Metabolite profiling and integrative modeling reveal metabolic constraints for carbon partitioning under nitrogen starvation in the green algae Haematococcus pluvialis

Journal of Biological Chemistry

Volumn 289, Issue 44, 2014, Pages 30387-30403

  Recht, Lee ^a   Töpfer, Nadine ^b   Batushansky, Albert ^a   Sikron, Noga ^a   Gibon, Yves ^c   Fait, Aaron ^a   Nikoloski, Zoran ^b   Boussiba, Sammy ^a   Zarka, Aliza ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^c UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALGAE; CARBON; ENZYME ACTIVITY; GALLIUM ALLOYS; METABOLISM; METABOLITES; NITROGEN; PHYSIOLOGICAL MODELS;

CHANGING ENVIRONMENT; FATTY ACID SYNTHESIS; HAEMATOCOCCUS PLUVIALIS; INTEGRATIVE MODELING; METABOLITE PROFILING; NITROGEN STARVATION; POSSIBLE MECHANISMS; TRICARBOXYLIC ACID CYCLE;

FATTY ACIDS;

CAROTENOID; FATTY ACID; NITROGEN; STARCH;

BIOSYNTHESIS; CARBOHYDRATE METABOLISM; CITRIC ACID CYCLE; CLUSTER ANALYSIS; COMPUTER SIMULATION; GREEN ALGA; LIGHT; METABOLIC FLUX ANALYSIS; METABOLISM; METABOLOME; PHYSIOLOGICAL STRESS; RADIATION RESPONSE;

CARBOHYDRATE METABOLISM; CAROTENOIDS; CHLOROPHYTA; CITRIC ACID CYCLE; CLUSTER ANALYSIS; COMPUTER SIMULATION; FATTY ACIDS; LIGHT; METABOLIC FLUX ANALYSIS; METABOLOME; NITROGEN; STARCH; STRESS, PHYSIOLOGICAL;

EID: 84908691547     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.555144     Document Type: Article

References (81)

1. Amin, S. (2009) Review on biofuel oil and gas production processes from microalgae. Energy Conversion and Management. 50, 1834-1840
2. Rosenberg, J. N., Oyler, G. A., Wilkinson, L., and Betenbaugh, M. J. (2008) A green light for engineered algae: redirecting metabolism to fuel a biotechnology revolution. Curr. Opin. Biotechnol. 19, 430-436
3. Siaut, M., Cuiné, S., Cagnon, C., Fessler, B., Nguyen, M., Carrier, P., Beyly, A., Beisson, F., Triantaphylidès, C., and Li-Beisson, Y. (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
4. Zhekisheva, M., Boussiba, S., Khozin-Goldberg, I., Zarka, A., and Cohen, Z. (2002) Accumulation of oleic acid in Haematococcus pluvialis (Chlorophyceae) under nitrogen starvation or high light is correlated with that of astaxanthin. J. Phycol. 38, 325-331
5. Rabbani, S., Beyer, P., Lintig, J., Hugueney, P., and Kleinig, H. (1998) Induced-carotene synthesis driven by triacylglycerol deposition in the unicellular alga Dunaliella bardawil. Plant Physiol. 116, 1239-1248
6. Boussiba, S., and Vonshak, A. (1991) Astaxanthin accumulation in the green alga Haematococcus pluvialis. Plant Cell Physiol. 32, 1077-1082
7. Spolaore, P., Joannis-Cassan, C., Duran, E., and Isambert, A. (2006) Commercial applications of microalgae. J. Biosci. Bioeng. 101, 87-96
8. Boussiba, S. (2000) Carotenogenesis in the green alga Haematococcus pluvialis: cellular physiology and stress response. Physiol. Plant. 108, 111-117
9. Borowitzka, M. A., Huisman, J. M., and Osborn, A. (1991) Culture of the astaxanthin-producing green alga Haematococcus pluvialis: effects of nutrients on growth and cell type. J. Appl. Phycol. 3, 295-304
10. Aflalo, C., Meshulam, Y., Zarka, A., and Boussiba, S. (2007) On the relative efficiency of two-vs. one-stage production of astaxanthin by the green alga: Haematococcus pluvialis. Biotechnol. Bioeng. 98, 300-305
11. Boussiba, S., Bing, W., Yuan, J., Zarka, A., and Chen, F. (1999) Changes in pigments profile in the green alga Haeamtococcus pluvialis exposed to environmental stresses. Biotechnol. Lett. 21, 601-604
12. Recht, L., Zarka, A., and Boussiba, S. (2012) Patterns of carbohydrate and fatty acid changes under nitrogen starvation in the microalgae Haematococcus pluvialis and Nannochloropsis sp. Appl. Microbiol. Biotechnol. 94, 1495-1503
13. Mizuno, Y., Sato, A., Watanabe, K., Hirata, A., Takeshita, T., Ota, S., Sato, N., Zachleder, V., Tsuzuki, M., and Kawano, S. (2013) Sequential accumulation of starch and lipid induced by sulfur deficiency in Chlorella and Parachlorella species. Bioresour. Technol. 129, 150-155
14. Goncalves, E. C., Johnson, J. V., and Rathinasabapathi, B. (2013) Conversion of membrane lipid acyl groups to triacylglycerol and formation of lipid bodies upon nitrogen starvation in biofuel green algae Chlorella UTEX29. Planta 238, 895-906
15. Sirevåg, R., and Levine, R. P. (1972) Fatty acid synthetase from Chlamydomonas reinhardi sites of transcription and translation. J. Biol. Chem. 247, 2586-2591
16. Rawsthorne, S. (2002) Carbon flux and fatty acid synthesis in plants. Prog. Lipid Res. 41, 182-196
17. Radakovits, R., Jinkerson, R. E., Darzins, A., and Posewitz, M. C. (2010) Genetic engineering of algae for enhanced biofuel production. Eukaryot. Cell 9, 486-501
18. Courchesne, N. M., Parisien, A., Wang, B., and Lan, C. Q. (2009) Enhancement of lipid production using biochemical, genetic and transcription factor engineering approaches. J. Biotechnol. 141, 31-41
19. Hu, Q., Sommerfeld, M., Jarvis, E., Ghirardi, M., Posewitz, M., Seibert, M., and Darzins, A. (2008) Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J. 54, 621-639
20. Beer, L. L., Boyd, E. S., Peters, J. W., and Posewitz, M. C. (2009) Engineering algae for biohydrogen and biofuel production. Curr. Opin. Biotechnol. 20, 264-271
21. Li, Y., Han, D., Hu, G., Dauvillee, D., Sommerfeld, M., Ball, S., and Hu, Q. (2010) Chlamydomonas starchless mutant defective in ADP-glucose pyrophosphorylase hyper-accumulates triacylglycerol. Metab. Eng. 12, 387-391
22. Sweetlove, L. J., Beard, K. F., Nunes-Nesi, A., Fernie, A. R., and Ratcliffe, R. G. (2010) Not just a circle: flux modes in the plant TCA cycle. Trends Plant Sci. 15, 462-470
23. Lee do, Y., Park, J. J., Barupal, D. K., and Fiehn, O. (2012) System response of metabolic networks in Chlamydomonas reinhardtii to total available ammonium. Mol. Cell. Proteomics 11, 973-988
24. Hockin, N. L., Mock, T., Mulholland, F., Kopriva, S., and Malin, G. (2012) The response of diatom central carbon metabolism to nitrogen starvation is different from that of green algae and higher plants. Plant Physiol. 158, 299-312
25. Kim, D., Hong, S., Bae, J., Yim, N., Jin, E., and Lee, C. (2011) Transcriptomic analysis of Haematococcus lacustris during astaxanthin accumulation under high irradiance and nutrient starvation. Biotechnol. Bioprocess Eng. 16, 698-705
26. Araújo, W. L., Nunes-Nesi, A., Nikoloski, Z., Sweetlove, L. J., and Fernie, A. R. (2012) Metabolic control and regulation of the tricarboxylic acid cycle in photosynthetic and heterotrophic plant tissues. Plant Cell Environ. 35, 1-21
27. Gibon, Y., Blaesing, O. E., Hannemann, J., Carillo, P., Höhne, M., Hendriks, J. H., Palacios, N., Cross, J., Selbig, J., and Stitt, M. (2004) A robotbased platform to measure multiple enzyme activities in Arabidopsis using a set of cycling assays: comparison of changes of enzyme activities and transcript levels during diurnal cycles and in prolonged darkness. Plant Cell 16, 3304-3325
28. Xiong, W., Liu, L., Wu, C., Yang, C., and Wu, Q. (2010) 13C-tracer and gas chromatography-mass spectrometry analyses reveal metabolic flux distribution in the oleaginous microalga Chlorella protothecoides. Plant Physiol. 154, 1001-1011
29. Wienkoop, S., Weiss, J., May, P., Kempa, S., Irgang, S., Recuenco-Munoz, L., Pietzke, M., Schwemmer, T., Rupprecht, J., and Egelhofer, V. (2010) Targeted proteomics for Chlamydomonas reinhardtii combined with rapid subcellular protein fractionation, metabolomics and metabolic flux analyses. Mol. Biosyst. 6, 1018-1031
30. Lewis, N. E., Nagarajan, H., and Palsson, B. O. (2012) Constraining the metabolic genotype-phenotype relationship using a phylogeny of in silico methods. Nat. Rev. Microbiol. 10, 291-305
31. Orth, J. D., Thiele, I., and Palsson, B. Ø. (2010) What is flux balance analysis?. Nat. Biotechnol. 28, 245-248
32. Stanier, R. Y., Kunisawa, R., Mandel, M., and Cohen-Bazire, G. (1971) Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriol. Rev. 35, 171-205
33. Zhekisheva, M., Zarka, A., Khozin-Goldberg, I., Cohen, Z., and Boussiba, S. (2005) Inhibition of astaxanthin synthesis under high irradiance does not abolish triacylglycerol accumulation in the green alga Haematococcus pluvialis (Chlorophyceae). J. Phycol. 41, 819-826
34. Smith, P. K., Krohn, R. I., Hermanson, G. T., Mallia, A. K., Gartner, F. H., Provenzano, M. D., Fujimoto, E. K., Goeke, N. M., Olson, B. J., and Klenk, D. C. (1985) Measurement of protein using bicinchoninic acid. Anal. Biochem. 150, 76-85
35. Roe, J. H. (1955) The determination of sugar in blood and spinal fluid with anthrone reagent. J. Biol. Chem. 212, 335-343
36. Hewitt, B. R. (1958) Spectrophotometric determination of total carbohydrate. Nature 182, 246-247
37. Gibon, Y., Pyl, E. T., Sulpice, R., Lunn, J. E., Höhne, M., Günther, M., and Stitt, M. (2009) Adjustment of growth, starch turnover, protein content and central metabolism to a decrease of the carbon supply when Arabidopsis is grown in very short photoperiods. Plant Cell Environ. 32, 859-874
38. Nunes-Nesi, A., Carrari, F., Gibon, Y., Sulpice, R., Lytovchenko, A., Fisahn, J., Graham, J., Ratcliffe, R. G., Sweetlove, L. J., and Fernie, A. R. (2007) Deficiency of mitochondrial fumarase activity in tomato plants impairs photosynthesis via an effect on stomatal function. Plant J. 50, 1093-1106
39. Piques, M., Schulze, W. X., Höhne, M., Usadel, B., Gibon, Y., Rohwer, J., and Stitt, M. (2009) Ribosome and transcript copy numbers, polysome occupancy and enzyme dynamics in Arabidopsis. Mol. Syst. Biol. 5, 314
40. Wheeler, M. C., Tronconi, M. A., Drincovich, M. F., Andreo, C. S., Flügge, U. I., and Maurino, V. G. (2005) A comprehensive analysis of the NADPmalic enzyme gene family of Arabidopsis. Plant Physiol. 139, 39-51
41. Lisec, J., Schauer, N., Kopka, J., Willmitzer, L., and Fernie, A. R. (2006) Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat. Protoc. 1, 387-396
42. Luedemann, A., Strassburg, K., Erban, A., and Kopka, J. (2008) TagFinder for the quantitative analysis of gas chromatography-mass spectrometry (GCMS) - based metabolite profiling experiments. Bioinformatics 24, 732-737
43. Erban, A., Schauer, N., Fernie, A. R., and Kopka, J. (2007) Nonsupervised construction and application of mass spectral and retention time index libraries from time-of-flight gas chromatography-mass spectrometry metabolite profiles. Methods Mol. Biol. 358, 19-38
44. Reynolds, A. P., Richards, G., de la Iglesia, B., and Rayward-Smith, V. J. (2006) Clustering rules: a comparison of partitioning and hierarchical clustering algorithms. Journal of Mathematical Modelling and Algorithms 5, 475-504
45. Chang, R. L., Ghamsari, L., Manichaikul, A., Hom, E. F., Balaji, S., Fu, W., Shen, Y., Hao, T., Palsson, B. Ø., and Salehi-Ashtiani, K. (2011) Metabolic network reconstruction of Chlamydomonas offers insight into lightdriven algal metabolism. Mol. Syst. Biol. 7, 518
46. Fan, L., Vonshak, A., Zarka, A., and Boussiba, S. (1998) Does astaxanthin protect Haematococcus against light damage?. Z. Naturforsch. C 53, 93-100
47. Heinrich, R., and Schuster, S. (1996) The Regulation of Cellular Systems. Chapman and Hall, New York
48. Mahadevan, R., and Schilling, C. (2003) The effects of alternate optimal solutions in constraint-based genome-scale metabolic models. Metab. Eng. 5, 264-276
49. Fait, A., and Fernie, A. R. (2009) Data integration. in Plant Metabolic Networks (Schwender, J., ed), Springer, NY
50. Caspi, R., Altman, T., Dreher, K., Fulcher, C. A., Subhraveti, P., Keseler, I. M., Kothari, A., Krummenacker, M., Latendresse, M., and Mueller, L. A. (2012) The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Res. 40, D742-D753
51. Lemoine, Y., and Schoefs, B. (2010) Secondary ketocarotenoid astaxanthin biosynthesis in algae: a multifunctional response to stress. Photosynth. Res. 106, 155-177
52. Han, D., Li, Y., and Hu, Q. (2013) Astaxanthin in microalgae: pathways, functions and biotechnological implications. Algae 28, 131-147
53. Schoefs, B., Rmiki, N., Rachadi, J., and Lemoine, Y. (2001) Astaxanthin accumulation in Haematococcus requires a cytochrome P450 hydroxylase and an active synthesis of fatty acids. FEBS Lett. 500, 125-128
54. Gwak, Y., Hwang, Y. S., Wang, B., Kim, M., Jeong, J., Lee, C. G., Hu, Q., Han, D., and Jin, E. (2014) Comparative analyses of lipidomes and transcriptomes reveal a concerted action of multiple defensive systems against photooxidative stress in Haematococcus pluvialis. J. Exp. Bot. 65, 4317-4334
55. Rismani-Yazdi, H., Haznedaroglu, B. Z., Hsin, C., and Peccia, J. (2012) Transcriptomic analysis of the oleaginous microalga Neochloris oleoabundans reveals metabolic insights into triacylglyceride accumulation. Biotechnol. Biofuels 5, 74
56. Sun, T. H., Liu, C. Q., Hui, Y. Y., Wu, W. K., Zhou, Z. G., and Lu, S. (2010) Coordinated regulation of gene expression for carotenoid metabolism in Chlamydomonas reinhardtii. J. Integrative Plant Biol. 52, 868-878
57. Roessner, U., Luedemann, A., Brust, D., Fiehn, O., Linke, T., Willmitzer, L., and Fernie, A. (2001) Metabolic profiling allows comprehensive phenotyping of genetically or environmentally modified plant systems. Plant Cell 13, 11-29
58. Boyle, N. R., and Morgan, J. A. (2009) Flux balance analysis of primary metabolism in. Chlamydomonas reinhardtii. BMC Syst. Biol. 3, 4
59. Xu, J., Fan, X., Zhang, X., Xu, D., Mou, S., Cao, S., Zheng, Z., Miao, J., and Ye, N. (2012) Evidence of coexistence of C3 and C4 photosynthetic pathways in a green-tide-forming alga, Ulva prolifera. PLoS One 7, e37438
60. Obata, T., Fernie, A. R., and Nunes-Nesi, A. (2013) The central carbon and energy metabolism of marine diatoms. Metabolites 3, 325-346
61. Lichtenthaler, H. K. (1999) The 1-deoxy-D-xylulose-5-phosphate pathway of isoprenoid biosynthesis in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 47-65
62. Paunier, L., and Favarger, P. (1960) Synthesis of fats from acetate or glucose. 9. Transformation of glucose into fatty acids by oxidation in the mouse in vivo. Helv. Chim. Acta 43, 118-129
63. Goyal, A. (2007) Osmoregulation in Dunaliella, Part II: photosynthesis and starch contribute carbon for glycerol synthesis during a salt stress in Dunaliella tertiolecta. Plant Physiol. Biochem. 45, 705-710
64. ElSayed, A., Rafudeen, M., and Golldack, D. (2013) Physiological aspects of raffinose family oligosaccharides in plants: protection against abiotic stress. Plant Biol. 10.1111/plb.12053
65. Berges, J. A., Charlebois, D. O., Mauzerall, D. C., and Falkowski, P. G. (1996) Differential effects of nitrogen limitation on photosynthetic efficiency of photosystems I and II in microalgae. Plant Physiol. 110, 689-696
66. Chollet, R., Vidal, J., and O'Leary, M. H. (1996) Phosphoenolpyruvate carboxylase: a ubiquitous, highly regulated enzyme in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 273-298
67. Duggleby, R. G., and Dennis, D. T. (1973) Pyruvate kinase, a possible regulatory enzyme in higher plants. Plant Physiol. 52, 312-317
68. Yong, Y. Y. R., and Lee, Y.-K. (1991) Do carotenoids play a photoprotective role in the cytoplasm of Haematococcus lacustris (Chlorophyta) ?. Phycologia 30, 257-261
69. Sweetlove, L. J., Heazlewood, J. L., Herald, V., Holtzapffel, R., Day, D. A., Leaver, C. J., and Millar, A. H. (2002) The impact of oxidative stress on Arabidopsis mitochondria. Plant J. 32, 891-904
70. Studart-Guimãraes, C., Fait, A., Nunes-Nesi, A., Carrari, F., Usadel, B., and Fernie, A. R. (2007) Reduced expression of succinyl-coenzymeAligase can be compensated for by up-regulation of the-aminobutyrate shunt in illuminated tomato leaves. Plant Physiol. 145, 626-639
71. Bolton, M. D. (2009) Primary metabolism and plant defense-fuel for the fire. Mol. Plant Microbe Interact. 22, 487-497
72. Bown, A. W., and Shelp, B. J. (1997) The metabolism and functions of-aminobutyric acid. Plant Physiol. 115, 1-5
73. Bouché, N., Fait, A., Zik, M., and Fromm, H. (2004) The root-specific glutamate decarboxylase (GAD1) is essential for sustaining GABA levels in Arabidopsis. Plant Mol. Biol. 55, 315-325
74. Bouché, N., Fait, A., Bouchez, D., Møller, S. G., and Fromm, H. (2003) Mitochondrial succinic-semialdehyde dehydrogenase of the-aminobutyrate shunt is required to restrict levels of reactive oxygen intermediates in plants. Proc. Natl. Acad. Sci. 100, 6843-6848
75. Shelp, B. J., Bown, A. W., and McLean, M. D. (1999) Metabolism and functions of-aminobutyric acid. Trends Plant Sci. 4, 446-452
76. Ma, Z., Richard, H., Tucker, D. L., Conway, T., and Foster, J. W. (2002) Collaborative regulation of Escherichia coli glutamate-dependent acid resistance by two AraC-like regulators, GadX and GadW (YhiW). J. Bacteriol. 184, 7001-7012
77. Bouché, N., Lacombe, B., and Fromm, H. (2003) GABA signaling: a conserved and ubiquitous mechanism. Trends Cell Biol. 13, 607-610
78. Fait, A., Fromm, H., Walter, D., Galili, G., and Fernie, A. R. (2008) Highway or byway: the metabolic role of the GABA shunt in plants. Trends Plant Sci. 13, 14-19
79. Tan, S., Cunningham, F. X., Youmans, M., Grabowski, B., Sun, Z., and Gantt, E. (1995) Cytochrome f loss in astaxanthin accumulating red cells of Haematococcus pluvialis (Chlorophyceae): comparison of photosynthetic activity, photosynthetic enzymes, and thylakoid membrane polypeptides in red and green cells. J. Phycol. 31, 897-905
80. Wang, S. B., Chen, F., Sommerfeld, M., and Hu, Q. (2004) Proteomic analysis of molecular response to oxidative stress by the green alga Haematococcus pluvialis (Chlorophyceae). Planta 220, 17-29
81. Peled, E., Leu, S., Zarka, A., Weiss, M., Pick, U., Khozin-Goldberg, I., and Boussiba, S. (2011) Isolation of a novel oil globule protein from the green alga Haematococcus pluvialis (Chlorophyceae). Lipids 46, 851-861