Nutritional value of the kelps Alaria esculenta and Saccharina latissima and effects of short-term storage on biomass quality

Abstract

Storage of macroalgae in seawater, prior to further processing, is a standard initial pre-treatment step after harvest to avoid rapid degradation of the biomass. In the context of using seaweeds in human food and animal feed products, such practice may affect the nutritional value and the overall quality of the biomass. The effects of seawater storage on the chemical composition (i.e., mineral fraction, carbohydrates, proteins, polyphenols, and fucoxanthin) and surface color of two cultivated kelps (Phaeophyceae), Alaria esculenta and Saccharina latissima, were investigated over a 22-h period. Storage treatments resulted in a rapid decrease in dry weight during the first 2 h (−21.4 and −20.4% in A. esculenta and S. latissima, respectively) with subsequent stabilization. Although it is not clear whether the reduction of dry weight was caused by the release of nutritional compounds from seaweed biomass or water uptake during storage treatment, the results from chemical analyses suggest the combined effect of both mechanisms. Seawater storage increased the ash and sodium contents and reduced carbohydrate and polyphenol levels in both species. Among carbohydrates, the levels of mannitol and glucose (laminaran) were particularly reduced in S. latissima samples while the fucose level, reflecting fucoidans, was reduced in A. esculenta. The protein content remained relatively stable in both species. These results provide evidence of the effect of seawater storage on the quality of the edible kelps A. esculenta and S. latissima. The results will contribute to selecting postharvest strategies adequate for maintaining biomass quality, minimizing losses of valuable compounds and increasing profitability for industrial stakeholders.

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References

  1. Abdullah MI, Fredriksen S (2004) Production, respiration and exudation of dissolved organic matter by the kelp Laminaria hyperborea along the west coast of Norway. J Mar Biol Assoc UK 84:887–894

    Article  Google Scholar 

  2. Adams JMM, Ross AB, Anastasakis K, Hodgson EM, Gallagher JA, Jones JM, Donnison IS (2011) Seasonal variation in the chemical composition of the bioenergy feedstock Laminaria digitata for thermochemical conversion. Bioresour Technol 102:226–234

    CAS  Article  PubMed  Google Scholar 

  3. Adams JMM, Schmidt A, Gallagher JA (2014) The impact of sample preparation of the macroalgae Laminaria digitata on the production of the biofuels bioethanol and biomethane. J Appl Phycol 27:985–991

    Article  Google Scholar 

  4. AFNOR (1977) Norme NF V18–101: aliments des animaux - Dosage des cendres brutes

  5. Ale MT, Maruyama H, Tamauchi H, Mikkelsen JD and Meyer AS (2011) Fucose-containing sulfated polysaccharides from brown seaweeds inhibit proliferation of melanoma cells and induce apoptosis by activation of caspase-3 in vitro. Mar Drugs 9(12):2605

  6. Angell AR, Mata L, de Nys R, Paul NA (2016) The protein content of seaweeds: a universal nitrogen-to-protein conversion factor of five. J Appl Phycol 28:511–524

    CAS  Article  Google Scholar 

  7. AOAC Iternational (2000) Official methods of analysis of AOAC international, 17th edn. Association of Official Analytical Chemistry, Maryland

    Google Scholar 

  8. Baghel RS, Trivedi N, Reddy CRK (2016) A simple process for recovery of a stream of products from marine macroalgal biomass. Bioresour Technol 203:160–165

    CAS  Article  PubMed  Google Scholar 

  9. Bischof K, Rautenberger R (2012) Seaweed responses to environmental stress: reactive oxygen and antioxidative strategies. In: Wiencke C, Bischof K (eds) Seaweed biology: novel insights into ecophysiology, ecology and utilization. Springer, Berlin, pp 109–132

    Google Scholar 

  10. Black W (1950) The seasonal variation in weight and chemical composition of the common British Laminariaceae. J Mar Biol Assoc UK 29:45–72

    CAS  Article  Google Scholar 

  11. Brinkhuis BH, Levine HG, Schlenk CG, Tobin S (1987) Laminaria cultivation in the far east and North America. In: Bird KT, Benson PH (eds) Seaweed cultivation for renewable resources. Development in aquaculture and fisheries science. Elsevier, New York, pp 107–146

    Google Scholar 

  12. Brownlee IA, Allen A, Pearson JP, Dettmar PW, Havler ME, Atherton MR, Onsøyen E (2005) Alginate as a source of dietary fiber. Crit Rev Food Sci 45:497–510

    CAS  Article  Google Scholar 

  13. Bruhn A, Tørring DB, Thomsen M, Canal-Vergés P, Nielsen MM, Rasmussen MB, Eybye KL, Larsen MM, Balsby TJS, Petersen JK (2016) Impact of environmental conditions on biomass yield, quality, and bio-mitigation capacity of Saccharina latissima. Aquac Environ Interac 8:619–636

    Article  Google Scholar 

  14. Burritt DJ, Larkindale J, Hurd CL (2002) Antioxidant metabolism in the intertidal red seaweed Stictosiphonia arbuscula following desiccation. Planta 215:829–838

    CAS  Article  PubMed  Google Scholar 

  15. Cabrita ARJ, Maia MRG, Oliveira HM, Sousa-Pinto I, Almeida AA, Pinto E, Fonseca AJM (2016) Tracing seaweeds as mineral sources for farm-animals. J Appl Phycol 28:3135–3150

    CAS  Article  Google Scholar 

  16. Chan JCC, Cheung PCK, Ang PO (1997) Comparative studies on the effect of three drying methods on the nutritional composition of seaweed Sargassum hemiphyllum (Turn.) C. Ag. J Agr Food Chem 45:3056–3059

    CAS  Article  Google Scholar 

  17. Chapman AS, Stévant P, Emblem Larssen W (2015) Food or fad? Challenges and opportunities for including seaweeds in a Nordic diet. Bot Mar 58:423–433

    Article  Google Scholar 

  18. Connan S, Delisle F, Deslandes E, Ar Gall E (2006) Intra-thallus phlorotannin content and antioxidant activity in Phaeophyceae of temperate waters. Bot Mar 49:39–46

    CAS  Article  Google Scholar 

  19. Dawczynski C, Schubert R, Jahreis G (2007) Amino acids, fatty acids, and dietary fibre in edible seaweed products. Food Chem 103:891–899

    CAS  Article  Google Scholar 

  20. Déléris P, Nazih H, Bard JM (2016) Seaweeds in human health. In: Fleurence J, Levine I (eds) Seaweed in health and disease prevention. Academic Press, Elsevier, Amsterdam, pp 319–367

    Google Scholar 

  21. Draget KI, Smidsrød O, Skjåk Bræk G (2002) Alginates from algae. In: De Baets S, Vandamme EJ, Steinbuchel A (eds) Biopolymers. Wiley, Weinheim, pp 215–244

    Google Scholar 

  22. Enríquez S, Duarte CM, Sand-Jensen K (1993) Patterns in decomposition rates among photosynthetic organisms: the importance of detritus C: N: P content. Oecologia 94:457–471

    Article  PubMed  Google Scholar 

  23. Evans FD, Critchley AT (2014) Seaweeds for animal production use. J Appl Phycol 26:891–899

    CAS  Article  Google Scholar 

  24. Fleurence J (2004) Seaweed proteins. In: Yada RY (ed) Proteins in food processing. Woodhead Publishing, Cambridge, pp 197–213

    Google Scholar 

  25. Fleurence J, Ar Gall E (2016) Antiallergic properties. In: Fleurance J, Levine I (eds) Seaweed in health and disease prevention. Academic Press, Elsevier, Amsterdam, pp 389–406

    Google Scholar 

  26. Flores-Molina MR, Thomas D, Lovazzano C, Núñez A, Zapata J, Kumar M, Correa JA, Contreras-Porcia L (2014) Desiccation stress in intertidal seaweeds: effects on morphology, antioxidant responses and photosynthetic performance. Aquat Bot 113:90–99

    CAS  Article  Google Scholar 

  27. Forbord S, Skjermo J, Arff J, Handå A, Reitan KI, Bjerregaard R, Lüning K (2012) Development of Saccharina latissima (Phaeophyceae) kelp hatcheries with year-round production of zoospores and juvenile sporophytes on culture ropes for kelp aquaculture. J Appl Phycol 24:393–399

    Article  Google Scholar 

  28. Francis FJ (1995) Quality as influenced by color. Food Qual Prefer 6:149–155

    Article  Google Scholar 

  29. Fung A, Hamid N, Lu J (2013) Fucoxanthin content and antioxidant properties of Undaria pinnatifida. Food Chem 136:1055–1062

    CAS  Article  PubMed  Google Scholar 

  30. Girolami A, Napolitano F, Faraone D, Braghieri A (2013) Measurement of meat color using a computer vision system. Meat Sci 93:111–118

    Article  PubMed  Google Scholar 

  31. Guiné RPF, Barroca MJ (2012) Effect of drying treatments on texture and color of vegetables (pumpkin and green pepper). Food Bioprod Process 90:58–63

    Article  Google Scholar 

  32. 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

    CAS  Article  Google Scholar 

  33. Handå A, Forbord S, Wang X, Broch OJ, Dahle SW, Størseth TR, Reitan KI, Olsen Y, Skjermo J (2013) Seasonal- and depth-dependent growth of cultivated kelp (Saccharina latissima) in close proximity to salmon (Salmo salar) aquaculture in Norway. Aquaculture 414-415:191–201

    Article  Google Scholar 

  34. Hayashi K, Nakano T, Hashimoto M, Kanekiyo K, Hayashi T (2008) Defensive effects of a fucoidan from brown alga Undaria pinnatifida against herpes simplex virus infection. Int Immunopharmacol 8:109–116

    CAS  Article  PubMed  Google Scholar 

  35. Herrmann C, FitzGerald J, O’Shea R, Xia A, O’Kiely P, Murphy JD (2015) Ensiling of seaweed for a seaweed biofuel industry. Bioresour Technol 196:301–313

    CAS  Article  PubMed  Google Scholar 

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

    CAS  Article  Google Scholar 

  37. Hou X, Hansen JH, Bjerre AB (2015) Integrated bioethanol and protein production from brown seaweed Laminaria digitata. Bioresour Technol 197:310–317

    CAS  Article  PubMed  Google Scholar 

  38. Jensen A (1993) Present and future needs for algae and algal products. Hydrobiologia 260:15–23

    Article  Google Scholar 

  39. Jiménez-Escrig A, Gómez-Ordóñez E, Tenorio MD, Rupérez P (2013) Antioxidant and prebiotic effects of dietary fiber co-travelers from sugar Kombu in healthy rats. J Appl Phycol 25:503–512

    Article  Google Scholar 

  40. Kanda H, Kamo Y, Machmudah S, Wahyudiono EY, Goto M (2014) Extraction of fucoxanthin from raw macroalgae excluding drying and cell wall disruption by liquefied dimethyl ether. Mar Drugs 12:2383–2396

    Article  PubMed  PubMed Central  Google Scholar 

  41. Kraan S, Verges Tramullas A, Guiry M (2000) The edible brown seaweed Alaria esculenta (Pheophyceae, Laminariales) hybridization growth and genetic comparisons of six Irish populations. J Appl Phycol 12:577–583

    Article  Google Scholar 

  42. Kumar CS, Ganesan P, Suresh PV, Bhaskar N (2008) Seaweeds as a source of nutritionally beneficial compounds. J Food Sci Tech Mys 45:1–13

    CAS  Google Scholar 

  43. Liot F, Colin A, Mabeau S (1993) Microbiology and storage life of fresh edible seaweeds. J Appl Phycol 5:243–247

    Article  Google Scholar 

  44. López-López I, Bastida S, Ruiz-Capillas C, Bravo L, Larrea MT, Sánchez-Muniz F, Cofrades S, Jiménez-Colmenero F (2009a) Composition and antioxidant capacity of low-salt meat emulsion model systems containing edible seaweeds. Meat Sci 83:492–498

    Article  PubMed  Google Scholar 

  45. López-López I, Cofrades S, Ruiz-Capillas C, Jiménez-Colmenero F (2009b) Design and nutritional properties of potential functional frankfurters based on lipid formulation, added seaweed and low salt content. Meat Sci 83:255–262

    Article  PubMed  Google Scholar 

  46. Lourenço SO, Barbarino E, De-Paula JC, da S. Pereira LO, Lanfer Marquez UM (2002) Amino acid composition, protein content and calculation of nitrogen-to-protein conversion factors for 19 tropical seaweeds. Phycol Res 50:233–241

    Article  Google Scholar 

  47. Mabeau S, Kloareg B, Joseleau J-P (1990) Fractionation and analysis of fucans from brown algae. Phytochemistry 29:2441–2445

    CAS  Article  Google Scholar 

  48. MacArtain P, Gill CIR, Brooks M, Campbell R, Rowland IR (2007) Nutritional value of edible seaweeds. Nutr Rev 65:535–543

    Article  PubMed  Google Scholar 

  49. Maeda H, Hosokawa M, Sashima T, Funayama K, Miyashita K (2005) Fucoxanthin from edible seaweed, Undaria pinnatifida, shows antiobesity effect through UCP1 expression in white adipose tissues. Biochem Biophys Res Commun 332:392–397

    CAS  Article  PubMed  Google Scholar 

  50. Maeda H, Tsukui T, Sashima T, Hosokawa M, Miyashita K (2008) Seaweed carotenoid, fucoxanthin, as a multi-functional nutrient. Asia Pac J Clin Nutr 17(S1):196–199

    CAS  PubMed  Google Scholar 

  51. Mæhre HK, Malde MK, Eilertsen KE, Elvevoll EO (2014) Characterization of protein, lipid and mineral contents in common Norwegian seaweeds and evaluation of their potential as food and feed. J Sci Food Agric 94:3281–3290

    Article  PubMed  Google Scholar 

  52. Magnusson M, Yuen AKL, Zhang R, Wright JT, Taylor RB, Maschmeyer T, de Nys R (2017) A comparative assessment of microwave assisted (MAE) and conventional solid-liquid (SLE) techniques for the extraction of phloroglucinol from brown seaweed. Algal Res 23:28–36

    Article  Google Scholar 

  53. Mouritsen OG (2016) Those tasty weeds. J Appl Phycol. doi:10.1007/s10811-016-0986-1:1-6

    Google Scholar 

  54. Newell R, Lucas M, Velimirov B, Seiderer L (1980) Quantitative significance of dissolved organic losses following fragmentation of kelp Ecklonia maxima and Laminaria pallida. Mar Ecol Prog Ser 2:45–59

    CAS  Article  Google Scholar 

  55. Pádua D, Rocha E, Gargiulo D, Ramos AA (2015) Bioactive compounds from brown seaweeds: phloroglucinol, fucoxanthin and fucoidan as promising therapeutic agents against breast cancer. Phytochem Lett 14:91–98

    Article  Google Scholar 

  56. Paull RE, Chen NJ (2008) Postharvest handling and storage of the edible red seaweed Gracilaria. Postharvest Biol Tec 48:302–308

    CAS  Article  Google Scholar 

  57. Perez V, Chang ET (2014) Sodium-to-potassium ratio and blood pressure, hypertension, and related factors. Adv Nutr 5:712–741

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  58. Quemener B, Marot C, Mouillet L, Da Riz V, Diris J (2000) Quantitative analysis of hydrocolloids in food systems by methanolysis coupled to reverse HPLC. Part 1. Gelling carrageenans. Food Hydrocolloid 14:9–17

    CAS  Article  Google Scholar 

  59. Quitain AT, Kai T, Sasaki M, Goto M (2013) Supercritical carbon dioxide extraction of fucoxanthin from Undaria pinnatifida. J Agr Food Chem 61:5792–5797

    CAS  Article  Google Scholar 

  60. R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna http://www.R-project.org

    Google Scholar 

  61. Ragan MA, Glombitza KW (1986) Phlorotannins, brown algal polyphenols. Prog Phycol Res 4:130–230

    Google Scholar 

  62. Rupérez P (2002) Mineral content of edible marine seaweeds. Food Chem 79:23–26

    Article  Google Scholar 

  63. Rupérez P, Saura-Calixto F (2001) Dietary fibre and physicochemical properties of edible Spanish seaweeds. Eur Food Res Technol 212:349–354

    Article  Google Scholar 

  64. Sánchez-Machado DI, López-Cervantes J, López-Hernández J, Paseiro-Losada P (2004) Fatty acids, total lipid, protein and ash contents of processed edible seaweeds. Food Chem 85:439–444

    Article  Google Scholar 

  65. Schiener P, Black KD, Stanley MS, Green DH (2015) The seasonal variation in the chemical composition of the kelp species Laminaria digitata, Laminaria hyperborea, Saccharina latissima and Alaria esculenta. J Appl Phycol 27:363–373

    CAS  Article  Google Scholar 

  66. Skriptsova AV (2015) Fucoidans of brown algae: biosynthesis, localization, and physiological role in thallus. Russ J Mar Biol 41:145–156

    CAS  Article  Google Scholar 

  67. Soler-Vila A, Coughlan S, Guiry M, Kraan S (2009) The red alga Porphyra dioica as a fish-feed ingredient for rainbow trout effects on growth, feed efficiency and carcass composition. J Appl Phycol 21:617–624

    Article  Google Scholar 

  68. Wang T, Jónsdóttir R, Ólafsdóttir G (2009) Total phenolic compounds, radical scavenging and metal chelation of extracts from Icelandic seaweeds. Food Chem 116:240–248

    CAS  Article  Google Scholar 

  69. Wang T, Jónsdóttir R, Kristinsson HG, Thorkelsson G, Jacobsen C, Hamaguchi PY, Ólafsdóttir G (2010) Inhibition of haemoglobin-mediated lipid oxidation in washed cod muscle and cod protein isolates by Fucus vesiculosus extract and fractions. Food Chem 123:321–330

    Article  Google Scholar 

  70. Yam KL, Papadakis SE (2004) A simple digital imaging method for measuring and analyzing color of food surfaces. J Food Eng 61:137–142

    Article  Google Scholar 

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Acknowledgements

This work was conducted as part of the PROMAC project (244244), funded by the Research Council of Norway and part of the Sustainable Innovation in Food- and Bio-based Industries Programme. Pierrick Stévant was supported by a doctoral fellowship from Sparebanken Møre. The authors are also grateful to two anonymous reviewers for their valuable comments and contribution in improving the manuscript.

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Stévant, P., Marfaing, H., Rustad, T. et al. Nutritional value of the kelps Alaria esculenta and Saccharina latissima and effects of short-term storage on biomass quality. J Appl Phycol 29, 2417–2426 (2017). https://doi.org/10.1007/s10811-017-1126-2

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Keywords

  • Alginate
  • Bioactive compounds
  • Carbohydrates
  • Chemical composition analysis
  • Edible seaweeds
  • Fucose
  • Fucoxanthin
  • Laminaran
  • Macroalgae
  • Mannitol
  • Minerals
  • Polyphenols
  • Potassium
  • Preservation
  • Processing
  • Protein
  • Sodium