Skip to main content

Advertisement

Log in

Drying process, storage conditions, and time alter the biochemical composition and bioactivity of the anti-greenhouse seaweed Asparagopsis taxiformis

  • Original Paper
  • Published:
European Food Research and Technology Aims and scope Submit manuscript

Abstract

The Azorean red seaweed Asparagopsis taxiformis may be used in human and animal diets. This seaweed is deemed to reduce the large production of methane—a major greenhouse gas—by ruminant digestion. Seaweed producers, however, have difficulties in ensuring a reliable and similar product throughout all year and in different years. Changes in biochemical composition and bioactivity are caused not only by natural variability, but also by the particular drying process, storage conditions, and storage time. Regarding the drying process, oven-dried samples had a lower EPA content, 1.9 ± 0.2% of the total FAs, than freeze-dried samples, 8.6 ± 1.7%. The same occurred with the phenolic contents and particularly with the ethanolic extracts. ABTS antioxidant activity results showed freeze-drying as advantageous. With respect to storage temperature, anti-inflammatory activity was higher in A. taxiformis at room temperature after three month storage. Moreover, EPA content in freeze-dried samples decreased to 0.3–1.0% after three month storage. Phenolic content in the ethanolic extracts also declined over storage time. In the case of aqueous extracts, however, variation was in the opposite direction. Antioxidant activity as measured by ABTS showed for almost all samples and types of extracts an increasing trend over time: from 0.26–1.75 to 0.75–4.40 mmol Trolox Eq/100 g dw. Anti-inflammatory activity increased over time from < 30% COX-2 inhibition at the beginning of the trial to > 30% COX-2 inhibition after three month storage. Therefore, there is a relevant bioactive potential in A. taxiformis and the drying process and storage conditions and time affect this potential.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

AA Eq:

Ascorbic acid equivalent

ABTS:

2,2′-Azino-bis(3-ethylbenzothiazoline-6-sulphonic acid

ARA:

Arachidonic acid

COX-2:

Cyclooxygenase-2

DHA:

Docosahexaenoic acid

DMSO:

Dimethyl sulphoxide

DPPH:

2,2-Diphenyl-1-picrylhydrazyl

ELISA:

Enzyme-Linked Immunosorbent Assay

EPA:

Eicosapentaenoic acid

F:

Freezing temperature

FA:

Fatty acid

FAME:

Fatty acid methyl ester

GA:

Gallic acid

GAE:

Gallic acid equivalent

HSD:

Honestly significant difference

L:

Freeze-dried samples

MUFA:

Monounsaturated fatty acid

O:

Oven-dried samples

PUFA:

Polyunsaturated fatty acid

R:

Room temperature

SFA:

Saturated fatty acid

TFC:

Total flavonoid content

TPC:

Total content of phenolic compounds

Trolox Eq:

Trolox equivalent

ω3 PUFA:

Omega-3 polyunsaturated fatty acid

ω6 PUFA:

Omega-6 polyunsaturated fatty acid

References

  1. Algaebase (2018) Global algal database of taxonomic, nomenclatural and distributional information. https://www.algaebase.org/search/species/detail/?species_id=636&sk=0&from=results. Accessed 19 Sept 2018

  2. Pereira L (2015) Seaweed flora of the European North Atlantic and Mediterranean. In: Kim S-K (ed) Springer handbook of marine biotechnology. Springer Verlag, Berlin, pp 65–178

    Chapter  Google Scholar 

  3. Roque B, Brooke C, Ladau J, Polley T, Marsh L, Najafi N, Pandey P, Singh L, Kinley R, Salwen J, Eloe-Fadrosh E, Kebreab E, Hess M (2019) Effect of the macroalgae Asparagopsis taxiformis on methane production and rumen microbiome assemblage. Anim Microbiome 1(4):1–14

    Google Scholar 

  4. Smith PM, Bustamante H, Ahammad H, Clark H, Dong EA, Elsiddig H, Haberl R, Harper J, House M, Jafari O, Masera C, Mbow NH, Ravindranath CW, Rice C, Robledo Abad A, Romanovskaya F, Sperling F, Tubiello F (2013) Agriculture, forestry and other land use (AFOLU). In: Edenhofer O, Pichs-Madruga R, Sokona Y, Farahani E, Kadner S, Seyboth K, Adler A, Baum I, Brunner S, Eickemeier P, Kriemann B, Savolainen J, Schlömer S, von Stechow C, Zwickel T, Minx JC (eds) Climate change: mitigation of climate change contribution of working group III to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, New York, pp 811–922

    Google Scholar 

  5. Maeda H (2013) Anti-obesity and anti-diabetic activities of algae. In: Domínguez H (ed) Functional ingredients from algae for foods and nutraceuticals. Woodhead Publishing Limited, Oxford, pp 453–472

    Chapter  Google Scholar 

  6. Pirian K, Moein S, Sohrabipour J, Rabiei R, Blomster J (2017) Antidiabetic and antioxidant activities of brown and red macroalgae from the Persian Gulf. J Appl Phycol 29(6):3151–3159

    Article  CAS  Google Scholar 

  7. Oumaskour K, Boujaber N, Etahiri S, Assobhei O (2013) Anti-inflammatory and antimicrobial activities of twenty-three marine red algae from the Coast of Sidi Bouzid (El Jadida-Morocco). Int J Pharm Pharmaceut Sci 5(3):145–149

    Google Scholar 

  8. Nunes N, Ferraz S, Valente S, Barreto C, Pinheiro de Carvalho MAA (2017) Biochemical composition, nutritional value, and antioxidant properties of seven seaweed species from Madeira archipelago. J Appl Phycol 29(5):2427–2437

    Article  CAS  Google Scholar 

  9. Ragonese C, Tedone L, Beccaria M, Torre G, Cichello F, Cacciola F, Dugo P, Mondello L (2014) Characterisation of lipid fraction of marine macroalgae by means of chromatography techniques coupled to mass spectrometry. Food Chem 145:932–940

    Article  CAS  PubMed  Google Scholar 

  10. Mellouk Z, Benammar I, Krouf D, Goudjil M, Okbi M, Malaisse W (2017) Antioxidant properties of the red alga Asparagopsis taxiformis collected on the North West Algerian coast. Exp Ther Med 13(6):3281–3290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Simopoulos AP (2002) Omega-3 fatty acids and cardiovascular disease: the epidemiological evidence. Environ Health Prev Med 6:203–209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Tanaka N, Ishida T, Nagao M, Mori T, Monguchi T, Sasaki M, Mori K, Kondo K, Nakajima H, Honjo T, Irino Y, Toh R, Shinohara M, Hirata K (2014) Administration of high dose eicosapentaenoic acid enhances anti-inflammatory properties of high-density lipoprotein in Japanese patients with dyslipidemia. Atherosclerosis 237(2):577–583

    Article  CAS  PubMed  Google Scholar 

  13. 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(5):1266–1272

    Article  CAS  Google Scholar 

  14. 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(4):238–245

    Article  CAS  Google Scholar 

  15. Kadam U, Álvarez C, Tiwari B, Donnell CPO (2015) Processing of seaweeds. In: Tiwari BK, Troy DJ (eds) Seaweed sustainability: food and non-food applications. Academic Press, Amsterdam, The Netherlands, pp 61–78

    Chapter  Google Scholar 

  16. Stévant P, Rebours C, Chapman A (2017) Seaweed aquaculture in Norway: recent industrial developments and future perspectives. Aquacult Int 25(4):1373–1390

    Article  Google Scholar 

  17. 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(5):530–534

    Article  Google Scholar 

  18. Le Gall L, Saunders GW (2010) DNA Barcoding is a powerful tool to uncover algal diversity: a case study of the Phyllophoraceae (Gigartinales, Rhodophyta) in the Canadian flora. J Phycol 46:374–389

    Article  CAS  Google Scholar 

  19. AOAC (2000) Official methods of analysis of the AOAC International, 17th edn. Association of Analytical Communities, Gaithersburg

    Google Scholar 

  20. Saint-Denis T, Goupy J (2004) Optimization of a nitrogen analyser based on the Dumas method. Anal Chim Acta 515(1):191–198

    Article  CAS  Google Scholar 

  21. Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509

    CAS  PubMed  Google Scholar 

  22. Bandarra NM, Batista I, Nunes ML, Empis JMA, Christie WW (1997) Seasonal changes in lipid composition of sardine Sardina pilchardus. J Food Sci 62(1):40–43

    Article  CAS  Google Scholar 

  23. Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Viticul 16:144–158

    CAS  Google Scholar 

  24. Miliauskas G, Venskutonis PR, Van Beek TA (2004) Screening of radical scavenging activity of some medicinal and aromatic plant extracts. Food Chem 85:231–237

    Article  CAS  Google Scholar 

  25. 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 Radical Biol Med 26:1231–1237

    Article  CAS  Google Scholar 

  26. Chan JC-C, Cheung PC-K, Ang PO (1997) Comparative studies on the effect of three drying methods on the nutritional composition of seaweed Sargassum hemiphyllum (Turn ) C Ag. J Agric Food Chem 45(8):3056–3059

    Article  CAS  Google Scholar 

  27. 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. Marine Drugs 10(9):1920–1935

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Graeve M, Kattner G, Wiencke C, Karsten U (2002) Fatty acid composition of Arctic and Antarctic macroalgae: indicator of phylogenetic and trophic relationships. Mar Ecol Prog Ser 231:67–74

    Article  CAS  Google Scholar 

  29. Mouritsen OG, Dawczynski C, Duelund L, Jahreis G, Vetter W, Schröder M (2013) On the human consumption of the red seaweed dulse (Palmaria palmata (L ) Weber, Mohr). J Appl Phycol 25(6):1777–1791

    Article  CAS  Google Scholar 

  30. Schmid M, Guihéneuf F, Stengel DB (2014) Fatty acid contents and profiles of 16 macroalgae collected from the Irish coast at two seasons. J Appl Phycol 26(1):451–463

    Article  CAS  Google Scholar 

  31. Munier M, Dumay J, Morancais M, Jaouen P, Fleurence J (2013) Variation in the biochemical composition of the edible seaweed Grateloupia turuturu Yamada harvested from two sampling sites on the Brittany Coast (France): the influence of storage method on the extraction of the seaweed pigment R-phycoerythrin. J Chem. https://doi.org/10.1155/2013/568548

    Article  Google Scholar 

  32. Schmid M, Guihéneuf F, Stengel DB (2017) Ecological and commercial implications of temporal and spatial variability in the composition of pigments and fatty acids in five Irish macroalgae. Mar Biol 164(8):158

    Article  Google Scholar 

  33. Turan A (2018) Effect of drying methods on fatty acid profile and oil oxidation of hazelnut oil during storage. Eur Food Res Technol 244(12):2181–2190

    Article  CAS  Google Scholar 

  34. Schmid M, Guihéneuf F, Stengel DB (2016) Evaluation of food grade solvents for lipid extraction and impact of storage temperature on fatty acid composition of edible seaweeds Laminaria digitata (Phaeophyceae) and Palmaria palmata (Rhodophyta). Food Chem 208:161–168

    Article  CAS  PubMed  Google Scholar 

  35. Choe E, Min DB (2006) Mechanisms and factors for edible oil oxidation. Compr Rev Food Sci Food Saf 5(4):169–186

    Article  CAS  Google Scholar 

  36. Farasat M, Khavari-Nejad RA, Nabavi SMB, Namjooyan F (2013) Antioxidant properties of two edible green seaweeds from northern coasts of the Persian Gulf Jundishapur. J Nat Pharm Prod 8(1):47–52

    Google Scholar 

  37. Bischof K, Gómez I, Molis M, Hanelt D, Karsten U, Lüder U, Roleda MY, Zacher K, Wiencke C (2006) Ultraviolet radiation shapes seaweed communities. Rev Environ Sci Bio/Technol 5(2/3):141

    Article  CAS  Google Scholar 

  38. Mrad ND, Boudhrioua N, Kechaou N, Courtois F, Bonazzi C (2012) Influence of air drying temperature on kinetics, physicochemical properties, total phenolic content and ascorbic acid of pears. Food Bioprod Process 90:433–441

    Article  CAS  Google Scholar 

  39. Wong K, Cheung PC (2001) Influence of drying treatment on three Sargassum species 2 Protein extractability, in vitro protein digestibility and amino acid profile of protein concentrates. J Appl Phycol 13(1):51–58

    Article  CAS  Google Scholar 

  40. Ling ALM, Yasir S, Matanjun P, Bakar MFA (2015) Effect of different drying techniques on the phytochemical content and antioxidant activity of Kappaphycus alvarezii. J Appl Phycol 27(4):1717–1723

    Article  CAS  Google Scholar 

  41. Tao L (2015) Oxidation of polyunsaturated fatty acids and its impact on food quality and human health. Adv Food Technol Nutr Sci Open J 1(6):135–142

    Article  Google Scholar 

  42. Norra I, Aminah A, Suri R, Zaidi JA (2017) Effect of drying temperature on the content of fucoxanthin, phenolic and antioxidant activity of Malaysian brown seaweed Sargassum sp. J Trop Agric Food Sci 45(1):25–36

    Google Scholar 

  43. Rajauria G, Kumar A, Abu-Ghannam N, Gupta S (2010) Effect of hydrothermal processing on colour, antioxidant and free radical scavenging capacities of edible Irish brown seaweeds. Int J Food Sci Technol 45:2485–2493

    Article  CAS  Google Scholar 

  44. Montoro P, Tuberoso CIG, Piacente S, Perrone A, De Feo V, Cabras P, Pizza C (2006) Stability and antioxidant activity of polyphenols in extracts of Myrtus communis L berries used for the preparation of myrtle liqueur. J Pharm Biomed Anal 41(5):1614–1619

    Article  CAS  PubMed  Google Scholar 

  45. Martysiak-Żurowska D, Wenta W (2012) A comparison of ABTS and DPPH methods for assessing the total antioxidant capacity of human milk Acta Scientiarum Polonorum Technologia. Alimentaria 11(1):83–89

    Google Scholar 

  46. Jin DQ, Lim CS, Sung JY, Choi HG, Ha I, Han JS (2006) Ulva conglobata, a marine algae, has neuroprotective and anti-inflammatory effects in murine hippocampal and microglial cells. Neurosci Lett 402:154–158

    Article  CAS  PubMed  Google Scholar 

  47. Montalvão S, Demirel Z, Devi P, Lombardi V, Hongisto V, Perälä M, Hattara J, Imamoglu E, Tilvi SS, Turan G, Dalay MC, Tammela P (2018) Large-scale bioprospecting of cyanobacteria, micro- and macroalgae from the Aegean Sea. New Biotechnol 33(3):399–406

    Article  CAS  Google Scholar 

  48. Yang EJ, Moon JY, Kim MJ, Kim DS, Lee WJ, Lee NH, Hyun CG (2010) Anti-inflammatory effect of Petalonia binghamiae in LPS-induced macrophages is mediated by suppression of iNOS and COX-2. Int J Agric Biol Eng 12(5):754–758

    CAS  Google Scholar 

  49. Pangestuti R, Vo TS, Ngo DH, Kim SK (2013) Fucoxanthin ameliorates inflammation and oxidative responses in microglia. J Agric Food Chem 61(16):3876–3883

    Article  CAS  PubMed  Google Scholar 

  50. Wong CH, Gan SY, Tan SC, Gany SA, Ying T, Gray AI, Igoli J, Chan EWL, Phang SM (2018) Fucosterol inhibits the cholinesterase activities and reduces the release of pro-inflammatory mediators in lipopolysaccharide and amyloid-induced microglial cells. J Appl Phycol 30(6):3261–3270

    Article  CAS  Google Scholar 

  51. Kim M, Li YX, Dewapriya P, Ryu B, Kim SK (2013) Floridoside suppresses pro-inflammatory responses by blocking MAPK signaling in activated microglia. BMB Reports 46(8):398–403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Ripol A, Cardoso C, Afonso C, Varela J, Quental-Ferreira H, Pousão-Ferreira P, Bandarra NM (2018) Composition, anti-inflammatory activity, and bioaccessibility of green seaweeds from fish pond aquaculture. Nat Prod Commun 13(5):603–608

    Google Scholar 

  53. Campos AM, Matos J, Afonso C, Gomes R, Bandarra NM, Cardoso C (2019) Azorean macroalgae (Petalonia binghamiae, Halopteris scoparia and Osmundea pinnatifida) bioprospection: a study of fatty acid profiles and bioactivity. Int J Food Sci Technol 54(3):880–890

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by the following Grants: Ref.: SFRH/BPD/102689/2014 (“Fundação para a Ciência e a Tecnologia”, FCT) for Carlos Cardoso, DIVERSIAQUA (MAR2020, Ref.: 16-02-01-FEAM-66) for Cláudia Afonso, and (SFRH/BD/129795/2017; FCT) for Joana Matos. The experimental work was funded by the projects AQUAMAX (Ref.: 16-02-01-FMP-0047), I9 + PROALGA (Ref.: 16-01-03-FMP-0011), and FCT (Ref.: UID/AGR/04129/2019).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to C. Cardoso.

Ethics declarations

Conflict of interest

There is no conflict of interest involving any of the authors.

Compliance with ethics requirements

This article does not contain any studies with human or animal subjects.

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

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Regal, A.L., Alves, V., Gomes, R. et al. Drying process, storage conditions, and time alter the biochemical composition and bioactivity of the anti-greenhouse seaweed Asparagopsis taxiformis. Eur Food Res Technol 246, 781–793 (2020). https://doi.org/10.1007/s00217-020-03445-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00217-020-03445-8

Keywords

Navigation