Flow cytometry for the development of biotechnological processes with microalgae

Biotechnology Advances

Volumn 31, Issue 1, 2013, Pages 2-16

  Hyka, P ^a,b   Lickova, S ^a,b   Pribyl P ^a,c   Melzoch, K ^b   Kovar, K ^a  

^a ZURICH UNIVERSITY OF APPLIED SCIENCES   (Switzerland)

^b INSTITUTE OF CHEMICAL TECHNOLOGY   (Czech Republic)

^c INSTITUTE OF BOTANY   (Czech Republic)

Author keywords

Cell sorting; Flow cytometry; Fluorescence; Microalga; Population heterogeneity; Production process; Single cell physiology

Indexed keywords

CELL SORTING; MICROALGA; POPULATION HETEROGENEITY; PRODUCTION PROCESS; SINGLE CELLS;

ALGAE; CELLS; FLOW CYTOMETRY; FLUORESCENCE; MICROORGANISMS; PHYSIOLOGY; PRODUCTION ENGINEERING;

CELL CULTURE;

BIOFUEL; CARBOHYDRATE; ENZYME; FLUORESCENT DYE; LIPID; PROTEIN;

BIOFUEL; BIOTECHNOLOGY; CHEMICAL COMPOSITION; FLOW CYTOMETRY; MICROALGA; POPULATION DISTRIBUTION; SPECIES DIVERSITY; TOXICOLOGY;

BIOMASS; BIOTECHNOLOGY; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CELL SIZE; CHEMISTRY; CYTOLOGY; EQUIPMENT; FLOW CYTOMETRY; METABOLISM; METHODOLOGY; MICROALGA; REVIEW;

BIOFUELS; BIOMASS; BIOTECHNOLOGY; CARBOHYDRATES; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CELL SIZE; ENZYMES; FLOW CYTOMETRY; FLUORESCENT DYES; LIPIDS; MICROALGAE; PROTEINS;

EID: 84871937976     PISSN: 07349750     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biotechadv.2012.04.007     Document Type: Review

References (182)

1. Acien FG, Fernandez JM, Magan JJ, Molina E. Production cost of a real microalgae production plant and strategies to reduce it. Biotechnol Adv in press. doi:. http://dx.doi:10.1016/j.biotechadv.2012.02.005.
2. Adler N.E., Schmitt-Jansen M., Altenburger R. Flow cytometry as a tool to study phytotoxic modes of action. Environ Toxicol Chem 2007, 26:297-306.
3. Andersen R.A. Algal culturing techniques 2005, Elsevier Academic press, Amsterdam-Boston-Heidelberg-London-New York-Oxford-Paris-San Diego-San Francisco-Sydney-Tokyo.
4. ASTM_E_2719 Annual book of ASTM standards. Standard guide for fluorescences instrument calibration and validation 2010, ASTM International, West Conshohocken.
5. Battye F.L., Light A., Tarlinton D.M. Single cell sorting and cloning. J Immunol Methods 2000, 243:25-32.
6. Becker E.W. Micro-algae as a source of protein. Biotechnol Adv 2007, 25:207-210.
7. Becker A., Meister A., Wilhelm C. Flow cytometric discrimination of various phycobilin-containing phytoplankton groups in a hypertrophic reservoir. Cytometry 2002, 48:45-57.
8. Berney M., Hammes F., Bosshard F., Weilenmann H.U., Egli T. Assessment and interpretation of bacterial viability by using the LIVE/DEAD BacLight Kit in combination with flow cytometry. Appl Environ Microbiol 2007, 73:3283-3290.
9. Branyikova I., Marsalkova B., Doucha J., Branyik T., Bisova K., Zachleder V., et al. Microalgae-novel highly efficient starch producers. Biotechnol Bioeng 2011, 108:766-776.
10. Brehm-Stecher B.F., Johnson E.A. Single-cell microbiology: tools, technologies, and applications. Microbiol Mol Biol Rev 2004, 68:538-559.
11. Brennan L., Owende P. Biofuels from microalgae-a review of technologies for production, processing, and extractions of biofuels and co-products. Renew Sustain Energy Rev 2010, 14:557-577.
12. Broger T., Odermatt R.P., Huber P., Sonnleitner B. Real-time on-line flow cytometry for bioprocess monitoring. J Biotechnol 2011, 154:240-247.
13. Brussaard C.P.D., Marie D., Thyrhaug R., Bratbak G. Flow cytometric analysis of phytoplankton viability following viral infection. Aquat Microb Ecol 2001, 26:157-166.
14. Bumbak F., Cook S., Zachleder V., Hauser S., Kovar K. Best practices in heterotrophic high-cell-density microalgal processes: achievements, potential and possible limitations. Appl Microbiol Biotechnol 2011, 91:31-46.
15. Burkill P.H., Mantoura R.F.C. The rapid analysis of single marine cells by flow-cytometry. Philos Trans R Soc Lond A 1990, 333:99-112.
16. Cellamare M., Rolland A., Jacquet S. Flow cytometry sorting of freshwater phytoplankton. J Appl Phycol 2010, 22:87-100.
17. Chao Y.Q., Zhang T. Optimization of fixation methods for observation of bacterial cell morphology and surface ultrastructures by atomic force microscopy. Appl Microbiol Biotechnol 2011, 92:381-392.
18. Chen W., Zhang C.W., Song L.R., Sommerfeld M., Hu Q. A high throughput Nile red method for quantitative measurement of neutral lipids in microalgae. J Microbiol Methods 2009, 77:41-47.
19. Chisti Y. Biodiesel from microalgae. Biotechnol Adv 2007, 25:294-306.
20. Cid A., Fidalgo P., Herrero C., Abalde J. Toxic action of copper on the membrane system of a marine diatom measured by flow cytometry. Cytometry 1996, 25:32-36.
21. Coleman A.W. Use of the fluorochrome 4',6-diamidino-2-phenylindole in genetic and developmental studies of chloroplast DNA. J Cell Biol 1979, 82:299-305.
22. Collier J.L. Flow cytometry and the single cell in phycology. J Phycol 2000, 36:628-644.
23. Collier J.L., Campbell L. Flow cytometry in molecular aquatic ecology. Hydrobiologia 1999, 401:33-53.
24. Comas-Riu J., Rius N. Flow cytometry applications in the food industry. J Ind Microbiol Biotechnol 2009, 36:999-1011.
25. Cooksey K.E., Guckert J.B., Williams S.A., Callis P.R. Fluorometric determination of the neutral lipid content of microalgal cells using Nile red. J Microbiol Methods 1987, 6:333-345.
26. Cooper M.S., Hardin W.R., Petersen T.W., Cattolico R.A. Visualizing "green oil" in live algal cells. J Biosci Bioeng 2010, 109:198-201.
27. Cregg J.M., Cereghino J.L., Shi J., Higgins D.R. Recombinant protein expression in Pichia pastoris. Mol Biotechnol 2000, 16:23-52.
28. Crosbie N.D., Pockl M., Weisse T. Rapid establishment of clonal isolates of freshwater autotrophic picoplankton by single-cell and single-colony sorting. J Microbiol Methods 2003, 55:361-370.
29. Cunningham A., Buonnacorsi G.A. Narrow-angle forward light-scattering from individual algal cells - implications for size and shape-discrimination in flow-cytometry. J Plankton Res 1992, 14:223-234.
30. Davey H.M. Flow cytometric techniques for the detection of microorganisms. Methods Cell Sci 2002, 24:91-97.
31. Davey H.M. Life, death, and in-between: meanings and methods in microbiology. Appl Environ Microbiol 2011, 77:5571-5576.
32. Davey H.M., Kell D.B. Flow cytometry and cell sorting of heterogeneous microbial populations: the importance of single-cell analyses. Microbiol Rev 1996, 60:641-678.
33. 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, 15:433-438.
34. Debelius B., Forja J.M., DelValls A., Lubian L.M. Toxicity and bioaccumulation of copper and lead in five marine microalgae. Ecotoxicol Environ Saf 2009, 72:1503-1513.
35. Debenest T., Gagne F., Petit A.N., Kohli M., Eullafroy P., Blaise C. Monitoring of a flame retardant (tetrabromobisphenol A) toxicity on different microalgae assessed by flow cytometry. J Environ Monit 2010, 12:1918-1923.
36. Demers S., Roy S., Gagnon R., Vignault C. Rapid light induced changes in cell fluorescence and in xanthophyll cycle pigments of Alexandrium excavatum (Dinophyceae) and Thalassiosira pseudonana (Bacillariophyceae) a photo-protection mechanism. Mar Ecol Prog Ser 1991, 76:185-193.
37. Deng X.D., Fei X.W., Li Y.J. The effects of nutritional restriction on neutral lipid accumulation in Chlamydomonas and Chlorella. Afr J Microbiol Res 2011, 5:260-270.
38. Diaz M., Herrero M., Garcia L.A., Quiros C. Application of flow cytometry to industrial microbial bioprocesses. Biochem Eng J 2010, 48:385-407.
39. Dignum M., Hoogveld H.L., Matthijs H.C.P., Laanbroek H.J., Pel R. Detecting the phosphate status of phytoplankton by enzyme-labelled fluorescence and flow cytometry. FEMS Microbiol Ecol 2004, 48:29-38.
40. Doan T.T.Y., Obbard J.P. Enhanced lipid production in Nannochloropsis sp. using fluorescence-activated cell sorting. Global Change Biol Bioenergy 2011, 3:264-270.
41. Doan T.T.Y., Obbard J.P. Improved Nile red staining of Nannochloropsis sp. J Appl Phycol 2011, 23:895-901.
42. Doan T.T.Y., Sivaloganathan B., Obbard J.P. Screening of marine microalgae for biodiesel feedstock. Biomass Bioenergy 2011, 35:2534-2544.
43. Dorsey J., Yentsch C.M., Mayo S., Mckenna C. Rapid analytical technique for the assessment of cell metabolic-activity in marine microalgae. Cytometry 1989, 10:622-628.
44. Dubelaar G.B.J., Jonker R.R. Flow cytometry as a tool for the study of phytoplankton. Sci Mar 2000, 64:135-156.
45. Duhamel S., Jacquet S. Flow cytometric analysis of bacteria- and virus-like particles in lake sediments. J Microbiol Methods 2006, 64:316-332.
46. Duhamel S., Gregori G., Van Wambeke F., Nedoma J. Detection of extracellular phosphatase activity at the single-cell level by enzyme-labeled fluorescence and flow cytometry: the importance of time kinetics in ELFA labeling. Cytometry A 2009, 75A:163-168.
47. Dyhrman S.T., Palenik B. Phosphate stress in cultures and field populations of the dinoflagellate Prorucentrum minimum detected by a single-cell alkaline phosphatase assay. Appl Environ Microbiol 1999, 65:3205-3212.
48. Elsey D., Jameson D., Raleigh B., Cooney M.J. Fluorescent measurement of microalgal neutral lipids. J Microbiol Methods 2007, 68:639-642.
49. Evans S.L., Anderson W.T., Jochem F.J. Spatial variability in Florida Bay particulate organic matter composition: combining flow cytometry with stable isotope analyses. Hydrobiologia 2006, 569:151-165.
50. Fitzgerald G.P., Nelson T.C. Extractive and enzymatic analyses for limiting or surplus phosphorus in algae. J Phycol 1975, 2:32-37.
51. Fleck R.A., Pickup R.W., Day J.G., Benson E.E. Characterisation of cryoinjury in Euglena gracilis using flow-cytometry and cryomicroscopy. Cryobiology 2006, 52:261-268.
52. Franklin N.M., Adams M.S., Stauber J.L., Lim R.P. Development of an improved rapid enzyme inhibition bioassay with marine and freshwater microalgae using flow cytometry. Arch Environ Contam Toxicol 2001, 40:469-480.
53. Franqueira D., Orosa M., Torres E., Herrero C., Cid A. Potential use of flow cytometry in toxicity studies with microalgae. Sci Total Environ 2000, 247:119-126.
54. Füchslin H.P., Kötzsch S., Keserue H.-A., Egli T. Rapid and quantitative detection of Legionella pneumophila applying immunomagnetic separation and flow cytometry. Cytometry A 2010, 77A:264-274.
55. Gonzalez-Barreiro O., Rioboo C., Herrero C., Cid A. Removal of triazine herbicides from freshwater systems using photosynthetic microorganisms. Environ Pollut 2006, 144:266-271.
56. Gouveia L., Marques A.E., da Silva T.L., Reis A. Neochloris oleabundans UTEX #1185: a suitable renewable lipid source for biofuel production. J Ind Microbiol Biotechnol 2009, 36:821-826.
57. Graham L.E., Wilcox L.W., Graham J. Algae 2009, Pearson, San Francisco, USA. Second Edition.
58. Gregori G., Denis M., Lefevre D., Beker B. A flow cytometric approach to assess phytoplankton respiration. Methods Cell Sci 2002, 24:99-106.
59. Guedes A.C., Amaro H.M., Malcata F.X. Microalgae as sources of high added-value compounds - a brief review of recent work. Biotechnol Prog 2011, 27:597-613.
60. Guindulain T., Comas J., Vives-Rego J. Use of nucleic acid dyes SYTO-13, TOTO-1, and YOYO-1 in the study of Escherichia coli and marine prokaryotic populations by flow cytometry. Appl Environ Microbiol 1997, 63:4608-4611.
61. Gutierrez-Rodriguez A., Latasa M., Estrada M., Vidal M., Marrase C. Carbon fluxes through major phytoplankton groups during the spring bloom and post-bloom in the Northwestern Mediterranean Sea. Deep Sea Res Part I 2010, 57:486-500.
62. Guzman H.M., Valido A.D., Duarte L.C., Presmanes K.F. Estimate by means of flow cytometry of variation in composition of fatty acids from Tetraselmis suecica in response to culture conditions. Aquacult Int 2010, 18:189-199.
63. Guzman H.M., Valido A.D., Duarte L.C., Presmanes K.F. 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.
64. Hadjoudja S., Vignoles C., Deluchat V., Lenain J.F., Le Jeune A.H., Baudu M. Short term copper toxicity on Microcystis aeruginosa and Chlorella vulgaris using flow cytometry. Aquat Toxicol 2009, 94:255-264.
65. Hammes F., Egli T. Cytometric methods for measuring bacteria in water: advantages, pitfalls and applications. Anal Bioanal Chem 2010, 397:1083-1095.
66. Hampel M., Moreno-Garrido I., Sobrino C., Lubian L.M., Blasco J. Acute toxicity of LAS homologues in marine microalgae: esterase activity and inhibition growth as endpoints of toxicity. Ecotoxicol Environ Saf 2001, 48:287-292.
67. Harper J.D.I., Wu L., Sakuanrungsirikul S., John P.C.L. Isolation and partial characterization of conditional cell-division cycle mutants in Chlamydomonas. Protoplasma 1995, 186:149-162.
68. Haugen E.M., Cucci T.L., Yentsch C.M., Shapiro L.P. Effects of flow cytometric analysis on morphology and viability of fragile phytoplankton. Appl Environ Microbiol 1987, 53:2677-2679.
69. Heilmann S.M., Jader L.R., Harned L.A., Sadowsky M.J., Schendel F.J., Lefebvre P.A., et al. Hydrothermal carbonization of microalgae II. Fatty acid, char, and algal nutrient products. Appl Energy 2011, 88:3286-3290.
70. Hoffman R.A. Standardization, calibration and control in flow cytometry. Current Protocols in Cytometry 1997, 1.3.1-1.3.19. John Wiley & Sons Inc., New York. J.P. Rebertson, Z. Darzynkiewicz, R.A. Hoffman, J.P. Nolan, P.S. Rabinovitsch, S. Watkins (Eds.).
71. Hu Z.Y., Li Y.T., Sommerfeld M., Chen F., Hu Q. Enhanced protection against oxidative stress in an astaxanthin-overproduction Haematococcus mutant (Chlorophyceae). Eur J Phycol 2008, 43:365-376.
72. Hutter K.J., Eipel H.E. Flow cytometric determinations of cellular substances in algae, bacteria, moulds and yeasts. Antonie Van Leeuwenhoek 1978, 44:269-282.
73. Hyka P., Zullig T., Ruth C., Looser V., Meier C., Klein J., et al. Combined use of fluorescent dyes and flow cytometry to quantify the physiological state of Pichia pastoris during the production of heterologous proteins in high cell density fed-batch cultures. Appl Environ Microbiol 2010, 76:4486-4496.
74. Ip P.F., Chen F. Employment of reactive oxygen species to enhance astaxanthin formation in Chlorella zofingiensis in heterotrophic culture. Process Biochem 2005, 40:3491-3496.
75. Ishii S., Tago K., Senoo K. Single-cell analysis and isolation for microbiology and biotechnology: methods and applications. Appl Microbiol Biotechnol 2010, 86:1281-1292.
76. Jahic M., Wallberg F., Bollok M., Garcia P., Enfors S.O. Temperature limited fed-batch technique for control of proteolysis in Pichia pastoris bioreactor cultures. Microb Cell Fact 2003, 2:6-17.
77. Jamers A., Lenjou M., Deraedt P., Van Bockstaele D., Blust R., de Coen W. Flow cytometric analysis of the cadmium-exposed green alga Chlamydomonas reinhardtii (Chlorophyceae). Eur J Phycol 2009, 44:541-550.
78. Javanmardian M., Palsson B.O. High density photoautotrophic algal cultures: design, construction, and operation of a novel photobioreactor system. Biotechnol Bioeng 1991, 38:1182-1189.
79. Jeffrey S.W., Humphrey G.F. New spectrophotometric equations for determining chlorophylls A, B, C1 and C2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanz 1975, 167:191-194.
80. Jehmlich N., Hubschmann T., Salazar M.G., Volker U., Benndorf D., Muller S., et al. Advanced tool for characterization of microbial cultures by combining cytomics and proteomics. Appl Microbiol Biotechnol 2010, 88:575-584.
81. Jiang Y., Chen F. Effects of salinity on cell growth and docosahexaenoic acid content of the heterotrophic marine microalga Crypthecodinium cohnii. J Ind Microbiol Biotechnol 1999, 23:508-513.
82. Jochem F.J. Dark survival strategies in marine phytoplankton assessed by cytometric measurement of metabolic activity with fluorescein diacetate. Mar Biol 1999, 135:721-728.
83. Jochem F.J. Probing the physiological state of phytoplankton at the single-cell level. Sci Mar 2000, 64:183-195.
84. Joux F., Lebaron P. Use of fluorescent probes to assess physiological functions of bacteria at single-cell level. Microbes Infect 2000, 2:1523-1535.
85. Kacmar J., Carlson R., Balogh S.J., Srienc F. Staining and quantification of poly-3-hydroxybutyrate in Saccharomyces cerevisiae and Cupriavidus necator cell populations using automated flow cytometry. Cytometry A 2006, 69A:27-35.
86. Keserue H.A., Fuchslin H.P., Egli T. Rapid detection and enumeration of Giardia lamblia cysts in water samples by immunomagnetic separation and flow cytometric analysis. Appl Environ Microbiol 2011, 77:5420-5427.
87. Knauert S., Knauer K. The role of reactive oxygen species in copper toxicity to two freshwater green algae. J Phycol 2008, 44:311-319.
88. Koch A.L., Robertson B.R., Button D.K. Deduction of the cell volume and mass from forward scatter intensity of bacteria analyzed by flow cytometry. J Microbiol Methods 1996, 27:49-61.
89. Kwok A.C.M., Wong J.T.Y. Cellulose synthesis is coupled to cell cycle progression at G(1) in the dinoflagellate Crypthecodinium cohnii. Plant Physiol 2003, 131:1681-1691.
90. Kwok A.C.M., Wong J.T.Y. Lipid biosynthesis and its coordination with cell cycle progression. Plant Cell Physiol 2005, 46:1973-1986.
91. Kwok A.C.M., Wong J.T.Y. The activity of a wall bound cellulase is required for and is coupled to cell cycle progression in the dinoflagellate Crypthecodinium cohnii. Plant Cell Physiol 2010, 22:1281-1298.
92. Leuko S., Legat A., Fendrihan S., Stan-Lotter H. Evaluation of the LIVE/DEAD BacLight kit for detection of extremophilic archaea and visualization of microorganisms in environmental hypersaline samples. Appl Environ Microbiol 2004, 70:6884-6886.
93. Leya T., Rahn A., Lutz C., Remias D. Response of arctic snow and permafrost algae to high light and nitrogen stress by changes in pigment composition and applied aspects for biotechnology. FEMS Microbiol Ecol 2009, 67:432-443.
94. Li W.K. Macroecological patterns of phytoplankton in the northwestern North Atlantic Ocean. Nature 2002, 419:154-157.
95. Li Y.T., Han D.X., Hu G.R., Sommerfeld M., Hu Q.A. Inhibition of starch synthesis results in overproduction of lipids in Chlamydomonas reinhardtii. Biotechnol Bioeng 2010, 107:258-268.
96. TM The Molecular Probes® Handbook 2010, 11th Edition.
97. Liu B.H., Lee Y.K. Secondary carotenoids formation by the green alga Chlorococcum sp. J Appl Phycol 2000, 12:301-307.
98. Liu H.L., Yu Y., Kong F.X., He L.N., Yu H.X., Giesy J.P., et al. Effects of tetrabromobisphenol A on the green alga Chlorella pyrenoidosa. J Environ Sci Health A Tox Hazard Subst Environ Eng 2008, 43:1271-1278.
99. Liu W., Chen S., Quan X., Jin Y.H. Toxic effect of serial perfluorosulfonic and perfluorocarboxylic acids on the membrane system of a freshwater alga measured by flow cytometry. Environ Toxicol Chem 2008, 27:1597-1604.
100. Looser V., Hammes F., Keller M., Berney M., Kovar K., Egli K. Flow-cytometric detection of changes in the physiological state of E. coli expressing a heterologous membrane protein during carbon-limited fedbatch cultivation. Biotechnol Bioeng 2005, 92:69-78.
101. Lopes da Silva T., Reis A. The use of multi-parameter flow cytometry to study the impact of n-dodecane additions to marine dinoflagellate microalga Crypthecodinium cohnii batch fermentations and DHA production. J Ind Microbiol Biotechnol 2008, 35:875-887.
102. Lopes da Silva T., Reis A., Medeiros R., Oliveira A.C., Gouveia L. Oil production towards biofuel from autotrophic microalgae aemicontinuous cultivations monitorized by flow cytometry. Appl Biochem Biotechnol 2009, 159:568-578.
103. Lopes da Silva T., Santos C.A., Reis A. Multi-parameter flow cytometry as a tool to monitor heterotrophic microalgal batch fermentations for oil production towards biodiesel. Biotechnol Bioprocess Eng 2009, 14:330-337.
104. Ma R.Y.N., Chen F. Induction of astaxanthin formation in the green microalga Chlorococcum sp. by reactive oxygen species (ROS) under mixotrophic conditions of growth. Algae Biotechnol Potentials 2001, 121-126.
105. Mackey D.J., Higgins H.W., Mackey M.D., Holdsworth D. Algal class abundances in the western equatorial Pacific: estimation from HPLC measurements of chloroplast pigments using CHEMTAX. Deep Sea Res Part I 1998, 45:1441-1468.
106. Mantoura R.F.C., Llewellyn C.A. The rapid determination of agal chlorophyll and carotenoid pigments and their breakdown products in natural waters by reverse phase high performance liquid chromatography. Anal Chim Acta 1983, 151:297-314.
107. Marie D., Vaulot D., Partensky F. Application of the novel nucleic acid dyes YOYO-1, YO-PRO-1, and PicoGreen for flow cytometric analysis of marine prokaryotes. Appl Environ Microbiol 1996, 62:1649-1655.
108. Marie D., Partensky F., Jacquet S., Vaulot D. Enumeration and cell cycle analysis of natural populations of marine picoplankton by flow cytometry using the nucleic acid stain SYBR Green I. Appl Environ Microbiol 1997, 63:186-193.
109. Mattila P., Piironen V., Haapala R., Hirvi T., UusiRauva E. Possible factors responsible for the high variation in the cholecalciferol contents of fish. J Agric Food Chem 1997, 45:3891-3896.
110. Mendoza H., de la Jara A., Freijanes K., Carmona L., Ramos A.A., Duarte V.D., et al. Characterization of Dunaliella salina strains by flow cytometry: a new approach to select carotenoid hyperproducing strains. J Biotechnol 2008, 11:1-13.
111. Michels M.H.A., van der Goot A.J., Norsker N.H., Wijffels R.H. Effects of shear stress on the microalgae Chaetoceros muelleri. Bioprocess Biosyst Eng 2010, 33:921-927.
112. Mieplot Mie scattering 2010.
113. Montero M.F., Aristizabal M., Reina G.G. 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, 23:1053-1057.
114. Moore C., Barnard A., Fietzek P., Lewis M.R., Sosik H.M., White S., et al. Optical tools for ocean monitoring and research. Ocean Sci 2009, 5:661-684.
115. Müller S., Nebe-von-Caron G. Functional single-cell analyses: flow cytometry and cell sorting of microbial populations and communities. FEMS Microbiol Rev 2010, 34:554-587.
116. Müller S., Harms H., Bley T. Origin and analysis of microbial population heterogeneity in bioprocesses. Curr Opin Biotechnol 2010, 21:100-113.
117. Nebe-von-Caron G. Standardization in microbial cytometry. Cytometry A 2009, 75A:86-89.
118. Nicklisch A., Steinberg C.E.W. RNA/protein and RNA/DNA ratios determined by flow cytometry and their relationship to growth limitation of selected planktonic algae in culture. Eur J Phycol 2009, 44:297-308.
119. Nonomura A.M., Coder D.M. Improved phycocatalysis of carotene production by flow cytometry and cell sorting. Biocatalysis 1988, 1:333-338.
120. Novotna J., Nedbalova L., Kopacek J., Vrba J. Cell-specific extracellular phosphatase activity of Dinoflagellate populations in acidified mountain lakes. J Phycol 2010, 46:635-644.
121. Olson R.J., Zettler E.R., Anderson O.K. Discrimination of eukaryotic phytoplankton cell types from light scatter and autofluorescence properties measured by flow cytometry. Cytometry 1989, 10:636-643.
122. Overnell J. Effect of heavy metals on photosynthesis and loss of cell potassium in 2 species of marine algae, Dunaliella tertiolecta and Phaeodactylum tricornutum. Mar Biol 1975, 29:99-103.
123. Paau A.S., Oro J., Cowles J.R. Application of flow microfluorometry to study of algal cells and isolated chloroplasts. J Exp Bot 1978, 29:1011-1020.
124. Parmar A., Singh N.K., Pandey A., Gnansounou E., Madamwar D. Cyanobacteria and microalgae: a positive prospect for biofuels. Bioresour Technol 2011, 102:10163-10172.
125. Pecorino L.T., Brockes J.P., Entwistle A. Semi-automated positional analysis using laser scanning microscopy of cells transfected in a regenerating newt limb. J Histochem Cytochem 1996, 44:559-569.
126. Peperzak L., Brussaard C.P.D. Flow cytometric applicability of fluorescent vitality probes on phytoplankton. J Phycol 2011, 47:692-702.
127. Peperzak L., Vrieling E.G., Sandee B., Rutten T. Immuno flow cytometry in marine phytoplankton research. Sci Mar 2000, 64:165-181.
128. Phinney D.A., Cucci T.L. Flow-cytometry and phytoplankton. Cytometry 1989, 10:511-521.
129. Pribyl P., Cepak V., Zachleder V. Production of lipids in 10 strains of Chlorella and Parachlorella, and enhanced lipid productivity in Chlorella vulgaris. Appl Microbiol Biotechnol 2012, 94:549-561.
130. Pulz O., Gross W. Valuable products from biotechnology of microalgae. Appl Microbiol Biotechnol 2004, 65:635-648.
131. Raja R., Hemaiswarya S., Kumar N.A., Sridhar S., Rengasamy R. A perspective on the biotechnological potential of microalgae. Crit Rev Microbiol 2008, 34:77-88.
132. Reckermann M. Flow sorting in aquatic ecology. Sci Mar 2000, 64:235-246.
133. Rengefors K., Ruttenberg K.C., Haupert C.L., Taylor C., Howes B.L., Anderson D.M. Experimental investigation of taxon-specific response of alkaline phosphatase activity in natural freshwater phytoplankton. Limnol Oceanogr 2003, 48:1167-1175.
134. Resina D., Maurer M., Cos O., Arnau C., Carnicer M., Marx H., et al. Engineering of bottlenecks in Rhizopus oryzae lipase production in Pichia pastoris using the nitrogen source-regulated FLD1 promoter. N Biotechnol 2009, 25:396-403.
135. Rioboo C., O'Connor J.E., Prado R., Herrero C., Cid A. Cell proliferation alterations in Chlorella cells under stress conditions. Aquat Toxicol 2009, 94:229-237.
136. Rodriguez J.J.G., Miron A.S., Camacho F.G., Garcia M.C.C., Belarbi E.H., Chisti Y., et al. Causes of shear sensitivity of the toxic dinoflagellate Protoceratium reticulatum. Biotechnol Prog 2009, 25:792-800.
137. Ronot X., Benel L., Mounolou J.C., Adolphe M. Rhodamine 123 uptake in living cells - a suitable alternative for mitochondrial research. Biol Cell 1986, 58:A19.
138. Rosenberg J.N., Oyler G.A., Wilkinson L., Betenbaugh M.J. A green light for engineered algae: redirecting metabolism to fuel a biotechnology revolution. Curr Opin Biotechnol 2008, 19:430-436.
139. Saison C., Perreault F., Daigle J.C., Fortin C., Claverie J., Morin M., et al. Effect of core-shell copper oxide nanoparticles on cell culture morphology and photosynthesis (photosystem II energy distribution) in the green alga, Chlamydomonas reinhardtii. Aquat Toxicol 2010, 96:109-114.
140. Sato M., Murata Y., Mizusawa M., Iwahashi H., Oka S. A simple and rapid dual-fluorescence viability assay for microalgae. Microbiol Cult Coll 2004, 20:53-59.
141. Sensen C.W., Heimann K., Melkonian M. The production of clonal and axenic cultures of microalgae using fluorescence-activated cell sorting. Eur J Phycol 1993, 28:93-97.
142. Shapiro H.M. Practical flow cytometry 2003, Wiley-Liss, Inc., New York, http://www.coulterflow.com/bciflow/practical.php. Fourth Edition.
143. Shen Y., Yuan W., Pei Z., Mao E. Heterotrophic culture of Chlorella protothecoides in various nitrogen sources for lipid production. Appl Biochem Biotechnol 2010, 160:1674-1684.
144. Shi X.L., Kong F.X., Yu Y., Yang Z. Survival of Microcystis aeruginosa and Scenedesmus obliquus under dark anaerobic conditions. Mar Freshw Res 2007, 58:634-639.
145. Sinigalliano C.D., Winshell J., Guerrero M.A., Scorzetti G., Fell J.W., Eaton R.W., et al. Viable cell sorting of dinoflagellates by multiparametric flow cytometry. Phycologia 2009, 48:249-257.
146. Sitton G., Srienc F. Mammalian cell culture scale-up and fed-batch control using automated flow cytometry. J Biotechnol 2008, 135:174-180.
147. Sosik H.M., Olson R.J. Automated taxonomic classification of phytoplankton sampled with imaging-in-flow cytometry. Limnol Oceanogr Methods 2007, 5:204-216.
148. Stauber J.L., Franklin N.M., Adams M.S. Applications of flow cytometry to ecotoxicity testing using microalgae. Trends Biotechnol 2002, 20:141-143.
149. Strauber H., Muller S. Viability states of bacteria-specific mechanisms of selected probes. Cytometry A 2010, 77A:623-634.
150. Strojsova A., Vrba J. Short-term variation in extracellular phosphatase activity: possible limitations for diagnosis of nutrient status in particular algal populations. Aquat Ecol 2009, 43:19-25.
151. Sun J., Liu D.Y. Geometric models for calculating cell biovolume and surface area for phytoplankton. J Plankton Res 2003, 25:1331-1346.
152. Surek B., Melkonian M. CCAC - Culture Collection of Algae at the University of Cologne: a new collection of axenic algae with emphasis on flagellates. Nova Hedwigia 2004, 79:77-92.
153. Szivak I., Behra R., Sigg L. Metal-induced reactive oxygen species production in Chlamydomonas reinhardtii (Chlorophyceae). J Phycol 2009, 45:427-435.
154. Tang Y.Z., Dobbs F.C. Green autofluorescence in dinoflagellates, diatoms, and other microalgae and its implications for vital staining and morphological studies. Appl Environ Microbiol 2007, 73:2306-2313.
155. Toepel J., Wilhelm C., Meister A., Beckert A., Martinez-Ballesta M.D. Cytometry of freshwater phytoplankton. New Developments 2004, 75:375-407. 4th Edition.
156. Tokusoglu O., Unal M.K. Biomass nutrient profiles of three microalgae: Spirulina platensis, Chlorella vulgaris, and Isochrisis galbana. J Food Sci 2003, 68:1144-1148.
157. Trainor F.R. Breaking the habit. Integrating plasticity into taxonomy. Syst Biodivers 2009, 7:95-100.
158. Troussellier M., Courties C., Vaquer A. Recent applications of flow-cytometry in aquatic microbial ecology. Biol Cell 1993, 78:111-121.
159. Umeno D., Tobias A.V., Arnold F.H. Diversifying carotenoid biosynthetic pathways by directed evolution. Microbiol Mol Biol Rev 2005, 69:51.
160. Umorin M., Lind O. Cell volume distribution dynamics of Chlorella vulgaris Beij. in batch cultures under continuous light. Biotechnol Lett 2005, 27:347-354.
161. Vaulot D., Marie D. Diel variability of photosynthetic picoplankton in the equatorial Pacific. J Geophys Res Oceans 1999, 104:3297-3310.
162. Veal D.A., Deere D., Ferrari B., Piper J., Attfield P.V. Fluorescence staining and flow cytometry for monitoring microbial cells. J Immunol Methods 2000, 243:191-210.
163. Veldhuis M.J.W., Kraay G.W. Application of flow cytometry in marine phytoplankton research: current applications and future perspectives. Sci Mar 2000, 64:121-134.
164. Veldhuis M.J.W., Kraay G.W., Timmermans K.R. Cell death in phytoplankton: correlation between changes in membrane permeability, photosynthetic activity, pigmentation and growth. Eur J Phycol 2001, 36:167-177.
165. Vicker M.G., Becker J., Gebauer G., Schill W., Rensing L. Circadian-rhythms of cell-cycle processes in the marine Dinoflagellate Gonyaulax-Polyedra. Chronobiol Int 1988, 5:5-17.
166. Vitova M., Hendrychova J., Cepak V., Zachleder V. Visualization of DNA-containing structures in various species of Chlorophyta, Rhodophyta and Cyanophyta using SYBR Green I dye. Folia Microbiol 2005, 50:333-340.
167. Vives-Rego J., Lebaron P., Nebe-von Caron G. Current and future applications of flow cytometry in aquatic microbiology. FEMS Microbiol Rev 2000, 24:429-448.
168. Wang W.X., Miao A.J. Relationships between cell-specific growth rate and uptake rate of cadmium and zinc by a coastal diatom. Mar Ecol Prog Ser 2004, 275:103-113.
169. Wang Y.Y., Hammes F., De Roy K., Verstraete W., Boon N. Past, present and future applications of flow cytometry in aquatic microbiology. Trends Biotechnol 2010, 28:416-424.
170. Watanabe M., Suzuki T. Cadmium-induced abnormality in strains of Euglena gracilis: morphological alteration and its prevention by zinc and cyanocobalamin. Comp Biochem Physiol C 2001, 130:29-39.
171. Weithoff G. Vertical niche separation of two consumers (Rotatoria) in an extreme habitat. Oecologia 2004, 139:594-603.
172. Winson M.K., Davey H.M. Flow cytometric analysis of microorganisms. Methods 2000, 21:231-240.
173. Wu Z.Y., Shi X.M. Rheological properties of Chlorella pyrenoidosa culture grown heterotrophically in a fermentor. J Appl Phycol 2008, 20:279-282.
174. Xiong W., Liu L.X., Wu C., Yang C., Wu Q.Y. C-13-tracer and gas chromatography-mass spectrometry analyses reveal metabolic flux distribution in the oleaginous microalga Chlorella protothecoides. Plant Physiol 2010, 154:1001-1011.
175. Yang Y.P., Juang Y.S., Hsu B.D. A quick method for assessing chloroplastic starch granules by flow cytometry. J Plant Physiol 2002, 159:103-106.
176. Yanpaisan W., King N.J.C., Doran P.M. Flow cytometry of plant cells with applications in large-scale bioprocessing. Biotechnol Adv 1999, 17:3-27.
177. Yentsch C.M., Campbell J.W. Phytoplankton growth perspectives gained by flow cytometry. J Plankton Res 1991, 13:S83-S108.
178. Yentsch C.S., Yentsch C.M. Single cell analysis in biological oceanography and its evolutionary implications. J Plankton Res 2008, 30:107-117.
179. Yoshida K., Igarashi E., Wakatsuki E., Miyamoto K., Hirata K. Mitigation of osmotic and salt stresses by abscisic acid through reduction of stress-derived oxidative damage in Chlamydomonas reinhardtii. Plant Sci (Amst, Neth) 2004, 167:1335-1341.
180. Zhang M., Kong F.X., Shi X.L., Xing P., Tan X. Differences in responses to darkness between Microcystis aeruginosa and Chlorella pyrenoidosa. J Freshw Ecol 2007, 22:93-99.
181. Zhang Y.W., Liu R.J., Wu X.Y. The proteolytic systems and heterologous proteins degradation in the methylotrophic yeast Pichia pastoris. Ann Microbiol 2007, 57:553-560.
182. Zubkov M.V., Sleigh M.A., Burkill P.H. Assaying picoplankton distribution by flow cytometry of underway samples collected along a meridional transect across the Atlantic Ocean. Aquat Microb Ecol 2000, 21:13-20.