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Lipidomic signature of the green macroalgae Ulva rigida farmed in a sustainable integrated multi-trophic aquaculture

  • Diana Lopes
  • Ana S. P. Moreira
  • Felisa Rey
  • Elisabete da Costa
  • Tânia Melo
  • Elisabete Maciel
  • Andreia Rego
  • Maria H. Abreu
  • Pedro Domingues
  • Ricardo Calado
  • Ana I. Lillebø
  • M. Rosário Domingues
Article

Abstract

Ulva species, green macroalgae, are widely distributed across the globe, being one of the most heavily traded edible seaweeds. Nonetheless, although this genus has been largely used in scientific studies, its lipidome remains rather unexplored. The present study sheds light over the lipid profile of Ulva rigida produced in a land-based integrated multi-trophic aquaculture (IMTA) system using liquid chromatography coupled to high-resolution mass spectrometry for molecular lipid species identification. The lipidome of U. rigida revealed the presence of distinct beneficial n-3 fatty acids for human health, namely alpha-linoleic acid (ALA) and docosapentaenoic acid (DPA). A total of 87 molecular species of glycolipids, 58 molecular species of betaine lipids, and 57 molecular species of phospholipids were identified in the lipidome of U. rigida including some species bearing PUFA and with described bioactive properties. Overall, the present study contributes to the valorization and quality validation of sustainably farmed U. rigida.

Keywords

Chlorophyta Edible Lipidome Mass spectrometry Seaweed Ulva rigida 

Notes

Acknowledgements

The authors are grateful to ALGAplus- Produção e Comércio de algas e seus derivados, Lda. for supplying the seaweed samples. Thanks are due to Fundação para a Ciência e a Tecnologia (FCT, Portugal), European Union, QREN, POPH, FEDER, and COMPETE for funding the QOPNA research unit (FCT UID/QUI/00062/2013), to RNEM (LISBOA-01-0145-FEDER-402-022125) for the Portuguese Mass Spectrometry Network, to CESAM (UID/AMB/50017/2013) financed by Portuguese funds through the FCT/MEC, and when applicable co-financed by FEDER under the PT2020 Partnership Agreement. Thanks are also due to FCT for the grants of Diana Lopes (SFRH/BD/119027/2016) and Felisa Rey (SFRH/BPD/115347/2016). Ana S.P. Moreira (BPD/UI51/5041/2017) and Elisabete da Costa (BPD/UI51/5042/2018) are grateful for the grants within framework of the project GENIALG—Genetic diversity exploitation for innovative macro-alga biorefinery (ANR-15-MRSE-0015) funded by European Union’s Horizon 2020 Framework Programme. Tânia Melo is grateful for her Post-Doc grant (BPD/UI 51/5388/2017) funded by RNEM. This work is a contribution of the Marine Lipidomics Laboratory and was also supported by the Integrated Programme of SR&TD “Smart Valorization of Endogenous Marine Biological Resources Under a Changing Climate” (Centro-01-0145-FEDER-000018), co-funded by Centro 2020 program, Portugal 2020, European Union, through the European Regional Development Fund.

References

  1. Abreu M, Pereira R, Sassi J-F (2014) Marine algae and the global food industry. In: Pereira L, Neto J (eds) Marine algae: biodiversity, taxonomy, assesment and biotechnology. CRC Press, Boca Raton, pp 300–319CrossRefGoogle Scholar
  2. Ak İ, Öztaşkent C, Özüdoğru Y, Göksan T (2014) Effect of sodium acetate and sodium nitrate on biochemical composition of green algae Ulva rigida. Aquac Int 23:1–12CrossRefGoogle Scholar
  3. 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 28:511–524CrossRefGoogle Scholar
  4. Banskota AH, Stefanova R, Sperker S, Melanson R, Osborne JA, O’Leary SJB (2013) Five new galactolipids from the freshwater microalga Porphyridium aerugineum and their nitric oxide inhibitory activity. J Appl Phycol 25:951–960CrossRefGoogle Scholar
  5. Banskota AH, Stefanova R, Sperker S, Lall SP, Craigie JS, Hafting JT, Critchley AT (2014) Polar lipids from the marine macroalga Palmaria palmata inhibit lipopolysaccharide-induced nitric oxide production in RAW264.7 macrophage cells. Phytochemistry 101:101–108CrossRefPubMedGoogle Scholar
  6. Barriga LGC, Ruvalcaba FS, Carmona GH, Briones ER, Herrera RMH (2017) Effect of seaweed liquid extracts from Ulva lactuca on seedling growth of mung bean (Vigna radiata). J Appl Phycol 29:2479–2488CrossRefGoogle Scholar
  7. Barrington K, Chopin T, Robinson S (2009) Integrated multi-trophic aquaculture (IMTA) in marine temperate waters. Integrated Mariculture - A Global Review - FAO Fish Aquac Tech Pap N0 529 7–46Google Scholar
  8. Berri M, Slugocki C, Olivier M, Helloin E, Jacques I, Salmon H, Demais H, Le Goff M, Collen PN (2016) Marine-sulfated polysaccharides extract of Ulva armoricana green algae exhibits an antimicrobial activity and stimulates cytokine expression by intestinal epithelial cells. J Appl Phycol 28:2999–3008CrossRefGoogle Scholar
  9. Blunt JW, Copp BR, Keyzers RA, Munro MHG, Prinsep MR (2016) Marine natural products. Nat Prod Rep 33:382–431CrossRefPubMedPubMedCentralGoogle Scholar
  10. Bolton J, Robertson-Andersson D, Shuuluka D, Kandjengo L (2008) Growing Ulva (Chlorophyta) in integrated systems as a commercial crop for abalone feed in South Africa: a SWOT analysis. J Appl Phycol 21:575–583CrossRefGoogle Scholar
  11. Bunea R, El Farrah K, Deutsch L (2004) Evaluation of the effects of Neptune krill oil on the clinical course of hyperlipidemia. Altern Med Rev 9:420–428PubMedGoogle Scholar
  12. Calder PC (2001) Polyunsaturated fatty acids, inflammation, and immunity. Lipids 36:1007–1024CrossRefPubMedGoogle Scholar
  13. Chopin T, Cooper JA, Reid G, Cross S, Moore C (2012) Open-water integrated multi-trophic aquaculture: environmental biomitigation and economic diversification of fed aquaculture by extractive aquaculture. Rev Aquac 4:209–220CrossRefGoogle Scholar
  14. Cottin SC, Sanders TA, Hall WL (2011) The differential effects of EPA and DHA on cardiovascular risk factors. Proc Nutr Soc 70:215–231CrossRefPubMedGoogle Scholar
  15. da Costa E, Melo T, Moreira ASP, Alves E, Domingues P, Calado R, Abreu MH, Domingues MR (2015) Decoding bioactive polar lipid profile of the macroalgae Codium tomentosum from a sustainable IMTA system using a lipidomic approach. Algal Res 12:388–397CrossRefGoogle Scholar
  16. da Costa E, Melo T, Moreira ASP, Bernardo C, Helguero L, Ferreira I, Cruz MT, Rego AM, Domingues P, Calado R, Abreu MH, Domingues MR (2017) Valorization of lipids from Gracilaria sp. through lipidomics and decoding of antiproliferative and anti-inflammatory activity. Mar Drugs 15:1–17CrossRefGoogle Scholar
  17. da Costa E, Azevedo V, Melo T, Rego AM, Evtuguin DV, Domingues P, Calado R, Pereira R, Abreu MH, Domingues MR (2018) High-resolution lipidomics of the early life stages of the red seaweed Porphyra dioica. Molecules 23:1–20Google Scholar
  18. Dembitsky VM, Rezanka T (1995) Distribution of acetylenic acids and polar lipids in some aquatic bryophytes. Phytochemistry 40:93–97CrossRefGoogle Scholar
  19. Dial EJ, Doyen JR, Lichtenberger LM (2006) Phosphatidylcholine-associated nonsteroidal anti-inflammatory drugs (NSAIDs) inhibit DNA synthesis and the growth of colon cancer cells in vitro. Cancer Chemother Pharmacol 57:295–300CrossRefPubMedGoogle Scholar
  20. Eitsuka T, Nakagawa K, Igarashi M, Miyazawa T (2004) Telomerase inhibition by sulfoquinovosyldiacylglycerol from edible purple laver (Porphyra yezoensis). Cancer Lett 212:15–20CrossRefPubMedGoogle Scholar
  21. El Baz FK, El Baroty GS, Abd El Baky HH, Abd El Salam OI, Ibrahim EA (2013) Structural characterization and biological activity of sulfolipids from selected marine algae. Grasas Aceites 64:561–571CrossRefGoogle Scholar
  22. Fabian CJ, Kimler BF, Hursting SD (2015) Omega-3 fatty acids for breast cancer prevention and survivorship. Breast Cancer Res 17:1–11CrossRefGoogle Scholar
  23. Fleurence J, Gutbier G, Mabeau S, Leray C (1994) Fatty acids from 11 marine macroalgae of the French Brittany coast. J Appl Phycol 6:527–532CrossRefGoogle Scholar
  24. Ginzberg A, Cohen M, Sod-Moriah UA, Shany S, Rosenshtrauch A, Arad SM (2000) Chickens fed with biomass of the red microalga Porphyridium sp. have reduced blood cholesterol level and modified fatty acid composition in egg yolk. J Appl Phycol 12:325–330CrossRefGoogle Scholar
  25. Gundermann KJ, Kuenker A, Kuntz E, Droździk M (2011) Activity of essential phospholipids (EPL) from soybean in liver diseases. Pharmacol Reports 63:643–659CrossRefGoogle Scholar
  26. Hardouin K, Bedoux G, Burlot AS, Donnay-Moreno C, Bergé JP, Nyvall-Collén P, Bourgougnon N (2016) Enzyme-assisted extraction (EAE) for the production of antiviral and antioxidant extracts from the green seaweed Ulva armoricana (Ulvales, Ulvophyceae). Algal Res 16:233–239CrossRefGoogle Scholar
  27. Holdt SL, Kraan S (2011) Bioactive compounds in seaweed: functional food applications and legislation. J Appl Phycol 23:543–597CrossRefGoogle Scholar
  28. Hölzl G, Dörmann P (2007) Structure and function of glycoglycerolipids in plants and bacteria. Prog Lipid Res 46:225–243CrossRefPubMedGoogle Scholar
  29. Hossain Z, Kurihara H, Hosokawa M, Takahashi K (2005) Growth inhibition and induction of differentiation and apoptosis mediated by sodium butyrate in Caco-2 cells with algal glycolipids. Vitr Cell Dev Biol 41:154–159CrossRefGoogle Scholar
  30. Husted KS, Bouzinova EV (2016) The importance of n-6/n-3 fatty acids ratio in the major depressive disorder. Med 52:139–147Google Scholar
  31. Jannace PW, Lerman RH, Santos JI, Vitale JJ (1992) Effects of oral soy phosphatidylcholine on phagocytosis, arachidonate concentrations, and killing by human polymorphonuclear leukocytes. Am J Clin Nutr 56:599–603CrossRefPubMedGoogle Scholar
  32. Kendel M, Wielgosz-collin G, Bertrand S, Roussakis C, Bourgougnon N, Bedoux G (2015) Lipid composition, fatty acids and sterols in the seaweeds Ulva armoricana, and Solieria chordalis from Brittany (France): an analysis from nutritional, chemotaxonomic, and antiproliferative activity perspectives. Mar Drugs 13:5606–5628CrossRefPubMedPubMedCentralGoogle Scholar
  33. Klug RM, Benning C (2001) Two enzymes of diacylglyceryl-O-4′-(N,N,N,-trimethyl)homoserine biosynthesis are encoded by btaA and btaB in the purple bacterium Rhodobacter sphaeroides. Proc Natl Acad Sci U S A 98:5910–5915CrossRefPubMedPubMedCentralGoogle Scholar
  34. Küllenberg de Gaudry D, Taylor LA, Schneider M, Massing U (2012) Health effects of dietary phospholipids. Lipids Health Dis 11:1–16CrossRefGoogle Scholar
  35. Kumari P, Kumar M, Gupta V, Reddy CRK, Jha B (2010) Tropical marine macroalgae as potential sources of nutritionally important PUFAs. Food Chem 120:749–757CrossRefGoogle Scholar
  36. Kunzler K, Eichenberger W (1997) Betaine lipids and zwitterionic phospholipids in plants and fungi. Phytochemistry 46:883–892CrossRefPubMedGoogle Scholar
  37. Lahaye M, Robic A (2007) Structure and function properties of ulvan, a polysaccharide from green seaweeds. Biomacromolecules 8:1765–1774CrossRefPubMedGoogle Scholar
  38. Lawton RJ, Mata L, de Nys R, Paul NA (2013) Algal bioremediation of waste waters from land-based aquaculture using Ulva: selecting target species and strains. PLoS One 8:e77344CrossRefPubMedPubMedCentralGoogle Scholar
  39. Leal MC, Munro MHG, Blunt JW, Puga J, Jesus B, Calado R, Rosa R, Madeira C (2013) Biogeography and biodiscovery hotspots of macroalgal marine natural products. Nat Prod Rep 30:1380–1390CrossRefPubMedGoogle Scholar
  40. Li MH, Robinson EH, Tucker CS, Manning BB, Khoo L (2009) Effects of dried algae Schizochytrium sp., a rich source of docosahexaenoic acid, on growth, fatty acid composition, and sensory quality of channel catfish Ictalurus punctatus. Aquaculture 292:232–236CrossRefGoogle Scholar
  41. Lichtenberger LM, Romero JJ, Dial EJ (2009) Gastrointestinal safety and therapeutic efficacy of parenterally administered phosphatidylcholine-associated indomethacin in rodent model systems. Br J Pharmacol 157:252–257CrossRefPubMedPubMedCentralGoogle Scholar
  42. Lopes G, Daletos G, Proksch P, Andrade PB, Valentão P (2014) Anti-inflammatory potential of monogalactosyl diacylglycerols and a monoacylglycerol from the edible brown seaweed Fucus spiralis Linnaeus. Mar Drugs 12:1406–1418CrossRefPubMedPubMedCentralGoogle Scholar
  43. Maciel E, Leal MC, Lillebø AI, Domingues P, Domingues MR, Calado R (2016) Bioprospecting of marine macrophytes using MS-based lipidomics as a new approach. Mar Drugs 14:1–28CrossRefGoogle Scholar
  44. Marinho G, Nunes C, Sousa Pinto I, Pereira R, Rema P, Valente L (2013) The IMTA-cultivated Chlorophyta Ulva spp. as a sustainable ingredient in Nile tilapia (Oreochromis niloticus) diets. J Appl Phycol 25:1359–1367CrossRefGoogle Scholar
  45. Marshall JA, Nichols PD, Hallegraeff GM (2002) Chemotaxonomic survey of sterols and fatty acids in six marine raphidophyte algae. J Appl Phycol 14:255–265CrossRefGoogle Scholar
  46. McHugh DJ (2003) A guide to the seaweed industry. FAO Fisheries Technical Paper. Rome, p 105Google Scholar
  47. Melo T, Alves E, Azevedo V, Martins AS, Neves B, Domingues P, Calado R, Abreu H, Domingues MR (2015) Lipidomics as a new approach for the bioprospecting of marine macroalgae—unraveling the polar lipid and fatty acid composition of Chondrus crispus. Algal Res 8:181–191CrossRefGoogle Scholar
  48. Mozaffarian D, Ascherio A, Hu FB, Stampfer MJ, Willett WC, Siscovick DS, Rimm EB (2005) Interplay between different polyunsaturated fatty acids and risk of coronary heart disease in men. Circulation 111:157–164CrossRefPubMedPubMedCentralGoogle Scholar
  49. Msuya FE, Neori A (2008) Effect of water aeration and nutrient load level on biomass yield, N uptake and protein content of the seaweed Ulva lactuca cultured in seawater tanks. J Appl Phycol 20:1021–1031CrossRefGoogle Scholar
  50. Murphy RC (2015) Tandem mass spectrometry of lipids. The Royal Society of Chemistry, CambridgeGoogle Scholar
  51. Naylor J (1976) Production, trade and utilization of seaweeds and seaweed products. FAO Fisheries Technical Paper 1–73Google Scholar
  52. Neori A (2008) Essential role of seaweed cultivation in integrated multi-trophic aquaculture farms for global expansion of mariculture: an analysis. J Appl Phycol 20:567–570CrossRefGoogle Scholar
  53. Ohta K, Mizushina Y, Hirata N, Takemura M, Sugawara F, Matsukage A, Yoshida S, Sakaguchi K (1998) Sulfoquinovosyldiacylglycerol, KM043, a new potent inhibitor of eukaryotic DNA polymerases and HIV-reverse transcriptase type 1 from a marine red alga, Gigartina tenella. Chem Pharm Bull (Tokyo) 46:684–686CrossRefGoogle Scholar
  54. Okuyama H, Kobayashi T, Watanabe S (1997) Carcinogenesis and metastasis are affected by dietary n-6/n-3 fatty acids. In: Ohigashi H, Osawa T, Terao J, Watanabe S, Yoshikawa T (eds) Food factors for cancer prevention. Springer, Tokyo, pp 509–512CrossRefGoogle Scholar
  55. Parveez Ahamed AA, Rasheed UM, Peer Muhamed Noorani K, Reehana N, Santhoshkumar S, Mohamed Imran YM, Alharbi SN, Arunachalam C, Alharbi AS, Akbarsha MA, Thajuddin N (2017) In vitro antibacterial activity of MGDG-palmitoyl from Oscillatoria acuminata NTAPC05 against extended-spectrum β-lactamase producers. J Antibiot (Tokyo) 70:754–762CrossRefGoogle Scholar
  56. Patterson RE, Flatt SW, Newman VA, Natarajan L, Rock CL, Thomson CA, Caan BJ, Parker BA, Pierce JP (2011) Marine fatty acid intake is associated with breast cancer prognosis. J Nutr 141:201–206CrossRefPubMedGoogle Scholar
  57. Peña-rodríguez A, Mawhinney TP, Ricque-marie D, Cruz-suárez LE (2011) Chemical composition of cultivated seaweed Ulva clathrata (Roth) C . Agardh. Food Chem 129:491–498CrossRefGoogle Scholar
  58. Plouguerné E, da Gama BAP, Pereira RC, Barreto-Bergter E (2014) Glycolipids from seaweeds and their potential biotechnological applications. Front Cell Infect Microbiol 4:1–5Google Scholar
  59. 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 145:932–940CrossRefPubMedGoogle Scholar
  60. Rajauria G (2015) Seaweeds: a sustainable feed source for livestock and aquaculture. In: seaweed sustainability: food and non-food applications. Elsevier Inc., University College Dublin, Lyons Research Farm, Newcastle, Co. Dublin, Ireland, pp 389–420Google Scholar
  61. Ridler N, Wowchuk M, Robinson B, Barrington K, Chopin T, Robinson S, Page F, Reid G, Szemerda M, Sewuster J, Boyne-Travis S (2007) Integrated multi-trophic aquaculture (IMTA): a potential strategic choice for farmers. Aquac Econ Manag 11:99–110CrossRefGoogle Scholar
  62. Riekhof WR, Andre C, Benning C (2005) Two enzymes, BtaA and BtaB, are sufficient for betaine lipid biosynthesis in bacteria. Arch Biochem Biophys 441:96–105CrossRefPubMedGoogle Scholar
  63. Roche SA, Leblond JD (2010) Betaine lipids in chlorarachniophytes. Phycol Res 58:298–305CrossRefGoogle Scholar
  64. Roohinejad S, Koubaa M, Barba FJ, Saljoughian S, Amid M, Greiner R (2016) Application of seaweeds to develop new food products with enhanced shelf-life, quality and health-related beneficial properties. Food Res Int 99:1066–1083CrossRefPubMedGoogle Scholar
  65. Rozentsvet OA, Nesterov VN (2012) Lipids and fatty acids from Ulva intestinalis from estuaries of the Caspian basin (elton region). Chem Nat Compd 48:544–547CrossRefGoogle Scholar
  66. Shpigel M, Guttman L, Shauli L, Odintsov V, Ben-Ezra D, Harpaz S (2017) Ulva lactuca from an integrated multi-trophic aquaculture (IMTA) biofilter system as a protein supplement in gilthead seabream (Sparus aurata) diet. Aquaculture 481:112–118CrossRefGoogle Scholar
  67. Simopoulos AP (2002) The importance of the ratio of omega-6 / omega-3 essential fatty acids. Biomed Pharmacother 56:365–379CrossRefPubMedGoogle Scholar
  68. Simopoulos AP (2008) The importance of the omega-6/omega-3 fatty acid ratio in cardiovascular disease and other chronic diseases. Exp Biol Med 233:674–688CrossRefGoogle Scholar
  69. Simopoulos AP (2016) An increase in the Omega-6/Omega-3 fatty acid ratio increases the risk for obesity. Nutrients 8:1–17CrossRefGoogle Scholar
  70. Siriwardhana N, Kalupahana NS, Moustaid-Moussa N (2012) Health benefits of n-3 polyunsaturated fatty acids. Eicosapentaenoic acid and docosahexaenoic acid. Adv Food Nutr Res 65:211–222CrossRefPubMedGoogle Scholar
  71. Stengel D, Connan S, Popper Z (2011) Algal Chemodiversity and bioactivity: sources of natural variability and implications for commercial application. Biotechnol Adv 29:483–501CrossRefPubMedGoogle Scholar
  72. Takahashi Y, Itoh K, Ishii M, Itabashi Y (2002) Induction of larval settlement and metamorphosis of the sea urchin Strongylocentrotus intermedius by glycoglycerolipids from the green alga Ulvella lens. Mar Biol 140:763–771CrossRefGoogle Scholar
  73. van Ginneken VJ, Helsper JP, de Visser W, van Keulen H, Brandenburg WA (2011) Polyunsaturated fatty acids in various macroalgal species from North Atlantic and tropical seas. Lipids Health Dis 10:1–8CrossRefGoogle Scholar
  74. van Ginneken V, Gittenberger A, Rensing M, de Vries E, Peeters ETHM, Verheij E (2017) Seaweed competition: Ulva sp. has the potential to produce the betaine lipid diacylglyceryl-O-4′-(N,N,N,-trimethyl) homoserine (DGTS) in order to replace phosphatidylcholine ( PC ) under phosphate-limiting conditions in the P-limited Dutch Wadden Sea and outcompete an aggressive non-indigenous Gracilaria vermiculophylla red drift algae out of this unique Unesco world heritage coastal area. Oceanogr Fish 2:555596Google Scholar
  75. Vieler A, Wilhelm C, Goss R, Süß R, Schiller J (2007) The lipid composition of the unicellular green alga Chlamydomonas reinhardtii and the diatom Cyclotella meneghiniana investigated by MALDI-TOF MS and TLC. Chem Phys Lipids 150:143–155CrossRefPubMedGoogle Scholar
  76. Wang H, Li YL, Shen WZ, Rui W, Ma XJ, Cen YZ (2007) Antiviral activity of a sulfoquinovosyldiacylglycerol (SQDG) compound isolated from the green alga Caulerpa racemosa. Bot Mar 50:185–190Google Scholar
  77. Wijesekara I, Lang M, Marty C, Gemin M-P, Boulho R, Douzenel P, Wickramasinghe I, Bedoux G, Bourgougnon N (2017) Different extraction procedures and analysis of protein from Ulva sp. in Brittany, France. J Appl Phycol 29:2503–2511CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018
corrected publication November/2018

Authors and Affiliations

  • Diana Lopes
    • 1
    • 2
    • 3
  • Ana S. P. Moreira
    • 1
    • 3
  • Felisa Rey
    • 1
    • 2
    • 3
  • Elisabete da Costa
    • 1
    • 2
    • 3
  • Tânia Melo
    • 1
  • Elisabete Maciel
    • 1
    • 2
    • 3
  • Andreia Rego
    • 4
  • Maria H. Abreu
    • 4
  • Pedro Domingues
    • 1
  • Ricardo Calado
    • 2
  • Ana I. Lillebø
    • 2
  • M. Rosário Domingues
    • 1
    • 3
  1. 1.Centro de Espectrometria de Massa, Departamento de Química & QOPNAUniversidade de AveiroAveiroPortugal
  2. 2.Departamento de Biologia & CESAM & ECOMAREUniversidade de AveiroAveiroPortugal
  3. 3.Departamento de Química & CESAM & ECOMARE, Universidade de Aveiro, Campus Universitário de SantiagoAveiroPortugal
  4. 4.ALGAplus - Produção e comercialização de algas e seus derivados, LdaÍlhavoPortugal

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