Phenotypic screening with oleaginous microalgae reveals modulators of lipid productivity

ACS Chemical Biology

Volumn 8, Issue 5, 2013, Pages 1053-1062

  Franz, Annaliese K ^a   Danielewicz, Megan A ^a   Wong, Diana M ^a   Anderson, Lisa A ^a   Boothe, Jordan R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BUTYLATED HYDROXYANISOLE; EPIGALLOCATECHIN GALLATE; FORSKOLIN; LIPID; MEPACRINE; ANTIOXIDANT; CATECHIN; FLUORESCENT DYE; MOLECULAR LIBRARY; NILE RED; OXAZINE DERIVATIVE;

ARTICLE; BACTERIUM CULTURE; BIOMASS PRODUCTION; CELL DENSITY; CONTROLLED STUDY; GROWTH RATE; LIPID METABOLISM; MICROALGA; NANNOCHLORIS; NANNOCHLOROPSIS OCULATA; NANNOCHLOROPSIS SALINA; NONHUMAN; PHAEODACTYLUM TRICORNUTUM; PHENOTYPE; PRIORITY JOURNAL; ANALOGS AND DERIVATIVES; BATCH CELL CULTURE; BIOMASS; BIOSYNTHESIS; DOSE RESPONSE; DRUG EFFECTS; DRUG SCREENING; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR LIBRARY; PHARMACOLOGY; PROCEDURES;

ANTIOXIDANTS; BATCH CELL CULTURE TECHNIQUES; BIOMASS; BUTYLATED HYDROXYANISOLE; CATECHIN; COLFORSIN; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG EVALUATION, PRECLINICAL; FLUORESCENT DYES; LIPID METABOLISM; LIPIDS; MICROALGAE; OXAZINES; PHENOTYPE; QUINACRINE; SMALL MOLECULE LIBRARIES;

EID: 84878063770     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb300573r     Document Type: Article

References (58)

1. 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 (Pubitemid 351678050)
2. Wijffels, R. H. and Barbosa, M. J. (2010) An outlook on microalgal biofuels Science 329, 796-799
3. Sheehan, J., Dunahay, T., Benemann, J., and Roessler, P. (1998) A look back at the US Department of Energy's Aquatic Species program-Biodiesel from Algae, p 328, National Renewable Energy Laboratory, Golden, CO.
4. Chisti, Y. (2007) Biodiesel from microalgae Biotechnol. Adv. 25, 294-306 (Pubitemid 46498675)
5. Suen, Y., Hubbard, J. S., Holzer, G., and Tornabene, T. G. (1987) Total lipid production of the green alga Nannochloropsis sp. qII under different nitrogen regimes J. Phycol. 23, 289-296
6. Cerón Garcia, M. C., Sánchez Mirón, A., Fernández Sevilla, J. M., Molina Grima, E., and Garcia Camacho, F. (2005) Mixotrophic growth of the microalga Phaeodactylum tricornutum: Influence of different nitrogen and organic carbon sources on productivity and biomass composition Process Biochem. 40, 297-305 (Pubitemid 39197421)
7. Kilian, O., Benemann, C. S. E., 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
8. Boussiba, S., Vonshak, A., Cohen, Z., Avissar, Y., and Richmond, A. (1987) Lipid and biomass production by the halotolerant microalga Nannochloropsis salina Biomass 12, 37-47 (Pubitemid 17623150)
9. Yu, W.-L., Ansari, W., Schoepp, N., Hannon, M., Mayfield, S., and Burkart, M. (2011) Modifications of the metabolic pathways of lipid and triacylglycerol production in microalgae Microb. Cell Fact. 10, 91-102
10. Roesler, K., Shintani, D., Savage, L., Boddupalli, S., and Ohlrogge, J. (1997) Targeting of the Arabidopsis homomeric acetyl-coenzyme A carboxylase to plastids of rapeseeds Plant Physiol. 113, 75-81 (Pubitemid 27111437)
11. Dehesh, K., Tai, H., Edwards, P., Byrne, J., and Jaworski, J. (2001) Overexpression of 3-ketoacyl-acyl-carrier protein synthase IIIs in plants reduces the rate of lipid synthesis Plant Physiol. 125, 1103-1114 (Pubitemid 32169915)
12. Vigeolas, H. and Geigenberger, P. (2004) Increased levels of glycerol-3-phosphate lead to a stimulation of flux into triacylglycerol synthesis after supplying glycerol to developing seeds of Brassica napus L. in planta Planta 219, 827-835 (Pubitemid 39282947)
13. Vigeolas, H., Waldeck, P., Zank, T., and Geigenberger, P. (2007) Increasing seed oil content in oil-seed rape (Brassica napus L.) by over-expression of a yeast glycerol-3-phosphate dehydrogenase under the control of a seed-specific promoter Plant Biotechnol. J. 5, 431-441 (Pubitemid 46558328)
14. Jain, R., Coffey, M., Lai, K., Kumar, A., and MacKenzie, S. (2000) Enhancement of seed oil content by expression of glycerol-3-phosphate acyltransferase genes Biochem. Soc. Trans. 28, 958-961 (Pubitemid 32163331)
15. Zou, J., Katavic, V., Giblin, E., Barton, D., MacKenzie, S., Keller, W., Hu, X., and Taylor, D. (1997) Modification of seed oil content and acyl composition in the Brassicaceae by expression of a yeast sn-2 acyltransferase gene Plant Cell 9, 909-923 (Pubitemid 28173841)
16. Wang, Z. T., Ullrich, N., Joo, S., Waffenschmidt, S., and Goodenough, U. (2009) Algal Lipid Bodies: Stress Induction, Purification, and Biochemical Characterization in Wild-Type and Starchless Chlamydomonas reinhardtii Eukaryotic Cell 8, 1856-1868
17. Siaut, M., Cuine, S., Cagnon, C., Fessler, B., Nguyen, M., Carrier, P., Beyly, A., Beisson, F., Triantaphylides, C., Li-Beisson, Y., and Peltier, G. (2011) Oil accumulation in the model green alga Chlamydomonas reinhardtii: characterization, variability between common laboratory strains and relationship with starch reserves BMC Biotechnol. 11, 7-21
18. Li, Y., Han, D., Hu, G., Sommerfeld, M., and Hu, Q. (2010) Inhibition of starch synthesis results in overproduction of lipids in Chlamydomonas reinhardtii Biotechnol. Bioeng. 107, 258-268
19. Moellering, E. R. and Benning, C. (2010) RNA interference silencing of a major lipid droplet protein affects lipid droplet size in Chlamydomonas reinhardtii Eukaryotic Cell 9, 97-106
20. Molnar, A., Bassett, A., Thuenemann, E., Schwach, F., Karkare, S., Ossowski, S., Weigel, D., and Baulcombe, D. (2009) Highly specific gene silencing by artificial microRNAs in the unicellular alga Chlamydomonas reinhardtii Plant J. 58, 165-174
21. Schreiber, S. L. (2005) Small molecules: the missing link in the central dogma Nat. Chem. Biol. 1, 64-66
22. Walsh, D. P. and Chang, Y.-T. (2006) Chemical genetics Chem. Rev. 106, 2476-2530
23. Stockwell, B. R. (2004) Exploring biology with small organic molecules Nature 432, 846-854 (Pubitemid 40037140)
24. Lemieux, G. A., Liu, J., Mayer, N., Bainton, R. J., Ashrafi, K., and Werb, Z. (2011) A whole-organism screen identifies new regulators of fat storage Nat. Chem. Biol. 7, 206-213
25. Kaufman, C. K., White, R. M., and Zon, L. (2009) Chemical genetic screening in the zebrafish embryo Nat. Protoc. 4, 1422-1432
26. Burns, A. R., Kwok, T. C. Y., Howard, A., Houston, E., Johanson, K., Chan, A., Cutler, S. R., McCourt, P., and Roy, P. J. (2006) High-throughput screening of small molecules for bioactivity and target identification in Caenorhabditis elegans Nat. Protoc. 1, 1906-1914 (Pubitemid 46773310)
27. Blackwell, H. E. and Zhao, Y. (2003) Chemical genetic approaches to plant biology Plant Physiol. 133, 448-455 (Pubitemid 37325655)
28. Maucourt, K., Agarwal, M., René, B., and Fermandjian, S. (2002) Use of Chlamydomonas reinhardtii mutants for anticancer drug screening Biochem. Pharmacol. 64, 1125-1131 (Pubitemid 35247819)
29. Avasthi, P., Marley, A., Lin, H., Gregori-Puigjane, E., Shoichet, B. K., von Zastrow, M., and Marshall, W. F. (2012) A chemical screen identifies Class A G-protein coupled receptors as regulators of cilia ACS Chem. Biol. 7, 911-919
30. Chen, W., Zhang, C., Song, L., Sommerfeld, M., and Hu, Q. (2009) A high throughput Nile red method for quantitative measurement of neutral lipids in microalgae J. Microbiol. Methods 77, 41-47
31. Danielewicz, M. A., Anderson, L. A., and Franz, A. K. (2011) Triacylglycerol profiling of marine microalgae by mass spectrometry J. Lipid Res. 52, 2101-2108
32. Knothe, G. (2009) Improving biodiesel fuel properties by modifying fatty ester composition Energy Environ. Sci. 2, 759-766
33. White, D. A., Pagarette, A., Rooks, P., and Ali, S. T. (2012) The effect of sodium bicarbonate supplementation on growth and biochemical composition of marine microalgae cultures J. Appl. Phycol. 1-13
34. Gardner, R. D., Cooksey, K. E., Mus, F., Macur, R., Moll, K., Eustance, E., Carlson, R. P., Gerlach, R., Fields, M. W., and Peyton, B. M. (2012) Use of sodium bicarbonate to stimulate triacylglycerol accumulation in the chlorophyte Scenedesmus sp. and the diatom Phaeodactylum tricornutum J. Appl. Phycol. 24, 1311-1320
35. Mazur, H., Konop, A., and Synak, R. (2001) Indole-3-acetic acid in the culture medium of two axenic green microalgae J. Appl. Phycol 13, 35-42 (Pubitemid 32143342)
36. Piotrowska, A., Czerpak, R., Pietryczuk, A., Olesiewicz, A., and Wedołowska, M. (2008) The effect of indomethacin on the growth and metabolism of green alga Chlorella vulgaris Beijerinck Plant Growth Regul. 55, 125-136
37. Bishop, D. G. and Smillie, R. M. (1970) The effect of chloramphenicol and cycloheximide on lipid synthesis during chloroplast development in Euglena gracilis Arch. Biochem. Biophys. 139, 179-189
38. Schimmel, R. J. (1984) Stimulation of cAMP accumulation and lipolysis in hamster adipocytes with forskolin Am. J. Physiol. 246, C63-C68
39. Jay, A. (1996) Effects of organic solvents and solvent-atrazine interactions on two algae, Chlorella vulgaris and Selenastrum capricornutum Arch. Environ. Contam. Toxicol. 31, 84-90 (Pubitemid 26286971)
40. Gurtovenko, A. A. and Anwar, J. (2007) Modulating the structure and properties of cell membranes: The molecular mechanism of action of dimethyl sulfoxide J. Phys. Chem. B 111, 10453-10460 (Pubitemid 47441849)
41. McNeil, S. D., Nuccio, M. L., and Hanson, A. D. (1999) Betaines and related osmoprotectants. Targets for metabolic engineering of stress resistance Plant Physiol. 120, 945-949 (Pubitemid 29411883)
42. Sanmartin-Suarez, C., Soto-Otero, R., Sanchez-Sellero, I., and Mendez-Alvarez, E. (2011) Antioxidant properties of dimethyl sulfoxide and its viability as a solvent in the evaluation of neuroprotective antioxidants J. Pharmacol. Toxicol. Methods 63, 209-215
43. De La Vega, F. M. and Mendoza-Figueroa, T. (1991) Dimethyl sulfoxide enhances lipid synthesis and secretion by long-term cultures of adult rat hepatocytes Biochimie 73, 621-624
44. Lee, P. A. and de Mora, S. J. (1999) Intracellular dimethylsulfoxide (DMSO) in unicellular marine algae: Speculations on its origin and possible biological role J. Phycol. 35, 8-18 (Pubitemid 29150514)
45. Sunda, W., Kieber, D. J., Kiene, R. P., and Huntsman, S. (2002) An antioxidant function for DMSP and DMS in marine algae Nature 418, 317-320 (Pubitemid 34790680)
46. Okumura, Y., Koyama, J., Takaku, H., and Satoh, H. (2001) Influence of organic solvents on the growth of marine microalgae Arch. Environ. Contam. Toxicol. 41, 123-128 (Pubitemid 32730322)
47. Wang, X. and Tian, W. (2001) Green tea epigallocatechin gallate: A natural inhibitor of fatty-acid synthase Biochem. Biophys. Res. Commun. 288, 1200-1206 (Pubitemid 33131728)
48. Kamiyama, O., Sanae, F., Ikeda, K., Higashi, Y., Minami, Y., Asano, N., Adachi, I., and Kato, A. (2010) In vitro inhibition of α-glucosidases and glycogen phosphorylase by catechin gallates in green tea Food Chem. 122, 1061-1066
49. Saffari, Y. and Sadrzadeh, S. M. H. (2004) Green tea metabolite EGCG protects membranes against oxidative damage in vitro Life Sci. 74, 1513-1518 (Pubitemid 38077213)
50. Foyer, C. H. and Shigeoka, S. (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis Plant Physiol. 155, 93-100
51. Ledford, H. K. and Niyogi, K. K. (2005) Singlet oxygen and photo-oxidative stress management in plants and algae Plant Cell Environ. 28, 1037-1045 (Pubitemid 41577020)
52. Tanaka, S., Ikeda, K., Miyasaka, H., Shioi, Y., Suzuki, Y., Tamoi, M., Takeda, T., Shigeoka, S., Harada, K., and Hirata, K. (2011) Comparison of three Chlamydomonas strains which show distinctive oxidative stress tolerance J. Biosci. Bioeng. 112, 462-468
53. Georgianna, D. R. and Mayfield, S. P. (2012) Exploiting diversity and synthetic biology for the production of algal biofuels Nature 488, 329-335
54. León-Bañares, R. (2004) Transgenic microalgae as green cell-factories Trends Biotechnol. 22, 45-52 (Pubitemid 38030320)
55. We have observed that increases in lipid levels based on Nile Red analysis are amplified in the initial microplate screening compared to effects observed using gravimetric analysis in batch cultures. While this may partially be attributed to the semi-quantitative nature of Nile Red analysis in high-throughput format when used for multiple algae strains, it may also be attributed to lower lipid recovery in batch cultures using standard lipid extraction conditions. See: Folch, J., Lees, M., and Sloane Stanley, G. H. (1957) A simple method for the isolation and purification of total lipides from animal tissues J. Biol. Chem. 226, 497-509
56. Recent investigations in our own lab have shown that a second extraction of buoyant high-lipid cells can lead to up to 10% increased recovery of lipids. Furthermore, Jones et al. have recently reported the use of 2-ethoxyethanol as a better solvent for lipid extraction that increases recovery up to 200% in Chlorella sp. See: Jones, J., Manning, S., Montoya, M., Keller, K., and Poenie, M. (2012) Extraction of Algal Lipids and Their Analysis by HPLC and Mass Spectrometry J. Am. Oil Chem. Soc. 89, 1371-1381
57. Folch, J., Lees, M., and Sloane Stanley, G. H. (1957) A simple method for the isolation and purification of total lipides from animal tissues J. Biol. Chem. 226, 497-509
58. Lee, J.-Y., Yoo, C., Jun, S.-Y., Ahn, C.-Y., and Oh, H.-M. (2010) Comparison of several methods for effective lipid extraction from microalgae Bioresour. Technol. 101, S75-S77