Skip to main content
SpringerLink
Log in

Commercial Red Seaweed in Portugal (Gelidium sesquipedale and Pterocladiella capillacea, Florideophyceae): Going beyond a Single-Purpose Product Approach by Valorizing Bioactivity

  • Published:
Thalassas: An International Journal of Marine Sciences Aims and scope Submit manuscript

Abstract

The red seaweed species Gelidium sesquipedale and Pterocladiella capillacea are commercially explored as one of the main seaweed resources in Portugal. However, they are essentially harvested for extraction of agar, leaving a large biomass share needing an adequate valorization. The two studied red seaweed species were characterized by a large share of saturated fatty acids (SFA) in the vicinity of 60% (of the total FAs). Concerning ω3 highly unsaturated FAs, only EPA reached a significant percentage in P. capillacea and G. sesquipedale, 13.0 ± 0.5% and 7.7 ± 0.1%, respectively. In comparison with other seaweeds, the phenolic content was low for both species and aqueous and ethanolic extracts. The antioxidant activity was also low or even undetected. Regarding anti-inflammatory activity, as measured by inhibition of cyclooxygenase-2, it was not detected in the aqueous extracts of the seaweed, but was significant in the ethanolic extracts, 69 ± 3% and 54 ± 6%, for P. capillacea and G. sesquipedale, respectively. Concerning cytotoxicity, while ethanolic extracts did not cause any detectable cytotoxicity, the biomass and the aqueous extracts reduced HeLa cell viability. Finally, the elemental composition showed differences between the two seaweed species. In particular, G. sesquipedale contained a higher I level than P. capillacea, 807 ± 51 mg/kg dw vs 435 ± 18 mg/kg dw. On the whole, attained results were promising and warrant further study.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Algaebase (2018) Global algal database of taxonomic, nomenclatural and distributional information. http://www.algaebase.org/ Accessed on 19th September 2018

  • AOAC (2000) Official methods of analysis of the AOAC international, 17th edn. Association of Analytical Communities, Gaithersburg, USA

    Google Scholar 

  • 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  Google Scholar 

  • Benzie IF, Strain JJ (1996) The ferric reducing ability of plasma (FRAP) as a measure of "antioxidant power": the FRAP assay. Anal Biochem 239(1):70–76

    Article  Google Scholar 

  • Besada V, Andrade JM, Schultze F, González JJ (2009) Heavy metals in edible seaweeds commercialised for human consumption. J Mar Syst 75:305–313

    Article  Google Scholar 

  • 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 Env Sci Bio/Technol 5(2/3):141

    Article  Google Scholar 

  • Bonanno G, Orlando-Bonaca M (2018) Chemical elements in Mediterranean macroalgae. A review. Ecotoxicol Env Safety 148:44–71

    Article  Google Scholar 

  • 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  Google Scholar 

  • de Alencar DB, Carvalho FCT, Rebouças RH, Santos DR, Pires-Cavalcante KMS, de Lima RL, Baracho BM, Bezerra RM, Viana FA, Vieira RHSF, Sampaio AH, de Sousa OV, Saker-Sampaio S (2016) Bioactive extracts of red seaweeds Pterocladiella capillacea and Osmundaria obtusiloba (Floridophyceae: Rhodophyta) with antioxidant and bacterial agglutination potential. As Pac J Trop Med 9(4):372–379

    Article  Google Scholar 

  • de Alencar DB, Diniz JC, Rocha SAS, Pires-Cavalcante KMS, de Lima RL, de Sousa KC, Freitas JO, Bezerra RM, Baracho BM, Sampaio AH, Viana FA, Saker-Sampaio S (2018) Fatty acid composition from the marine red algae Pterocladiella capillacea (S. G. Gmelin) Santelices and Hommersand 1997 and Osmundaria obtusiloba (C. Agardh) R. E. Norris 1991 and its antioxidant activity. An Acad Bras Cienc 90(1):449–459

    Article  Google Scholar 

  • Dillehay TD, Ramirez C, Pino M, Collins MB, Rossen J, Pinot-Navarro JD (2008) Monte Verde: seaweed, food, medicine and the peopling of South America. Sci 320:784–789

    Article  Google Scholar 

  • EFSA (European food safety authority) panel on dietetic products, nutrition, and allergies (NDA) (2010) Scientific opinion on dietary reference values for fats, including saturated fatty acids, polyunsaturated fatty acids, monounsaturated fatty acids, trans fatty acids, and cholesterol. EFSA J 8(3), 1461. http://www.efsa.europa.eu/en/efsajournal/pub/1461.htm (Accessed October 24, 2018)

  • EPA (United States Environmental Protection Agency) (1998) Test method 7473: Mercury in solids and solutions by thermal decomposition, amalgamation and atomic absorption spectrometry. SW-846, USA

  • 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

    Article  Google Scholar 

  • 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  Google Scholar 

  • Ito M, Koba K, Hikihara R, Ishimaru M, Shibata T, Hatate H, Tanaka R (2018) Analysis of functional components and radical scavenging activity of 21 algae species collected from the Japanese coast. Food Chem 255:147–156

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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  Google Scholar 

  • Kelman D, Posner EK, McDermid KJ, Tabandera NK, Wright PR, Wright AD (2012) Antioxidant activity of Hawaiian algae. Mar Drugs 10(2):403–416

    Article  Google Scholar 

  • Khaled A, Hessein A, Abdel-Halim AM, Morsy FM (2014) Distribution of heavy metals in seaweeds collected along Marsa-Matrouh beaches, Egyptian Mediterranean Sea. Eg J Aq Res 40:363–371

    Google Scholar 

  • Khotimchenko SV, Gusarova IS (2004) Red algae of Peter the Great Bay as a source of arachidonic and eicosapentaenoic acids. Russ J Mar Biol 30(3):183–187

    Article  Google Scholar 

  • Khotimchenko SV, Vaskovsky VE (1990) Distribution of C20 polyenoic fatty acids in red macrophytic algae. Bot Mar 33(6):525–528

    Article  Google Scholar 

  • Lee Y, Oh H, Lee M (2018) Anti-inflammatory effects of agar free-Gelidium amansii (GA) extracts in high-fat diet-induced obese mice. Nutr Res Pract 12(6):479–485

    Article  Google Scholar 

  • Li X, Fan X, Han L, Lou Q (2002) Fatty acids of some algae from the Bohai Sea. Phytochem 59:157–161

    Article  Google Scholar 

  • Ling ALM, Yasir SM, Matanjun P, Bakar MFA (2013) Antioxidant activity, total phenolic and flavonoid contents of selected commercial seaweeds of Sabah, Malaysia. Int J Pharm Phytopharmacol Res 3(3):234–238

    Google Scholar 

  • Metidji H, Dob T, Toumi M, Krimat S, Ksouri A, Nouasri A (2015) In vitro screening of secondary metabolites and evaluation of antioxidant, antimicrobial and cytotoxic properties of Gelidium sesquipedale Thuret et Bornet red seaweed from Algeria. J Mat Env Sci 6(11):3184–3196

    Google Scholar 

  • 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  Google Scholar 

  • 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  Google Scholar 

  • Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55–63

    Article  Google Scholar 

  • 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 and Mohr). J Appl Phycol 25(6):1777–1791

    Article  Google Scholar 

  • 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  Google Scholar 

  • Munda IM, Hudnik V (1991) Trace metal content in some seaweeds from the northern Adriatic. Bot Mar 34:241–249

    Article  Google Scholar 

  • Nascimento AC, Mota C, Coelho I, Gueifão S, Santos M, Matos AS, Castanheira I (2014) Characterisation of nutrient profile of quinoa (Chenopodium quinoa), amaranth (Amaranthus caudatus), and purple corn (Zea mays L.) consumed in the North of Argentina: Proximates, minerals and trace elements. Food Chem 148:420–426

    Article  Google Scholar 

  • 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 Pharm Sci 5(3):145–149

    Google Scholar 

  • Paiva L, Lima E, Neto AI, Marcone M, Baptista J (2016) Health-promoting ingredients from four selected Azorean macroalgae. Food Res Int 89:432–438

    Article  Google Scholar 

  • Pereira L (2016) Edible seaweeds of the world. Pp. 453. Boca Raton, FL, USA: CRC Press, Taylor and Francis Group, LLC

  • Prior RL, Wu X, Schaich K (2005) Standardized methods for the determination of antioxidant capacity and phenolics in foods and dietary supplements. J Agric Food Chem 53:4290–4302

    Article  Google Scholar 

  • 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 

  • Rodrigues D, Freitas AC, Pereira L, Rocha-Santos TAP, Vasconcelos MW, Roriz M, Rodríguez-Alcalá LM, Gomes AMP, Duarte AC (2015) Chemical composition of red, brown and green macroalgae from Buarcos bay in central west coast of Portugal. Food Chem 183:197–207

    Article  Google Scholar 

  • Romaríz-Hortas V, Bermejo-Barrera P, Moreda-Piñeiro J, Moreda-Piñeiro A (2012) Speciation of the bio-available iodine and bromine forms in edible seaweed by high performance liquid chromatography hyphenated with inductively coupled plasma-mass spectrometry. Anal Chim Acta 745:24–32

    Article  Google Scholar 

  • Rubio C, Napoleone G, Luis-González G, Gutiérrez AJ, González-Weller D, Hardisson A, Revert C (2017) Metals in edible seaweed. Chemosphere 173:572–579

    Article  Google Scholar 

  • 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  Google Scholar 

  • 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  Google Scholar 

  • Schmid M, Kraft LGK, van der Loos LM, Kraft GT, Virtue P, Nichols PD, Hurd CL (2018) Southern Australian seaweeds: a promising resource for omega-3 fatty acids. Food Chem 265:70–77

    Article  Google Scholar 

  • Shams El-Din NG, Mohamedein LI, El-Moselhy KM (2014) Seaweeds as bioindicators of heavy metals off a hot spot area on the Egyptian Mediterranean coast during 2008–2010. Env Monitor Assessment 186(9):5865–5881

    Article  Google Scholar 

  • Silva LM, Lima V, Holanda ML, Pinheiro PG, Rodrigues JA, Lima ME, Benevides NM (2010) Antinociceptive and anti-inflammatory activities of lectin from marine red alga Pterocladiella capillacea. Biol Pharm Bull 33(5):830–835

    Article  Google Scholar 

  • Silva M, Vieira LMM, Almeida AP, Silva AMS, Seca AML, Barreto MC, Neto AI, Pedro M, Pinto E, Kijjoa A (2013) Chemical study and biological activity evaluation of two Azorean macroalgae: Ulva rigida and Gelidium microdon. J Oceanography Marine Res 1(1):102–108

    Google Scholar 

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

    Article  Google Scholar 

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

    Google Scholar 

  • Smith JL, Summers G, Wong R (2010) Nutrient and heavy metal content of edible seaweeds in New Zealand. New Zealand J Crop Hortic Sci 38(1):19–28

    Article  Google Scholar 

  • Suffness M, Pezzuto JM (1999) Assays related to cancer drug discovery. In methods in plant biochemistry: assays for bioactivity; Vol. 6 (Hostettmann K; editor) London; UK: Academic Press; pp. 71–133

  • 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  Google Scholar 

  • Tarhouni-Jabberi S, Zakraoui O, Ioannou E, Riahi-Chebbi I, Haoues M, Roussis V, Kharrat R, Essafi-Benkhadir K (2017) Mertensene, a halogenated monoterpene, induces G2/M cell cycle arrest and caspase dependent apoptosis of human colon adenocarcinoma HT29 cell line through the modulation of ERK-1/−2, AKT and NF-κB signaling. Mar Drugs 15(7):221

    Article  Google Scholar 

  • Teas J, Pino S, Critchley AT, Braverman LE (2004) Variability of iodine content in common commercially available edible seaweeds. Thyroid 14(10):836–841

    Article  Google Scholar 

  • Wallenstein FM, Couto RP, Amaral AS, Wilkinson M, Neto AI, Rodrigues AS (2009) Baseline metal concentrations in marine algae from São Miguel (Azores) under different ecological conditions – urban proximity and shallow water hydrothermal activity. Mar Pollut Bull 58:438–443

    Article  Google Scholar 

  • 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(2):949–982

    Article  Google Scholar 

Download references

Acknowledgments

This work 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) and I9+ PROALGA (Ref.: 16-01-03-FMP-0011). The authors also thank Iberagar for supplying the seaweed samples.

Author information

Authors and Affiliations

  1. Faculdade de Ciências da Universidade de Lisboa, Campo Grande, 16, 1749-016, Lisbon, Portugal

    J. Matos, A. Gomes, C. Cardoso, C. Afonso, A. M. Campos, R. Gomes, P. Falé & N. M. Bandarra

  2. Division of Aquaculture and Upgrading (DivAV), Portuguese Institute for the Sea and Atmosphere (IPMA, IP), Rua Alfredo Magalhães Ramalho, 6, 1495-006, Lisbon, Portugal

    J. Matos & A. M. Campos

  3. CIIMAR, Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Rua dos Bragas 289, 4050-123, Porto, Portugal

    A. Gomes, C. Cardoso, C. Afonso & N. M. Bandarra

  4. Food and Nutrition Department, National Health Institute Doutor Ricardo Jorge (INSA, IP), Av. Padre Cruz, 1649-016, Lisbon, Portugal

    Inês Delgado, Inês Coelho & Isabel Castanheira

Authors
  1. J. Matos
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Gomes
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. C. Cardoso
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. C. Afonso
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. M. Campos
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. R. Gomes
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. P. Falé
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Inês Delgado
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Inês Coelho
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Isabel Castanheira
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. N. M. Bandarra
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to C. Cardoso or C. Afonso.

Ethics declarations

Conflict of Interest

No conflict of interest involving any of the authors.

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

Matos, J., Gomes, A., Cardoso, C. et al. Commercial Red Seaweed in Portugal (Gelidium sesquipedale and Pterocladiella capillacea, Florideophyceae): Going beyond a Single-Purpose Product Approach by Valorizing Bioactivity. Thalassas 36, 213–224 (2020). https://doi.org/10.1007/s41208-019-00181-z

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s41208-019-00181-z

Keywords

Search

Navigation