Abstract
The water-soluble polysaccharides of brown algae attract the increasing attention of researchers as an important class of polymeric materials of biotechnological interest. The sole source for production of these polysaccharides has been large brown seaweeds such as members of Laminariales and Fucales. A new source of water-soluble polysaccharides is suggested here: it is a filamentous brown alga Streblonema sp., which can be cultivated under controlled conditions in photobioreactors that allow obtaining algal biomass with reproducible content and quality of polysaccharides. The accumulation of water-soluble polysaccharides can be stimulated by macronutrient limitation. In response to nitrogen deficiency, Streblonema sp. accumulated water-soluble polysaccharides (WSPs) rich in laminaran. WSP accumulation started after 3–4 days following nitrate depletion and reached a plateau at around day 7. Polysaccharide accumulation was related to cellular nitrogen content. The critical internal N level that triggered the onset of polysaccharide accumulation was 2.3% dry weight (DW); at a cellular N concentration less than 1.4% DW, the polysaccharide synthesis stopped. Upon nitrate re-supply, mobilization of WSP occurred after 3 days. These results suggest that a two-stage cultivation process could be used to obtain large algal biomass with high water-soluble polysaccharide production: a first cultivation stage using nitrate-supplemented medium to accumulate algal biomass followed by a second cultivation stage in a nitrate-free medium for 3 to 7 days to enhance polysaccharide content in the alga.
Similar content being viewed by others
References
Abd El Baky H, Hanaa El Baz KF, El-Latife SA (2013) Induction of sulfated polysaccharides in Spirulina platensis as response to nitrogen concentration and its biological evaluation. J Aquac Res Development 5:206
Adams C, Godfrey V, Wahlen B, Seefeldt L, Bugbee B (2013) Understanding precision nitrogen stress to optimize the growth and lipid content tradeoff in oleaginous green microalgae. Bioresour Technol 131:188–194
Arad SM, Lerental YB, Dubinsky O (1992) Effect of nitrate and sulfate starvation on polysaccharide formation in Rhodella reticulata. Bioresour Technol 42:141–148
Bellefeuille SD, Dorion S, Rivoal J, Morse D (2014) The dinoflagellate Lingulodinium polyedrum responds to N depletion by a polarized deposition of starch and lipid bodies. PLoS One 9:e111067
Black WAP (1954) The seasonal variation in the combined L-fucose content of the common British laminariaceae and fucaceae. J Sci Food Agric 5:445–448
Dragone G, Fernandes BD, Abreu AP, Vicente AA, Teixeira JA (2011) Nutrient limitation as a strategy for increasing starch accumulation in microalgae. Appl Energy 88:3331–3335
Dubois M, Gilles KA, Hamilton JK (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356
Ehrig K, Alban S (2014) Sulfated galactofucan from the brown alga Saccharina latissima—variability of yield, structural composition and bioactivity. Mar Drugs 13(1):76–101
Giroldo D, Vieira AAH (2002) An extracellular sulfated fucose-rich polysaccharide produced by a tropical strain of Cryptomonas obovata (Cryptophyceae). J Appl Phycol 14:185–191
Imbs TI, Shevchenko NM, Sukhoverkhov SV, Semenova TL, Skriptsova AV, Zvyagintseva TN (2009) Seasonal variations of the composition and structural characteristics of the polysaccharide from the brown alga Costaria costata. Chem Nat Comp 45:786–791
Iwao T, Kurashima A, Maegawa M (2008) Effect of seasonal changes in the photosynthates mannitol and laminaran on maturation of Ecklonia cava (Phaeophyceae, Laminariales) in Nishiki Bay, Central Japan. Phycol Res 56:1–6
Iwao T, Yamaguchi T, Kurashima A, Maegawa M (2010) Effect of laminaran accumulation on maturation in sporophyte fragments from Ecklonia cava (Phaeophyceae, Laminariales) under various laboratory light and temperature conditions. Phycol Res 58:132–137
Jeffrey SW, Humphrey GF (1975) New spectrophotometric equations for determining chlorophylls a, b, c1, and c2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanz 167:191–194
Kilham SS, Kreeger DA, Goulden CE, Lynn SG (1997) Effect of nutrient limitation on biochemical constituents of Ankistrodesmus falcatus. Freshw Biol 38:591–596
Klein U (1987) Intracellular carbon partitioning in Chlamydomonas reinhardtii. Plant Physiol 85:892–897
Macler BA (1986) Rugulation of carbon flow by nitrogen and light in the red alga, Gelidium couteri. Plant Physiol 82:136–141
Magaletti E, Urbani R, Sist P, Ferrari CR, Cicero AM (2004) Abundance and chemical characterization of extracellular carbohydrates released by the marine diatom Cylindrotheca fusiformis under N- and P-limitation. Eur J Phycol 39:133–142
McLachlan J (1964) Some considerations of the growth of marine algae in artificial media. Can J Microbiol 10:769–782
Msanne J, Xu D, Konda AR, Casas-Mollano JA, Awada T, Cahoon EB, Cerutti H (2012) Metabolic and gene expression changes triggered by nitrogen deprivation in the photoautotrophically grown microalgae Chlamydomonas reinhardtii and Coccomyxa sp. C-169. Phytochemistry 75:50–59
Otero A, Vincenzini M (2004) Nostoc (Cyanophyceae) goes nude: extracellular polysaccharides serve as a sink for reducing power under unbalanced C/N metabolism. J Phycol 40:74–81
Pearl R, Reed LJ (1920) On the rate of growth of the population of the United States since 1790 and its mathematical representation. Proc Natl Acad Sci U S A 6:275–288
Provasoli L (1968) Media and prospects for the cultivation of marine algae. In: Watanabe A, Hattori A (eds) Cultures and collections of algae. Proceedings of the U.S.–Japan Conference, Hakone, Japan, September 1966. Japanese Society of Plant Physiology
Razaghi A, Godhe A, Albers E (2014) Effects of nitrogen on growth and carbohydrate formation in Porphyridium cruentum. Cent Eur J Biol 9:156–162
Rioux LE, Turgeon SL, Beaulieu M (2009) Effect of season on the composition of bioactive polysaccharides from the brown seaweed Saccharina longicruris. Phytochemistry 70:1069–1075
Sharma KK, Schuhmann H, Schenk PM (2012) High lipid induction in microalgae for biodiesel production. Energies 5:1532–1553
Shevchenko NM, Anastiuk SD, Gerasimenko NI, Dmitrenok PS, Isakov VV, Zviagintseva TN (2007) Polysaccharide and lipid composition of the brown seaweed Laminaria gurjanovae. Russ J Bioorg Chem 33:88–98
Siaut M, Cuiné S, Cagnon C, Fessler B, Nguyen M, Carrier P, Beyly A, Beisson F, Triantaphylidès C, Li-Beisson Y, Peltier G (2011) Oil accumulation in the model green alga Chlamydomonas reinhardtii: characterization, variability between common laboratory strains and relationship with starch reserves. BMC Biotechnol 11:7
Sjøtun K, Gunnarsson K (1995) Seasonal growth pattern of an Icelandic Laminaria population (section Simplices, Laminariaceae, Phaeophyta) containing solid- and hollow-stiped plants. Eur J Phycol 30:281–287
Speziale BJ, Schreiner SP, Ciarnrnatteo PA, Schindler JE (1984) Comparison of N,N-dimethylformamide, dimethyl sulfoxide, and acetone for extraction of phytoplankton chlorophyll. Can J Fish Aquat Sci 41:1519–1522
Strickland JDH, Parsons TR (1972) A practical handbook of seawater analysis. Bulletin 167. Fisheries Research Board of Canada, Ottawa
Usov AI, Smirnova GP, Klochkova NG (2001) Algae polysaccharides. 55. Polysaccharide composition of some brown Kamchatka algae. Bioorg Khim 27(6):444–448 (in Russian)
Vítová M, Bišová K, Kawano S, Zachleder V (2015) Accumulation of energy reserves in algae: from cell cycles to biotechnological applications. Biothechnol Adv. doi:10.1016/j.biotechadv.2015.04.012
Yang Z, Geng G, Wang W, Zhang J (2012) Combined effects of temperature, light intensity, and nitrogen concentration on the growth and polysaccharide content of Microcystis aeruginosa in batch culture. Biochem Syst Ecol 41:130–135
Yao CH, Ai JN, Cao XP, Xue S, Zhang W (2012) Enhancing starch production of a marine green microalga Tetraselmis subcordiformis through nutrient limitation. Bioresour Technol 118:438–444
Zvyagintseva TN, Shevchenko NM, Chizhov AO, Krupnova TN, Sundukova EV, Isakov VV (2003) Water-soluble polysaccharides of some far-eastern brown seaweeds. Distribution, structure, and their dependence on the developmental conditions. J Exp Mar Biol Ecol 294:1–13
Acknowledgments
This study was partially supported by the Russian Foundation for Basic Research (project 14-04-00973).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Skriptsova, A.V. Nitrogen Effect on Water-Soluble Polysaccharide Accumulation in Streblonema sp. (Ectocarpales, Phaeophyceae). Mar Biotechnol 19, 410–419 (2017). https://doi.org/10.1007/s10126-017-9759-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10126-017-9759-3