{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,4]],"date-time":"2026-05-04T18:18:07Z","timestamp":1777918687821,"version":"3.51.4"},"reference-count":58,"publisher":"MDPI AG","issue":"10","license":[{"start":{"date-parts":[[2020,9,29]],"date-time":"2020-09-29T00:00:00Z","timestamp":1601337600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia","doi-asserted-by":"publisher","award":["UIDB\/50006\/2020; CEECIND\/01120\/2017"],"award-info":[{"award-number":["UIDB\/50006\/2020; CEECIND\/01120\/2017"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Foods"],"abstract":"<jats:p>Seaweeds are a recognized source of bioactive compounds and techno-functional ingredients. However, its protein fraction is still underexplored. The aim of this study was to determine the total and free amino acid profile and protein content of four seaweeds species (Porphyra dioica, Porphyra umbilicalis,Gracilaria vermiculophylla, and Ulva rigida) produced in an integrated multi-trophic aquaculture system, while assessing their protein quality. Samples were submitted to acid and alkaline hydrolysis (total amino acids) and to an aqueous extraction (free amino acids) followed by an automated online derivatization procedure, and analyzed by reverse phase-high performance liquid chromatography. Protein-, non-protein and total-nitrogen were quantified by the Kjeldahl method. Crude and true protein contents were estimated based on the nitrogen and amino acid composition. Protein quality was assessed based on the amino acids profile. Porphyra species presented the highest protein content compared to the remaining three seaweed species tested. All samples presented a complete profile of essential amino acids and a high quality protein profile, according to World Health Organization and Food and Agriculture Organization standards. Methionine and tryptophan were the first limiting amino acids in all species. Red species (Porphyra and Gracilaria) presented high levels of free alanine, glutamic, and aspartic acids. The results highlight the potential of using seaweeds as an alternative and sustainable source of protein and amino acids for human nutrition and industrial food processing.<\/jats:p>","DOI":"10.3390\/foods9101382","type":"journal-article","created":{"date-parts":[[2020,9,29]],"date-time":"2020-09-29T20:56:22Z","timestamp":1601412982000},"page":"1382","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":153,"title":["Amino Acid Profile and Protein Quality Assessment of Macroalgae Produced in an Integrated Multi-Trophic Aquaculture System"],"prefix":"10.3390","volume":"9","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-4104-4435","authenticated-orcid":false,"given":"Marlene","family":"Machado","sequence":"first","affiliation":[{"name":"LAQV, REQUIMTE, Department of Chemical Sciences, Faculty of Pharmacy, University of Porto, 4050-313 Porto, Portugal"}]},{"given":"Susana","family":"Machado","sequence":"additional","affiliation":[{"name":"LAQV, REQUIMTE, Department of Chemical Sciences, Faculty of Pharmacy, University of Porto, 4050-313 Porto, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4597-8198","authenticated-orcid":false,"given":"Filipa B.","family":"Pimentel","sequence":"additional","affiliation":[{"name":"LAQV, REQUIMTE, Department of Chemical Sciences, Faculty of Pharmacy, University of Porto, 4050-313 Porto, Portugal"}]},{"given":"Victor","family":"Freitas","sequence":"additional","affiliation":[{"name":"LAQV, REQUIMTE, Department of Chemical and Biochemistry, Faculty of Sciences, University of Porto, 4169-007 Porto, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5053-513X","authenticated-orcid":false,"given":"Rita C.","family":"Alves","sequence":"additional","affiliation":[{"name":"LAQV, REQUIMTE, Department of Chemical Sciences, Faculty of Pharmacy, University of Porto, 4050-313 Porto, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6767-6596","authenticated-orcid":false,"given":"M. Beatriz P. P.","family":"Oliveira","sequence":"additional","affiliation":[{"name":"LAQV, REQUIMTE, Department of Chemical Sciences, Faculty of Pharmacy, University of Porto, 4050-313 Porto, Portugal"}]}],"member":"1968","published-online":{"date-parts":[[2020,9,29]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"218","DOI":"10.1111\/j.1529-8817.2011.00969.x","article-title":"Bioactive proteins, peptides, and amino acids from macroalgae","volume":"47","author":"Harnedy","year":"2011","journal-title":"J. Phycol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1066","DOI":"10.1016\/j.foodres.2016.08.016","article-title":"Application of seaweeds to develop new food products with enhanced shelf-life, quality and health-related beneficial properties","volume":"99","author":"Roohinejad","year":"2017","journal-title":"Food Res. Int."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"993","DOI":"10.1007\/s10811-014-0375-6","article-title":"Effect of seaweed liquid extracts and plant growth regulators on in vitro mass propagation of brinjal (Solanum melongena L.) through hypocotyl and leaf disc explants","volume":"27","author":"Satish","year":"2015","journal-title":"J. Appl. Phycol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"27254","DOI":"10.1007\/s11356-017-0296-4","article-title":"Rapid biosynthesized AgNPs from Gelidiella acerosa aqueous extract mitigates quorum sensing mediated biofilm formation of Vibrio species\u2014An in vitro and in vivo approach","volume":"24","author":"Satish","year":"2017","journal-title":"Environ. Sci. Pollut. Res"},{"key":"ref_5","first-page":"949","article-title":"Algae as nutritional and functional food sources: Revisiting our understanding","volume":"29","author":"Wells","year":"2016","journal-title":"Environ. Biol. Fishes"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1093\/nutrit\/nuy066","article-title":"Risks and benefits of consuming edible seaweeds","volume":"77","author":"Cherry","year":"2019","journal-title":"Nutr. Rev."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"194","DOI":"10.1016\/j.foodhyd.2018.07.047","article-title":"Extraction of proteins from two marine macroalgae, Ulva sp. and Gracilaria sp., for food application, and evaluating digestibility, amino acid composition and antioxidant properties of the protein concentrates","volume":"87","author":"Kazir","year":"2019","journal-title":"Food Hydrocoll."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"264","DOI":"10.1016\/j.foodchem.2018.06.145","article-title":"Seaweeds from the Portuguese coast as a source of proteinaceous material: Total and free amino acid composition profile","volume":"269","author":"Vieira","year":"2018","journal-title":"Food Chem."},{"key":"ref_9","unstructured":"Wu, G. (2013). Amino Acids: Biochemistry and Nutrition, CRC Press. [1st ed.]."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.neuint.2017.10.011","article-title":"Dysregulation of methionine metabolism in multiple sclerosis","volume":"112","author":"Singhal","year":"2018","journal-title":"Neurochem. Int."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1186\/s13041-020-00601-9","article-title":"Arginine is neuroprotective through suppressing HIF-1\u03b1\/LDHA-mediated inflammatory response after cerebral ischemia\/reperfusion injury","volume":"13","author":"Chen","year":"2020","journal-title":"Mol. Brain"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"72","DOI":"10.15430\/JCP.2019.24.2.72","article-title":"Therapeutic Effects of Amino Acids in Liver Diseases: Current Studies and Future Perspectives","volume":"24","author":"Lee","year":"2019","journal-title":"J. Cancer Prev."},{"key":"ref_13","first-page":"I","article-title":"The global status of seaweed production, trade and utilization","volume":"Volume 124","author":"Ferdouse","year":"2018","journal-title":"Globefish Research Programme"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1373","DOI":"10.1007\/s10499-017-0120-7","article-title":"Seaweed aquaculture in Norway: Recent industrial developments and future perspectives","volume":"25","author":"Rebours","year":"2017","journal-title":"Aquac. Int."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1","DOI":"10.4490\/algae.2017.32.3.3","article-title":"Seaweed aquaculture: Cultivation technologies, challenges and its ecosystem services","volume":"32","author":"Kim","year":"2017","journal-title":"Algae"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1016\/j.tifs.2019.12.008","article-title":"Integrated multitrophic aquaculture systems\u2014Potential risks for food safety","volume":"96","author":"Rosa","year":"2020","journal-title":"Trends Food Sci. Technol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"136","DOI":"10.1016\/j.aquaculture.2018.02.035","article-title":"Is Europe ready for integrated multi-trophic aquaculture? A survey on the perspectives of European farmers and scientists with IMTA experience","volume":"490","author":"Kleitou","year":"2018","journal-title":"Aquaculture"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"174","DOI":"10.1016\/j.aquaculture.2018.07.051","article-title":"Application of open water integrated multi-trophic aquaculture to intensive monoculture: A review of the current status and challenges in Korea","volume":"497","author":"Park","year":"2018","journal-title":"Aquaculture"},{"key":"ref_19","first-page":"511","article-title":"The protein content of seaweeds: A universal nitrogen-to-protein conversion factor of five","volume":"28","author":"Angell","year":"2015","journal-title":"Environ. Biol. Fishes"},{"key":"ref_20","first-page":"1671","article-title":"Evaluation of IMTA-produced seaweeds (Gracilaria, Porphyra, and Ulva) as dietary ingredients in Nile tilapia, Oreochromis niloticus L., juveniles. Effects on growth performance and gut histology","volume":"27","author":"Silva","year":"2014","journal-title":"Environ. Biol. Fishes"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1016\/j.tplants.2010.10.004","article-title":"Porphyra: A marine crop shaped by stress","volume":"16","author":"Blouin","year":"2011","journal-title":"Trends Plant Sci."},{"key":"ref_22","unstructured":"Chen, J., and Pu, X. (2005). Cultured Aquatic Species Information Programme. Porphyra spp., Food and Agriculture Organization of the United Nations. Available online: http:\/\/www.fao.org\/fishery\/culturedspecies\/Porphyra_spp\/en."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1016\/j.aquaculture.2010.12.036","article-title":"IMTA with Gracilaria vermiculophylla: Productivity and nutrient removal performance of the seaweed in a land-based pilot scale system","volume":"312","author":"Abreu","year":"2011","journal-title":"Aquaculture"},{"key":"ref_24","first-page":"1369","article-title":"Lipidomic signature of the green macroalgae Ulva rigida farmed in a sustainable integrated multi-trophic aquaculture","volume":"31","author":"Lopes","year":"2018","journal-title":"Environ. Biol. Fishes"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"126940","DOI":"10.1016\/j.foodchem.2020.126940","article-title":"A study on the protein fraction of coffee silverskin: Protein\/non-protein nitrogen and free and total amino acid profiles","volume":"326","author":"Machado","year":"2020","journal-title":"Food Chem."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Oser, B.L. (1959). An Integrated Essential Amino Acid Index for Predicting the Biological Value of Proteins. Protein and Amino Acid Nutrition, Elsevier.","DOI":"10.1016\/B978-0-12-395683-5.50014-6"},{"key":"ref_27","unstructured":"FAO\/WHO\/UNU (2007). Protein and Amino Acid Requirements in Human Nutrition. Report of a Joint FAO\/WHO\/UNU Expert Consultation, World Health Organization."},{"key":"ref_28","unstructured":"AOAC (2012). Official Method of Analysis: Association of Analytical Chemists, AOAC International. [19th ed.]."},{"key":"ref_29","first-page":"1001","article-title":"Amino acid composition, protein content, and nitrogen-to-protein conversion factors of 21 seaweed species from Norwegian waters","volume":"29","author":"Biancarosa","year":"2016","journal-title":"Environ. Biol. Fishes"},{"key":"ref_30","first-page":"677","article-title":"Protein content, amino acid composition and nitrogen-to-protein conversion factors of Ulva rigida and Ulva capensis from natural populations and Ulva lactuca from an aquaculture system, in South Africa","volume":"25","author":"Shuuluka","year":"2012","journal-title":"Environ. Biol. Fishes"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"302","DOI":"10.1016\/j.foodchem.2016.10.066","article-title":"Chemical composition and physicochemical properties of tropical red seaweed","volume":"221","author":"Chan","year":"2017","journal-title":"Gracilaria Changii. Food Chem."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"585","DOI":"10.1016\/j.foodchem.2009.10.028","article-title":"Lipid, fatty acid, protein, amino acid and ash contents in four Brazilian red algae species","volume":"120","author":"Gressler","year":"2010","journal-title":"Food Chem."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1016\/j.jfca.2016.09.004","article-title":"Amino acid content in seaweeds from the Magellan Straits (Chile)","volume":"53","year":"2016","journal-title":"J. Food Compos. Anal."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1016\/j.foodchem.2014.04.119","article-title":"Edible Azorean macroalgae as source of rich nutrients with impact on human health","volume":"164","author":"Paiva","year":"2014","journal-title":"Food Chem."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"208","DOI":"10.1111\/j.1529-8817.2010.00933.x","article-title":"Phycobilin content of the conchocelis phase of alaskan Porphyra (Bangiales, Rhodophyta) species: Responses to environmental variables","volume":"47","author":"Lin","year":"2010","journal-title":"J. Phycol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"192","DOI":"10.1111\/j.1529-8817.1981.tb00839.x","article-title":"Chemical composition and structure of the cell walls of the conchocelis and thallus phases of Porphyra tenera (Rhodophyceae)","volume":"17","author":"Mukai","year":"2008","journal-title":"J. Phycol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"891","DOI":"10.1016\/j.foodchem.2006.09.041","article-title":"Amino acids, fatty acids, and dietary fibre in edible seaweed products","volume":"103","author":"Dawczynski","year":"2007","journal-title":"Food Chem."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"212","DOI":"10.1016\/j.foodres.2018.05.037","article-title":"Characterization of Spanish powdered seaweeds: Composition, antioxidant capacity and technological properties","volume":"111","author":"Fuentes","year":"2018","journal-title":"Food Res. Int."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1021\/jf9400167","article-title":"Nutritional value of proteins from different food sources. A Review","volume":"44","author":"Friedman","year":"1996","journal-title":"J. Agric. Food Chem."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"EFSA Panel on Dietetic Products, and Nutrition and Allergies (NDA) (2012). Scientific opinion on dietary reference values for protein. EFSA J., 10, 2557.","DOI":"10.2903\/j.efsa.2012.2557"},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Monirujjaman, M., and Ferdouse, A. (2014). Metabolic and physiological roles of branched-chain amino acids. Adv. Mol. Biol., 2014.","DOI":"10.1155\/2014\/364976"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"492","DOI":"10.1016\/j.meatsci.2009.06.031","article-title":"Composition and antioxidant capacity of low-salt meat emulsion model systems containing edible seaweeds","volume":"83","author":"Bastida","year":"2009","journal-title":"Meat Sci."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"170","DOI":"10.1016\/j.tifs.2020.01.011","article-title":"Plant proteins as high-quality nutritional source for human diet","volume":"97","author":"Moreno","year":"2020","journal-title":"Trends Food Sci. Technol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"210","DOI":"10.1016\/j.anifeedsci.2018.05.003","article-title":"Amino acid profiles of nine seaweed species and their In Situ degradability in dairy cows","volume":"241","author":"Gaillard","year":"2018","journal-title":"Anim. Feed. Sci. Technol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1016\/j.foodchem.2013.11.040","article-title":"Amino acid composition of algal products and its contribution to RDI","volume":"151","author":"Samek","year":"2014","journal-title":"Food Chem."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1757","DOI":"10.1111\/1750-3841.13778","article-title":"Nutritional and functional bioactivity value of selected azorean macroalgae: Ulva compressa, Ulva rigida, Gelidium microdon, and Pterocladiella capillacea","volume":"82","author":"Paiva","year":"2017","journal-title":"J. Food Sci."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1111\/j.1440-1835.2002.tb00156.x","article-title":"Amino acid composition, protein content and calculation of nitrogen-to-protein conversion factors for 19 tropical seaweeds","volume":"50","author":"Barbarino","year":"2002","journal-title":"Phycol. Res."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1007\/s11130-018-0660-7","article-title":"Nutritional value of commercial protein-rich plant products","volume":"73","author":"Mattila","year":"2018","journal-title":"Plant Foods Hum. Nutr."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1007\/s00726-008-0152-4","article-title":"Amino acids and gut function","volume":"37","author":"Wang","year":"2008","journal-title":"Amino Acids"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1155\/2017\/1716701","article-title":"Multifarious beneficial effect of nonessential amino acid, glycine: A review","volume":"2017","author":"Razak","year":"2017","journal-title":"Oxidative Med. Cell. Longev."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"4735","DOI":"10.1172\/JCI57549","article-title":"Oral L-serine supplementation reduces production of neurotoxic deoxysphingolipids in mice and humans with hereditary sensory autonomic neuropathy type 1","volume":"121","author":"Garofalo","year":"2011","journal-title":"J. Clin. Investig."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"216","DOI":"10.1111\/jpy.12154","article-title":"Variation in amino acid content and its relationship to nitrogen content and growth rate in Ulva ohnoi (Chlorophyta)","volume":"50","author":"Angell","year":"2014","journal-title":"J. Phycol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"1299","DOI":"10.2331\/suisan.41.1299","article-title":"Studies on the flavor substances of \u201cnori\u201d, the dried laver Porphyra spp. II. Free amino acids and 5\u201d-nucleotides","volume":"41","author":"Noda","year":"1975","journal-title":"Bull. Jpn. Soc. Sci. Fish."},{"key":"ref_54","first-page":"149","article-title":"Proximate, mineral and amino acid composition of dried laver (Porphyra spp.) seaweed","volume":"6","author":"Admassu","year":"2018","journal-title":"J. Acad. Ind. Res."},{"key":"ref_55","unstructured":"FAO (2013). Dietary Protein Quality Evaluation in Human Nutrition, Food and Agriculture Organization of the United Nations. Report of an FAO Expert Consultation."},{"key":"ref_56","first-page":"223","article-title":"Biochemical composition and physicochemical properties of two red seaweeds (Gracilaria fisheri and G. tenuistipitata) from the Pattani Bay in Southern Thailand","volume":"34","author":"Benjama","year":"2012","journal-title":"Songklanakarin J. Sci. Technol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1016\/0022-0981(92)90192-D","article-title":"Biochemical composition of microalgae from the green algal classes Chlorophyceae and Prasinophyceae. 1. Amino acids, sugars and pigments","volume":"161","author":"Brown","year":"1992","journal-title":"J. Exp. Mar. Biol. Ecol."},{"key":"ref_58","unstructured":"World Health Organization (2007). Iodine Deficiency in Europe: A Continuing Public Health Problem, World Health Organization."}],"container-title":["Foods"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2304-8158\/9\/10\/1382\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T10:15:03Z","timestamp":1760177703000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2304-8158\/9\/10\/1382"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,9,29]]},"references-count":58,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2020,10]]}},"alternative-id":["foods9101382"],"URL":"https:\/\/doi.org\/10.3390\/foods9101382","relation":{},"ISSN":["2304-8158"],"issn-type":[{"value":"2304-8158","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,9,29]]}}}