Quantitative proteomics provides insight into the response of the marine dinoflagellate <i>Prorocentrum donghaiense</i> to changes in ambient phosphorus -- Journal of Oceanology and Limnology,2022,40(2):563-576

	Cite this paper:
	Shufeng ZHANG, Chunjuan YUAN, Ying CHEN, Lin LIN, Dazhi WANG. Quantitative proteomics provides insight into the response of the marine dinoflagellate Prorocentrum donghaiense to changes in ambient phosphorus[J]. Journal of Oceanology and Limnology, 2022, 40(2): 563-576

Quantitative proteomics provides insight into the response of the marine dinoflagellate Prorocentrum donghaiense to changes in ambient phosphorus

Shufeng ZHANG¹, Chunjuan YUAN¹, Ying CHEN¹, Lin LIN¹, Dazhi WANG^1,2

1 State Key Laboratory of Marine Environmental Science/College of the Environment and Ecology, Xiamen University, Xiamen 361102, China;
2 Key Laboratory of Marine Ecology&Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China

Abstract:

Dinoflagellates are the major causative agents of harmful algal blooms in the global ocean and they usually form blooms under conditions of very low dissolved inorganic phosphorus (DIP). However, the mechanisms underpinning the dinoflagellate blooms remain unclear. Here, we quantitatively compared protein expression profiles of a marine dinoflagellate, Prorocentrum donghaiense, grown in inorganic P-replete, P-deficient, and DIP- and dissolved organic phosphorus (DOP)-resupplied conditions by employing a Tandem Mass Tag (TMT)-based quantitative proteomic approach. Proteins involved in intracellular P reallocation, organic P, and non-P lipid utilization were up-regulated under the P-deficient condition, while inorganic phosphate transporters varied insignificantly. In response to the P resupplementation, nitrogen metabolism, ribosome, porphyrin, and chlorophyll metabolism were up-regulated, while lysosome, and starch and sucrose metabolism were down-regulated. Notably, photosynthesis was up-regulated and secondary metabolism was down-regulated only in the DIP-resupplied cells, whereas amino acid metabolism and vitamin B6 metabolism were up-regulated in the DOP-resupplied cells, indicating differential response mechanisms of P. donghaiense to DIP or DOP resupplementation. Our results indicated that P. donghaiense initiated multiple strategies in response to an ambient inorganic P-deficiency, and its efficient DOP assimilation by providing both P and carbon sources might be a key factor driving bloom formations of P. donghaiense in a low DIP environment.

Key words: marine dinoflagellates|harmful algal blooms|Prorocentrum donghaiense|phosphorus|quantitative proteomics

Received: 2020-10-19 Revised:

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Articles by Dazhi WANG

References:
Anderson D M, Glibert P M, Burkholder J M.2002.Harmful algal blooms and eutrophication:nutrient sources, composition, and consequences.Estuaries, 25(4):704-726, https://doi.org/10.1007/BF02804901.
Bargmann B O R, Munnik T.2006.The role of phospholipase D in plant stress responses.Current Opinion in Plant Biology, 9(5):515-522, https://doi.org/10.1016/j.pbi.2006.07.011.
Bassham D C.2009.Function and regulation of macroautophagy in plants.Biochimica et Biophysica Acta(BBA) -Molecular Cell Research, 1793(9):1397-1403, https://doi.org/10.1016/j.bbamcr.2009.01.001.
Benitez-Nelson C R.2000.The biogeochemical cycling of phosphorus in marine systems.Earth-Science Reviews, 51(1-4):109-135, https://doi.org/10.1016/S0012-8252(00) 00018-0.
Beyenbach K W, Wieczorek H.2006.The V-type H+ ATPase:molecular structure and function, physiological roles and regulation.Journal of Experimental Biology, 209(Pt4):577-589, https://doi.org/10.1242/jeb.02014.
Cañellas M, Agustí S, Duarte C M.2000.Latitudinal variability in phosphate uptake in the Central Atlantic.Marine Ecology Progress Series, 194:283-294, https://doi.org/10.3354/meps194283.
Cembella A D, Antia N J, Harrison P J, Rhee G Y.1984.The utilization of inorganic and organic phosphorous compounds as nutrients by eukaryotic microalgae:a multidisciplinary perspective:Part 2.CRC Critical Reviews in Microbiology, 11(1):13-81, https://doi.org/10.3109/10408418409105902.
Cembella A D, Antia N J, Harrison P J.1982.The utilization of inorganic and organic phosphorous compounds as nutrients by eukaryotic microalgae:a multidisciplinary perspective:Part 1.CRC Critical Reviews in Microbiology, 10(4):317-391, https://doi.org/10.3109/10408418209113567.
Chen H, Xiong L M.2005.Pyridoxine is required for postembryonic root development and tolerance to osmotic and oxidative stresses.The Plant Journal, 44(3):396-408, https://doi.org/10.1111/j.1365-313X.2005.02538.x.
Cramer W A, Yamashita E, Baniulis D, Hasan S S.2013.Cytochrome B₆f complex.In:Roberts G C K ed.Encyclopedia of Biophysics.Springer, Berlin Heidelberg, https://doi.org/10.1007/978-3-642-16712-6_24.
Currie D J, Bentzen E, Kalff J.1986.Does algal-bacterial phosphorus partitioning vary among lakes? A comparative study of orthophosphate uptake and alkaline phosphatase activity in freshwater.Canadian Journal of Fisheries and Aquatic Sciences, 43(2):311-318, https://doi.org/10.1139/f86-040.
Do Rosário Gomes H, Goes J I, Matondkar S G P, Buskey E J, Basu S, Parab S, Thoppil P.2014.Massive outbreaks of Noctiluca scintillans blooms in the Arabian Sea due to spread of hypoxia.Nature Communications, 5:4862, https://doi.org/10.1038/ncomms5862.
Doelling J H, Walker J M, Friedman E M, Thompson A R, Vierstra R D.2002.The APG8/12-activating enzyme APG7 is required for proper nutrient recycling and senescence in Arabidopsis thaliana.The Journal of Biological Chemistry, 277(36):33105-33114, https://doi.org/10.1074/jbc.M204630200.
Dyhrman S T, Jenkins B D, Rynearson T A, Saito M A, Mercier M L, Alexander H, Whitney L P, Drzewianowski A, Bulygin V V, Bertrand E M, Wu Z J, 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):e33768, https://doi.org/10.1371/journal.pone.0033768.
Dyhrman S T.2016.Nutrients and their acquisition:phosphorus physiology in microalgae.In:Physiology of Microalgae.
Springer International Publishing, Switzerland.p.155-183, https://doi.org/10.1007/978-3-319-24945-2_8.
Erb M, Kliebenstein D J.2020.Plant secondary metabolites as defenses, regulators, and primary metabolites:the blurred functional trichotomy.Plant Physiology, 184(1):39-52, https://doi.org/10.1104/pp.20.00433.
Falkowski P G, Raven J A.2013.Aquatic Photosynthesis.Princeton University Press, Princeton.
Feng S G, Jiao K L, Guo H, Jiang M Y, Hao J, Wang H Z, Shen C J.2017.Succinyl-proteome profiling of Dendrobium officinale, an important traditional Chinese orchid herb, revealed involvement of succinylation in the glycolysis pathway.BMC Genomics, 18(1):598, https://doi.org/10.1186/s12864-017-3978-x.
Fricke A, Jauzein C, Lemée R, Mangialajo L.2015.Dynamics of benthic bloom-forming dinoflagellates:environmental factors and interspecific relations.European Journal of Phycology, 50(Sup1), https://doi.org/10.1080/09670262.2015.1069493.
Fu M, Song X X, Yu Z M, Liu Y.2013.Responses of phosphate transporter gene and alkaline phosphatase in Thalassiosira pseudonana to phosphine.PLoS One, 8(3):e59770, https://doi.org/10.1371/journal.pone.0059770.
Gong W, Browne J, Hall N, Schruth D, Paerl H, Marchetti A.2017.Molecular insights into a dinoflagellate bloom.The ISME Journal, 11(2):439-452, https://doi.org/10.1038/ismej.2016.129.
Gooch J W.2011.Light reaction.In:Encyclopedic Dictionary of Polymers.Springer, New York, https://doi.org/10.1007/978-1-4419-6247-8_14120.
Harris R A.2013.Glycolysis overview.In:Encyclopedia of Biological Chemistry.2^nd edn.Academic Press, New York.p.443-447.
Herrero S, Daub M E.2007.Genetic manipulation of Vitamin B-6 biosynthesis in tobacco and fungi uncovers limitations to up-regulation of the pathway.Plant Science, 172(3):609-620, https://doi.org/10.1016/j.plantsci.2006.11.011.
Hildebrandt T M, Nesi A N, Araújo W L, Braun H P.2015.Amino acid catabolism in plants.Molecular Plant, 8(11):1563-1579, https://doi.org/10.1016/j.molp.2015.09.005.
Jauzein C, Labry C, Youenou A, Quéré J, Delmas D, Collos Y.2010.Growth and phosphorus uptake by the toxic dinoflagellate Alexandrium catenella (dinophyceae) in response to phosphate limitation.Journal of Phycology, 46(5):926-936, https://doi.org/10.1111/j.1529-8817.2010.00878.x.
Kan C C, Chung T Y, Juo Y A, Hsieh M H.2015.Glutamine rapidly induces the expression of key transcription factor genes involved in nitrogen and stress responses in rice roots.BMC Genomics, 16(1):731, https://doi.org/10.1186/s12864-015-1892-7.
Keller M D, Selvin R C, Claus W, Guillard R R L.1987.Media for the culture of oceanic ultraphytoplankton.Journal of Phycology, 23(4):633-638, https://doi.org/10.1111/j.1529-8817.1987.tb04217.x.
Lea P J, Miflin B J.2003.Glutamate synthase and the synthesis of glutamate in plants.Plant Physiology and Biochemistry, 41(6-7):555-564, https://doi.org/10.1016/S0981-9428(03) 00060-3.
Lei Q Y, Lü S H.2011.Molecular ecological responses of the dinoflagellate Karenia mikimotoi to phosphate stress.Harmful Algae, 12:39-45, https://doi.org/10.1016/j.hal.2011.08.010.
Li H M, Tang H J, Shi X Y, Zhang C S, Wang X L.2014.Increased nutrient loads from the Changjiang (Yangtze) River have led to increased Harmful Algal Blooms.Harmful Algae, 39:92-101, https://doi.org/10.1016/j.hal.2014.07.002.
Lin S J, Litaker R W, Sunda W G.2016.Phosphorus physiological ecology and molecular mechanisms in marine phytoplankton.Journal of Phycology, 52(1):10-36, https://doi.org/10.1111/jpy.12365.
Lu S C.2000.S-adenosylmethionine.International Journal of Biochemistry and Cell Biology, 32(4):391-395, https://doi.org/10.1016/s1357-2725(99) 00139-9.
Luo H, Lin X, Li L, Lin L X, Zhang C, Lin S J.2017.Transcriptomic and physiological analyses of the dinoflagellate Karenia mikimotoi reveal non-alkaline phosphatase-based molecular machinery of ATP utilisation.Environmental Microbiology, 19(11):4506-4518, https://doi.org/10.1111/1462-2920.13899.
Moffatt B A, Weretilnyk E A.2001.Sustaining S-adenosyl-Lmethionine-dependent methyltransferase activity in plant cells.Physiologia Plantarum, 113(4):435-442, https://doi.org/10.1034/j.1399-3054.2001.1130401.x.
Morot-Gaudry J F, Job D, Lea P J.2001.Amino acid metabolism.In:Plant Nitrogen.Springer, Berlin, Heidelberg.p.167-211.
Munnik T, Musgrave A.2001.Phospholipid signaling in plants:holding on to phospholipase D.Science Signaling, 2001(111):pe42, https://doi.org/10.1126/stke.2001.111.pe42.
Ou L J, Huang X Y, Huang B Q, Qi Y Z, Lu S H.2015.Growth and competition for different forms of organic phosphorus by the dinoflagellate Prorocentrum donghaiense with the dinoflagellate Alexandrium catenella and the diatom Skeletonema costatum s.l.Hydrobiologia, 754(1):29-41, https://doi.org/10.1007/s10750-014-1994-2.
Ou L J.2006.Ecophysiological responses of typical harmful algal bloom species to phosphorus.Xiamen University, Xiamen.p.96-102. (in Chinese with English abstract)
Paolo F, Suzanne J.2009.Membrane phospholipid synthesis and endoplasmic reticulum function.Journal of Lipid Research, 50(Suppl):S311-S316, https://doi.org/10.1194/jlr.r800049-jlr200.
Plaxton W C.1996.The organization and regulation of plant glycolysis.Annual Review of Plant Physiology and Plant Molecular Biology, 147:185-214, https://doi.org/10.1146/annurev.arplant.47.1.185.
Raschke M, Boycheva S, Crèvecoeur M, Nunes-Nesi A, Witt S, Fernie A R, Amrhein N, Fitzpatrick T B.2011.Enhanced levels of vitamin B6 increase aerial organ size and positively affect stress tolerance in Arabidopsis.The Plant Journal, 66(3):414-432, https://doi.org/10.1111/j.1365-313X.2011.04499.x.
Secco D, Wang C, Arpat B A, Wang Z Y, Poirier Y, Tyerman S D, Wu P, Shou H X, Whelan J.2012.The emerging importance of the SPX domain-containing proteins in phosphate homeostasis.New Phytologist, 193(4):842-851, https://doi.org/10.1111/j.1469-8137.2011.04002.x.
Shi X G, Lin X, Li L, Li M Z, Palenik B, Lin S J.2017.Transcriptomic and microRNAomic profiling reveals multi-faceted mechanisms to cope with phosphate stress in a dinoflagellate.The ISME Journal, 11(10):2209-2218, https://doi.org/10.1038/ismej.2017.81.
Stewart A J, Chapman W, Jenkins G I, Graham I, Martin T, Crozier A.2001.The effect of nitrogen and phosphorus deficiency on flavonol accumulation in plant tissues.Plant, Cell and Environment, 24(11):1189-1197, https://doi.org/10.1046/j.1365-3040.2001.00768.x.
Szydlowski N, Bürkle L, Pourcel L, Moulin M, Stolz J, Fitzpatrick T B.2013.Recycling of pyridoxine (vitamin B6) by PUP1 in Arabidopsis.The Plant Journal, 75(1):40-52, https://doi.org/10.1111/tpj.12195.
Temple S J, Vance C P, Gantt J S.1998.Glutamate synthase and nitrogen assimilation.Trends in Plant Science, 3(2):51-56, https://doi.org/10.1016/S1360-1385(97) 01159-X.
TeSlaa T, Teitell M A.2014.Chapter five-techniques to monitor glycolysis.Methods in Enzymology, 542:91-114, https://doi.org/10.1016/B978-0-12-416618-9.00005-4.
Van Mooy B A S, Fredricks H F, Pedler B E, Dyhrman S T, Karl D M, Koblížek M, Lomas M W, Mincer T J, Moore L R, Moutin T, Rappé M S, Webb E A.2009.Phytoplankton in the ocean use non-phosphorus lipids in response to phosphorus scarcity.Nature, 458(7234):69-72, https://doi.org/10.1038/nature07659.
Walker B J, Strand D D, Kramer D M, Cousins A B.2014.The response of cyclic electron flow around photosystem I to changes in photorespiration and nitrate assimilation.Plant Physiology, 165:453-462, https://doi.org/10.1104/pp.114.238238.
Wells M L, Karlson B, Wulff A, Kudela R, Trick C, Asnaghi V, Berdalet E, Cochlan W, Davidson K, De Rijcke M, Dutkiewicz S, Hallegraeff G, Flynn K J, Legrand C, Paerl H, Silke J, Suikkanen S, Thompson P, Trainer V L.2020.Future HAB science:directions and challenges in a changing climate.Harmful Algae, 91:101632, http://doi.org/10.1016/j.hal.2019.101632.
Wells M L, Trainer V L, Smayda T J, Karlson B S O, Trick C G, Kudela R M, Ishikawa A, Bernard S, WulffA, Anderson D M, Cochlan W P.2015.Harmful algal blooms and climate change:learning from the past and present to forecast the future.Harmful Algae, 49:68-93, https://doi.org/10.1016/j.hal.2015.07.009.
Xiao W P, Liu X, Irwin A J, Laws E A, Wang L, Chen B Z, Zeng Y, Huang B Q.2018.Warming and eutrophication combine to restructure diatoms and dinoflagellates.Water Research, 128:206-216, https://doi.org/10.1016/j.watres.2017.10.051.
Yu B, Xu C C, Benning C.2002.Arabidopsis disrupted in SQD2 encoding sulfolipid synthase is impaired in phosphate-limited growth.Proceedings of the National Academy of Sciences of the United States of America, 99(8):5732-5737, https://doi.org/10.1073/pnas.082696499.
Yu R C, Lü S H, Liang Y B.2018.Harmful algal blooms in the coastal waters of China.In:Global Ecology and Oceanography of Harmful Algal Blooms.Springer.p.309-316, https://doi.org/10.1007/978-3-319-70069-4_15.
Zhang C Y, Chen G F, Wang Y Y, Guo C L, Zhou J.2018.Physiological and molecular responses of Prorocentrum donghaiense to dissolved inorganic phosphorus limitation.Marine Pollution Bulletin, 129(2):562-572, https://doi.org/10.1016/j.marpolbul.2017.10.031.
Zhang C, Lin S J, Huang L M, Lu W, Li M Z, Liu S.2014.Suppression subtraction hybridization analysis revealed regulation of some cell cycle and toxin genes in Alexandrium catenella by phosphate limitation.Harmful Algae, 39:26-39, https://doi.org/10.1016/j.hal.2014.06.005.
Zhang S F, Chen Y, Xie Z X, Zhang H, Lin L, Wang D Z.2019a.Unraveling the molecular mechanism of the response to changing ambient phosphorus in the dinoflagellate Alexandrium catenella with quantitative proteomics.Journal of Proteomics, 196:141-149, https://doi.org/10.1016/j.jprot.2018.11.004.
Zhang S F, Yuan C J, Chen Y, Chen X H, Li D X, Liu J L, Lin L, Wang D Z.2016.Comparative transcriptomic analysis reveals novel insights into the adaptive response of Skeletonema costatum to changing ambient phosphorus.Frontiers in Microbiology, 7:1476, https://doi.org/10.3389/fmicb.2016.01476.
Zhang S F, Yuan C J, Chen Y, Lin L, Wang D Z.2019b.Transcriptomic response to changing ambient phosphorus in the marine dinoflagellate Prorocentrum donghaiense.Science of the Total Environment, 692:1037-1047, https://doi.org/10.1016/j.scitotenv.2019.07.291.
Zhang S F, Zhang Y, Xie Z X, Zhang H, Lin L, Wang D Z.2015.iTRAQ-based quantitative proteomic analysis of a toxigenic dinoflagellate Alexandrium catenella and its non-toxic mutant.Proteomics, 15(23-24):4041-4050, https://doi.org/10.1002/pmic.201500156.
Zhou Z X, Yu R C, Zhou M J.2017.Seasonal succession of microalgal blooms from diatoms to dinoflagellates in the East China Sea:a numerical simulation study.Ecological Modelling, 360:150-162, https://doi.org/10.1016/j.ecolmodel.2017.06.027.