Abstract
The extensive variation in the biochemical composition of algal species is used as a source of potential bioactive compounds for applications in the agri-food industry and in the field of functional foods. Among these species, Porphyra/Pyropia spp. (nori, laver) are red sea vegetables which provide the foundation for a billion-dollar industry. In this study, we determine the growth and biochemical composition of distinct reproductive traits (females vs. males) in Porphyra dioica. In order to characterize and enhance through cultivation the bioactive profiles and biochemical composition of this sea vegetable, we determined the effects of environmental parameters (light and nutrients) on the growth of different life history traits (females vs. males) in cultured and field samples of P. dioica. In field-collected samples, females contained higher contents of phycoerythrin (9.71 ± 3.13 mg g−1 DW), PUFA (omega-3 fatty acids, 12.25 ± 0.78 mg g−1 DW; eicosapentaenoic acid, 11.54 ± 0.92 mg g−1 DW) and total fatty acids (TFA) (31.58 ± 2.5 mg g−1 DW) than males. The total nitrogen (TN) content was similar in both traits in the field, but the protein nitrogen (PN) was higher in males from field collections (42.80 mg g−1 DW). In culture, males and females responded differently to applied environmental factors, with an increase of some omega-6 fatty acids (e.g. 20:4 n-6 with an increase of 4.98 %TFA, 0.1 mg g−1 DW) in females and omega-7,9 fatty acids in males (increase of 13.75 %TFA, 0.79 mg g−1 DW in omega-7 and 1.59 %TFA in omega-9) associated with exposure to adverse conditions (N starvation under low light intensity). We discuss the possibility of using P. dioica as a promising source of functional new food products such as enriched nori in bioactive compounds such as monounsaturated and polyunsaturated fatty acids.
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References
Beer S, Eshel A (1985) Determining phycoerythrin and phycocyanin concentrations in aqueous crude extracts of red algae. Aust J Mar Fresh Res 36:785–792
Blouin NA, Brodie JA, Grossman AC, Xu P, Brawley SH (2011) Porphyra: a marine crop shaped by stress. Trends Plant Sci 16:29–37
Breuer G, Lamers PP, Martens DE, Draaisma RB, Wijffels RH (2012) The impact of nitrogen starvation on the dynamics of triacyglycerol accumulation in nine microalgae strains. Bioresour Technol 124:217–226
Brodie JA, Irvine LM (2003) Seaweeds of the British Isles: volume 1 Rhodophyta. Part 3B Bangiophycidae. Natural History Museum, London, p 167
Chopin T, Gallant T, Davison I (1995) Phosphorus and nitrogen nutrition in Chondrus crispus (Rhodophyta): effects on total phosphorous and nitrogen content, carrageenan production, and photosynthetic pigments and metabolism. J Phycol 31:283–293
Connan S, Stengel DB (2011) Impacts of ambient salinity and copper on brown algae: interactive effects on phenolic pool and assessment of metal binding capacity of phlorotannin. Aquat Toxicol 104:1–13
Connolly A, Piggott CO, FitzGerald RJ (2013) Characterisation of protein-rich isolates and antioxidative phenolic extracts from pale and black brewers’ spent grain. Int J Food Sci Technol 48:1670–1681
Curb JD, Wergowske G, Dobbs JC, Abbott RD, Huang BJ (2000) Serum lipid effects of a high-monounsaturated fat diet based on macadamia nuts. Arch Intern Med 160:1154–1158
Drew KM (1949) Conchocelis-phase in the life-history of Porphyra umbilicalis (L.) Kutz. Nature 164:748–749
Esteban R, Barrutia O, Artetxe U, Fernández-Marín B, Hernández A, García-Plazaola JI (2015) Internal and external factors affecting photosynthetic pigment composition in plants: a meta-analytical approach. New Phytol 206:268–280
Ferreira VS, Pinto RF, Sant’Anna C (2016) Low light intensity and nitrogen starvation modulate the chlorophyll content of Scenedesmus dimorphus. J Appl Microbiol 120:661–670
Figueroa FL, Salles S, Aguilera J, Jiménez C, Mercado J, Viñegla B, Flores-Moya A, Altamirano M (1997) Effects of solar radiation on photoinhibition and pigmentation in the red alga Porphyra leucosticta. Mar Ecol Prog Ser 151:81–90
Floreto EAT, Teshima S (1998) The fatty acid composition of seaweeds exposed to different levels of light intensity and salinity. Bot Mar 41:467–481
Guihéneuf F, Stengel DB (2015) Towards the biorefinery concept: interaction of light, temperature and nitrogen for optimizing the co-production of high-value compounds in Porphyridium purpureum. Algal Res 10:152–163
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
Hafting JT, Craigie JS, Stengel DB, Loureiro RR, Buschmann AH, Yarish C, Critchley EMD (2015) Prospects and challenges for industrial production of seaweed bioactives. J Phycol 51:821–837
Hasler CM (1998) Functional foods: their role in disease prevention and health promotion. Food Technol 52:63e70
Hotimchenko SV (2002) Fatty acid composition of algae from habitats with varying amounts of illumination. Russ J Mar Biol 28:218–220
Ishihara K, Oyamada C, Matsushima R, Murata M, Muraoka T (2005) Inhibitory effect of porphyran, prepared from dried ‘nori’ on contact hypersensitivity in mice. Biosci Biotechnol Biochem 69:1824–1830
Khotimchenko SV (2006) Variations in lipid composition among different developmental stages of Gracilaria verrucosa (Rhodophyta). Bot Mar 49:34–38
Kris-Etherton PM, Harris WS, Appel LJ, Nutrition C (2002) Fish consumption, fish oil, omega-3 fatty acids, and cardiovascular disease. Circulation 106:2747–2757
Lin R (2000) Physiological ecology of Porphyra sporophytes: growth, photosynthesis, respiration and pigments. PhD thesis, University of Alaska Fairbanks, Fairbanks, USA
Lin R, Stekoll MS (2011) Phycobilin content of the conchocelis phase of Alaskan Porphyra (Bangiales, Rhodophyta) species: responses to environmental variables. J Phycol 47:208–214
Lobban CS, Harrison PJ (1994) Seaweed ecology and physiology. Cambridge University Press, Cambridge
Martinez B, Rico JM (2002) Seasonal variation of P content and major N pools in Palmaria palmata (Rhodophyta). J Phycol 38:1082–1089
McCandless EL, Craigie JS, Water JA (1973) Carrageenan in the gametophytic and sporophytic stages of Chondrus crispus. Planta 112:201–212
Morita K, Tobiishi K (2002) Increasing effect of nori on the fecal excretion of dioxin by rats. Biosci Biotechnol Biochem 66:2306–2313
Mumford TF, Miura A (1988) Porphyra as food: cultivation and economics. In: Lemby CA, Waaland JR (eds) Algae and human affairs. Cambridge University Press, Cambridge, pp 87–117
Noda H, Amano H, Arashima K, Hashimoto S, Nisizawa K (1989) Antitumor activity of polysaccharides and lipids from marine algae. Nippon Suisan Gakk 55:1265–1271
Okai Y, Higashi-Okai K, Yano Y, Otani S (1996) Identification of antimutagenic substances in an extract of edible red alga, Porphyra tenera (Asakusa-nori). Cancer Lett 100:235–240
Pereira R, Yarish C, Sousa-Pinto I (2006) The influence of stocking density, light and temperature on the growth, production and nutrient removal capacity of Porphyra dioica (Bangiales, Rhodophyta). Aquaculture 252:66–78
Pereira R, Kraemer G, Yarish C, Sousa-Pinto I (2008) Nitrogen uptake by gametophytes of Porphyra dioica (Bangiales, Rhodophyta) under controlled-culture conditions. Eur J Phycol 43:107–118
Sahoo D, Tang X, Yarish C (2002) Porphyra—the economic seaweed as a new experimental system. Curr Sci 83:1313–1316
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 26:451–463
Schmid M, Guihéneuf F, Stengel DB (2017) Ecological and commercial implications of temporal and spatial variability in the composition of pigments and fatty acids in five Irish macroalgae. Mar Biol 164:158
Schneider JC, Roessler P (1994) Radiolabeling studies of lipids and fatty acids in Nannochloropsis (Eustigmatophyceae), an oleaginous marine alga. J Phycol 30:594–598
Sloan AE (2002) The top ten functional food trends: the next generation. Food Technol 56:32e56
Stengel DB, Connan S, Popper ZA (2011) Algal chemodiversity and bioactivity: sources of natural variability and implications for commercial application. Biotechnol Adv 29:483–501
Stengel DB, Conde-Álvarez R, Connan S, Nitschke U, Arenas F, Abreu H, Bonomi Barufi J, Chow F, Robledo D, Malta EJ, Mata M, Konotchick T, Nassar C, Pérez-Ruzafa Á, López D, Marquardt R, Vaz-Pinto F, Celis-Plá PSM, Hermoso M, Ruiz E, Ordoñez G, Flores P, Zanolla M, Bañares-España E, Altamirano M, Korbee N, Bischof K, Figueroa FL (2014) Short-term effects of CO2, nutrients and temperature on three marine macroalgae under solar radiation. Aquat Biol 22:159–176
Tasende MG (2000) Fatty acid and sterol composition of gametophyte and sporophytes of Chondrus crispus (Gigartinaceae, Rhodophyta). Sci Mar 64:421–426
Terés S, Barceló-Coblijn G, Benet M, Álvarez R, Bressani R, Halver JE, Escribá PV (2008) Oleic acid content is responsible for the reduction in blood pressure induced by olive oil. Proc Natl Acad Sci U S A 105:13811–13816
Thompson PA, Harrison PJ, Whyte JNC (1990) Influence of irradiance on the fatty acid composition of phytoplankton. J Phycol 26:278–288
Varela-Álvarez E, Stengel DB, Guiry MD (2004) The use of image processing in assessing conchocelis growth and conchospore production in Porphyra linearis. Phycologia 43:282–287
Varela-Álvarez E, Stengel DB, Guiry MD (2007) Seasonal growth and phenotypic variation in Porphyra linearis (Rhodophyta) populations on the west coast of Ireland. J Phycol 43:90–100
Varela-Álvarez E, Loureiro J, Paulino C, Serrão EA (2018) Polyploid lineages in the genus Porphyra. Sci Rep 8:8696
Ward OP, Singh A (2005) Omega-3/6 fatty acids: alternative sources of production. Process Biochem 40:3627–3652
Welters HJ, Diakogiannaki E, Mordue JM, Tadayyon M, Smith SA, Morgan NG (2006) Differential protective effects of palmitoleic acid and cAMP on caspase activation and cell viability in pancreatic beta-cells exposed to palmitate. Apoptosis 11:1231–1238
Yoshizawa Y, Enomoto A, Todoh H, Ametani A, Kaminogawa S (1993) Activation of murine macrophages by polysaccharide fractions from marine algae (Porphyra yezoensis). Biosci Biotechnol Biochem 57:1862–1866
Zhang Q, Li N, Zhou G, Lu X, Xu Z, Li Z (2003) In vivo antioxidant activity of polysaccharide fraction from Porphyra haitanesis (Rhodophyta) in aging mice. Pharmacol Res 48:151–155
Acknowledgements
This study was funded by the Department of Agriculture, Food and the Marine (Ireland) Project Reference No: 13/F/536 ‘Profiling and optimising chemical composition of red sea vegetables for enhanced bioactive yields’. We thank Liam Cronin for assistance with field sampling.
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TABLE S1
Fatty acid composition (% of total FAME) of samples of P. dioica in Experiment 1, after 5 days culture under: 90 μmol photons m−2 s−1, 60 μmol photons m−2 s−1, 30 μmol photons m−2 s−1 with lab control values, and after 2.5 days culture under a post N-starvation treatment at 20 μmol photons m−2 s−1. TFA, total fatty acid contents are given as % of DW. Omega fatty acid families were considering grouping single fatty acids as: omega 3: 16:3 n-3, 18:3 n-3, 18:4 n-3, 20:5 n-3; omega 6: 18:2 n-6; 18:3 n-6, 20:2 n-6; 20:3 n-6, 20:4 n-6; omega 7: 16:1 n-7 and 18:1 n-7; omega 9: 18:1 n-9, 20:1 n-9, 22:1 n-9. Mean ± SD (n = 3–6). (DOCX 67 kb)
TABLE S2
Fatty acid composition (mg g-1 DW) of samples of P. dioica in Experiment 1, after in 5 days culture under: 90 μmol photons m−2 s−1, 60 μmol photons m−2 s−1, 30 μmol photons m−2 s−1 with lab control values, and after 2.5 days culture under a post N-starvation treatment at 20 μmol photons m−2 s−1. Omega 3: 16:3 n-3, 18:3 n-3, 18:4 n-3, 20:5 n-3; omega 6: 18:2 n-6; 18:3 n-6, 20:2 n-6; 20:3 n-6, 20:4 n-6; omega 7: 16:1 n-7 and 18:1 n-7; omega 9: 18:1 n-9, 20:1 n-9, 22:1 n-9. Mean ± SD (n = 3–6). (DOCX 231 kb)
TABLE S3
ANOVA summary table for 20:4 n-6 (% TFA), Experiment 1, Stage 1 (5 days culture). (DOCX 231 kb)
TABLE S4
ANOVA summary table for 18:2 n-6 (mg g-1 DW), Experiment 1, Stage 1 (5 days culture). (DOCX 231 kb)
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Varela-Álvarez, E., Tobin, P.R., Guihéneuf, F. et al. Phycobiliproteins, nitrogenous compounds and fatty acid contents in field-collected and cultured gametophytes of Porphyra dioica, a red sea vegetable. J Appl Phycol 31, 3849–3860 (2019). https://doi.org/10.1007/s10811-019-01841-6
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DOI: https://doi.org/10.1007/s10811-019-01841-6