Manipulation of oil synthesis in Nannochloropsis strain NIES-2145 with a phosphorus starvation-inducible promoter from Chlamydomonas reinhardtii

Frontiers in Microbiology

Volumn 6, Issue SEP, 2015, Pages

  Iwai, Masako ^a,b   Hori, Koichi ^a,b   Sasaki Sekimoto, Yuko ^a   Shimojima, Mie ^a   Ohta, Hiroyuki ^a,b  

^a TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Algae; Inducible promoter; Nannochloropsis; Phosphorus starvation; Triacylglycerol

Indexed keywords

COMPLEMENTARY DNA; FATTY ACID ESTER; MEMBRANE LIPID; PHOSPHORUS; TRIACYLGLYCEROL;

ALGAL GROWTH; AMINO ACID SEQUENCE; ARTICLE; CHLAMYDOMONAS REINHARDTII; CONTROLLED STUDY; GENE EXPRESSION; GENETIC TRANSFORMATION; LIPID ANALYSIS; LIPID COMPOSITION; LIPID STORAGE; LIPOGENESIS; MASS FRAGMENTOGRAPHY; NANNOCHLOROPSIS; NONHUMAN; NUTRIENT LIMITATION; PHYLOGENETIC TREE; PHYLOGENY; PROMOTER REGION; PROTEIN MOTIF; SEQUENCE ALIGNMENT; STARVATION;

EID: 84946736606     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00912     Document Type: Article

References (67)

1. Aoki, M., Sato, N., Meguro, A., and Tsuzuki, M. (2004). Differing involvement of sulfoquinovosyl diacylglycerol in photosystem II in two species of unicellular cyanobacteria. Eur. J. Biochem. 271, 685-693. doi: 10.1111/j.1432-1033.2003.03970.x
2. Arudchelvam, Y., and Nirmalakhandan, N. (2012). Optimizing net energy gain in algal cultivation for biodiesel production. Bioresour. Technol. 114, 294-302. doi: 10.1016/j.biortech.2012.02.126
3. Benning, C., Beatty, J. T., Prince, R. C., and Somerville, C. R. (1993). The sulfolipid sulfoquinovosyldiacylglycerol is not required for photosynthetic electron transport in Rhodobacter sphaeroides but enhances growth under phosphate limitation. Proc. Natl. Acad. Sci. U.S.A. 90, 1561-1565. doi: 10.1073/pnas.90.4.1561
4. Benning, C., Huang, Z. H., and Gage, D. A. (1995). Accumulation of a novel glycolipid and a betaine lipid in cells of Rhodobacter sphaeroides grown under phosphate limitation. Arch. Biochem. Biophys 317, 103-111. doi: 10.1006/abbi.1995.1141
5. Bligh, E. G., and Dyer, W. J. (1959). A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911-917. doi: 10.1139/o59-099
6. Bondioli, P., Della Bella, L., Rivolta, G., Chini Zittelli, G., Bassi, N., Rodolfi, L., et al. (2012). Oil production by the marine microalgae Nannochloropsis sp. F&M-M24 and Tetraselmis suecica F&M-M33. Bioresour. Technol. 114, 567-572. doi: 10.1016/j.biortech.2012.02.123
7. Boyle, N. R., Page, M. D., Liu, B., Blaby, I. K., Casero, D., Kropat, J., et al. (2012). Three acyltransferases and nitrogen-responsive regulator are implicated in nitrogen starvation-induced triacylglycerol accumulation in Chlamydomonas. J. Biol. Chem. 287, 15811-15825. doi: 10.1074/jbc.M111.334052
8. Brueggeman, A. J., Kuehler, D., and Weeks, D. P. (2014). Evaluation of three herbicide resistance genes for use in genetic transformations and for potential crop protection in algae production. Plant Biotechnol. J. 12, 894-902. doi: 10.1111/pbi.12192
9. Bustos, R., Castrillo, G., Linhares, F., Puga, M. I., Rubio, V., Pérez-Pérez, J., et al. (2010). A central regulatory system largely controls transcriptional activation and repression responses to phosphate starvation in Arabidopsis. PLoS Genet. 6:e1001102. doi: 10.1371/journal.pgen.1001102
10. Cases, S., Smith, S. J., Zheng, Y. W., Myers, H. M., Lear, S. R., Sande, E., et al. (1998). Identification of a gene encoding an acyl CoA:diacylglycerol acyltransferase, a key enzyme in triacylglycerol synthesis. Proc. Natl. Acad. Sci. U.S.A. 95, 13018-13023. doi: 10.1073/pnas.95.22.13018
11. Chang, C. W., Moseley, J. L., Wykoff, D., and Grossman, A. R. (2005). The LPB1 gene is important for acclimation of Chlamydomonas reinhardtii to phosphorus and sulfur deprivation. Plant Physiol. 138, 319-329. doi: 10.1104/pp.105.059550
12. Converti, A., Casazza, A. A., Ortiz, E. Y., Perego, P., and Borghi, M. D. (2009). Effect of temperature and nitrogen concentration on the growth and lipid content of Nannochloropsis oculata and Chlorella vulgaris for biodiesel production. Chem. Eng. Process. 48, 1146-1151. doi: 10.1016/j.cep.2009.03.006
13. Eichler-Stahlberg, A., Weisheit, W., Ruecker, O., and Heitzer, M. (2009). Strategies to facilitate transgene expression in Chlamydomonas reinhardtii. Planta 229, 873-883. doi: 10.1007/s00425-008-0879-x
14. Essigmann, B., Güler, S., Narang, R. A., Linke, D., and Benning, C. (1998). Phosphate availability affects the thylakoid lipid composition and the expression of SQD1, a gene required for sulfolipid biosynthesis in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 95, 1950-1955. doi: 10.1073/pnas.95.4.1950
15. Franco-Zorrilla, J. M., González, E., Bustos, R., Linhares, F., Leyva, A., and Paz-Ares, J. (2004). The transcriptional control of plant responses to phosphate limitation. J. Exp. Bot. 55, 285-293. doi: 10.1093/jxb/erh009
16. Gaude, N., Nakamura, Y., Scheible, W. R., Ohta, H., and Dörmann, P. (2008). Phospholipase C5 (NPC5) is involved in galactolipid accumulation during phosphate limitation in leaves of Arabidopsis. Plant J. 56, 28-39. doi: 10.1111/j.1365-313X.2008.03582.x
17. Giroud, C., Gerber, A., and Eichenberger, W. (1988). Lipids of Chlamydomonas reinhardtii. Analysis of molecular species and intracellular site(s) of biosynthesis. Plant Cell Physiol. 29, 587-595.
18. Grossman, A. (2000). Acclimation of Chlamydomonas reinhardtii to its nutrient environment. Protist 151, 201-224. doi: 10.1078/1434-4610-00020
19. Guillard, R. R., and Ryther, J. H. (1962). Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt, and Detonula confervacea (cleve) Gran. Can. J. Microbiol. 8, 229-239. doi: 10.1139/m62-029
20. Guschina, I. A., and Harwood, J. L. (2006). Lipids and lipid metabolism in eukaryotic algae. Prog. Lipid. Res. 45, 160-186. doi: 10.1016/j.plipres.2006.01.001
21. Harris, E. H. (2009). The Chlamydomonas Sourcebook: Introduction to Chlamydomonas and its Laboratory Use, 2nd Edn. Oxford, UK: AcademicPress.
22. Hirata, R., Jeong, W. J., Saga, N., and Mikami, K. (2011). Heterologous activation of the Porphyra tenera HSP70 promoter in Bangiophycean algal cells. Bioeng. Bugs 2, 271-274. doi: 10.4161/bbug.2.5.16938
23. Hodgson, P. A., Henderson, R. J., Sargent, J. R., and Leftley, J. W. (1991). Patterns of variation in the lipid class and fatty acid composition of Nannochloropsis oculata (Eustigmatophyceae) during batch culture. J. Appl. Phycol. 3, 169-181. doi: 10.1007/BF00003699
24. Hu, H., and Gao, K. (2006). Response of growth and fatty acid compositions of Nannochloropsis sp. to environmental factors under elevated CO2 concentration. Biotechnol. Lett. 28, 987-992. doi: 10.1007/s10529-006-9026-6
25. Hu, Q., Sommerfeld, M., Jarvis, E., Ghirardi, M., Posewitz, M., Seibert, M., et al. (2008). Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J. 54, 621-639. doi: 10.1111/j.1365-313X.2008.03492.x
26. Huerlimann, R., de Nys, R., and Heimann, K. (2010). Growth, lipid content, productivity, and fatty acid composition of tropical microalgae for scale-up production. Biotechnol. Bioeng. 107, 245-257. doi: 10.1002/bit.22809
27. Iwai, M., Ikeda, K., Shimojima, M., and Ohta, H. (2014). Enhancement of extraplastidic oil synthesis in Chlamydomonas reinhardtii using a type-2 diacylglycerol acyltransferase with a phosphorus starvation-inducible promoter. Plant Biotechnol. J. 12, 808-819. doi: 10.1111/pbi.12210
28. Katoh, K., and Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772-780. doi: 10.1093/molbev/mst010
29. Khozin-Goldberg, I., and Cohen, Z. (2006). The effect of phosphate starvation on the lipid and fatty acid composition of the fresh water eustigmatophyte Monodus subterraneus. Phytochemistry 67, 696-701. doi: 10.1016/j.phytochem.2006.01.010
30. Kilian, O., Benemann, C. S., Niyogi, K. K., and Vick, B. (2011). High-efficiency homologous recombination in the oil-producing alga Nannochloropsis sp. Proc. Natl. Acad. Sci. U.S.A. 108, 21265-21269. doi: 10.1073/pnas.1105861108
31. Lardizabal, K. D., Mai, J. T., Wagner, N. W., Wyrick, A., Voelker, T., and Hawkins, D. J. (2001). DGAT2 is a new diacylglycerol acyltransferase gene family: purification, cloning, and expression in insect cells of two polypeptides from Mortierella ramanniana with diacylglycerol acyltransferase activity. J. Biol. Chem. 276, 38862-38869. doi: 10.1074/jbc.M106168200
32. Lerche, K., and Hallmann, A. (2013). Stable nuclear transformation of Eudorina elegans. BMC Biotechnol. 13:11. doi: 10.1186/1472-6750-13-11
33. Lerche, K., and Hallmann, A. (2014). Stable nuclear transformation of Pandorina morum. BMC Biotechnol. 14:65. doi: 10.1186/1472-6750-14-65
34. Li, J., Han, D., Wang, D., Ning, K., Jia, J., Wei, L., et al. (2014). Choreography of transcriptomes and lipidomes of Nannochloropsis reveals the mechanisms of oil synthesis in microalgae. Plant Cell 26, 1645-1665. doi: 10.1105/tpc.113.121418
35. Li-Beisson, Y., Shorrosh, B., Beisson, F., Andersson, M. X., Arondel, V., Bates, P. D., et al. (2010). Acyl-lipid metabolism. Arabidopsis Book 8:e0133. doi: 10.1199/tab.0133
36. Lung, S. C., and Weselake, R. J. (2006). Diacylglycerol acyltransferase: a key mediator of plant triacylglycerol synthesis. Lipids 41, 1073-1088. doi: 10.1007/s11745-006-5057-y
37. Martin, G. J., Hill, D. R., Olmstead, I. L., Bergamin, A., Shears, M. J., Dias, D. A., et al. (2014). Lipid profile remodeling in response to nitrogen deprivation in the microalgae Chlorella sp. (Trebouxiophyceae) and Nannochloropsis sp. (Eustigmatophyceae). PLoS ONE 9:e103389. doi: 10.1371/journal.pone.0103389
38. Maruyama, I., Nakamura, T., Matubayashi, T., Ando, Y., and Maeda, T. (1986). Identification of the alga known as "marine Chlorella" as a member of the Eustigmatophyceae. Jpn. J. Phycol. 34, 319-325.
39. Miller, R., Wu, G., Deshpande, R. R., Vieler, A., Gärtner, K., Li, X., et al. (2010). Changes in transcript abundance in Chlamydomonas reinhardtii following nitrogen deprivation predict diversion of metabolism. Plant Physiol. 154, 1737-1752. doi: 10.1104/pp.110.165159
40. Minoda, A., Sato, N., Nozaki, H., Okada, K., Takahashi, H., Sonoike, K., et al. (2002). Role of sulfoquinovosyl diacylglycerol for the maintenance of photosystem II in Chlamydomonas reinhardtii. Eur. J. Biochem. 269, 2353-2358. doi: 10.1046/j.1432-1033.2002.02896.x
41. Okazaki, Y., Otsuki, H., Narisawa, T., Kobayashi, M., Sawai, S., Kamide, Y., et al. (2013). A new class of plant lipid is essential for protection against phosphorus depletion. Nat. Commun. 4, 1510. doi: 10.1038/ncomms2512
42. Okazaki, Y., Shimojima, M., Sawada, Y., Toyooka, K., Narisawa, T., Mochida, K., et al. (2009). A chloroplastic UDP-glucose pyrophosphorylase from Arabidopsis is the committed enzyme for the first step of sulfolipid biosynthesis. Plant Cell 21, 892-909. doi: 10.1105/tpc.108.063925
43. Pant, B. D., Burgos, A., Pant, P., Cuadros-Inostroza, A., Willmitzer, L., and Scheible, W. R. (2015). The transcription factor PHR1 regulates lipid remodeling and triacylglycerol accumulation in Arabidopsis thaliana during phosphorus starvation. J. Exp. Bot. 66, 1907-1918. doi: 10.1093/jxb/eru535
44. Patil, V., Källqvist, T., Olsen, E., Vogt, G., and Gislerød, H. R. (2007). Fatty acid composition of 12 microalgae for possible use in aquaculture feed. Aquacult Int. 15, 1-9. doi: 10.1007/s10499-006-9060-3
45. Radakovits, R., Jinkerson, R. E., Fuerstenberg, S. I., Tae, H., Settlage, R. E., Boore, J. L., et al. (2012). Draft genome sequence and genetic transformation of the oleaginous alga Nannochloropis gaditana. Nat. Commun. 3, 686. doi: 10.1038/ncomms1688
46. Rajakumari, S., Grillitsch, K., and Daum, G. (2008). Synthesis and turnover of non-polar lipids in yeast. Prog. Lipid. Res. 47, 157-171. doi: 10.1016/j.plipres.2008.01.001
47. Rodolfi, L., Chini Zittelli, G., Bassi, N., Padovani, G., Biondi, N., Bonini, G., et al. (2009). Microalgae for oil: strain selection, induction of lipid synthesis and outdoor mass cultivation in a low-cost photobioreactor. Biotechnol. Bioeng. 102, 100-112. doi: 10.1002/bit.22033
48. Ronquist, F., Teslenko, M., Van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., et al. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539-542. doi: 10.1093/sysbio/sys029
49. Sakurai, K., Moriyama, T., and Sato, N. (2014). Detailed identification of fatty acid isomers sheds light on the probable precursors of triacylglycerol accumulation in photoautotrophically grown Chlamydomonas reinhardtii. Eukaryot. Cell 13, 256-266. doi: 10.1128/EC.00280-13
50. Sato, N. (2004). Roles of the acidic lipids sulfoquinovosyl diacylglycerol and phosphatidylglycerol in photosynthesis: their specificity and evolution. J. Plant Res. 117, 495-505. doi: 10.1007/s10265-004-0183-1
51. Sato, N., Aoki, M., Maru, Y., Sonoike, K., Minoda, A., and Tsuzuki, M. (2003). Involvement of sulfoquinovosyl diacylglycerol in the structural integrity and heat-tolerance of photosystem II. Planta 217, 245-251. doi: 10.1007/s00425-003-0992-9
52. Sato, N., and Furuya, M. (1985). Distribution of diacylglyceryltrimethylhomoserine and phosphatidylcholine in non-vascular green plants. Plant Sci. 38, 81-85. doi: 10.1016/0168-9452(85)90134-7
53. Sato, N., Hagio, M., Wada, H., and Tsuzuki, M. (2000). Environmental effects on acidic lipids of thylakoid membranes. Biochem. Soc. Trans. 28, 912-914. doi: 10.1042/bst0280912
54. Shockey, J. M., Gidda, S. K., Chapital, D. C., Kuan, J. C., Dhanoa, P. K., Bland, J. M., et al. (2006). Tung tree DGAT1 and DGAT2 have nonredundant functions in triacylglycerol biosynthesis and are localized to different subdomains of the endoplasmic reticulum. Plant Cell 18, 2294-2313. doi: 10.1105/tpc.106.043695
55. Siaut, M., Cuiné, S., Cagnon, C., Fessler, B., Nguyen, M., Carrier, P., et al. (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. doi: 10.1186/1472-6750-11-7
56. Simionato, D., Block, M. A., La Rocca, N., Jouhet, J., Maréchal, E., Finazzi, G., et al. (2013). The response of Nannochloropsis gaditana to nitrogen starvation includes de novo biosynthesis of triacylglycerols, a decrease of chloroplast galactolipids, and reorganization of the photosynthetic apparatus. Eukaryot. Cell 12, 665-676. doi: 10.1128/EC.00363-12
57. Simionato, D., Sforza, E., Corteggiani Carpinelli, E., Bertucco, A., Giacometti, G. M., and Morosinotto, T. (2011). Acclimation of Nannochloropsis gaditana to different illumination regimes: effects on lipids accumulation. Bioresour. Technol. 102, 6026-6032. doi: 10.1016/j.biortech.2011.02.100
58. Talavera, G., and Castresana, J. (2007). Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst. Biol. 56, 564-577. doi: 10.1080/10635150701472164
59. Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol. Biol. Evol. 30, 2725-2729. doi: 10.1093/molbev/mst197
60. Tanabe, A. S. (2011). Kakusan4 and Aminosan: two programs for comparing nonpartitioned, proportional and separate models for combined molecular phylogenetic analyses of multilocus sequence data. Mol. Ecol. Resour. 11, 914-921. doi: 10.1111/j.1755-0998.2011.03021.x
61. Vieler, A., Brubaker, S. B., Vick, B., and Benning, C. (2012a). A lipid droplet protein of Nannochloropsis with functions partially analogous to plant oleosins. Plant Physiol. 158, 1562-1569. doi: 10.1104/pp.111.193029
62. Vieler, A., Wu, G., Tsai, C. H., Bullard, B., Cornish, A. J., Harvey, C., et al. (2012b). Genome, functional gene annotation, and nuclear transformation of the heterokont oleaginous alga Nannochloropsis oceanica CCMP1779. PLoS Genet. 8:e1003064. doi: 10.1371/journal.pgen.1003064
63. Wang, D., Ning, K., Li, J., Hu, J., Han, D., Wang, H., et al. (2014). Nannochloropsis genomes reveal evolution of microalgal oleaginous traits. PLoS Genet. 10:e1004094. doi: 10.1371/journal.pgen.1004094
64. Weyer, K. M., Bush, D. R., Darzins, A., and Wilso, B. D. (2010). Theoretical maximum algal oil production. Bioenergy Res. 3, 204-213. doi: 10.1007/s12155-009-9046-x
65. Yu, B., and Benning, C. (2003). Anionic lipids are required for chloroplast structure and function in Arabidopsis. Plant J. 36, 762-770. doi: 10.1046/j.1365-313X.2003.01918.x
66. Yu, B., Xu, C., and Benning, C. (2002). Arabidopsis disrupted in SQD2 encoding sulfolipid synthase is impaired in phosphate-limited growth. Proc. Natl. Acad. Sci. U.S.A. 99, 5732-5737. doi: 10.1073/pnas.082696499
67. Zhang, Z., Shrager, J., Jain, M., Chang, C. W., Vallon, O., and Grossman, A. R. (2004). Insights into the survival of Chlamydomonas reinhardtii during sulfur starvation based on microarray analysis of gene expression. Eukaryot. Cell 3, 1331-1348. doi: 10.1128/EC.3.5.1331-1348.2004