Skip to main content
Log in

LC-MSn profiling reveals seasonal variation in the composition of Osmundea pinnatifida (Hudson) Stackhouse

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

The metabolic profile of seaweeds can fluctuate depending on environmental factors and biotic/abiotic stresses. Osmundea pinnatifida is a red alga, known as Pepper Dulse in the UK, harvested from the wild and sold as seasoning due to its unique peppery taste. This paper highlights the seasonal variation in the compositional profile of biomass harvested from a single location over 12 months, linking this to variation in flavour. Hydrophilic interaction chromatography with tandem mass spectrometry (HILIC-PDA-MS) analysis putatively identified 33 major components. Some of these have been noted in other Osmundea species (e.g. chilenones) or identified as osmoregulators in other seaweeds (e.g. mycosporines, betaines or sugar-glycerol components). Central metabolites were identified (e.g. amino or organic acids), as were others not previously recorded in seaweeds. The metabolites varied in abundance across the seasons and could be allocated into five trends those that decreased in summer/increased in winter, increased or decreased in autumn, increased in summer/decreased in winter, those which did not vary, and those with no apparent pattern. Components were identified that increased in abundance in winter when the flavour of Pepper Dulse is more potent. Many of these components were extracted under aqueous conditions that replicate those in the mouth and could therefore contribute to the flavour of this seaweed. This information increases our knowledge about the biochemical composition and its seasonal variation of Osmundea pinnatifida providing insights on compounds that might be related to its taste, thus providing information relevant to future commercialization and harvest management of this species.

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
Fig. 3
Fig. 4

Similar content being viewed by others

Data availability

The authors confirm that all relevant data supporting the findings of this study are included in the article and its supplementary information files.

References

  • Aaronson S (1986) A role for algae as human food in antiquity. Food Foodways 1:311–315

    Article  CAS  PubMed  Google Scholar 

  • Aguilera J, Bischof K, Karsten U, Hanelt D, Wiencke C (2002) Seasonal variation in ecophysiological patterns in macroalgae from an Arctic fjord. II. Pigment accumulation and biochemical defence systems against high light stress. Mar Biol 140:1087–1095

    Article  CAS  Google Scholar 

  • Ahmad VU, Ali MS (1991) Terpenoids from marine red alga Laurencia pinnatifida. Phytochemistry 30:4172–4174

    Article  CAS  Google Scholar 

  • Anantharaman P, Devi GK, Manivannan K, Thangavel B (2011) Vitamin-C content of some marine macroalgae from Gulf of Mannar marine biosphere reserve, southeast coast of India. Plant Arch 11:343–346

    Google Scholar 

  • Ascêncio S, Orsato A, França R, Duarte ME, Noseda M (2006) Complete H-1 and C-13 NMR assignment of digeneaside, a low-molecular-mass carbohydrate produced by red seaweeds. Carbohydr Res 341:677–682

    Article  PubMed  CAS  Google Scholar 

  • Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216

    Article  CAS  Google Scholar 

  • Atta-ur-Rahman AVU, Bano S, Abbas SA, Alvi KA, Ali MS, Lu HSM, Clardy J (1988) Pinnatazane, a bridged cyclic ether sesquiterpene from Laurencia pinnatifida. Phytochemistry 27:3879–3880

    Article  Google Scholar 

  • Bano S, Ali M, Ahmad V (1988) Marine natural products, VIII: two minor halogenated sesquiterpenoids from the red alga Laurencia pinnatifida. Sci Pharm 56:125

    CAS  Google Scholar 

  • Barceló-Villalobos M, Figueroa FL, Korbee N, Álvarez-Gómez F, Abreu MH (2017) Production of mycosporine-like amino acids from Gracilaria vermiculophylla (Rhodophyta) cultured through one year in an Integrated Multi-trophic Aquaculture (IMTA) system. Mar Biotechnol 19:246–254

    Article  CAS  Google Scholar 

  • Barrow KD, Karsten U, King RI, West JA (1995) Floridoside in the genus Laurencia (Rhodomelaceae: Ceramiales)–a chemosystematic study. Phycologia 34:279–283

    Article  Google Scholar 

  • Bazes A, Silkina A, Douzenel P, Faÿ F, Kervarec N, Morin D, Berge J-P, Bourgougnon N (2009) Investigation of the antifouling constituents from the brown alga Sargassum muticum (Yendo) Fensholt. J Appl Phycol 21:395–403

    Article  CAS  Google Scholar 

  • Bedoux G, Hardouin K, Marty C, Taupin L, Vandanjon L, Bourgougnon N (2014) Chemical characterization and photoprotective activity measurement of extracts from the red macroalga Solieria chordalis. Bot Mar 57:291

    Article  CAS  Google Scholar 

  • Biancacci C (2019) Towards a sustainable production of Osmundea pinnatifida: insight into the cultivation and biochemical composition of the species. Doctoral Thesis, p 342

  • Bittner M, Silva M, Paul V, Fenical W (1985) a rearranged chamigrene derivative and its potential biogenetic precursor from a new species of the marine red algal genus Laurencia (Rhodomelaceae). Phytochemistry 24:987–989

    Article  CAS  Google Scholar 

  • Bixler HJ, Porse H (2011) A decade of change in the seaweed hydrocolloids industry. J Appl Phycol 23:321–335

    Article  Google Scholar 

  • Blunden G (2003) Betaines in the plant kingdom and their use in ameliorating stress conditions in plants. Acta Hortic 597:23–29

    Article  CAS  Google Scholar 

  • Blunden G, Gorden SM (1986) Betaines and their sulphonio analogues in marine algae. In: Round FE, Chapman DJ (eds) Progress in Phycological Research, vol 4. Biopress, Bristol, pp 39–80

    Google Scholar 

  • Borowitzka MA (2013) High-value products from microalgae-their development and commercialisation. J Appl Phycol 25:743–756

    Article  CAS  Google Scholar 

  • Brito I, Cueto M, Dorta E, Darias J (2002) Bromocyclococanol, a halogenated sesquiterpene with a novel carbon skeleton from the red alga Laurencia obtusa. Tetrahedron Lett 43:2551–2553

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Callow ME, Callow JE (2002) Marine biofouling: a sticky problem. Biologist (London) 49:10–14

    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 54:880–890

    Article  CAS  Google Scholar 

  • Cardozo KHM, Carvalho VM, Pinto E, Colepicolo P (2006) Fragmentation of mycosporine-like amino acids by hydrogen/deuterium exchange and electrospray ionisation tandem mass spectrometry. Rapid Commn Mass Spectrom 20:253–258

    Article  CAS  Google Scholar 

  • Carreto JI, Carignan MO (2011) Mycosporine-like amino acids: relevant secondary metabolites. Chemical and ecological aspects. Mar Drugs 9:387–446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Černá M (2011) Seaweed proteins and amino acids as nutraceuticals. Adv Food Nutr Res 64:297–312

    Article  PubMed  CAS  Google Scholar 

  • Chandrashekar J, Hoon M, Ryba N, Zuker C (2006) The receptors and cells for mammalian taste. Nature 444:288–294

    Article  CAS  PubMed  Google Scholar 

  • Cole KM, Sheath RG (2011) Biology of the Red algae. Cambridge University Press, Cambridge, 517

    Google Scholar 

  • Courtois A, Simon-Colin C, Boisset C, Berthou C, Deslandes E, Guézennec J, Bordron A (2008) Floridoside extracted from the red alga Mastocarpus stellatus is a potent activator of the classical complement pathway. Mar Drugs 6:407–417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Craigie JS (2010) Seaweed extract stimuli in plant science and agriculture. J Appl Phycol 23:371–393

    Article  CAS  Google Scholar 

  • Dailey A, Vuong QV (2015) Effect of extraction solvents on recovery of bioactive compounds and antioxidant properties from macadamia (Macadamia tetraphylla) skin waste. J Food Sci Technol 1:1115646

    Google Scholar 

  • Davis GDJ, Vasanthi AHR (2011) Seaweed metabolite database (SWMD): a database of natural compounds from marine algae. Bioinformatics 5:361–364

    Google Scholar 

  • de Nys R, Dworjanyn SA, Steinberg PD (1998) A new method for determining surface concentrations of marine natural products on seaweeds. Mar Ecol Prog Ser 162:79–87

    Article  Google Scholar 

  • Debonnel G, Beauchesne L, de Montigny C (1989) Domoic acid, the alleged “mussel toxin,” might produce its neurotoxic effect through kainate receptor activation: an electrophysiological study in the dorsal hippocampus. Can J Physiol Pharmacol 67:29–33

    Article  CAS  PubMed  Google Scholar 

  • Dillehay TD, Ramírez C, Pino M, Collins MB, Rossen J, Pino-Navarro JD (2008) Monte Verde: seaweed, food, medicine, and the peopling of South America. Science 320:784–786

    Article  CAS  PubMed  Google Scholar 

  • Dominguez H (2013) Functional ingredients from algae for foods and nutraceuticals. Woodhead Publishing Ltd, Oxford,

  • Dunlap WC, Yamamoto Y (1995) Small-molecule antioxidants in marine organisms: antioxidant activity of mycosporine-glycine. Comp Biochem Physiol B 112:105–114

    Article  Google Scholar 

  • Dworjanyn SA, De Nys R, Steinberg PD (1999) Localisation and surface quantification of secondary metabolites in the red alga Delisea pulchra. Mar Biol 133:727–736

    Article  CAS  Google Scholar 

  • Ekman P, Yu S, Pedersen M (1991) Effects of altered salinity, darkness and algal nutrient status on floridoside and starch content, α-galactosidase activity and agar yield of cultivated Gracilaria sordida. Br Phycol J 26:123–131

    Article  Google Scholar 

  • Erickson KL (1983) Constituents of Laurencia. In: Scheuer PJ (ed) Marine natural products: chemical and biological perspectives, vol 5. Academic Press, New York, pp 131–257

    Chapter  Google Scholar 

  • FAO (2014) The state of World Fisheries and Aquaculture. Rome, Italy. pp. 243

  • FAO (2018) The state of World Fisheries and Aquaculture. Rome, Italy. pp. 227

  • FAO (2020) The state of world fisheries and aquaculture: sustainability in action. Rome (Italy), pp., 1–206

  • Faulkner DJ (1986) Marine natural products. Nat Prod Rep 3:1–33

  • Fehling J, Davidson K, Bolch CJ, Bates SS (2004) Growth and domoic acid production of Pseudo-nitzschia seriata (P.T. Cleve) H. Peragallo (Bacillariophyceae) under phosphate and silicate limitation. J Phycol 40:674–683

    Article  CAS  Google Scholar 

  • Fraga BM (2012) Natural sesquiterpenoids. Nat Prod Rep 29:1334–1366

    Article  CAS  PubMed  Google Scholar 

  • Gaubert J, Payri C, Vieira C, Solanki H, Thomas O (2019) High metabolic variation for seaweeds in response to environmental changes: a case study of the brown algae Lobophora in coral reefs. Sci Rep 9:993

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gianturco MA, Giammarino AS, Friedel P, Flanagan V (1964) The volatile constituents of coffee—IV: furanic and pyrrolic compounds. Tetrahedron Lett 20:2951–2961

    Article  CAS  Google Scholar 

  • Gika HG, Theodoridis GA, Plumb RS, Wilson ID (2014) Current practice of liquid chromatography–mass spectrometry in metabolomics and metabonomics. J Pharm Biomed Anal 87:12–25

    Article  CAS  PubMed  Google Scholar 

  • Greff S, Zubia M, Payri C, Thomas OP, Pćrez T (2017a) Chemogeography of the red macroalgae Asparagopsis: metabolomics, bioactivity, and relation to invasiveness. Metabolomics 13:33

    Article  CAS  Google Scholar 

  • Greff S, Aires T, Serrão EA, Engelen AH, Thomas OP, Pćrez T (2017b) The interaction between the proliferating macroalga Asparagopsis taxiformis and the coral Astroides calycularis induces changes in microbiome and metabolomic fingerprints. Sci Rep 7:42625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grina F, Ullah Z, Kaplaner E, Moujahid A, Eddoha R, Nasser B, Terzioğlu P, Yilmaz MA, Ertaş A, Öztürk M, Essamadi A (2020) In vitro enzyme inhibitory properties, antioxidant activities, and phytochemical fingerprints of five Moroccan seaweeds. S Afr J Bot 128:152–160

    Article  CAS  Google Scholar 

  • Guihéneuf F, Gietl A, Stengel DB (2018) Temporal and spatial variability of mycosporine-like amino acids and pigments in three edible red seaweeds from western Ireland. J Appl Phycol 30:2573–2586

    Article  CAS  Google Scholar 

  • Gupta V, Thakur R, Baghel R, Reddy CRK, Jha B (2014) Seaweed metabolomics: a new facet of functional genomics. Adv Bot Res 71:32–52

    Google Scholar 

  • Güven KC, Percot A, Sezik E (2010) Alkaloids in marine algae. Mar Drugs 8:269–284

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hardjani D, Suantika G, Aditiawati P (2017) Nutritional profile of red seaweed Kappaphycus alvarezii after fermentation using Saccharomyces cerevisiae as a feed supplement for white shrimp Litopenaeus vannamei nutritional profile of fermented red seaweed. J Pure Appl Microbiol 11:1637–1645

    Article  CAS  Google Scholar 

  • Hartmann A, Murauer A, Ganzera M (2017) Quantitative analysis of mycosporine-like amino acids in marine algae by capillary electrophoresis with diode-array detection. J Pharm Biomed Anal 138:153–157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hellio C, Simon-Colin C, Clare AS, Deslandes E (2004) Isethionic acid and floridoside isolated from the red alga, Grateloupia turuturu, inhibit settlement of Balanus amphitrite cyprid larvae. Biofouling 20:139–145

    Article  CAS  PubMed  Google Scholar 

  • Higa T, Kuniyoshi M (2000) Toxins associated with medicinal and edible seaweeds. J Toxicol: Toxin Reviews 19:119–137

    CAS  Google Scholar 

  • Higashi Y, Saito K (2013) Network analysis for gene discovery in plant-specialized metabolism. Plant Cell Environ 36:1597–1606

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Ichikawa M, Mizuno I, Yoshida J, Ide N, Ushijima M, Kodera Y, Hayama M, Ono K (2006) Pharmacokinetics of cycloalliin, an organosulfur compound found in garlic and onion, in rats. J Agric Food Chem 54:9811–9819

    Article  CAS  PubMed  Google Scholar 

  • Ide WS, Buck JS (1937) Pharmacologically active compounds from alkoxy-β-phenylethylamines. J Am Chem Soc 59(4):726–731

  • Jeukendrup AE, Randell R (2011) Fat burners: nutrition supplements that increase fat metabolism. Obes Rev 12:841–851

    Article  CAS  PubMed  Google Scholar 

  • Josephson DB, Lindsay RC (1986) Enzymic generation of volatile aroma compounds from fresh fish. In: Biogeneration of Aromas, vol 317. ACS Symposium Series, vol 317. American Chemical Society, pp 201-219

  • Kang O, Ghani M, Hassan O, Rahmati S, Ramli N (2014) Novel agaro-oligosaccharide production through enzymatic hydrolysis: physicochemical properties and antioxidant activities. Food Hydrocoll 42:304–308

    Article  CAS  Google Scholar 

  • Karsten U, Wiencke C (1999) Factors controlling the formation of UV-absorbing mycosporine-like amino acids in the marine red alga Palmaria palmata from Spitsbergen (Norway). J Plant Physiol 155:407–415

    Article  CAS  Google Scholar 

  • Karsten U, Sawall T, Wiencke C. (1998) A survey of the distribution of UV-absorbing substances in tropical macroalgae. Phycol Res 46:271–279

  • Kato H, Rhue MR, Nishimura T (1989) Role of free amino acids and peptides in food taste. In: Flavor Chemistry, vol 388. ACS Symposium Series, vol 388. American Chemical Society, pp 158-174

  • Khatkar D, Kuhad MS (2000) Short-term salinity induced changes in two wheat cultivars at different growth stages. Biol Plant 43:629–632

    Article  CAS  Google Scholar 

  • Kim SK, Pangestuti R, Rahamadi P (2011) Sea lettuces: culinary uses and nutritional value. In: Kim S-K (ed) Advances in food and nutrition research. Marine medicinal foods: implications and applications, macro and microalgae. Academic Press, Waltham, pp 57–68

    Chapter  Google Scholar 

  • Kim TW, Lee K, Lee CK, Jeong HD, Suh YS, Lim WA, Kim KY, Jeong HJ (2013) Interannual nutrient dynamics in Korean coastal waters. Harmful Algae 30:15–27

    Article  CAS  Google Scholar 

  • Kirst GO (1980) Low MW carbohydrates and ions in Rhodophyceae: quantitative measurement of floridoside and digeneaside. Phytochem 19:1107–1110

    Article  CAS  Google Scholar 

  • Kjelleberg S, Steinberg P, Givskov M, Gram L, Mj M, de Nys R (1997) Do marine natural products interfere with prokaryotic AHL regulatory systems? Aquat Microb Ecol 13:85–93

    Article  Google Scholar 

  • Kremer BP (1978) Patterns of photo assimilatory products in Pacific Rhodophyceae. Can J Bot 56:1655–1659

    Article  CAS  Google Scholar 

  • Kumar V, Kaladharan P (2007) Amino acids in the seaweeds as an alternate source of protein for animal feed. J Mar Biol Ass India 49:35–40

  • Kumar V, Zozaya-Valdes E, Kjelleberg S, Thomas T, Egan S (2016) Multiple opportunistic pathogens can cause a bleaching disease in the red seaweed Delisea pulchra. Environ Microbiol 18:3962–3975

    Article  CAS  PubMed  Google Scholar 

  • Kumari P, Kumar M, Reddy CRK, Jha B (2013) Algal lipids, fatty acids and sterols. In: Domínguez H (ed) Functional Ingredients from Algae for Foods and Nutraceuticals. Woodhead Publishing, Oxford, pp 87–134

    Chapter  Google Scholar 

  • Kumari P, Bijo AJ, Mantri VA, Reddy CRK, Jha B (2013b) Fatty acid profiling of tropical marine macroalgae: an analysis from chemotaxonomic and nutritional perspectives. Phytochemistry 86:44–56

    Article  CAS  PubMed  Google Scholar 

  • Kundel M, Thorenz U, Petersen J, Huang R-J, Bings N, Hoffmann T (2012) Application of mass spectrometric techniques for the trace analysis of short-lived iodine-containing volatiles emitted by seaweed. Anal Bioanal Chem 402:3345–3357

    Article  CAS  PubMed  Google Scholar 

  • Kurata K, Amiya T (1975) Chemical studies on constituents of marine algae-II. Constituents of the red alga, Rhodomela subfusa. Bull Jap Soc Sci Fish 41(6):657–659

  • Kurata K, Taniguchi K, Agatsuma Y, Suzuki M (1998) Diterpenoid feeding-deterrents from Laurencia saitoi. Phytochemistry 47:363–369

    Article  CAS  Google Scholar 

  • Kuriyama M, Tagagi M, Murata K (1960) Ninhydrin reactive substances in marine algae. Bull Fac Fish Hokkaido Univ 11:58–63

    Google Scholar 

  • Li X, Staszewski L, Xu H, Durick K, Zoller M, Adler E (2002) Human receptors for sweet and umami taste. Proc Natl Acad Sci U S A 99:4692–4696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maeda M, Kodama T, Tanaka T, Yoshizumi H, Takemoto T, Nomoto K, Fujita T (1986) Structures of isodomoic acids a, b and c, novel insecticidal amino acids from the red alga Chondria armata. Chem Pharm Bull 34:4892–4895

    Article  CAS  Google Scholar 

  • Maeda M, Kodama T, Tanaka T, Yoshizumi H, Takemoto T, Nomoto K, Fujita T (1987) Structures of domoilactone A and B, novel amino acids from the red alga, Chondria armata. Tetrahedron Lett 28:633–636

    Article  CAS  Google Scholar 

  • Maggs CA, Hommersand MH (1993) Seaweeds of the British Isles. Volume 1. Rhodophyta. Part 3A. Ceramiales. Natural History Museum Publications, London pp. 1-444.

  • Mao Y, Chen N, Cao M, Chen R, Guan X, Wang D (2019) Functional characterization and evolutionary analysis of glycine-betaine biosynthesis pathway in red seaweed Pyropia yezoensis. Mar Drugs 17:70

    Article  CAS  PubMed Central  Google Scholar 

  • Martínez-García M, Stuart MC, van der Maarel MJ (2016) Characterization of the highly branched glycogen from the thermoacidophilic red microalga Galdieria sulphuraria and comparison with other glycogens. Int J Biol Macromol 89:12–18

    Article  PubMed  CAS  Google Scholar 

  • McDougall G, Martinussen I, Stewart D (2008) Towards fruitful metabolomics: high throughput analyses of polyphenol composition in berries using direct infusion mass spectrometry. J Chromatogr B 871:362–369

    Article  CAS  Google Scholar 

  • Meng J, Rosell K-G, Srivastava LM (1987) Chemical characterization of floridosides from Porphyra perforata. Carbohydr Res 161:171–180

    Article  CAS  Google Scholar 

  • Mouritsen OG (2013) Seaweeds: edible, available, and sustainable. Food Security 6:441–442

    Google Scholar 

  • Mouritsen OG, Williams L, Bjerregaard R, Duelund L (2012) Seaweeds for umami flavour in the New Nordic Cuisine. Flavour 1:1–12

    Article  Google Scholar 

  • Muranaka T, Saito K (2013) Phytochemical genomics on the way. Plant Cell Physiol 54:645–646

    Article  CAS  PubMed  Google Scholar 

  • Nagahama T, Fujimoto K, Takami S, Kinugawa A, Narusuye K (2009) Effective amino acid composition of seaweeds inducing food preference behaviours in Aplysia kurodai. Neurosci Res 64:243–250

    Article  CAS  PubMed  Google Scholar 

  • Newman SJ, Dunlap WC, Nicol S, Ritz D (2000) Antarctic krill (Euphausia superba) acquire a UV-absorbing mycosporine-like amino acid from dietary algae. J Exp Mar Biol Ecol 255:93–110

    Article  CAS  PubMed  Google Scholar 

  • Newton L (1951) Seaweed utilization. Sampson Low, London.

  • Nielsen CW, Rustad T, Holdt SL (2021) Vitamin C from seaweed: a review assessing seaweed as contributor to daily intake. Foods 10:198

    Article  PubMed  PubMed Central  Google Scholar 

  • Norte M, Fernández JJ, Ruano JZ (1989) Three new bromo ethers from the red alga Laurencia obtusa. Tetrahedron Lett 45:5987–5994

    Article  CAS  Google Scholar 

  • Nylund GM, Weinberger F, Rempt M, Pohnert G (2011) Metabolomic assessment of induced and activated chemical defence in the invasive red alga Gracilaria vermiculophylla. PLoS One 6:e29359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oliveira AS, Sudatti DB, Fujii MT, Rodrigues SV, Pereira RC (2013) Inter- and intrapopulation variation in the defensive chemistry of the red seaweed Laurencia dendroidea (Ceramiales, Rhodophyta). Phycologia 52:130–136

    Article  CAS  Google Scholar 

  • Omar H, Al-Judaibiand A, El-Gendy A (2018) Antimicrobial, antioxidant, anticancer activity and phytochemical analysis of the red alga, Laurencia papillosa. Int J Pharmacol 14:572–583

    Article  CAS  Google Scholar 

  • Orfanoudaki M, Hartmann A, Ngoc HN, Gelbrich T, West J, Karsten U, Ganzera M (2020) Mycosporine-like amino acids, brominated and sulphated phenols: suitable chemotaxonomic markers for the reassessment of classification of Bostrychia calliptera (Ceramiales, Rhodophyta). Phytochemistry 174:112344

    Article  CAS  PubMed  Google Scholar 

  • Pereira L (2011) A review of the nutrient composition of selected edible seaweeds. In: Pomin VH (ed) Seaweed: ecology, nutrient composition and medicinal uses. Nova Science Publishers, London, pp 15–47

    Google Scholar 

  • Picone G, Engelsen SB, Savorani F, Testi S, Badiani A, Capozzi F (2011) Metabolomics as a powerful tool for molecular quality assessment of the fish Sparus aurata. Nutrients 3:212–227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Plouguerné E, Ioannou E, Georgantea P, Vagias C, Roussis V, Hellio C, Kraffe E, Stiger V (2010) Anti-microfouling activity of lipidic metabolites from the invasive brown alga Sargassum muticum (Yendo) Fensholt. Mar Biotechnol 12:52–61

    Article  CAS  Google Scholar 

  • Prathep A, Marrs RH, Norton TA (2003) Spatial and temporal variations in sediment accumulation in an algal turf and their impact on associated fauna. Mar Biol 142:381–390

    Article  Google Scholar 

  • Putri SP, Nakayama Y, Matsuda F, Uchikata T, Kobayashi S, Matsubara A, Fukusaki E (2013) Current metabolomics: practical applications. J Biosci Bioeng 115:579–589

    Article  CAS  PubMed  Google Scholar 

  • Rajaseakr T, Pandiyan P, Subramanian K, Balaraman D, Manikkam S, Sadaiyappan B, George EGJ (2014) Screening of marine seaweeds for bioactive compound against fish pathogenic bacteria and active fraction analysed by gas chromatography–mass spectrometry. J Coast Life Med 2

  • Reed RH (1985) Osmo-acclimatisation in Bangia atropurpurea (Rhodophyta, Bangiales): the osmotic role of floridoside. Br Phycol J 20:211–218

    Article  Google Scholar 

  • Reed RH, Collins JC, Russell G (1980) Effects of salinity upon the galactosyl-glycerol content and concentration of the marine red algae Porphyra purpurea. J Exp Bot 31:1539–1554

    Article  CAS  Google Scholar 

  • Rodrigues D, Costa-Pinto AR, Sousa S, Vasconcelos MW, Pintado MM, Pereira L, Rocha-Santos TAP, Costa JPd, Silva AMS, Duarte AC, Gomes AMP, Freitas AC (2019) Sargassum muticum and Osmundea pinnatifida enzymatic extracts: chemical, structural, and cytotoxic characterization. Mar Drugs 17 (4):209

  • Ryu J, Kwon MJ, Nam TJ (2015). Nrf2 and NF-kB signalling pathways contribute to porphyra-334-mediated inhibition of UVA-induced inflammation in skin fibroblasts. Mar Drugs 13:4721–4732

  • Sabina H, Aliya R (2011) Bioactive assessment of selected marine red algae against Leishmania major and chemical constituents of Osmundea pinnatifida. Pak J Bot 43:3053–3056

    CAS  Google Scholar 

  • San-Martín A, Rovirosa J, Muñoz O, Chen MHM, Guneratne RD, Clardy J (1983) The isolation and structure determination of chilenone A, a putative dimer of 2-methyl-3(2H)-furanone from the marine alga Laurencia chilensis. Tetrahedron Lett 24:4063–4066

    Article  Google Scholar 

  • San-Martín A, Rovirosa J, Xu C, Lu HSM, Clardy J (1987) Further structural studies on the 2-methyl-3 (2H)-furanone derived metabolites of the marine alga Laurencia chilensis. Tetrahedron Lett 28:6013–6014

    Article  Google Scholar 

  • Sarojini Y, Sarma NS (1999) Vitamin C content of some macroalgae of Visakhapatnam, east coast of India. Ind J Mar Sci 28:408–412

    Google Scholar 

  • Sawangwan T, Goedl C, Nidetzky B (2010) Glucosylglycerol and glucosylglycerate as enzyme stabilizers. Biotechnol J 5:187–191

    Article  CAS  PubMed  Google Scholar 

  • Schieberle P, Hofmann T (1997) Evaluation of the character impact odorants in fresh strawberry juice by quantitative measurements and sensory studies on model mixtures. J Agric Food Chem 45:227–232

    Article  CAS  Google Scholar 

  • Shick JM, Dunlap WC (2002) Mycosporine-like amino acids and related Gadusols: biosynthesis, accumulation, and UV-protective functions in aquatic organisms. Annu Rev Physiol 64:223–262

    Article  CAS  PubMed  Google Scholar 

  • Silva P, Fernandes C, Barros L, Ferreira I, Pereira L, Gonçalves T (2018) The antifungal activity of extracts of Osmundea pinnatifida, an edible seaweed, indicates its usage as a safe environmental fungicide or as a food additive preventing post-harvest fungal food contamination. Food Funct 9:6187–6195

    Article  CAS  PubMed  Google Scholar 

  • Sinha RP, Klisch M, Gröniger A, Häder DP (1998) Ultraviolet-absorbing/screening substances in cyanobacteria, phytoplankton and macroalgae. J Photochem Photobiol B 47:83–94

    Article  CAS  Google Scholar 

  • Škrovánková S (2011) Seaweed vitamins as nutraceuticals. Adv Food Nutr Res 64: 357–369

  • Slattery M, Lesser MP (2014) Allelopathy in the tropical alga Lobophora variegata (Phaeophyceae): mechanistic basis for a phase shift on mesophotic coral reefs? J Phycol 50:493–505

    Article  PubMed  Google Scholar 

  • Slaughter CJ (1999) The naturally occurring furanones: formation and function from pheromone to food. Biol Rev Camb Philos Soc 74:259–276

    Article  Google Scholar 

  • Suh SS, Hwang J, Park M, Seo H, Kim H-S, Lee J, Moh SH (2014) Anti-inflammation activities of mycosporine-like amino acids (MAAs) in response to UV radiation suggest potential anti-skin aging activity. Mar Drugs 12:5174–5187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suh SS, Oh SK, Lee SG, Kim IC, Kim S (2017) Porphyra-334, a mycosporine-like amino acid, attenuates UV-induced apoptosis in HaCaT cells. Acta Pharma 67:257–264

    Article  CAS  Google Scholar 

  • Sumner LW, Amberg A, Barrett D, Beale MH, Beger R, Daykin CA, Fan TWM, Fiehn O, Goodacre R, Griffin JL, Hankemeier T, Hardy N, Harnly J, Higashi R, Kopka J, Lane AN, Lindon JC, Marriott P, Nicholls AW, Reily MD, Thaden JJ, Viant MR (2007) Proposed minimum reporting standards for chemical analysis. Metabolomics 3:211–221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takano S, Uemura D, Hirata Y (1978) Isolation and structure of two new amino acids, palythinol and palythene, from the zoanthid Palythoa tuberculosa. Tetrahedron Lett 49:4909–4912

    Article  Google Scholar 

  • Takenaka F, Uchiyama H (2000) Synthesis of α-D-glucosylglycerol by α-glucosidase and some of its characteristics. Biosci Biotechnol Biochem 64:1821–1826

    Article  CAS  PubMed  Google Scholar 

  • Tao C, Sugawara T, Maeda S, Wang X, Hirata T (2008) Antioxidative activities of a mycosporine-like amino acid, porphyra-334. Fish Sci 74:1166–1172

    Article  CAS  Google Scholar 

  • Thiem J, Scheel O, Schneider G (1997) Cosmetic preparations with an effective amount of glycosylglycerides as skin moisturizers. European Patent EP 0 770378

  • Tominaga F, Oka K (1963) On the isolation and identification of 1,4-thiazane-3-carboxylic acid s-oxide from the brown alga Undaria pinnatifida. J Biochem 54:222–224

    Article  CAS  PubMed  Google Scholar 

  • Tseng CK (1981) Commercial cultivation. In: Lobban CS, Wynne MJ (eds) The biology of seaweeds. Blackwell, Oxford, pp 680–725

    Google Scholar 

  • Tyihák E, Blunden G, Ma YC (1994) Quantitative estimation of betaines in commercial seaweed extracts using overpressured layer chromatography. J Appl Phycol 6:469–473

    Article  Google Scholar 

  • Usmanghani K, Shameel M, Sualeh M, Khan K, Mahmood Z (1984) Antibacterial and antifungal activities of marine algae from Karachi seashore of Pakistan. Fitoterapia 55:73–78

    Google Scholar 

  • Winter R (2009) A consumer’s dictionary of food additives, 7th edn. Three River Press, New York (USA), p 595

    Google Scholar 

  • Wishart DS (2008) Metabolomics: applications to food science and nutrition research. Trends Food Sci Technol 19:482–493

    Article  CAS  Google Scholar 

  • Wright JT, de Nys R, Steinberg PD (2000) Geographic variation in halogenated furanones from the red alga Delisea pulchra and associated herbivores and epiphytes. Mar Ecol Prog Ser 207:227–242

    Article  CAS  Google Scholar 

  • Yuan YV (2007) Antioxidants from edible seaweeds. In: Antioxidant measurement and applications, vol 956. ACS Symposium Series, vol 956. American Chemical Society, pp 268-301

  • Yuan YV, Westcott ND, Hu C, Kitts DD (2009) Mycosporine-like amino acid composition of the edible red alga, Palmaria palmata (dulse) harvested from the west and east coasts of Grand Manan Island, New Brunswick. Food Chem 112:321–328

    Article  CAS  Google Scholar 

  • Zaman L, Arakawa O, Shimosu A, Onoue Y, Nishio S, Shida Y, Noguchi T (1997) Two new isomers of domoic acid from a red alga, Chondria armata. Toxicon 35:205–212

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This research was part of a Ph.D. project awarded by the University of Aberdeen, with The Scottish Association for Marine Science (SAMS), the University of the Highlands and Islands (UHI), and The James Hutton Institute as academic partners and with the financial support from the Industrial Biotechnology Innovation Centre (IBioIC), Highlands and Islands Enterprise (HIE) and Marine Alliance for Science and Technology for Scotland (MASTS). We appreciate the contribution of Julie Sungurtas at The James Hutton Institute for helping with HILIC-MS data analyses and of Sharon Mcneill at SAMS for helping with the analyses of the physicochemical data.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to C. Biancacci.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

ESM 1

(DOCX 2031 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Biancacci, C., McDougall, G.J., Allwood, J.W. et al. LC-MSn profiling reveals seasonal variation in the composition of Osmundea pinnatifida (Hudson) Stackhouse. J Appl Phycol 33, 2443–2458 (2021). https://doi.org/10.1007/s10811-021-02482-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-021-02482-4

Keywords

Navigation