Abstract
Investigation of the production and structural characteristics of the extracellular polysaccharides (ECPS) released by diatoms according to nutrient status is urgently necessary for our understanding of the roles of ECPS in aquatic ecosystem. In this study, the effects of N and P depletion and variable nutrient sources on the production and structural characterization of the soluble ECPS released by the marine diatom Thalassiosira pseudonana in batch culture were examined. The abundance of the soluble ECPS produced under N (NO3 −) depletion was higher than that obtained in the P (PO4 3−) depletion and control treatments. NH4 + rather than NO3 − and urea and sodium-glycerophosphate rather than PO4 3− were found to induce a higher abundance of soluble ECPS production at the end of the experiment, indicating that the abundance of soluble ECPS is also affected by the nutrient source. Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) analysis of the structural characteristics of the soluble ECPS samples showed that the degree of polymerization (d.p.) profiles and the distribution of the polymers with different molecular masses varied in response to nutrient depletion and different nutrient sources. An increase in the proportion of both low- and high-molecular-weight polymers under the N (NO3 −) and P (PO4 3−) depletion treatments was found. Based on the different characteristics of high- and low-molecular-weight polymers, our results suggest that the production of soluble ECPS may be one of the strategies that T. pseudonana utilizes to survive under nutrient stress conditions.
Similar content being viewed by others
References
Alcoverro T, Conte E, Mazzella L (2000) Production of mucilage by the Adriatic epipelic diatom Cylindrotheca closterium (Bacillariophyceae) under nutrient limitation. J Phycol 36:1087–1095
Chrost RJ, Faust MA (1983) Organic carbon release by phytoplankton: its composition and utilization by bacterioplankton. J Plankton Res 5:477–493
de Brouwer JFC, Stal LJ (2002) Daily fluctuations of exopolymers in cultures of the benthic diatoms Cylindrotheca closterium and Nitzschia sp (Bacillariophyceae). J Phycol 38:464–472
Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356
Dyhrman ST, Jenkins BD, Rynearson TA, Saito MA, Mercier ML, Alexander H, Whitney LP, Drzewianowski A, Bulygin VV, Bertrand EM, Wu Z, Benitez-Nelson C, Heithoff A (2012) The transcriptome and proteome of the diatom Thalassiosira pseudonana reveal a diverse phosphorus stress response. PLoS One 7(3):1–10
Fogg GE (1983) The ecological significance of extracellular products of phytoplankton photosynthesis. Bot Mar 26:3–14
Giroldo D, Vieira AAH, Paulsen BS (2003) Relative increase of deoxy sugars during microbial degradation of an extracellular polysaccharide released by a tropical freshwater Thalassiosira sp. (Bacillariophyceae). J Phycol 39:1109–1115
Granum E, Kirkvold S, Myklestad SM (2002) Cellular and extracellular production of carbohydrates and amino acids by the marine diatom Skeletonema costatum: diel variations and effects of N depletion. Mar Ecol Prog Ser 242:83–94
Guerrini F, Cangini M, Boni L, Trost P, Pistocchi R (2000) Metabolic responses of the diatom Achnanthes brevipes (Bacillariophyceae) to nutrient limitation. J Phycol 36:882–890
Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea (Cleve) Gran. Can J Microbiol 8:229–239
Janse I, van Rijssel M, Ottema A, Gottschal JC (1999) Microbial breakdown of Phaeocystis mucopolysaccharides. Limnol Oceanogr 44:1447–1457
Kato K, Stabel HH (1984) Studies on the carbon flux from phyto to bacterioplankton communities in Lake Constance. Arch Hydrobiol 102:177–192
Liang JR, Ai XX, Gao YH, Chen CP (2013) MALDI-TOF MS analysis of the extracellular polysaccharides released by the diatom Thalassiosira pseudonana. J Appl Phycol 25:477–484
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
Mooy BASV, Fredricks HF, Pedler BE, Dyhrman ST, Karl DM, Koblížek M, Lomas MW, Mincer TJ, Moore LR, Moutin T, Rappe MS, Webb EA (2009) Phytoplankton in the ocean use non-phosphorus lipids in response to phosphorus scarcity. Nature 458:69–72
Myklestad S (1977) Production of carbohydrates by marine planktonic diatoms. II. Influence of the N/P ratio in the growth medium on the assimilation ratio, growth rate, and production of cellular and extracellular carbohydrates by Chaetoceros affinis var willei (Gran) Hustedt and Skeletonema costatum (Grev) Cleve. J Exp Mar Biol Ecol 29:161–179
Myklestad S (1995) Release of extracellular products by phytoplankton with special emphasis on polysaccharides. Sci Total Environ 165:155–164
Myklestad S, Haug A (1972) Production of carbohydrates by the marine diatom Chaetoceros affinis var willei (Gran) Hustedt. I. Effect of the concentration of nutrients in the culture medium. J Exp Mar Biol Ecol 9:125–136
Nelson DM, Treguer P, Brzezinski MA, Leynaert A, Queguiner B (1995) Production and dissolution of biogenic silica in the ocean: revised global estimates, comparison with regional data and relationship to biogenic sedimentation. Global Biogeochem Cycles 9:359–372
Obernosterer I, Herndl GJ (1995) Phytoplankton extracellular release and bacterial growth: dependence on the inorganic N:P ratio. Mar Ecol Prog Ser 116:247–257
Passow U, Alldredge AL (1995) Aggregation of a diatom bloom in a mesocosm: the role of transparent exopolymer particles (TEP). Deep-Sea Res II 42:99–110
Penna A, Berluti S, Penna N, Magnani M (1999) Influence of nutrient ratios on the in vitro extracellular polysaccharide production by marine diatoms from the Adriatic Sea. J Plankton Res 21:1681–1690
Pete R, Davidson K, Hart MC, Gutierrez T, Miller AEJ (2010) Diatom derived dissolved organic matter as a driver of bacterial productivity: the role of nutrient limitation. J Exp Mar Biol Ecol 391:20–26
Pistocchi R, Guerrini F, Balboni V, Boni L (1997) Copper toxicity and carbohydrate production in the microalgae Cylindrotheca fusiformis and Gymnodinium sp. Eur J Phycol 32:125–132
Puddu A, Zoppini A, Fazi S, Rosati M, Amalfitano S, Magaletti E (2003) Bacterial uptake of DOM released from P-limited phytoplankton. FEMS Microbiol Ecol 46:257–268
Ragueneau O, Schultes S, Bidle K, Claquin P, Moriceau B (2006) Si and C interactions in the world ocean: importance of ecological processes and implications for the role of diatoms in the biological pump. Global Biogeochem Cycles 20:GB4SO2
Sharp JH (1977) Excretion of organic matter by marine phytoplankton: do healthy cells do it? Limnol Oceanogr 22:381–399
Smith DJ, Underwood GJC (2000) The production of extracellular carbohydrates by estuarine benthic diatoms: the effects of growth phase and light and dark treatment. J Phycol 36:321–333
Smith GJ, Zimmerman RC, Alberte RS (1992) Molecular and physiological responses of diatoms to variable levels of irradiance and nitrogen availability: growth of Skeletonema costatum in simulated upwelling conditions. Limnol Oceanogr 37:989–1007
Solomon CM, Lessard EJ, Keil RG, Foy MS (2003) Characterization of extracellular polymers of Phaeocystis globosa and P. antarctica. Mar Ecol Prog Ser 250:81–89
Staats N, Stal LJ, Mur LR (2000) Exopolysaccharide production by the epipelic diatom Cylindrotheca closterium: effects of nutrient conditions. J Exp Mar Biol Ecol 249:13–27
Turpin DH (1991) Effects of inorganic N availability on algal photosynthesis and carbon metabolism. J Phycol 27:14–20
Underwood GJC, Boulcott M, Raines CA, Waldron K (2004) Environmental effects on exopolymer production by marine benthic diatoms: dynamics, changes in composition, and pathways of production. J Phycol 40:293–304
Urbani R, Magaletti E, Sist P, Cicero AM (2005) Extracellular carbohydrates released by the marine diatoms Cylindrotheca closterium, Thalassiosira pseudonana and Skeletonema costatum: effect of P-depletion and growth status. Sci Total Environ 353:300–306
Wilhelm C, Büchel C, Fisahn J, Goss R, Jakob T, Laroche J, Lavaud J, Lohr M, Riebesell U, Stehfest K, Valentin K, Kroth PG (2006) The regulation of carbon and nutrient assimilation in diatoms is significantly different from green algae. Protist 157:91–124
Acknowledgments
This work was supported by the National Natural Science Foundation of China (NSFC) under grant numbers 40876079, the National 973 project under grant number 2011CB200901 and 2010CB428704, the NSFC under grant numbers 41276130, and the Natural Science Foundation of the Fujian Province of China under grant number 2008J0139.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ai, XX., Liang, JR., Gao, YH. et al. MALDI-TOF MS analysis of the extracellular polysaccharides released by the diatom Thalassiosira pseudonana under various nutrient conditions. J Appl Phycol 27, 673–684 (2015). https://doi.org/10.1007/s10811-014-0360-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10811-014-0360-0