stafford GI, Jäger AK, Van Staden J (2005) Effect of storage on the chemical composition and biological activity of several popular South African medicinal plants. J Ethnopharmacol 97:107–115

  48. Stévant P, Indergård E, Ólafsdóttir A, Marfaing H, Larssen WE, Fleurence J, Roleda MY, Rustad T, Slizyte R, Nordtvedt TS (2018) Effects of drying on the nutrient content and physicochemical and sensory characteristics of the edible kelp Saccharina latissima. J Appl Phycol 30:2587–2599

  49. 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 44:2112–2118

  50. 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

  51. Uribe E, Vega-Gálvez A, García V, Pastén A, López J, Goñi G (2019) Effect of different drying methods on phytochemical content and amino acid and fatty acid profiles of the green seaweed, Ulva spp. J Appl Phycol 31:1967–1979

  52. 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

  53. Ursi S, Plastino EM (2001) Crescimento in vitro de linhagens de coloração vermelha e verde clara de Gracilaria birdiae (Gracilariales, Rhodophyta) em dois meios de cultura: análise de diferentes estádios reprodutivos. Braz J Bot 24:587–594

  54. 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 29:949–982

  55. Zubia M, Robledo D, Freile-Pelegrin Y (2007) Antioxidant activities in tropical marine macroalgae from the Yucatan peninsula, Mexico. J Appl Phycol 19:449–458

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Acknowledgments

We are thankful to Rosário Petti and Willian Oliveira for technical support.

Funding

Financial support was provided by FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo) (15/02008-4; BIOTA/FAPESP 13/50731-1).

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Correspondence to Fungyi Chow.

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Amorim, A.M., Nardelli, A.E. & Chow, F. Effects of drying processes on antioxidant properties and chemical constituents of four tropical macroalgae suitable as functional bioproducts. J Appl Phycol (2020). https://doi.org/10.1007/s10811-020-02059-7

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Keywords

  • Antioxidant
  • Drying process
  • Functional ingredient
  • Pigments
  • Rhodophyceae
  • Phaeophyceae
  • Chlorophyceae