The metabolite profiling of coastal coccolithophorid species <i>Pleurochrysis carterae</i> (Haptophyta) -- Journal of Oceanology and Limnology,2016,34(4):749-756

	Cite this paper:
	ZHOU Chengxu, LUO Jie, YE Yangfang, YAN Xiaojun, LIU Baoning, WEN Xin. The metabolite profiling of coastal coccolithophorid species Pleurochrysis carterae (Haptophyta)[J]. Journal of Oceanology and Limnology, 2016, 34(4): 749-756

The metabolite profiling of coastal coccolithophorid species Pleurochrysis carterae (Haptophyta)

ZHOU Chengxu, LUO Jie, YE Yangfang, YAN Xiaojun, LIU Baoning, WEN Xin

School of Marine Sciences, Ningbo University, Ningbo 315211, China

Abstract:

Pleurochrysis carterae is a calcified coccolithophorid species that usually blooms in the coastal area and causes aquaculture losses. The cellular calcification, blooming and many other critical species specific eco-physiological processes are closely related to various metabolic pathways. The purpose of this study is to apply the unbiased and non-destructive method of nuclear magnetic resonance (NMR) to detect the unknown holistic metabolite of P. carterae. The results show that NMR spectroscopic method is practical in the analysis of metabolites of phytoplankton. The metabolome of P. carterae was dominated by 26 metabolites involved in a number of different primary and secondary metabolic pathways. Organic acids and their derivatives, amino acids, sugars, nucleic aides were mainly detected. The abundant metabolites are that closely related to the process of cellular osmotic adjustment, which possibly reflect the active ability of P. carterae to adapt to the versatile coastal niche. DMSP (dimethylsulphoniopropionate) was the most dominant metabolite in P. carterae, up to 2.065±0.278 mg/g lyophilized cells, followed by glutamate and lactose, the contents were 0.349±0.035 and 0.301±0.073 mg/g lyophilized cells respectively. Other metabolites that had the content ranged between 0.1-0.2 mg/g lyophilized cells were alanine, isethionate and arabinose. Amino acid (valine, phenylalanine, isoleucine, tyrosine), organic acid salts (lactate, succinate), scyllitol and uracil had content ranged from 0.01 to below 0.1 mg/g lyophilized cells. Trigonelline, fumarate and formate were detected in very low content (only thousandths of 1 mg per gram of lyophilized cells or below). Our results of the holistic metabolites of P. carterae are the basic references for the further studies when multiple problems will be addressed to this notorious blooming calcifying species.

Key words: coccolithophore|Pleurochrysis carterae|metabolites|metabolome|dimethylsulphoniopropionate (DMSP)

Received: 2015-02-03 Revised: 2015-05-08

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References:
Aue W P, Bartholdi E, Ernst R R. 1976a. Two-dimensional spectroscopy. Application to nuclear magnetic-resonance. J. Chem. Phys., 64 (5): 2 229-2 246.
Aue W P, Karhan J, Ernst R R. 1976b. Homonuclear broad band decoupling and two-dimensional J-resolved NMR spectroscopy. J. Chem. Phys., 64 (10): 4 226-4 227.
Blunden G, Guiry M D, Druehl L D, Kogame K, Kawai H. 2012. Trigonelline and other betaines in species of laminariales. Nat. Prod. Commun., 7 (7): 863-865.
Braunschweiler L, Ernst R R. 1983. Coherence transfer by isotropic mixing: application to proton correlation spectroscopy. J. Magn. Reson., 53 (3): 521-528.
Fan T W M, Lane A N. 2008. Structure-based profiling of metabolites and isotopomers by NMR. Prog. Nucl. Magn. Reson. Spectrosc., 52 (2-3): 69-117.
Fan T W M. 1996. Metabolite profiling by one-and twodimensional NMR analysis of complex mixtures. Prog. Nucl. Magn. Reson. Spectrosc., 28 (2): 161-219.
Fernández E, Balch W M, Marãnón E, Holligan P M. 1994. High rates of lipid biosynthesis in cultured, mesocosm and coastal populations of the cocco-lithophore Emiliania huxleyi. Mar. Ecol. Prog. Ser., 114: 13-22.
Fichtinger-Schepman A M J, Kamerling J P, Vliegenthart J F G, De Jong E W, Bosch L, Westbroek P. 1979. Composition of a methylated, acidic polysaccharide associated with coccoliths of Emiliania huxleyi (Lohmann) Kamptner. Carbohydrate Research, 69 (1): 181-189.
Gebser B, Pohnert G. 2013. Synchronized regulation of different zwitterionic metabolites in the osmoadaption of phytoplankton. Mar. Drugs, 11 (6): 2 168-2 182.
Hanson A D, Rivoal J, Paquet L, Cage D A. 1994. Biosynthesis of 3-dimethylsulfoniopropionate in Wollastonia biflora (L.) DC. Evidence that S-methylmethionine is an intermediate. Plant Physiol., 105 (1): 103-110.
Holligan P M, Fernández E, Aiken J, Balch W M, Burkill P H, Finch M, Groom S B, Malin G, Muller K, Purdie D A, Robinson C, Trees C C, Turner S M, Van der Wal P. 1993. A biogeochemical study of the coccolithophore Emiliania huxleyi, in the north Atlantic. Global Biogeochem. Cy., 7 (4): 879-900.
Houdan A, Bonnard A, Fresnel J, Fouchard S, Billard C, Probert I. 2004. Toxicity of coastal coccolithophores (Prymnesiophyceae, Haptophyta). J. Plankton Res., 26 (8): 875-883.
Jamers A, Blust R, De Coen W, Griffin J L, Jones O A H. 2013. An omics based assessment of cadmium toxicity in the green alga Chlamydomonas reinhardtii. Aquat. Toxicol., 126: 355-364.
Jiang Y, Zhou C X, Luo Q J, Ma B. 2009. Lethal effects of different Pleurochrysis carterae cells on brine shrimp. Asian Journal of Ecotoxicology, 4 (4): 561-568. (in Chinese with English abstract)
Keller M D, Kiene R P, Matrai P A, Bellows W K. 1999. Production of glycine betaine and dimethylsulfoniopropionate in marine phytoplankton. I. Batch cultures. Mar. Biol., 135 (2): 237-248.
Keller M D. 1989. Dimethyl sulfide production and marine phytoplankton: the importance of species composition and cell size. Biol. Oceanogr., 6 (5-6): 375-382.
Kiene R P. 1996. Production of methanethiol from dimethylsulfoniopropionate in marine surface waters. Mar. Chem., 54 (1-2): 69-83.
Kirst G O. 1996. Osmotic adjustment in phytoplankton and MacroAlgae. The use of Dimethylsulfoniopropionate (DMSP). In: Kiene R P, Visscher P T, Keller M D, Kirst G O eds. Biological and Environmental Chemistry of DMSP and Related Sulfonium Compounds. Plenum Press, New York, USA. p.121-129.
Kobayashi Y, Torii A, Kato M, Adachi K. 2007. Accumulation of cyclitols functioning as compatible solutes in the Haptophyte alga Pavlova sp. Phycological Research, 55 (2): 81-90.
Malin G, Erst G O. 1997. Algal production of dimethyl sulfide and its atmospheric role. J. Phycol., 33 (6): 889-896.
Marsh M E, Chang D K, King G C. 1992. Isolation and characterization of a novel acidic polysaccharide containing tartrate and glyoxylate residues from the mineralized scales of a unicellular coccolithophorid alga Pleurochrysis carterae. The Journal of Biological Chemistry, 267 (28): 20 507-20 512.
Marsh M E, Dickinson D P. 1997. Polyanion-mediated mineralization-mineralization in coccolithophore (Pleurochrysis carterae) variants which do not express PS2, the most abundant and acidic mineral-associated polyanion in wild-type cells. Protoplasma, 199 (1-2): 9-17.
Marsh M E. 1994. Polyanion-mediated mineralizationassembly and reorganization of acidic polysaccharides in the Golgi system of a coccolithophorid alga during mineral deposition. Protoplasma, 177 (3-4): 108-122.
Marsh M E. 1996. Polyanion-mediated mineralization-a kinetic analysis of the calcium-carrier hypothesis in the phytoflagellate Pleurochrysis carterae. Protoplasma, 190 (3): 181-188.
Mausz M A, Pohnert G. 2015. Phenotypic diversity of diploid and haploid Emiliania huxleyi cells and of cells in different growth phases revealed by comparative metabolomics. J. Plant Physiol., 172: 137-148.
Maxwell J R, Mackenzie A S, Volkman J K. 1980. Configuration at C-24 in steranes and sterols. Nature, 286 (5774): 694-697.
Nevitt G A, Bonadonna F. 2005. Sensitivity to dimethyl sulphide suggests a mechanism for olfactory navigation by seabirds. Biology Letters, 1 (3): 303-305.
Obata T, Schoenefeld S, Krahnert I, Bergmann S, Scheffel A, Fernie A R. 2013. Gas-Chromatography Mass-Spectrometry (GC-MS) based metabolite profiling reveals mannitol as a major storage carbohydrate in the coccolithophorid alga Emiliania huxleyi. Metabolites, 3 (1): 168-184.
Rokitta S D, John U, Rost B. 2012. Ocean acidification affects redox-balance and ion-homeostasis in the life-cycle stages of Emiliania huxleyi. PLoS One, 7 (12): e52212, http://dx.doi.org/10.1371/journal.pone.0052212.
Rokitta S D, von Dassow P, Rost B, John U. 2014. Emiliania huxleyi endures N-limitation with an efficient metabolic budgeting and effective ATP synthesis. BMC Genomics, 15: 1 051, http://www.biomedcentral.com/1471-2164/15/1051.
Salmon D L. 2013. Metabolite Profiling of the Coccolithophore Emiliania huxleyi to Examine Links between Calcification and Central Metabolism. University of Exeter, Exeter, UK, https://ore.exeter.ac.uk/repository/handle/10871/14932.
Seymour J R, Simó R, Ahmed T, Stocker R. 2010. Chemoattraction to dimethylsulfoniopropionate throughout the marine microbial food web. Science, 329 (5989): 342-345.
Stefels J. 2000. Physiological aspects of the production and conversion of DMSP in marine algae and higher plants. Journal of Sea Research, 43 (3-4): 183-197.
Strom S L, Bright K J. 2009. Inter-strain differences in nitrogen use by the coccolithophore Emiliania huxleyi, and consequences for predation by a planktonic ciliate. Harmful Algae, 8 (5): 811-816.
Sukhanova I N, Flint M V. 1998. Anomalous blooming of coccolithophorids over the eastern Bering Sea shelf. Oceanology, 38 (4): 502-505.
Sunda W, Kieber D J, Kiene R P, Huntsman S. 2002. An antioxidant function for DMSP and DMS in marine algae. Nature, 418 (6895): 317-320.
Thierstein H R, Young J R. 2004. Coccolithophores: From Molecular Processes to Global Impact. Springer-Verlag, Berlin Heidelberg, Germany.
Viso A C, Marty J C. 1993. Fatty acids from 28 marine microalgae. Phytochemistry, 34 (6): 1 521-1 533.
Wiesemeier T, Pohnert G. 2007. Direct quantification of dimethylsulfoniopropionate (DMSP) in marine microand macroalgae using HPLC or UPLC/MS. J ournal of Chromatogr aphy B, 850 (1-2): 493-498.
Winter A, Henderiks J, Beaufort L, Rickaby R E M, Brown C W. 2013. Poleward expansion of the coccolithophore Emiliania huxleyi. J. Plankton Res., 36 (2): 316-325, http://dx.doi.org/10.1093/plankt/fbt110.
Wolfe G V, Steinke M, Kirst G O. 1997. Grazing-activated chemical defence in a unicellular marine alga. Nature, 387 (6636): 894-897.
Wolfe G V, Steinke M. 1996. Grazing-activated production of dimethyl sulfide (DMS) by two clones of Emiliania huxleyi. Limnology and Oceanography, 41 (6): 1 151-1 160.
Yancey P H. 2005. Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. The Journal of Experimental Biology, 208 (15): 2 819-2 830.
Zhang W L, Tan N G J, Li S F Y. 2014. NMR-based metabolomics and LC-MS/MS quantification reveal metal-specific tolerance and redox homeostasis in Chlorella vulgaris. Mol. BioSyst., 10 (1): 149-160.
Zhou C X, Xu J L, Yan X J, Hou Y D, Jiang Y. 2009. Analysis of dimethylsulfide and dimethylsulfoniopropionate in marine microalgae culture. Chin. J. Anal. Chem., 37 (9): 1 308-1 312.