The use of fluorescent Nile red and BODIPY for lipid measurement in microalgae

Biotechnology for Biofuels

Volumn 8, Issue 1, 2015, Pages

  Rumin, Judith ^a   Bonnefond, Hubert ^b   Saint Jean, Bruno ^a   Rouxel, Catherine ^a   Sciandra, Antoine ^b   Bernard, Olivier ^c   Cadoret, Jean Paul ^a   Bougaran, Gaël ^a  

^a IFREMER   (France)

^b LABORATOIRE D OCÉANOGRAPHIE DE VILLEFRANCHE   (France)

^c INRIA   (France)

Author keywords

Biodiesel; BODIPY 505 515; Fluorescence; Microalgae; Neutral lipid; Nile red

Indexed keywords

ALGAE; BIODIESEL; FLUORESCENCE; GRAVIMETRIC ANALYSIS; LIPIDS;

BODIPY 505/515; CELL CONCENTRATIONS; FLUORESCENT STAINING; INCUBATION DURATION; MICRO-ALGAE; NEUTRAL LIPID; NILE RED; SPECTRAL PROPERTIES;

MICROORGANISMS;

ARABLE LAND; BIOFUEL; LIPID; MICROALGA; MICROORGANISM;

ALGAE;

EID: 84928238407     PISSN: 17546834     EISSN: None     Source Type: Journal    
DOI: 10.1186/s13068-015-0220-4     Document Type: Review

References (107)

1. Chisti Y. Biodiesel from microalgae. Biotechnol Adv. 2007;25:294-306.
2. Wijffels RH, Barbosa MJ. An outlook on microalgal biofuels. Science. 2010;329:796-9.
3. Chacón-Lee TL, González-Mariño GE. Microalgae for "healthy" foods - possibilities and challenges. Compr Rev Food Sci Food Saf. 2010;9:655-75.
4. Daroch M, Geng S, Wang G. Recent advances in liquid biofuel production from algal feedstocks. Appl Energy. 2013;102:1371-81.
5. Hu Q, Sommerfeld M, Jarvis E, Ghirardi M, Posewitz M, Seibert M, et al. Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J. 2008;54:621-39.
6. Konur O. The scientometric evaluation of the research on the algae and bio-energy. Appl Energy. 2011;88:3532-40.
7. Pragya N, Pandey KK, Sahoo PK. A review on harvesting, oil extraction and biofuels production technologies from microalgae. Renew Sustain Energy Rev. 2013;24:159-71.
8. Singh J, Gu S. Commercialization potential of microalgae for biofuels production. Renew Sustain Energy Rev. 2010;14:2596-610.
9. Cadoret J-P, Bernard O. La production de biocarburant lipidique avec des microalgues: promesses et défis. J Soc Biol. 2008;202:201-11.
10. Chisti Y. Constraints to commercialization of algal fuels. J Biotechnol. 2013;167:201-14.
11. Montagne X, Porot P, Aymard C, Querleu C, Bouter A, Lorne D, et al. Algogroup: towards a shared vision of the possible deployment of algae to biofuels. Oil Gas Sci Technol. 2013;68:875-98.
12. Ríos SD, Torres CM, Torras C, Salvadó J, Mateo-Sanz JM, Jiménez L. Microalgae-based biodiesel: economic analysis of downstream process realistic scenarios. Bioresour Technol. 2013;136:617-25.
13. Han Y, Wen Q, Chen Z, Li P. Review of methods used for microalgal lipid-content analysis. Energy Procedia. 2011;12:944-50.
14. Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959;37(8):911-7. doi:10.1139/o59-099.
15. Folch J, Lee M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem. 1957;226(1):497-509.
16. Eltgroth ML, Watwood RL, Wolfe GV. Production and cellular localization of neutral long-chain lipids in the haptophyte algae Isochrysis galbana and Emiliania huxleyi. J Phycol. 2005;41:1000-9.
17. De la Jara A, Mendoza H, Martel A, Molina C, Nordstron L, de la Rosa V, et al. Flow cytometric determination of lipid content in a marine dinoflagellate, Crypthecodinium cohnii. J Appl Phycol. 2003;15:433-8.
18. Lee SJ, Yoon B-D, Oh H-M. Rapid method for the determination of lipid from the green alga Botryococcus braunii. Biotechnol Tech. 1998;12:553-6.
19. Cooksey KE, Guckert JB, Williams SA, Callis PR. Fluorometric determination of the neutral lipid content of microalgal cells using Nile red. J Microbiol Methods. 1987;6:333-45.
20. Cooper MS, Hardin WR, Petersen TW, Cattolico RA. Visualizing "green oil" in live algal cells. J Biosci Bioeng. 2010;109:198-201.
21. Mutanda T, Ramesh D, Karthikeyan S, Kumari S, Anandraj A, Bux F. Bioprospecting for hyper-lipid producing microalgal strains for sustainable biofuel production. Bioresour Technol. 2011;102:57-70.
22. Chisti Y. Biodiesel from microalgae beats bioethanol. Trends Biotechnol. 2008;26:126-31.
23. Elsey D, Jameson D, Raleigh B, Cooney MJ. Fluorescent measurement of microalgal neutral lipids. J Microbiol Methods. 2007;68:639-42.
24. Huang G-H, Chen G, Chen F. Rapid screening method for lipid production in alga based on Nile red fluorescence. Biomass Bioenergy. 2009;33:1386-92.
25. Govender T, Ramanna L, Rawat I, Bux F. BODIPY staining, an alternative to the Nile red fluorescence method for the evaluation of intracellular lipids in microalgae. Bioresour Technol. 2012;91(2):321-8.
26. Smith JL. On the simultaneous staining of neutral fat and fatty acid by oxazine dyes. J Pathol Bacteriol. 1908;12:1-4.
27. Lison L. Sur le mécanisme et la signification de la coloration des lipides par le bleu de Nil. Bull Histol Appl. 1935;12:279-89.
28. Menschik Z. Nile blue histochemical method for phospholipids. Biotech Histochem. 2009;28:13-8.
29. Vergara J. Nile blue fluorescence signals from cut single muscle fibers under voltage or current clamp conditions. J Gen Physiol. 1978;72:775-800.
30. Cleine JH, Dixon KE. The effect of egg rotation on the differentiation of primordial germ cells in Xenopus laevis. J Embryol Exp Morphol. 1985;90:79-99.
31. Dale L, Smith JC, Slack JMW. Mesoderm induction in Xenopus laevis: a quantitative study using a cell lineage label and tissue-specific antibodies. J Embryol Exp Morphol. 1985;89:289-312.
32. Fowler SD, Greenspan P. Application of Nile red, a fluorescent hydrophobic probe, for the detection of neutral lipid deposits in tissue sections: comparison with oil red O. J Histochem Cytochem. 1985;33:833-6.
33. Greenspan P, Mayer EP, Fowler SD. Nile red: a selective fluorescent stain for intracellular lipid droplets. J Cell Biol. 1985;100:965-73.
34. Greenspan P, Fowler SD. Spectrofluorometric studies of the lipid probe, Nile red. J Lipid Res. 1985;26:781-9.
35. Ira KG. Probing the link between proton transport and water content in lipid membranes. J Phys Chem B. 2001;105:1484-8.
36. Sackett DL, Wolff J. Nile red as a polarity-sensitive fluorescent probe of hydrophobic protein surfaces. Anal Biochem. 1987;167:228-34.
37. Ruvinov S, Yang X, Parris K, Banik U, Ahmed S, Miles E, et al. Ligand-mediated changes in the tryptophan synthase indole tunnel probed. J Biol Chem. 1995;270:6357-69.
38. Kimura K, Yamaoka M, Kamisaka Y. Rapid estimation of lipids in oleaginous fungi and yeasts using Nile red fluorescence. J Microbiol Methods. 2004;56:331-8.
39. Chen W, Zhang C, Song L, Sommerfeld M, Hu Q. A high throughput Nile red method for quantitative measurement of neutral lipids in microalgae. J Microbiol Methods. 2009;77:41-7.
40. Guzmán HM, Valido A, De La J, Duarte LC, Presmanes KF. Estimate by means of flow cytometry of variation in composition of fatty acids from Tetraselmis suecica in response to culture conditions. Aquacult Int. 2010;18:189-99.
41. Simionato D, Sforza E, Corteggiani Carpinelli E, Bertucco A, Giacometti GM, Morosinotto T. Acclimation of Nannochloropsis gaditana to different illumination regimes: effects on lipids accumulation. Bioresour Technol. 2011;102:6026-32.
42. Bougaran G, Rouxel C, Dubois N, Kaas R, Grouas S, Lukomska E, et al. Enhancement of neutral lipid productivity in the microalga Isochrysis affinis Galbana (T-Iso) by a mutation-selection procedure. Biotechnol Bioeng. 2012;109:2737-45.
43. Pereira H, Barreira L, Mozes A, Florindo C, Polo C, Duarte CV, et al. Microplate-based high throughput screening procedure for the isolation of lipid-rich marine microalgae. Biotechnol Biofuels. 2011;4:61.
44. Wong DM, Franz AK. A comparison of lipid storage in Phaeodactylum tricornutum and Tetraselmis suecica using laser scanning confocal microscopy. J Microbiol Methods. 2013;95:122-8.
45. Velmurugan N, Sung M, Yim SS, Park MS, Yang JW, Jeong KJ. Evaluation of intracellular lipid bodies in Chlamydomonas reinhardtii strains by flow cytometry. Bioresour Technol. 2013;138:30-7.
46. Mou S, Xu D, Ye N, Zhang X, Liang C, Liang Q, et al. Rapid estimation of lipid content in an Antarctic ice alga (Chlamydomonas sp.) using the lipophilic fluorescent dye BODIPY505/515. J Appl Phycol. 2012;24:1169-76.
47. Guzmán HM, Valido A, De La J, Presmanes KF, Duarte LC. Quick estimation of intraspecific variation of fatty acid composition in Dunaliella salina using flow cytometry and Nile red. J Appl Phycol. 2012;24:1237-43.
48. Brennan L, Blanco Fernández A, Mostaert AS, Owende P. Enhancement of BODIPY505/515 lipid fluorescence method for applications in biofuel-directed microalgae production. J Microbiol Methods. 2012;90:137-43.
49. Cirulis JT, Strasser BC, Scott JA, Ross GM. Optimization of staining conditions for microalgae with three lipophilic dyes to reduce precipitation and fluorescence variability. Cytometry A. 2012;81A:618-26.
50. Vigeolas H, Duby F, Kaymak E, Niessen G, Motte P, Franck F, et al. Isolation and partial characterization of mutants with elevated lipid content in Chlorella sorokiniana and Scenedesmus obliquus. J Biotechnol. 2012;162:3-12.
51. Chen Z, Gong Y, Fang X, Hu H. Scenedesmus sp. NJ-1 isolated from Antarctica: a suitable renewable lipid source for biodiesel production. World J Microbiol Biotechnol. 2012;28:3219-25.
52. Gardner RD, Cooksey KE, Mus F, Macur R, Moll K, Eustance E, et al. Use of sodium bicarbonate to stimulate triacylglycerol accumulation in the chlorophyte Scenedesmus sp. and the diatom Phaeodactylum tricornutum. J Appl Phycol. 2012;24:1311-20.
53. Ren H-Y, Liu B-F, Ma C, Zhao L, Ren N-Q. A new lipid-rich microalga Scenedesmus sp. strain R-16 isolated using Nile red staining: effects of carbon and nitrogen sources and initial pH on the biomass and lipid production. Biotechnol Biofuels. 2013;6:143.
54. Hu G, Fan Y, Zhang L, Yuan C, Wang J, Li W, et al. Enhanced lipid productivity and photosynthesis efficiency in a Desmodesmus sp mutant induced by heavy carbon ions. PLoS ONE. 2013;8:e60700.
55. Roleda MY, Slocombe SP, Leakey RJG, Day JG, Bell EM, Stanley MS. Effects of temperature and nutrient regimes on biomass and lipid production by six oleaginous microalgae in batch culture employing a two-phase cultivation strategy. Bioresour Technol. 2013;129:439-49.
56. Doan T-TY, Obbard JP. Improved Nile red staining of Nannochloropsis sp. J Appl Phycol. 2011;23:895-901.
57. Feng G-D, Zhang F, Cheng L-H, Xu X-H, Zhang L, Chen H-L. Evaluation of FT-IR and Nile red methods for microalgal lipid characterization and biomass composition determination. Bioresour Technol. 2013;128:107-12.
58. Doan T-TY, Obbard JP. Enhanced lipid production in Nannochloropsis sp. using fluorescence-activated cell sorting. GCB Bioenergy. 2011;3:264-70.
59. Doan TTY, Obbard JP. Enhanced intracellular lipid in Nannochloropsis sp. via random mutagenesis and flow cytometric cell sorting. Algal Res. 2012;1:17-21.
60. Montero MF, Aristizabal M, Garcia RG. Isolation of high-lipid content strains of the marine microalga Tetraselmis suecica for biodiesel production by flow cytometry and single-cell sorting. J Appl Phycol. 2011;23:1053-7.
61. Xu D, Gao Z, Li F, Fan X, Zhang X, Ye N, et al. Detection and quantitation of lipid in the microalga Tetraselmis subcordiformis (Wille) Butcher with BODIPY 505/515 staining. Bioresour Technol. 2013;127:386-90.
62. Guzmán HM, Valido A, De La J, Duarte LC, Presmanes KF. Analysis of interspecific variation in relative fatty acid composition: use of flow cytometry to estimate unsaturation index and relative polyunsaturated fatty acid content in microalgae. J Appl Phycol. 2011;23:7-15.
63. Lacour T. Influence du statut azoté et du cycle lumineux diurne sur le métabolisme lipidique d'Isochrysis sp. (Haptophyceae). PhD thesis. Aix Marseille 2; 2010.
64. De la Hoz SH, Ayidzoe W, Ben-Zvi A, Burrell RE, McCaffrey WC. Improving the reliability of fluorescence-based neutral lipid content measurements in microalgal cultures. Algal Res. 2012;1:176-84.
65. Isleten-Hosoglu M, Gultepe I, Elibol M. Optimization of carbon and nitrogen sources for biomass and lipid production by Chlorella saccharophila under heterotrophic conditions and development of Nile red fluorescence based method for quantification of its neutral lipid content. Biochem Eng J. 2012;61:11-9.
66. Su L-C, Hsu Y-H, Wang H-Y. Enhanced labeling of microalgae cellular lipids by application of an electric field generated by alternating current. Bioresour Technol. 2012;111:323-7.
67. Loudet A, Burgess K. BODIPY dyes and their derivatives: syntheses and spectroscopic properties. Chem Rev. 2007;107:4891-932.
68. Elle IC, Olsen LCB, Pultz D, Rødkær SV, Færgeman NJ. Something worth dyeing for: molecular tools for the dissection of lipid metabolism in Caenorhabditis elegans. FEBS Lett. 2010;584:2183-93.
69. Gocze PM, Freeman DA. Factors underlying the variability of lipid droplet fluorescence in MA-10 Leydig tumor cells. Cytometry. 1994;17:151-8.
70. Listenberger LL, Brown DA. Fluorescent detection of lipid droplets and associated proteins. In Current Protocols in Cell Biology. John Wiley & Sons, Inc.; 2007.
71. Cooper MS, D'Amico LA, Henry CA. Confocal microscopic analysis of morphogenetic movements. Methods Cell Biol. 1999;59:179-204.
72. De Gottardi A, Vinciguerra M, Sgroi A, Moukil M, Ravier-Dall'Antonia F, Pazienza V, et al. Microarray analyses and molecular profiling of steatosis induction in immortalized human hepatocytes. Lab Invest. 2007;87:792-806.
73. Greenspan P, Mayer E, Fowler S. Use of Nile red in fluorescence microscopy and flow cytometer analysis. J Cell Biol. 1984;99:A58-8.
74. Ghoneim N. Photophysics of Nile red in solution: steady state spectroscopy. Spectrochim Acta A Mol Biomol Spectrosc. 2000;56:1003-10.
75. Alonzo F, Mayzaud P. Spectrofluorometric quantification of neutral and polar lipids in zooplankton using Nile red. Mar Chem. 1999;67:289-301.
76. Dutta AK, Kamada K, Ohta K. Spectroscopic studies of Nile red in organic solvents and polymers. J Photochem Photobiol, A: Chemistry. 1996;93:57-64.
77. Brown WJ, Sullivan TR, Greenspan P. Nile red staining of lysosomal phospholipid inclusions. Histochemistry. 1992;97:349-54.
78. O'Rourke EJ, Soukas AA, Carr CE, Ruvkun G. C. elegans major fats are stored in vesicles distinct from lysosome-related organelles. Cell Metab. 2009;10:430-5.
79. Mendoza H, de la Jara A, Freijanes K, Carmona L, Ramos AA, de Sousa DV, et al. Characterization of Dunaliella salina strains by flow cytometry: a new approach to select carotenoid hyperproducing strains. Electronic Journal of Biotechnology. 2008;11.
80. Wolfrum E, Laurens L. Rapid compositional analysis of microalgae by NIR spectroscopy. NIR News. 2012;23:9.
81. Diaz G, Melis M, Batetta B, Angius F, Falchi AM. Hydrophobic characterization of intracellular lipids in situ by Nile red red/yellow emission ratio. Micron. 2008;39:819-24.
82. Castell LL, Mann R. Optimal staining of lipids in bivalve larvae with Nile red. Aquaculture. 1994;119:89-100.
83. Lakowicz J, editor. Quenching of fluorescence. In: Principles of Fluorescence Spectroscopy. US New York: Springer; 2006:277-330.
84. Pick U, Rachutin-Zalogin T. Kinetic anomalies in the interactions of Nile red with microalgae. J Microbiol Methods. 2012;88:189-96.
85. Suman K, Kiran T, Devi UK, Sarma NS. Culture medium optimization and lipid profiling of Cylindrotheca, a lipid- and polyunsaturated fatty acid-rich pennate diatom and potential source of eicosapentaenoic acid. Botanica Marina. 2012;55:289-99.
86. Priscu JC, Priscu LR, Palmisano AC, Sullivan CW. Estimation of neutral lipid levels in Antarctic sea ice microalgae by Nile red fluorescence. Antarctic Science. 1990;2:149-55.
87. 2+ concentration. Cytometry A. 2010;77A:1091-7.
88. Davis RW, Volponi JV, Jones HDT, Carvalho BJ, Wu H, Singh S. Multiplex fluorometric assessment of nutrient limitation as a strategy for enhanced lipid enrichment and harvesting of Neochloris oleoabundans. Biotechnol Bioeng. 2012;109:2503-12.
89. Bertozzini E, Galluzzi L, Penna A, Magnani M. Application of the standard addition method for the absolute quantification of neutral lipids in microalgae using Nile red. J Microbiol Methods. 2011;87:17-23.
90. Chen W, Sommerfeld M, Hu Q. Microwave-assisted Nile red method for in vivo quantification of neutral lipids in microalgae. Bioresour Technol. 2011;102:135-41.
91. Ahmad I, Fatma Z, Yazdani SS, Kumar S. DNA barcode and lipid analysis of new marine algae potential for biofuel. Algal Res. 2012;2:10-5.
92. Notman R, Noro M, O'Malley B, Anwar J. Molecular basis for dimethylsulfoxide (DMSO) action on lipid membranes. J Am Chem Soc. 2006;128:13982-3.
93. Sitepu IR, Ignatia L, Franz AK, Wong DM, Faulina SA, Tsui M, et al. An improved high-throughput Nile red fluorescence assay for estimating intracellular lipids in a variety of yeast species. J Microbiol Methods. 2012;91:321-8.
94. Doan TTY, Sivaloganathan B, Obbard JP. Screening of marine microalgae for biodiesel feedstock. Biomass Bioenergy. 2011;35:2534-44.
95. Massart A, Aubry E, Hantson A-L. Study of culture strategies of Dunaliella tertiolecta combining high cell density and accumulation of lipids to produce biodiesel. Biotechnol Agron Soc. 2010;14:567-72.
96. Azencott HR, Peter GF, Prausnitz MR. Influence of the cell wall on intracellular delivery to algal cells by electroporation and sonication. Ultrasound Med Biol. 2007;33:1805-17.
97. Guilbault GG. Practical fluorescence; theory, methods, and techniques. Guilbault GG, editor. New York: M. Dekker; 1973.
98. Pick U. Adaptation of the halotolerant Alga dunaliella to high salinity. In: Läuchli A, Lüttge U, editors. Salinity: Environment - Plants - Molecules. Netherlands Dordrecht: Springer; 2004. p. 97-112.
99. Benbouzid H, Le Floch S, Stephan L, Olier R, Privat M. Combined effects of salinity and temperature on the solubility of organic compounds. J Chem Thermodyn. 2012;48:54-64.
100. Castro GR, Kamdar RR, Panilaitis B, Kaplan DL. Triggered release of proteins from emulsan-alginate beads. J Control Release. 2005;109:149-57.
101. Murphy JJ, Furusho H, Paton RM, Nomura K. Precise synthesis of poly(macromonomer)s containing sugars by repetitive ROMP and their attachments to poly(ethylene glycol): synthesis, TEM analysis and their properties as amphiphilic block fragments. Chemistry. 2007;13:8985-97.
102. Hyka P, Lickova S, Přibyl P, Melzoch K, Kovar K. Flow cytometry for the development of biotechnological processes with microalgae. Biotechnol Adv. 2013;31:2-16.
103. Manandhar-Shrestha K, Hildebrand M. Development of flow cytometric procedures for the efficient isolation of improved lipid accumulation mutants in a Chlorella sp. microalga. J Appl Phycol. 2013;25:1643-51.
104. Traller JC, Hildebrand M. High throughput imaging to the diatom Cyclotella cryptica demonstrates substantial cell-to-cell variability in the rate and extent of triacylglycerol accumulation. Algal Research. 2013;2:244-52.
105. Bader M. A systematic approach to standard addition methods in instrumental analysis. J Chem Educ. 1980;57:703.
106. Gardner R, Peters P, Peyton B, Cooksey KE. Medium pH and nitrate concentration effects on accumulation of triacylglycerol in two members of the chlorophyta. J Appl Phycol. 2011;23:1005-16.
107. Carrier G, Garnier M, Le Cunff L, Bougaran G, Probert I, De Vargas C, et al. Comparative transcriptome of wild type and selected strains of the microalgae Tisochrysis lutea provides insights into the genetic basis, lipid metabolism and the life cycle. PLoS One. 2014;9:e86889.