Abstract
The metabolic profile of the brown macroalga Sargassum cymosum was analyzed after 7 days of laboratory cultivation in three salinities (30, 35, and 40 psu) and four irradiation treatments for 3 h per day: PAR-only (control; 70 μmol photons m−2 s−1), PAR+UVA (0.70 W m−2), PAR+UVB (0.35 W m−2), and PAR+UVA+UVB. Carbon (C) and nitrogen (N) levels, protein content, free polyamines (PAs), carbohydrates, phenolics, and enzymatic activities of NADH dehydrogenase and complex II were analyzed. Treatments showed variations in CN levels, with a significant reduction of C, but no evident trend for N, probably as a result of C-N balance allocation for basic biological maintenance and stress defense metabolism. Three different PAs were detected, including putrescine (PUT), spermidine (SPD), and spermine (SPM), and their variation could be explained by a defense mechanism in which PAs bound to phenolic compounds migrate through the cell wall and then degrade, concurrent with the photoprotective degradation of chlorophyll. Metabolic profiles detected through attenuated total reflection Fourier transform infrared spectroscopy/principal component analysis (ATR-FTIR/PCA) mostly showed differences in the metabolism of proteins and phenolics. It can be concluded that S. cymosum is less affected by salinity than exposure to ultraviolet radiation (UVR). Further studies are required to better understand the variation in PAs under resistance to stress. In addition to its exploitation as a complementary compound in fertilizer, it is suggested that S. cymosum could also be studied as a natural product for its antioxidant properties and high presence of phenolics and PAs, in addition to its use in nutraceutical products, human food, and animal feed.
Access this article
We’re sorry, something doesn't seem to be working properly.
Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.
Similar content being viewed by others
References
Allen AC, Fluhr R (1997) Two distinct sources of elicited reactive oxygen species in tobacco epidermal cells. Plant Cell 9:1559–1572
Andria JR, Vergara JJ, Llorens LP (1999) Biochemical responses and photosynthetic performance of Gracilaria sp. (Rhodophyta) from Cádiz, Spain, cultured under different inorganic carbon and nitrogen levels. Eur J Phycol 34:497–504
Arnold KE, Manley SL (1985) Carbon allocation in Macrocystis pyrifera (Phaeophyta): intrinsic variability in photosynthesis and respiration. J Phycol 21:154–167
Baldini L, Pitocchi R, Bagni N (1994) Polyamine transport in the seaweed Ulva rigida (Chlorophyta). J Phycol 30:599–605
Bandy B, Davison AJ (1990) Mitochondrial mutations may increase oxidative stress: implications for carcinogenesis and aging? Free Rad Biol Med 8:523–539
Baron K, Stasolla C (2008) The role of polyamines during in vivo and in vitro development. In Vitro Cell Dev Biol Plant 44:384–395
Beigbeder A, Kotzabasis K (1994) The influence of exogenously supplied spermine on protochlorophyllide and chlorophyll biosynthesis. J Photochem Photobiol B23:201–206
Beigbeder A, Vavadakis M, Navakoudis E, Kotzabasis K (1995) Influence of polyamine inhibitors on light-independent and light-dependent chlorophyll biosynthesis and on the photosynthetic rate. J Photochem Photobiol B28:235–242
Berta G, Altamura MM, Fusconi A, Cerruti F, Capitani F, Bagni N (1997) The plant cell wall is altered by inhibition of polyamine biosynthesis. New Phytol 137:569–577
Besford R, Richardson C, Campos J, Tiburcio AF (1993) Effect of polyamines on stabilisation complexes in thylakoid membranes of osmotically stressed oat leaves. Planta 189:201–206
Bird K, Hablg T, DeBusk T (1982) Nitrogen allocation and storage patterns in Gracilaria tikvahiae (Rhodophyta). J Phycol 18:344–348
Bors W, Langebartels C, Michel C, Sandermann HJ (1989) Polyamines as radical scavengers and protectants against ozone damage. Phytochemistry 28:1589–1595
Burritt DJ (2008) The polycyclic aromatic hydrocarbon phenanthrene causes oxidative stress and alters polyamine metabolism in the aquatic liverwort Riccia fluitans L. Plant Cell Environ 31:1416–1431
Cen YP, Bornman JF (1990) The response of bean plants to UV-B radiation under different irradiances of background visible light. J Exp Bot 41:1489–1495
Chen Q, Vazquez EJ, Moghaddas S, Hoppel CL, Lesnefsky EJ (2003) Production of reactive oxygen species by mitochondria: central role of complex III. J Biol Chem 278:36027–36031
Chow F (2012) Nitrate assimilation: the role of in vitro nitrate reductase assay as nutritional predictor. In: Najafpour MM (ed) Agricultural and Biological Sciences, Applied photosynthesis, In Tech, pp. 105–120.
Chow F, Oliveira MC (2008) Rapid and slow modulation of nitrate reductase activity in the red macroalga Gracilaria chilensis (Gracilariales, Rhodophyta): influence of different nitrogen sources. J Appl Phycol 20:325–332
Cohen E, Shoshana A, Heimer YH, Mizrahi Y (1984) Polyamine biosynthetic enzymes in the cell cycle of Chlorella. Plant Physiol 74:385–388
Coimbra MA, Barros A, Barros M, Rutledge DN, Delgadillo I (1998) Multivariate analysis of uronic acid and neutral sugars in whole pectic samples by FT-IR spectroscopy. Carbohydr Polym 37:41–248
de Paula MR, Glaser V, da Luz Scheffer D, de Paula Ferreira PM, Wannmacher CM, Farina M, de Oliveira PA, Prediger RD, Latini A (2013) Platelet oxygen consumption as a peripheral blood marker of brain energetics in a mouse model of severe neurotoxicity. J Bioenerg Biomembr 45:449–57
DeBoer JA, Guigli HJ, Israel TL, D’Elia CF (1978) Nutritional studies of two red algae. I. Growth rate as a function of nitrogen source and concentration. J Phycol 14:261–266
Diffey BL (2002) Sources and measurement of ultraviolet radiation. Methods 28:4–13
Doernemann D, Navakoudis E, Kotzabasis K (1996) Changes in the polyamine content of plastidal membranes in light- and dark-grown wildtype and pigment mutants of the unicellular green alga Scenedesmus obliquus and their possible role in chloroplast photodevelopment. J Photochem Photobiol B 36:293–299
Ferreira G, Fontes RF, Fontes M, Alvares V (2001) Comparing calcium chloride, barium chloride, and hot water extractions and testing activated charcoal plus azomethine-H dosage for boron determination in Brazilian soils. Commun Soil Sci Plant Anal 32:3153–3167
Fischer JC, Ruitenbeek W, Berden JA, Trijbels JM, Veerkamp JH et al (1985) Differential investigation of the capacity of succinate oxidation in human skeletal muscle. Clin Chim Acta 153:23–36
Flores HE (1991) Changes in polyamine metabolism in response to abiotic stress. In: Slocum RD, Flores HE (eds) Biochemistry and physiology of polyamines in plants. CRC Press Ltd., Boca Raton, pp 41–56
Fredersdorf J, Müller R, Becker S, Wiencke C, Bischof K (2009) Interactive effects of radiation, temperature and salinity on different life history stages of the Arctic kelp Alaria esculenta (Phaeophyceae). Oecologia 160:483–492
Fuell C, Elliott KA, Hanfrey CC, Franceschetti M, Michael AJ (2012) Polyamine biosynthetic diversity in plants and algae. Plant Physiol Biochem 48:513–520
Galston AW, Kaur-Sawhney R (1995) Polyamines as endogenous growth regulators. In: Davies PJ (ed) Plant hormones: physiology, biochemistry, and molecular biology. Kluwer, Dordrecht, pp 158–178
Gao K, Xu J (2008) Effects of solar UV radiation on diurnal photosynthetic performance and growth of Gracilaria lemaneiformis (Rhodophyta). Eur J Phycol 43:297–307
García-Jiménez P, Rodrigo M, Robaina R (1998) Influence of plant growth regulators, polyamines and glycerol interaction on growth and morphogenesis of carposporelings of Grateloupia cultured in vitro. J Appl Phycol 10:95–100
García-Sánchez MJ, Fernández JA, Niel FX (1993) Biochemical and physiological responses of Gracilaria tenuistipitata under two different nitrogen treatments. Physiol Plant 88:631–637
Glaser V, Moritz B, Schmitz A, Dafré AL, Nazari EM, Rauh Müller YM, Feksa L, Straliottoa MR, de Bem AF, Farina M, da Rocha JB, Latini A (2013) Protective effects of diphenyl diselenide in a mouse model of brain toxicity. Chem Biol Interact 206:18–26
Gómez I, Huovinen P (2011) Morpho-functional patterns and zonation of 13 South Chilean seaweeds: the importance of photosynthetic and bio-optical traits. Mar Ecol Prog Ser 422:77–91
Gordillo F, Dring M, Savidge G (2002) Nitrate and phosphate uptake characteristics of three species of brown algae cultured at low salinity. Mar Ecol Prog Ser 234:111–118
Häder DP, Figueroa FL (1997) Photoecophysiology of marine macroalgae. Photochem Photobiol 66:1–14
Häder DP, Kumar HD, Smith RC, Worrest RC (2007) Effects of solar UV radiation on aquatic ecosystems and interactions with climate change. J Photochem Photobiol 46:53–68
Hales J, Fletcher R (1990) Studies on the recently introduced brown alga Sargassum muticum (Yendo) Fensholt. V. Receptacle initiation and growth, and gamete release in laboratory culture. Bot Mar 33:241–249
Hamana K, Matsuzaki S (1982) Widespread occurrence of norspermidine and norspermine in eukaryotic algae. J Biochem 91:1321–1328
Hamilton J, Thomas R, DeLucia E (2001) Direct and indirect effects of elevated CO2 on leaf respiration in a forest ecosystem. Plant Cell Environ 24:975–982
Hanelt D, Roleda MY (2009) UVB radiation may ameliorate photoinhibition in specific shallow-water tropical marine macrophytes. Aquat Bot 91:6–12
Hanisak MD (1990) The use of Gracilaria tikvahiae (Gracilariales, Rhodophyta) as a model system to understand the nitrogen nutrition of culture seaweeds. Hydrobiologia 204(205):79–87
Hausladen A, Fridovich I (1994) Superoxide and peroxynitrite inactivate aconitases, but nitric oxide does not. J Biol Chem 269:29405–29408
Hunter DC, Burritt DJ (2005) Light quality influences the polyamine content of lettuce (Lactuca sativa L.) cotyledon explants during shoot production in vitro. Plant Growth Regul 45:53–61
Hwang SP, Williams SL, Brinkhuis BH (1987) Changes in internal dissolved nitrogen pools as related to nitrate uptake and assimilation in Gracilaria tikvahiae McLachlan (Rhodophyta). Bot Mar 30:11–19
Karsten U (2007) Salinity tolerance of Arctic kelps from Spitsbergen. Phycol Res 55:257–262
Kotzabasis K, Fontinou C, Roubelakis-Angelakis KA, Ghanotakis D (1993) Polyamines in the photosynthetic apparatus. Photosystem II highly resolved subcomplexes are enriched in spermine. Photosynth Res 38:83–88
Kramer GF, Norman HA, Krizek DT, Mirecki RM (1991) Influence of UV-B radiation on polyamines, lipid peroxidation and membrane lipids in cucumber. Phytochemistry 30:2101–2108
Kramer GF, Krizek DT, Mirecki RM (1992) Influence of photosynthetically active radiation and spectral quality on UV-B induced polyamine accumulation in soybean. Phytochemistry 31:1119–1125
Kuhnen S, Bernard-Ogliari J, Dias PF, Boffo EF, Correia I, Ferreira AG, Delgadillo I, Maraschin M (2010) ATR-FTIR spectroscopy and chemometric analysis applied to discrimination of landrace maize flours produced in southern Brazil. Int J Food Sci Technol 45:1673–1681
Lapointe BE (1981) The effects of light and nitrogen on growth, pigment content, and biochemical composition of Gracilaria foliifera v. angustissima (Gigartinales, Rhodophyta). J Phycol 17:90–95
Lapointe BE, Duke CS (1984) Biochemical strategies for growth of Gracilaria tikvahiae (Rhodophyta) in relation to light intensity and nitrogen availability. J Phycol 20:488–495
Latini A, Rodriguez M, Borba Rosa R, Scussiato K, Leipnitz G, Reir de Assis D, da Costa FG, Funchal C, Jacques-Silva MC, Buzin L, Giugliani R, Cassiana A, Radi R, Wajner M (2005) 3-Hydroxyglutaric acid moderately impairs energy metabolism in brain of young rats. Neuroscience 135:111–120
Lee TM (1998) Investigations of some intertidal green macroalgae to hyposaline stress: detrimental role of putrescine under extreme hyposaline conditions. Plant Sci 138:1–8
Lee SH, Whitledge TE, Kang SH (2008) Carbon uptake rates of sea ice algae and phytoplankton under different light intensities in a landfast Sea Ice zone, Barrow, Alaska. Artic 61:281–291
Legendre L, Ackley SF, Dieckmann GS, Gulliksen B, Horner R, Hoshiai T, Melnikov IA, Reeburgh WS, Spindler M, Sullivan CW (1992) Ecology of sea ice biota. Polar Biol 12:429–444
Lerdau M, Coley PD (2002) Benefits of the carbon-nutrient balance hypothesis. Oikos 98:534–536
Li ZL, Burritt DJ (2003) Changes in endogenous polyamines during the formation of somatic embryos from isogenic lines of Dactylis glomerata L. with different regenerative capacities. Plant Growth Regul 40:65–74
Lobban CS, Harrison PJ (1994) Seaweed ecology and physiology. Cambridge University Press, Cambridge
Lowry OH, Rosebough N, Farr AL (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275
Lütz C, Navakoudis E, Seidlitz HK, Kotzabasis K (2005) Simulated solar irradiation with enhanced UV-B adjust plastid- and thylakoid-associated polyamine changes for UV-B protection. Biochim Biophys Acta 1710:24–33
Macler BA (1988) Salinity effects on photosynthesis, carbon allocation and nitrogen assimilation in the red alga, Gelidium coulteri. Plant Physiol 88:690–694
Marián FD, García-Jiménez P, Robaina R (2000) Polyamines in marine macroalgae: levels of putrescine, spermidine and spermine in the thalli and changes in their concentration during glycerol-induced cell growth in vitro. Physiol Plant 110:530–534
Martins I, Oliveira J, Flindt M, Marques J (1999) The effect of salinity on the growth rate of the macroalgae Enteromorpha intestinalis (Chlorophyta) in the Mondego estuary (west Portugal). Acta Oecol 20:259–265
Martin-Tanguy J (2001) Metabolism and function of polyamines in plants: recent development (new approaches). Plant Growth Regul 34:135–148
Michler T, Aguilera J, Hanelt D, Bischof K, Wiencke C (2002) Long-term effects of ultraviolet radiation on growth and photosynthetic performance of polar and cold-temperate macroalgae. Mar Biol 140:1117–1127
Miret JJ, Solari AJ, Barderi PA, Goldemberg SH (1992) Polyamines and cell wall organization in Saccharomyces cerevisiae. Yeast 8:1033–1041
Mock T, Gradinger R (2000) Changes in photosynthetic carbon allocation in algal assemblages of Arctic sea ice with decreasing nutrient concentrations and irradiance. Mar Ecol Prog Ser 202:1–11
Norton TA (1977) The growth and development of Sargassum muticum (Yendo) Fensholt. J Exp Mar Biol Ecol 26:41–53
Norton T, Melkonian M, Andersen R (1996) Algal biodiversity. J Appl Phycol 35:308–326
Pakker H, Martins R, Boelen P, Buma A, Nikaido O, Breeman A (2000a) Effects of temperature on the photoreactivation of ultraviolet-B-induced DNA damage in Palmaria palmata (Rhodophyta). J Phycol 36:334–341
Pakker H, Beekman C, Breeman A (2000b) Efficient photoreactivation of UVBR-induced DNA damage in the sublittoral macroalga Rhodymenia pseudopalmata (Rhodophyta). Eur J Phycol 35:109–114
Papenfus HB, Stirk WA, Finnie JF, Van SJ (2012) Seasonal variation in the polyamines of Ecklonia maxima. Bot Mar 55:539–546
Parry ML, Canziani OF, Palutikof JP, van der Linden PJ, Hanson CE (2007) Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, pp 581–615
Pescheck F, Lohbeck K, Roleda M, Bilger W (2014) UVB-induced DNA and photosystem II damage in two intertidal green macroalgae: distinct survival strategies in UV-screening and non-screening Chlorophyta. J Photochem Photobiol B 132:85–93
Plante AJ, Arts MT (2000) Effects of chronic, low levels of UV radiation on carbon allocation in Cryptomona serosa and competition between C. erosa and bacteria in continuous cultures. J Plankton Res 22:1277–1298
Polo LK, Felix MR, Kreush M, Pereira D, Costa G, Simioni C, Ouriques L, Chow F, Ramlov F, Maraschin M, Bouzon ZL, Schmidt EC (2014) Photoacclimation responses of the brown macroalga Sargassum cymosum to the combined influence of UV radiation and salinity: cytochemical and ultrastructural organization and photosynthetic performance. Photochem Photobiol 90:560–573
Poppe F, Hanelt D, Wiencke C (2002) Changes in ultrastructure, photosynthetic activity and pigments in the Antarctic red alga Palmaria decipiens during acclimation to UV radiation. Bot Mar 45:253–261
Roleda M, Hanelt D, Kräbs G, Wiencke C (2004) Morphology, growth, photosynthesis and pigments in Laminaria ochroleuca (Laminariales, Phaeophyta) under ultraviolet radiation. Phycologia 43:603–613
Ryther JG, Dustan W (1971) Nitrogen, phosphorus and eutrophication in the coastal environment. Science 171:1008–1013
Santa-Catarina C, Silveira V, Scherer GFE, Floh EIS (2007) Polyamine and nitric oxide levels correlate with morphogenetic evolution in somatic embryogenesis of Ocotea catharinensis. Plant Cell Tissue Org Cult 90:93–101
Scherner F, Ventura R, Barufi J, Horta P (2012) Salinity critical threshold values for photosynthesis of two cosmopolitan seaweed species: providing baselines for potential shifts on seaweed assemblages. Mar Environ Res 79:1–12
Schmidt ÉC, Pereira B, Pontes CLM, Santos R, Scherner F, Horta PA, Martins RP, Latini A, Maraschin M, Bouzon ZL (2012a) Alterations in architecture and metabolism induced by ultraviolet radiation-B in the carragenophyte Chondracanthus teedei (Rhodophyta, Gigartinales). Protoplasma 249:353–367
Schmidt ÉC, Pereira B, Santos R, Gouveia C, Costa GB, Faria GSM, Scherner F, Horta PA, Martins RP, Latini A, Ramlov F, Maraschin M, Bouzon ZL (2012b) Responses of the macroalgae Hypnea musciformis after in vitro exposure to UV-B. Aquat Bot 100:8–17
Schulz H, Baranska M (2007) Identification and quantification of valuable plant substances by IR and Raman spectroscopy. Vib Spectrosc 43:13–25
Schweikert K, Sutherland JES, Hurd CL, Burritt DJ (2011) UV-B radiation induces changes in polyamine metabolism in the red seaweed Porphyra cinnamomea. Plant Growth Regul 65:389–399
Schweikert K, Hurd CL, Sutherland JE, Burritt DJ (2014) Regulation of polyamine metabolism in Pyropia cinnamomea (W.A. Nelson), an important mechanism for reducing UV-B-induced oxidative damage. J Phycol 50:267–279
Sfichi L, Ioannidis N, Kotzabasis K (2004) Thylakoid-associated polyamines adjust the UV-B sensitivity of the photosynthetic apparatus by means of light-harvesting complex II changes. Photochem Photobiol 80:499–506
Sfichi-Duke L, Ioannidis NE, Kotzabasis K (2008) Fast and reversible response of thylakoid-associated polyamines during and after UV-B stress: a comparative study of the wild type and a mutant lacking chlorophyll b of unicellular green alga Scenedesmus obliquus. Planta 228:341–353
Shuter B (1979) A model of physiological adaptation in unicellular algae. J Theor Biol 8:519–552
Silveira V, Floh EIS, Handro W, Guerra MP (2004) Effect of plant growth regulators on the cellular growth and levels of intracellular protein, starch and polyamines in embryogenic suspension cultures of Pinustaeda. Plant Cell Tissue Org Cult 76:53–60
Smith RE, Clement P, Cota GF, Li WK (1989) Intracellular photosynthate allocation and the control of arctic marine ice algal production. J Phycol 23:124–132
Smith J, Burrit D, Bannister P (2001) Ultraviolet-B radiation leads to a reduction in free polyamines in Phaseolus vulgaris L. Plant Growth Regul 35:289–294
Steen H (2004) Effects of reduced salinity on reproduction and germling development in Sargassum muticum (Phaeophyceae, Fucales). Eur J Phycol 39:293–299
Tiburcio AF, Kaur-Sawhney R, Galston AW (1993) Spermidine biosynthesis as affected by osmotic-stress in oat leaves. Plant Growth Regul 13:103–109
Torrigiani P, Rabiti AL, Bortolotti C, Betti L, Marai F, Canova A (1997) Polyamine synthesis and accumulation in the hypersensitive response to TMV in Nicotiana tabacum. New Phytol 135:467–473
Turpin DH, Elrifi IR, Birch DG, Weger HG, Holmes JJ (1988) Interactions between photosynthesis, respiration and nitrogen assimilation in microalgae. Can J Bot 66:2083–2097
Turrens JF (1997) Superoxide production by the mitochondrial respiratory chain. Biosci Rep 17:3–8
Turrens JF, Boveris A (1980) Generation of superoxide anion by the NADH dehydrogenase of bovine heart mitochondria. Biochem J 191:421–427
Vergara JJ, Bird KT, Niell FX (1995) Nitrogen assimilation following NH4 + pulses in the red alga Gracilariopsis lemaneiformis: effect on C metabolism. Mar Ecol Prog Ser 122:253–263
Viñegla B, Figueroa LF (2009) Effect of solar and artificial UV radiation on photosynthetic performance and carbonic anhydrase activity in intertidal macroalgae from southern Spain. Cienc Mar 35:59–74
Wilkinson M (1981) Survival strategies of attached algae in estuaries. Mar Sci 15:29–38
Wilkinson M, Wood P, Wells E, Scanlan C (2007) Using attached macroalgae to assess ecological status of British estuaries for the European Water Framework Directive. Mar Pollut Bull 55:136–150
Xu Z, Gao K (2009) Impacts of UV radiation on growth and photosynthetic carbon acquisition in Gracilaria lemaneiformis (Rhodophyta) under phosphorus-limited and replete conditions. Funct Plant Biol 36:1057–1064
Zhang Y, Marcillat O, Giulivi C, Ernster L, Davies KJ (1990) The oxidative inactivation of mitochondrial electron transport chain components and ATPase. J Biol Chem 265:16330–16336
Acknowledgments
The authors would like to acknowledge CAPES. Éder C. Schmidt holds a postdoctoral fellowship from CAPES. Zenilda L. Bouzon is a CNPq fellow. Fungyi Chow is a FAPESP and CAPES fellow. This study is part of the MSc dissertation of the first author.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Polo, L.K., Felix, M.R.L., Kreusch, M. et al. Metabolic profile of the brown macroalga Sargassum cymosum (Phaeophyceae, Fucales) under laboratory UV radiation and salinity conditions. J Appl Phycol 27, 887–899 (2015). https://doi.org/10.1007/s10811-014-0381-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10811-014-0381-8