Microalgae Biotechnology pp 89-142

Part of the Advances in Biochemical Engineering/Biotechnology book series (ABE, volume 153) | Cite as

Monitoring of Microalgal Processes

Chapter

Abstract

Process monitoring, which can be defined as the measurement of process variables with the smallest possible delay, is combined with process models to form the basis for successful process control. Minimizing the measurement delay leads inevitably to employing online, in situ sensors where possible, preferably using noninvasive measurement methods with stable, low-cost sensors. Microalgal processes have similarities to traditional bioprocesses but also have unique monitoring requirements. In general, variables to be monitored in microalgal processes can be categorized as physical, chemical, and biological, and they are measured in gaseous, liquid, and solid (biological) phases. Physical and chemical process variables can be usually monitored online using standard industrial sensors. The monitoring of biological process variables, however, relies mostly on sensors developed and validated using laboratory-scale systems or uses offline methods because of difficulties in developing suitable online sensors. Here, we review current technologies for online, in situ monitoring of all types of process parameters of microalgal cultivations, with a focus on monitoring of biological parameters. We discuss newly introduced methods for measuring biological parameters that could be possibly adapted for routine online use, should be preferably noninvasive, and are based on approaches that have been proven in other bioprocesses. New sensor types for measuring physicochemical parameters using optical methods or ion-specific field effect transistor (ISFET) sensors are also discussed. Reviewed methods with online implementation or online potential include measurement of irradiance, biomass concentration by optical density and image analysis, cell count, chlorophyll fluorescence, growth rate, lipid concentration by infrared spectrophotometry, dielectric scattering, and nuclear magnetic resonance. Future perspectives are discussed, especially in the field of image analysis using in situ microscopy, infrared spectrophotometry, and software sensor systems.

Graphical Abstract

Keywords

Image analysis Microalgal cultivations Online monitoring Optical sensors Software sensors 

References

  1. 1.
    Malcata FX (2011) Microalgae and biofuels: a promising partnership? Trends Biotechnol 29:542–549CrossRefGoogle Scholar
  2. 2.
    Scott SA, Davey MP, Dennis JS, Horst I, Howe CJ, Lea-Smith DJ, Smith AG (2010) Biodiesel from algae: challenges and prospects. Curr Opin Biotech 21:277–286CrossRefGoogle Scholar
  3. 3.
    Brennan L, Owende P (2010) Biofuels from microalgae—a review of technologies for production, processing, and extractions of biofuels and co-products. Renew Sust Energ Rev 14:557–577CrossRefGoogle Scholar
  4. 4.
    Masojidek J, Torzillo G (2009) Mass cultivation of freshwater microalgae. In: Jorgensen SE (ed), Applications in ecological engineering. Oxford Elsevier B.V., Oxford, pp 176–186Google Scholar
  5. 5.
    Borowitzka MA (1999) Commercial production of microalgae: ponds, tanks, tubes and fermenters. J Biotechnol 70:313–321CrossRefGoogle Scholar
  6. 6.
    Hunt RW, Zavalin A, Bhatnagar A, Chinnasamy S, Das KC (2009) Electromagnetic biostimulation of living cultures for biotechnology, biofuel and bioenergy applications. Int J Mol Sci 10:4515–4558CrossRefGoogle Scholar
  7. 7.
    Han YC, Wen QX, Chen ZQ, Li PF (2011) Review of methods used for microalgal lipid-content analysis. Energy Procedia 12:944–950CrossRefGoogle Scholar
  8. 8.
    Lee TH, Chang JS, Wang HY (2013) Current developments in high-throughput analysis for microalgae cellular contents. Biotechnol J 8:1301–1314CrossRefGoogle Scholar
  9. 9.
    ABO, Technical Standards Committee (2013) Industrial algae measurements, version 6.0. Algae Biomass Organization (ABO), San Diego, 28 p. http://www.algaebiomass.org/resource-center/technical-standards/introduction/ Accessed 19 May 2015
  10. 10.
    Posten C (2012) Design and Performance Parameters of Photobioreactors. Technikfolgenabschätzung – Theorie und Praxis (TATuP) 21:38–45Google Scholar
  11. 11.
    Roquette Klötze GmbH and Co. KG (2011), Microalgae cultivated in a 500 km long system of glass tubes, http://www.algomed.de/index.php?lang=eng&op=algenfarm_anlage. Accessed 19 May 2015
  12. 12.
    van Beilen JB (2010) Why microalgal biofuels won’t save the internal combustion machine. Biofuel Bioprod Bior 4:41–52CrossRefGoogle Scholar
  13. 13.
    Benemann J (2013) Microalgae for biofuels and animal feeds. Energies 6:5869–5886CrossRefGoogle Scholar
  14. 14.
    Craggs R, Sutherland D, Campbell H (2012) Hectare-scale demonstration of high rate algal ponds for enhanced wastewater treatment and biofuel production. J Appl Phycol 24:329–337CrossRefGoogle Scholar
  15. 15.
    Posten C (2009) Design principles of photo-bioreactors for cultivation of microalgae. Eng Life Sci 9:165–177CrossRefGoogle Scholar
  16. 16.
    Yen H-W, Hu IC, Chen C-Y, Chang J-S (2014) Chapter 2—design of photobioreactors for algal cultivation. In: Pandey A, Lee D-J, Chisti Y, Soccol CR (eds) Biofuels from algae. Elsevier, Amsterdam, pp 23–45CrossRefGoogle Scholar
  17. 17.
    Nedbal L, Trtilek M, Cerveny J, Komarek O, Pakrasi HB (2008) A photobioreactor system for precision cultivation of photoautotrophic microorganisms and for high-content analysis of suspension dynamics. Biotechnol Bioeng 100:902–910CrossRefGoogle Scholar
  18. 18.
    Cerveny J, Setlik I, Trtilek M, Nedbal L (2009) Photobioreactor for cultivation and real-time, in-situ measurement of O2 and CO2 exchange rates, growth dynamics, and of chlorophyll fluorescence emission of photoautotrophic microorganisms. Eng Life Sci 9:247–253CrossRefGoogle Scholar
  19. 19.
    Cuaresma M, Janssen M, Vilchez C, Wijffels RH (2011) Horizontal or vertical photobioreactors? How to improve microalgae photosynthetic efficiency. Bioresour Technol 102:5129–5137CrossRefGoogle Scholar
  20. 20.
    Dillschneider R, Posten C (2013) A linear programming approach for modeling and simulation of growth and lipid accumulation of phaeodactylum tricornutum. Energies 6:5333–5356CrossRefGoogle Scholar
  21. 21.
    Malapascua JRF, Jerez CG, Sergejevová M, Figueroa FL, Masojídek J (2014) Photosynthesis monitoring to optimize growth of microalgal mass cultures: application of chlorophyll fluorescence techniques. Aquat Biol 22:123–140CrossRefGoogle Scholar
  22. 22.
    Kliphuis AMJ, de Winter L, Vejrazka C, Martens DE, Janssen M, Wijffels RH (2010) Photosynthetic efficiency of chlorella sorokiniana in a turbulently mixed short light-path photobioreactor. Biotechnol Prog 26:687–696CrossRefGoogle Scholar
  23. 23.
    Dillschneider R, Steinweg C, Rosello-Sastre R, Posten C (2013) Biofuels from microalgae: photoconversion efficiency during lipid accumulation. Bioresour Technol 142:647–654CrossRefGoogle Scholar
  24. 24.
    Glindkamp A, Riechers D, Rehbock C, Hitzmann B, Scheper T, Reardon KF (2009) Sensors in disposable bioreactors status and trends. Adv Biochem Eng Biot 115:145–169Google Scholar
  25. 25.
    Bluma A, Hopfner T, Prediger A, Glindkamp A, Beutel S, Scheper T (2011) Process analytical sensors and image-based techniques for single-use bioreactors. Eng Life Sci 11:550–553CrossRefGoogle Scholar
  26. 26.
    Slegers PM, Wijffels RH, van Straten G, van Boxtel AJB (2011) Design scenarios for flat panel photobioreactors. Appl Energ 88:3342–3353CrossRefGoogle Scholar
  27. 27.
    Quinn JC, Turner CW, Bradley TH (2012) Scale-up of flat plate photobioreactors considering diffuse and direct light characteristics. Biotechnol Bioeng 109:363–370CrossRefGoogle Scholar
  28. 28.
    Franz A, Lehr F, Posten C, Schaub G (2012) Modeling microalgae cultivation productivities in different geographic locations—estimation method for idealized photobioreactors. Biotechnol J 7:546–557CrossRefGoogle Scholar
  29. 29.
    Slegers PM, Lösing MB, Wijffels RH, van Straten G, van Boxtel AJB (2013) Scenario evaluation of open pond microalgae production. Algal Res 2:358–368CrossRefGoogle Scholar
  30. 30.
    Schmidt-Hager J, Ude C, Findeis M, John GT, Scheper T, Beutel S (2014) Noninvasive online biomass detector system for cultivation in shake flasks. Eng Life Sci 14:467–476CrossRefGoogle Scholar
  31. 31.
    Noack K, Eskofier B, Kiefer J, Dilk C, Bilow G, Schirmer M, Buchholz R, Leipertz A (2013) Combined shifted-excitation Raman difference spectroscopy and support vector regression for monitoring the algal production of complex polysaccharides. Analyst 138:5639–5646CrossRefGoogle Scholar
  32. 32.
    Merzlyak MN, Chivkunova OB, Melo TB, Naqvi KR (2002) Does a leaf absorb radiation in the near infrared (780–900 nm) region? A new approach to quantifying optical reflection, absorption and transmission of leaves. Photosynth Res 72:263–270CrossRefGoogle Scholar
  33. 33.
    van den Hoek C, Mann D, Jahns HM (1995) Algae. An introduction to phycology. Cambridge University Press, CambridgeGoogle Scholar
  34. 34.
    Papageorgiou GC, Govindjee (2004) Chlorophyll a fluorescence: a signature of photosynthesis. Springer, DordrechtCrossRefGoogle Scholar
  35. 35.
    Nadadoor VR, De la Hoz Siegler H, Shah SL, McCaffrey WC, Ben-Zvi A (2012) Online sensor for monitoring a microalgal bioreactor system using support vector regression. Chemometrics Intell Lab Syst 110:38–48CrossRefGoogle Scholar
  36. 36.
    Su CH, Fu CC, Chang YC, Nair GR, Ye JL, Chu IM, Wu WT (2008) Simultaneous estimation of chlorophyll a and lipid contents in microalgae by three-color analysis. Biotechnol Bioeng 99:1034–1039CrossRefGoogle Scholar
  37. 37.
    Scheper T, Reardon KF (1992) Sensors in Biotechnology. In: Goepel W, Hesse J, Zemel JN (eds) Sensors: a comprehensive survey. VCH Verlagsgesellschaft, Weinheim, pp 1023–1046Google Scholar
  38. 38.
    Suh IS, Lee CG (2003) Photobioreactor engineering: design and performance. Biotechnol Bioproc Eng 8:313–321CrossRefGoogle Scholar
  39. 39.
    Eriksen NT (2008) The technology of microalgal culturing. Biotechnol Lett 30:1525–1536CrossRefGoogle Scholar
  40. 40.
    Kunjapur AM, Eldridge RB (2010) Photobioreactor design for commercial biofuel production from microalgae. Ind Eng Chem Res 49:3516–3526CrossRefGoogle Scholar
  41. 41.
    Markou G, Georgakakis D (2011) Cultivation of filamentous cyanobacteria (blue-green algae) in agro-industrial wastes and wastewaters: a review. Appl Energ 88:3389–3401CrossRefGoogle Scholar
  42. 42.
    Douskova I, Doucha J, Livansky K, Machat J, Novak P, Umysova D, Zachleder V, Vitova M (2009) Simultaneous flue gas bioremediation and reduction of microalgal biomass production costs. Appl Microbiol Biotechnol 82:179–185CrossRefGoogle Scholar
  43. 43.
    Suh IS, Lee SB (2003) A light distribution model for an internally radiating photobioreactor. Biotechnol Bioeng 82:180–189CrossRefGoogle Scholar
  44. 44.
    Doucha J, Livansky K (2009) Outdoor open thin-layer microalgal photobioreactor: potential productivity. J Appl Phycol 21:111–117CrossRefGoogle Scholar
  45. 45.
    Grobbelaar JU (2010) Microalgal biomass production: challenges and realities. Photosynth Res 106:135–144CrossRefGoogle Scholar
  46. 46.
    Ketheesan B, Nirmalakhandan N (2011) Development of a new airlift-driven raceway reactor for algal cultivation. Appl Energ 88:3370–3376CrossRefGoogle Scholar
  47. 47.
    Chinnasamy S, Bhatnagar A, Claxton R, Das KC (2010) Biomass and bioenergy production potential of microalgae consortium in open and closed bioreactors using untreated carpet industry effluent as growth medium. Bioresour Technol 101:6751–6760CrossRefGoogle Scholar
  48. 48.
    Doucha J, Straka F, Livansky K (2005) Utilization of flue gas for cultivation of microalgae (Chlorella sp.) in an outdoor open thin-layer photobioreactor. J Appl Phycol 17:403–412CrossRefGoogle Scholar
  49. 49.
    Masojidek J, Prasil O (2010) The development of microalgal biotechnology in the Czech Republic. J Ind Microbiol Biotechnol 37:1307–1317CrossRefGoogle Scholar
  50. 50.
    Sandnes JM, Ringstad T, Wenner D, Heyerdahl PH, Kallqvist I, Gislerod HR (2006) Real-time monitoring and automatic density control of large-scale microalgal cultures using near infrared (NIR) optical density sensors. J Biotechnol 122:209–215CrossRefGoogle Scholar
  51. 51.
    Briassoulis D, Panagakis P, Chionidis M, Tzenos D, Lalos A, Tsinos C, Berberidis K, Jacobsen A (2010) An experimental helical-tubular photobioreactor for continuous production of Nannochloropsis sp. Bioresour Technol 101:6768–6777CrossRefGoogle Scholar
  52. 52.
    Marxen K, Vanselow KH, Lippemeier S, Hintze R, Ruser A, Hansen UP (2005) A photobioreactor system for computer controlled cultivation of microalgae. J Appl Phycol 17:535–549CrossRefGoogle Scholar
  53. 53.
    Solovchenko A, Pogosyan S, Chivkunova O, Selyakh I, Semenova L, Voronova E, Scherbakov P, Konyukhov I, Chekanov K, Kirpichnikov M, Lobakova E (2014) Phycoremediation of alcohol distillery wastewater with a novel Chlorella sorokiniana strain cultivated in a photobioreactor monitored on-line via chlorophyll fluorescence. Algal Res Part B 6:234–241Google Scholar
  54. 54.
    Havlik I, Lindner P, Scheper T, Reardon KF (2013) On-line monitoring of large cultivations of microalgae and cyanobacteria. Trends Biotechnol 31:406–414CrossRefGoogle Scholar
  55. 55.
    Kromkamp JC, Beardall J, Sukenik A, Kopecky J, Masojidek J, van Bergeijk S, Gabai S, Shaham E, Yamshon A (2009) Short-term variations in photosynthetic parameters of Nannochloropsis cultures grown in two types of outdoor mass cultivation systems. Aquat Microb Ecol 56:309–322CrossRefGoogle Scholar
  56. 56.
    Sukenik A, Beardall J, Kromkamp JC, Kopecky J, Masojidek J, van Bergeijk S, Gabai S, Shaham E, Yamshon A (2009) Photosynthetic performance of outdoor Nannochloropsis mass cultures under a wide range of environmental conditions. Aquat Microb Ecol 56:297–308CrossRefGoogle Scholar
  57. 57.
    Garcia-Malea MC, Acien FG, Fernandez JM, Ceron MC, Molina E (2006) Continuous production of green cells of Haematococcus pluvialis: modeling of the irradiance effect. Enzyme Microb Technol 38:981–989CrossRefGoogle Scholar
  58. 58.
    Lopez MCGM, Sanchez ED, Lopez JLC, Fernandez FGA, Sevilla JMF, Rivas J, Guerrero MG, Grima EM (2006) Comparative analysis of the outdoor culture of Haematococcus pluvialis in tubular and bubble column photobioreactors. J Biotechnol 123:329–342CrossRefGoogle Scholar
  59. 59.
    Tebbani S, Lopes F, Filali R, Dumur D, Pareau D (2014) Nonlinear predictive control for maximization of CO2 bio-fixation by microalgae in a photobioreactor. Bioprocess Biosyst Eng 37:83–97CrossRefGoogle Scholar
  60. 60.
    Heaven S, Banks CJ, Zotova EA (2005) Light attenuation parameters for waste stabilisation ponds. Water Sci Technol 51:143–152Google Scholar
  61. 61.
    Masojidek J, Sergejevova M, Rottnerova K, Jirka V, Korecko J, Kopecky J, Zat’kova I, Torzillo G, Stys D (2009) A two-stage solar photobioreactor for cultivation of microalgae based on solar concentrators. J Appl Phycol 21:55–63CrossRefGoogle Scholar
  62. 62.
    Kliphuis AMJ, Janssen M, van den End EJ, Martens DE, Wijffels RH (2011) Light respiration in Chlorella sorokiniana. J Appl Phycol 23:935–947CrossRefGoogle Scholar
  63. 63.
    Melnicki MR, Pinchuk GE, Hill EA, Kucek LA, Stolyar SM, Fredrickson JK, Konopka AE, Beliaev AS (2013) Feedback-controlled LED photobioreactor for photophysiological studies of cyanobacteria. Bioresour Technol 134:127–133CrossRefGoogle Scholar
  64. 64.
    Barsanti L, Gualtieri P (2006) Algae. Anatomy, Biochemistry, and Biotechnology. CRC Press, Taylor & Francis Group, Boca RatonGoogle Scholar
  65. 65.
    Livansky K, Doucha J (1998) Influence of solar irradiance, culture temperature and CO2 supply on daily course of O2 evolution by Chlorella mass cultures in outdoor open thin-layer culture units. Arch Hydrobiol Suppl Algol Stud 89:137–149Google Scholar
  66. 66.
    Li J, Xu S, Su WW (2003) Online estimation of stirred-tank microalgal photobioreactor cultures based on dissolved oxygen measurement. Biochem Eng J 14:51–65CrossRefGoogle Scholar
  67. 67.
    Rodolfi L, Zittelli GC, Bassi N, Padovani G, Biondi N, Bonini G, Tredici MR (2009) Microalgae for oil: strain selection, induction of lipid synthesis and outdoor mass cultivation in a low-cost photobioreactor. Biotechnol Bioeng 102:100–112CrossRefGoogle Scholar
  68. 68.
    Pruvost J, Van Vooren G, Le Gouic B, Couzinet-Mossion A, Legrand J (2011) Systematic investigation of biomass and lipid productivity by microalgae in photobioreactors for biodiesel application. Bioresour Technol 102:150–158CrossRefGoogle Scholar
  69. 69.
    Bosma R, de Vree JH, Slegers PM, Janssen M, Wijffels RH, Barbosa MJ (2014) Design and construction of the microalgal pilot facility AlgaePARC. Algal Res Part B 6:160–169Google Scholar
  70. 70.
    Obata M, Toda T, Taguchi S (2009) Using chlorophyll fluorescence to monitor yields of microalgal production. J Appl Phycol 21:315–319CrossRefGoogle Scholar
  71. 71.
    Jiménez C, Cossío BR, Niell FX (2003) Relationship between physicochemical variables and productivity in open ponds for the production of Spirulina: a predictive model of algal yield. Aquaculture 221:331–345CrossRefGoogle Scholar
  72. 72.
    Torzillo G, Pushparaj B, Masojidek J, Vonshak A (2003) Biological constraints in algal biotechnology. Biotechnol Bioproc Eng 8:338–348CrossRefGoogle Scholar
  73. 73.
    Ugwu CU, Aoyagi H (2008) Influence of shading inclined tubular photobioreactor surfaces on biomass productivity of C. sorokiniana. Photosynthetica 46:283–285CrossRefGoogle Scholar
  74. 74.
    Livansky K, Doucha J, Hu HJ, Li YG (2006) CO2 partial pressure—pH relationships in the medium and relevance to CO2 mass balance in outdoor open thin-layer Arthrospira (Spirulina) cultures. Arch Hydrobiol 165:365–381CrossRefGoogle Scholar
  75. 75.
    Belkin S, Boussiba S (1991) Resistance of Spirulina platensis to Ammonia at High pH Values. Plant Cell Physiol 32:953–958Google Scholar
  76. 76.
    De Swaaf ME, Sijtsma L, Pronk JT (2003) High-cell-density fed-batch cultivation of the docosahexaenoic acid producing marine alga Crypthecodinium cohnii. Biotechnol Bioeng 81:666–672CrossRefGoogle Scholar
  77. 77.
    Berenguel M, Rodriguez F, Acien FG, Garcia JL (2004) Model predictive control of pH in tubular photobioreactors. J Process Contr 14:377–387CrossRefGoogle Scholar
  78. 78.
    Sanchez JLG, Berenguel M, Rodriguez F, Sevilla JMF, Alias CB, Fernandez FGA (2003) Minimization of carbon losses in pilot-scale outdoor photobioreactors by model-based predictive control. Biotechnol Bioeng 84:533–543CrossRefGoogle Scholar
  79. 79.
    Orellana G, Haigh D (2008) New trends in fiber-optic chemical and biological sensors. Curr Anal Chem 4:273–295CrossRefGoogle Scholar
  80. 80.
    Sandifer JR, Voycheck JJ (1999) A review of biosensor and industrial applications of pH-ISFETs and an evaluation of Honeywell’s “DuraFET”. Mikrochim Acta 131:91–98CrossRefGoogle Scholar
  81. 81.
    Malinowski J, Geiger EJ (2013) Development of a wireless sensor network for algae cultivation using ISFET pH probes. Algal Res 4:19–22CrossRefGoogle Scholar
  82. 82.
    Grobbelaar JU (2007) Photosynthetic characteristics of Spirulina platensis grown in commercial-scale open outdoor raceway ponds: what do the organisms tell us? J Appl Phycol 19:591–598CrossRefGoogle Scholar
  83. 83.
    Lee YK, Ding SY, Low CS, Chang YC, Forday WL, Chew PC (1995) Design and performance of an alpha-type tubular photobioreactor for mass cultivation of microalgae. J Appl Phycol 7:47–51CrossRefGoogle Scholar
  84. 84.
    Baquerisse D, Nouals S, Isambert A, dos Santos PF, Durand G (1999) Modelling of a continuous pilot photobioreactor for microalgae production. J Biotechnol 70:335–342CrossRefGoogle Scholar
  85. 85.
    Doucha J, Livansky K (2006) Productivity, CO2/O2 exchange and hydraulics in outdoor open high density microalgal (Chlorella sp.) photobioreactors operated in a Middle and Southern European climate. J Appl Phycol 18:811–826CrossRefGoogle Scholar
  86. 86.
    Janata J (2009) Principles of chemical sensors, 2nd edn. Springer, DordrechtCrossRefGoogle Scholar
  87. 87.
    Hill GA (2006) Measurement of overall volumetric mass transfer coefficients for carbon dioxide in a well-mixed reactor using a pH probe. Ind Eng Chem Res 45:5796–5800CrossRefGoogle Scholar
  88. 88.
    Moran D, Tirsgard B, Steffensen JF (2010) The accuracy and limitations of a new meter used to measure aqueous carbon dioxide. Aquacult Eng 43:101–107CrossRefGoogle Scholar
  89. 89.
    Borges MT, Domingues JO, Jesus JM, Pereira CM (2012) Direct and continuous dissolved CO2 monitoring in shallow raceway systems: from laboratory to commercial-scale applications. Aquacult Eng 49:10–17CrossRefGoogle Scholar
  90. 90.
    Nedbal L, Cerveny J, Keren N, Kaplan A (2010) Experimental validation of a nonequilibrium model of CO2 fluxes between gas, liquid medium, and algae in a flat-panel photobioreactor. J Ind Microbiol Biotechnol 37:1319–1326CrossRefGoogle Scholar
  91. 91.
    Zosel J, Oelssner W, Decker M, Gerlach G, Guth U (2011) The measurement of dissolved and gaseous carbon dioxide concentration. Meas Sci Technol 22Google Scholar
  92. 92.
    Livansky K (1996) Effect of O2, CO2 and temperature on the light saturated growth of Scenedesmus obliquus. Arch Hydrobiol Suppl Algol Stud 82:69–82Google Scholar
  93. 93.
    Lindner P, Endres C, Bluma A, Höpfner T, Glindkamp A, Haake C, Landgrebe D, Riechers D, Baumfalk R, Hitzmann B, Scheper T, Reardon KF (2011) Disposable Sensor Systems. In: Eibl R, Eibl D (eds) Single-use technology in biopharmaceutical manufacture. Wiley, Hoboken, pp 67–81CrossRefGoogle Scholar
  94. 94.
    Brindley C, Acien FG, Fernandez-Sevilla JM (2010) The oxygen evolution methodology affects photosynthetic rate measurements of microalgae in well-defined light regimes. Biotechnol Bioeng 106:228–237Google Scholar
  95. 95.
    Bosma R, van Zessen E, Reith JH, Tramper J, Wijffels RH (2007) Prediction of volumetric productivity of an outdoor photobioreactor. Biotechnol Bioeng 97:1108–1120CrossRefGoogle Scholar
  96. 96.
    Ugwu CU, Aoyagi H, Uchiyama H (2007) Influence of irradiance, dissolved oxygen concentration, and temperature on the growth of Chlorella sorokiniana. Photosynthetica 45:309–311CrossRefGoogle Scholar
  97. 97.
    Vonshak A, Laorawat S, Bunnag B, Tanticharoen M (2014) The effect of light availability on the photosynthetic activity and productivity of outdoor cultures of Arthrospira platensis (Spirulina). J Appl Phycol 26:1309–1315CrossRefGoogle Scholar
  98. 98.
    YSI Inc. (2009) The dissolved oxygen handbook. YSI Inc., Yellow Springs, Ohio, USA, 43 p., https://www.ysi.com/weknowdo (19.05.2015)
  99. 99.
    Collos Y, Harrison PJ (2014) Acclimation and toxicity of high ammonium concentrations to unicellular algae. Mar Pollut Bull 80:8–23CrossRefGoogle Scholar
  100. 100.
    Powell N, Shilton AN, Pratt S, Chisti Y (2008) Factors influencing luxury uptake of phosphorus by microalgae in waste stabilization ponds. Environ Sci Technol 42:5958–5962CrossRefGoogle Scholar
  101. 101.
    Eriksen NT, Iversen JJL (1995) Online determination of pigment composition and biomass in cultures of microalgae. Biotechnol Tech 9:49–54CrossRefGoogle Scholar
  102. 102.
    Eriksen NT, Geest T, Iversen JJL (1996) Phototrophic growth in the lumostat: A photo-bioreactor with on-line optimization of light intensity. J Appl Phycol 8:345–352CrossRefGoogle Scholar
  103. 103.
    Bao YL, Wen SM, Cong W, Wu X, Ning ZX (2012) An optical-density-based feedback feeding method for ammonium concentration control in Spirulina platensis cultivation. J Microbiol Biotechnol 22:967–974CrossRefGoogle Scholar
  104. 104.
    Jiménez C, Cossío BR, Labella D, Xavier Niell F (2003) The feasibility of industrial production of Spirulina (Arthrospira) in Southern Spain. Aquaculture 217:179–190CrossRefGoogle Scholar
  105. 105.
    Chioccioli M, Hankamer B, Ross IL (2014) Flow cytometry pulse width data enables rapid and sensitive estimation of biomass dry weight in the microalgae Chlamydomonas reinhardtii and Chlorella vulgaris. PLoS One 9:e97269CrossRefGoogle Scholar
  106. 106.
    Quinn J, de Winter L, Bradley T (2011) Microalgae bulk growth model with application to industrial scale systems. Bioresour Technol 102:5083–5092CrossRefGoogle Scholar
  107. 107.
    Lucker BF, Hall CC, Zegarac R, Kramer DM (2014) The environmental photobioreactor (ePBR): an algal culturing platform for simulating dynamic natural environments. Algal Res Part B 6:242–249Google Scholar
  108. 108.
    MacIntyre HL, Cullen JJ (2005) Using cultures to investigate the physiological ecology of microalgae. In: Andersen RA (ed) Algal culturing techniques. Elsevier Academic Press, New York, pp 287–326Google Scholar
  109. 109.
    Meireles LA, Azevedo JL, Cunha JP, Malcata FX (2002) On-line determination of biomass in a microalga bioreactor using a novel computerized flow injection analysis system. Biotechnol Prog 18:1387–1391CrossRefGoogle Scholar
  110. 110.
    Meireles LA, Guedes AC, Barbosa CR, Azevedo JL, Cunha JP, Malcata FX (2008) On-line control of light intensity in a microalgal bioreactor using a novel automatic system. Enzyme Microb Technol 42:554–559CrossRefGoogle Scholar
  111. 111.
    Olaizola M (2003) Microalgal removal of CO2 from flue gases: Changes in medium pH and flue gas composition do not appear to affect the photochemical yield of microalgal cultures. Biotechnol Bioproc Eng 8:360–367CrossRefGoogle Scholar
  112. 112.
    Murphy TE, Macon K, Berberoglu H (2013) Multispectral image analysis for algal biomass quantification. Biotechnol Prog 29:808–816CrossRefGoogle Scholar
  113. 113.
    Brown LM, Gargantini I, Brown DJ, Atkinson HJ, Govindarajan J, Vanlerberghe GC (1989) Computer-based image analysis for the automated counting and morphological description of microalgae in culture. J Appl Phycol 1:211–225CrossRefGoogle Scholar
  114. 114.
    Gray AJ, Young D, Martin NJ, Glasbey CA (2002) Cell identification and sizing using digital image analysis for estimation of cell biomass in high rate algal ponds. J Appl Phycol 14:193–204CrossRefGoogle Scholar
  115. 115.
    Hyka P, Lickova S, Přibyl P, Melzoch K, Kovar K (2013) Flow cytometry for the development of biotechnological processes with microalgae. Biotechnol Adv 31:2–16CrossRefGoogle Scholar
  116. 116.
    Mairet F, Bernard O, Masci P, Lacour T, Sciandra A (2011) Modelling neutral lipid production by the microalga Isochrysis aff. galbana under nitrogen limitation. Bioresour Technol 102:142–149CrossRefGoogle Scholar
  117. 117.
    Fluid Imaging Technologies Inc. (2013) FlowCAM® particle imaging within processing line. http://www.algaeindustrymagazine.com/flowcam-particle-imaging-within-processing-line/, http://www.fluidimaging.com/products-on-line-systems.htm (19.05.2015)
  118. 118.
    Rehbock C, Riechers D, Hopfner T, Bluma A, Lindner P, Hitzmann B, Beutel S, Scheper T (2010) Development of a flow-through microscopic multitesting system for parallel monitoring of cell samples in biotechnological cultivation processes. J Biotechnol 150:87–93CrossRefGoogle Scholar
  119. 119.
    Prediger A, Bluma A, Hopfner T, Lindner P, Beutel S, Scheper T, Muller JJ, Hilterhaus L, Liese A (2011) In situ microscopy for online monitoring of enzyme carriers and two-phase processes. Chem Eng Technol 34:837–840CrossRefGoogle Scholar
  120. 120.
    Bluma A, Hopfner T, Lindner P, Rehbock C, Beutel S, Riechers D, Hitzmann B, Scheper T (2010) In-situ imaging sensors for bioprocess monitoring: state of the art. Anal Bioanal Chem 398:2429–2438CrossRefGoogle Scholar
  121. 121.
    Hopfner T, Bluma A, Rudolph G, Lindner P, Scheper T (2010) A review of non-invasive optical-based image analysis systems for continuous bioprocess monitoring. Bioprocess Biosyst Eng 33:247–256CrossRefGoogle Scholar
  122. 122.
    Akin M, Prediger A, Yuksel M, Hopfner T, Demirkol DO, Beutel S, Timur S, Scheper T (2011) A new set up for multi-analyte sensing: at-line bio-process monitoring. Biosens Bioelectron 26:4532–4537CrossRefGoogle Scholar
  123. 123.
    Opitz B, Prediger A, Luder C, Eckstein M, Hilterhaus L, Lindner P, Beutel S, Scheper T, Liese A (2013) In situ microscopy for in-line monitoring of the enzymatic hydrolysis of cellulose. Anal Chem 85:8121–8126CrossRefGoogle Scholar
  124. 124.
    Lüder C, Lindner P, Bulnes-Abundis D, Lu Shaobin M, Lücking T, Solle D, Scheper T (2014) In situ microscopy and MIR-spectroscopy as non-invasive optical sensors for cell cultivation process monitoring. Pharm Bioprocess 2:157–166CrossRefGoogle Scholar
  125. 125.
    Havlik I, Reardon KF, Unal M, Lindner P, Prediger A, Babitzky A, Beutel S, Scheper T (2013) Monitoring of microalgal cultivations with on-line, flow-through microscopy. Algal Res 2:253–257CrossRefGoogle Scholar
  126. 126.
    Brown L (2014) Rapid, automated characterization of algae using dynamic imaging particle analysis. Industrial Biotechnology 10:164–168CrossRefGoogle Scholar
  127. 127.
    Park BS, Baek SH, Ki JS, Cattolico RA, Han MS (2012) Assessment of EvaGreen-based quantitative real-time PCR assay for enumeration of the microalgae Heterosigma and Chattonella (Raphidophyceae). J Appl Phycol 24:1555–1567CrossRefGoogle Scholar
  128. 128.
    Fulbright SP, Dean MK, Wardle G, Lammers PJ, Chisholm S (2014) Molecular diagnostics for monitoring contaminants in algal cultivation. Algal Res 4:41–51CrossRefGoogle Scholar
  129. 129.
    McBride RC, Lopez S, Meenach C, Burnett M, Lee PA, Nohilly F, Behnke C (2014) Contamination management in low cost open algae ponds for biofuels production. Ind Biotechnol 10:221–227CrossRefGoogle Scholar
  130. 130.
    White S, Anandraj A, Bux F (2011) PAM fluorometry as a tool to assess microalgal nutrient stress and monitor cellular neutral lipids. Bioresour Technol 102:1675–1682CrossRefGoogle Scholar
  131. 131.
    Baker NR, Oxborough K (2004) Chlorophyll fluorescence as a probe of photosynthetic productivity. In: Papageorgiou GC, Govindjee (eds), Chlorophyll a fluorescence: a signature of photosynthesis. Springer, Dordrecht, pp 65–82Google Scholar
  132. 132.
    Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668CrossRefGoogle Scholar
  133. 133.
    Schreiber U (2004) Pulse-Amplitude-Modulation (PAM) fluorometry and saturation pulse method: an overview. In: Papageorgiou GC, Govindjee (eds), Chlorophyll a fluorescence: a signature of photosynthesis. Springer, Dordrecht, pp 279–319Google Scholar
  134. 134.
    Masojidek J, Kopecky J, Giannelli L, Torzillo G (2011) Productivity correlated to photobiochemical performance of Chlorella mass cultures grown outdoors in thin-layer cascades. J Ind Microbiol Biotechnol 38:307–317CrossRefGoogle Scholar
  135. 135.
    Hulatt CJ, Thomas DN (2011) Productivity, carbon dioxide uptake and net energy return of microalgal bubble column photobioreactors. Bioresour Technol 102:5775–5787CrossRefGoogle Scholar
  136. 136.
    Murphy TE, Macon K, Berberoglu H (2014) Rapid algal culture diagnostics for open ponds using multispectral image analysis. Biotechnol Prog 30:233–240CrossRefGoogle Scholar
  137. 137.
    Gunther A, Jakob T, Goss R, Konig S, Spindler D, Rabiger N, John S, Heithoff S, Fresewinkel M, Posten C, Wilhelm C (2012) Methane production from glycolate excreting algae as a new concept in the production of biofuels. Bioresour Technol 121:454–457CrossRefGoogle Scholar
  138. 138.
    Fresewinkel M, Rosello R, Wilhelm C, Kruse O, Hankamer B, Posten C (2014) Integration in microalgal bioprocess development: design of efficient, sustainable, and economic processes. Eng Life Sci 14:560–573CrossRefGoogle Scholar
  139. 139.
    Jacobi A, Bucharsky EC, Schell KG, Habisreuther P, Oberacker R, Hoffmann MJ, Zarzalis N, Posten C (2012) The application of transparent glass sponge for improvement of light distribution in photobioreactors. J Bioprocess Biotechniq 2:113. doi:10.4172/2155-9821.1000113 Google Scholar
  140. 140.
    Solovchenko AE, Khozin-Goldberg I, Cohen Z, Merzlyak MN (2009) Carotenoid-to-chlorophyll ratio as a proxy for assay of total fatty acids and arachidonic acid content in the green microalga Parietochloris incisa. J Appl Phycol 21:361–366CrossRefGoogle Scholar
  141. 141.
    Solovchenko A, Khozin-Goldberg I, Recht L, Boussiba S (2011) Stress-Induced Changes in optical properties, pigment and fatty acid content of Nannochloropsis sp. implications for Non-destructive assay of total fatty acids. Mar Biotechnol 13:527–535CrossRefGoogle Scholar
  142. 142.
    Lichtenthaler HK, Wenzel O, Buschmann C, Gitelson A (1998) Plant stress detection by reflectance and fluorescence. In: Csermely P (ed) Stress of life: from molecules to man. New York Acad Sciences, New York, pp 271–285Google Scholar
  143. 143.
    Buschmann C, Langsdorf G, Lichtenthaler HK (2000) Imaging of the blue, green, and red fluorescence emission of plants: an overview. Photosynthetica 38:483–491CrossRefGoogle Scholar
  144. 144.
    Buschmann C (2007) Variability and application of the chlorophyll fluorescence emission ratio red/far-red of leaves. Photosynth Res 92:261–271CrossRefGoogle Scholar
  145. 145.
    Lenk S, Chaerle L, Pfundel EE, Langsdorf G, Hagenbeek D, Lichtenthaler HK, Van der Straeten D, Buschmann C (2007) Multispectral fluorescence and reflectance imaging at the leaf level and its possible applications. J Exp Bot 58:807–814CrossRefGoogle Scholar
  146. 146.
    Srinivas SP, Mutharasan R (1987) Inner filter effects and their interferences in the interpretation of culture fluorescence. Biotechnol Bioeng 30:769–774CrossRefGoogle Scholar
  147. 147.
    Kouril R, Ilik P, Naus J, Schoefs B (1999) On the limits of applicability of spectrophotometric and spectrofluorimetric methods for the determination of chlorophyll a/b ratio. Photosynth Res 62:107–116CrossRefGoogle Scholar
  148. 148.
    Forehead HI, O’Kelly CJ (2013) Small doses, big troubles: modeling growth dynamics of organisms affecting microalgal production cultures in closed photobioreactors. Bioresour Technol 129:329–334CrossRefGoogle Scholar
  149. 149.
    Sue T, Obolonkin V, Griffiths H, Villas-Boas SG (2011) An exometabolomics approach to monitoring microbial contamination in microalgal fermentation processes by using metabolic footprint analysis. Appl Environ Microbiol 77:7605–7610CrossRefGoogle Scholar
  150. 150.
    Görs M, Schumann R, Hepperle D, Karsten U (2010) Quality analysis of commercial Chlorella products used as dietary supplement in human nutrition. J Appl Phycol 22:265–276CrossRefGoogle Scholar
  151. 151.
    Lakaniemi AM, Intihar VM, Tuovinen OH, Puhakka JA (2012) Growth of Chlorella vulgaris and associated bacteria in photobioreactors. Microb Biotechnol 5:69–78CrossRefGoogle Scholar
  152. 152.
    Abomohra AE, El-Sheekh M, Hanelt D (2014) Extracellular secretion of free fatty acids by the chrysophyte Ochromonas danica under photoautotrophic and mixotrophic growth. World J Microbiol Biotechnol 30:3111–3119CrossRefGoogle Scholar
  153. 153.
    Tamburic B, Zemichael FW, Crudge P, Maitland GC, Hellgardt K (2011) Design of a novel flat-plate photobioreactor system for green algal hydrogen production. Int J Hydrogen Energ 36:6578–6591CrossRefGoogle Scholar
  154. 154.
    Oncel S, Kose A (2014) Comparison of tubular and panel type photobioreactors for biohydrogen production utilizing Chlamydomonas reinhardtii considering mixing time and light intensity. Bioresour Technol 151:265–270CrossRefGoogle Scholar
  155. 155.
    Gao ZX, Zhao H, Li ZM, Tan XM, Lu XF (2012) Photosynthetic production of ethanol from carbon dioxide in genetically engineered cyanobacteria. Energy Environ Sci 5:9857–9865CrossRefGoogle Scholar
  156. 156.
    Balogh K, Jesus JM, Gouveia C, Domingues JO, Markovics A, Baptista JM, Kovacs B, Pereira CM, Borges MT, Jorge PAS (2013) Characterization of a novel dissolved CO2 sensor for utilization in environmental monitoring and aquaculture industry. In: Proceedings of SPIE 8785, 8th Iberoamerican Optics Meeting and 11th Latin American Meeting on Optics, Lasers, and Applications, 8785FC. doi:10.1117/12.2027518
  157. 157.
    Szita N, Boccazzi P, Zhang ZY, Boyle P, Sinskey AJ, Jensen KF (2005) Development of a multiplexed microbioreactor system for high-throughput bioprocessing. Lab Chip 5:819–826CrossRefGoogle Scholar
  158. 158.
    Han A, Hou HJ, Li L, Kim HS, de Figueiredo P (2013) Microfabricated devices in microbial bioenergy sciences. Trends Biotechnol 31:225–232CrossRefGoogle Scholar
  159. 159.
    Vanrolleghem PA, Lee DS (2003) On-line monitoring equipment for wastewater treatment processes: state of the art. Water Sci Technol 47:1–34Google Scholar
  160. 160.
    Lynggaard-Jensen A, Eisum NH, Rasmussen I, Jacobsen HS, Stenstrom T (1996) Description and test of a new generation of nutrient sensors. Water Sci Technol 33:25–35CrossRefGoogle Scholar
  161. 161.
    Ingildsen P, Jeppsson U, Olsson G (2002) Dissolved oxygen controller based on on-line measurements of ammonium combining feed-forward and feedback. Water Sci Technol 45:453–460Google Scholar
  162. 162.
    Radomska A, Singhal S, Ye H, Lim M, Mantalaris A, Yue XC, Drakakis EM, Toumazou C, Cass AEG (2008) Biocompatible ion selective electrode for monitoring metabolic activity during the growth and cultivation of human cells. Biosens Bioelectron 24:435–441CrossRefGoogle Scholar
  163. 163.
    Gutierrez M, Alegret S, Caceres R, Casadesus J, Marfa O, Del Valle M (2008) Nutrient solution monitoring in greenhouse cultivation employing a potentiometric electronic tongue. J Agric Food Chem 56:1810–1817CrossRefGoogle Scholar
  164. 164.
    Mueller AV, Hemond HF (2013) Extended artificial neural networks: incorporation of a priori chemical knowledge enables use of ion selective electrodes for in-situ measurement of ions at environmentally relevant levels. Talanta 117:112–118CrossRefGoogle Scholar
  165. 165.
    Masojidek J, Vonshak A, Torzillo G (2011) Chlorophyll fluorescence applications in microalgal mass cultures. In: Suggett DJ, Prášil O, Borowitzka MA (eds) Chlorophyll a fluorescence in aquatic sciences: methods and applications. Springer, Dordrecht, pp 277–292Google Scholar
  166. 166.
    Davey PT, Hiscox WC, Lucker BF, O’Fallon JV, Chen S, Helms GL (2012) Rapid triacylglyceride detection and quantification in live micro-algal cultures via liquid state 1H NMR. Algal Res 1:166–175CrossRefGoogle Scholar
  167. 167.
    Sanchez-Silva L, Lopez-Gonzalez D, Garcia-Minguillan AM, Valverde JL (2013) Pyrolysis, combustion and gasification characteristics of Nannochloropsis gaditana microalgae. Bioresour Technol 130:321–331CrossRefGoogle Scholar
  168. 168.
    Chen W-H, Wu Z-Y, Chang J-S (2014) Isothermal and non-isothermal torrefaction characteristics and kinetics of microalga Scenedesmus obliquus CNW-N. Bioresour Technol 155:245–251CrossRefGoogle Scholar
  169. 169.
    Marcilla A, Gomez-Siurana A, Gomis C, Chapuli E, Catala MC, Valdes FJ (2009) Characterization of microalgal species through TGA/FTIR analysis: application to Nannochloropsis sp. Thermochim Acta 484:41–47CrossRefGoogle Scholar
  170. 170.
    Biller P, Ross AB (2014) Pyrolysis GC–MS as a novel analysis technique to determine the biochemical composition of microalgae. Algal Res Part A 6:91–97Google Scholar
  171. 171.
    Hantelmann K, Kollecker A, Hull D, Hitzmann B, Scheper T (2006) Two-dimensional fluorescence spectroscopy: a novel approach for controlling fed-batch cultivations. J Biotechnol 121:410–417CrossRefGoogle Scholar
  172. 172.
    Roychoudhury P, O’Kennedy R, McNeil B, Harvey LM (2007) Multiplexing fibre optic near infrared (NIR) spectroscopy as an emerging technology to monitor industrial bioprocesses. Anal Chim Acta 590:110–117CrossRefGoogle Scholar
  173. 173.
    Porizka P, Prochazkova P, Prochazka D, Sladkova L, Novotny J, Petrilak M, Brada M, Samek O, Pilat Z, Zemanek P, Adam V, Kizek R, Novotny K, Kaiser J (2014) Algal biomass analysis by laser-based analytical techniques-a review. Sensors 14:17725–17752CrossRefGoogle Scholar
  174. 174.
    Bono MS Jr, Ahner BA, Kirby BJ (2013) Detection of algal lipid accumulation due to nitrogen limitation via dielectric spectroscopy of Chlamydomonas reinhardtii suspensions in a coaxial transmission line sample cell. Bioresour Technol 143:623–631CrossRefGoogle Scholar
  175. 175.
    Tartakovsky B, Sheintuch M, Hilmer JM, Scheper T (1996) Application of scanning fluorometry for monitoring of a fermentation process. Biotechnol Prog 12:126–131CrossRefGoogle Scholar
  176. 176.
    Podrazky O, Kuncova G, Krasowska A, Sigler K (2003) Monitoring the growth and stress responses of yeast cells by two-dimensional fluorescence spectroscopy: first results. Folia Microbiol 48:189–192CrossRefGoogle Scholar
  177. 177.
    Landgrebe D, Haake C, Hopfner T, Beutel S, Hitzmann B, Scheper T, Rhiel M, Reardon KF (2010) On-line infrared spectroscopy for bioprocess monitoring. Appl Microbiol Biotechnol 88:11–22CrossRefGoogle Scholar
  178. 178.
    Roychoudhury P, Harvey LM, McNeil B (2006) The potential of mid infrared spectroscopy (MIRS) for real time bioprocess monitoring. Anal Chim Acta 571:159–166CrossRefGoogle Scholar
  179. 179.
    Ellis DI, Goodacre R (2006) Metabolic fingerprinting in disease diagnosis: biomedical applications of infrared and Raman spectroscopy. Analyst 131:875–885CrossRefGoogle Scholar
  180. 180.
    Laurens LML, Wolfrum EJ (2013) High-Throughput quantitative biochemical characterization of algal biomass by NIR spectroscopy; multiple linear regression and multivariate linear regression analysis. J Agric Food Chem 61:12307–12314CrossRefGoogle Scholar
  181. 181.
    Tan S-T, Balasubramanian RK, Das P, Obbard JP, Chew W (2013) Application of mid-infrared chemical imaging and multivariate chemometrics analyses to characterise a population of microalgae cells. Bioresour Technol 134:316–323CrossRefGoogle Scholar
  182. 182.
    Riley MR, Crider HM, Nite ME, Garcia RA, Woo J, Wegge RM (2001) Simultaneous measurement of 19 components in serum-containing animal cell culture media by Fourier transform near-infrared spectroscopy. Biotechnol Prog 17:376–378CrossRefGoogle Scholar
  183. 183.
    Laurens LML, Wolfrum EJ (2011) Feasibility of spectroscopic characterization of algal lipids: chemometric correlation of NIR and FTIR spectra with exogenous lipids in algal biomass. Bioenerg Res 4:22–35CrossRefGoogle Scholar
  184. 184.
    Brown MR, Frampton DMF, Dunstan GA, Blackburn SI (2014) Assessing near-infrared reflectance spectroscopy for the rapid detection of lipid and biomass in microalgae cultures. J Appl Phycol 26:191–198CrossRefGoogle Scholar
  185. 185.
    Challagulla V, Walsh KB, Subedi P (2014) Biomass and total lipid content assessment of microalgal cultures using near and short wave infrared spectroscopy. Bioenerg Res 7:306–318CrossRefGoogle Scholar
  186. 186.
    Sigee DC, Dean A, Levado E, Tobin MJ (2002) Fourier-transform infrared spectroscopy of Pediastrum duplex: characterization of a micro-population isolated from a eutrophic lake. Eur J Phycol 37:19–26CrossRefGoogle Scholar
  187. 187.
    Stehfest K (2006) Die FT-IR-Spektroskopie in der Pflanzenphysiologie—Anwendungsmöglichkeiten für die Zellinhaltsstoffanalytik [Ph.D. Thesis], Universität Leipzig, LeipzigGoogle Scholar
  188. 188.
    Jakob T, Wagner H, Stehfest K, Wilhelm C (2007) A complete energy balance from photons to new biomass reveals a light- and nutrient-dependent variability in the metabolic costs of carbon assimilation. J Exp Bot 58:2101–2112CrossRefGoogle Scholar
  189. 189.
    Pistorius AMA, DeGrip WJ, Egorova-Zachernyuk TA (2009) Monitoring of biomass composition from microbiological sources by means of FT-IR spectroscopy. Biotechnol Bioeng 103:123–129CrossRefGoogle Scholar
  190. 190.
    Dean AP, Sigee DC, Estrada B, Pittman JK (2010) Using FTIR spectroscopy for rapid determination of lipid accumulation in response to nitrogen limitation in freshwater microalgae. Bioresour Technol 101:4499–4507CrossRefGoogle Scholar
  191. 191.
    Palmucci M, Ratti S, Giordano M (2011) Ecological and evolutionary implications of carbon allocation in marine phytoplankton as a function of nitrogen availability: a fourier transform infrared spectroscopy approach. J Phycol 47:313–323CrossRefGoogle Scholar
  192. 192.
    Holm-Nielsen JB, Andree H, Lindorfer H, Esbensen KH (2007) Transflexive embedded near infrared monitoring for key process intermediates in anaerobic digestion/biogas production. J Near Infrared Spectrosc 15:123–135CrossRefGoogle Scholar
  193. 193.
    Stockl A (2013) Entwicklung und erprobung eines online-messsystems für biogasanlagen auf basis der Nah-Infrarot-Reflexionsspektroskopie (NIRS) [Ph.D. Thesis], Universität Hohenheim, HohenheimGoogle Scholar
  194. 194.
    Holm-Nielsen JB, Lomborg CJ, Oleskowicz-Popiel P, Esbensen KH (2008) On-line near infrared monitoring of glycerol-boosted anaerobic digestion processes: evaluation of process analytical technologies. Biotechnol Bioeng 99:302–313CrossRefGoogle Scholar
  195. 195.
    Mayers JJ, Flynn KJ, Shields RJ (2013) Rapid determination of bulk microalgal biochemical composition by fourier-transform infrared spectroscopy. Bioresour Technol 148:215–220CrossRefGoogle Scholar
  196. 196.
    Coat R, Montalescot V, León E, Kucma D, Perrier C, Jubeau S, Thouand G, Legrand J, Pruvost J, Gonçalves O (2014) Unravelling the matrix effect of fresh sampled cells for in vivo unbiased FTIR determination of the absolute concentration of total lipid content of microalgae. Bioprocess Biosyst Eng 1–13Google Scholar
  197. 197.
    Schenk J, Marison IW, von Stockar U (2007) A simple method to monitor and control methanol feeding of Pichia pastoris fermentations using mid-IR spectroscopy. J Biotechnol 128:344–353CrossRefGoogle Scholar
  198. 198.
    Silva TLd, Roseiro JC, Reis A (2012) Applications and perspectives of multi-parameter flow cytometry to microbial biofuels production processes. Trends Biotechnol 30:225–232CrossRefGoogle Scholar
  199. 199.
    Davis RW, Volponi JV, Jones HDT, Carvalho BJ, Wu H, Singh S (2012) Multiplex fluorometric assessment of nutrient limitation as a strategy for enhanced lipid enrichment and harvesting of Neochloris oleoabundans. Biotechnol Bioeng 109:2503–2512CrossRefGoogle Scholar
  200. 200.
    da Silva TL, Santos CA, Reis A (2009) Multi-parameter flow cytometry as a tool to monitor heterotrophic microalgal batch fermentations for oil production towards biodiesel. Biotechnol Bioproc Eng 14:330–337CrossRefGoogle Scholar
  201. 201.
    Gouveia L, Marques AE, da Silva TL, Reis A (2009) Neochloris oleabundans UTEX #1185: a suitable renewable lipid source for biofuel production. J Ind Microbiol Biotechnol 36:821–826CrossRefGoogle Scholar
  202. 202.
    da Silva TL, Reis A, Medeiros R, Oliveira AC, Gouveia L (2009) Oil production towards biofuel from autotrophic microalgae semicontinuous cultivations monitorized by flow cytometry. Appl Biochem Biotechnol 159:568–578CrossRefGoogle Scholar
  203. 203.
    Brennan L, Fernandez AB, Mostaert AS, Owende P (2012) Enhancement of BODIPY505/515 lipid fluorescence method for applications in biofuel-directed microalgae production. J Microbiol Meth 90:137–143CrossRefGoogle Scholar
  204. 204.
    Guzman HM, de la Jara Valido A, Duarte LC, Presmanes KF (2011) 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 23:7–15CrossRefGoogle Scholar
  205. 205.
    Mendoza Guzman H, de la Jara Valido A, Carmona Duarte L, Freijanes Presmanes K (2010) Estimate by means of flow cytometry of variation in composition of fatty acids from Tetraselmis suecica in response to culture conditions. Aquacult Int 18:189–199CrossRefGoogle Scholar
  206. 206.
    Cooksey KE, Guckert JB, Williams SA, Callis PR (1987) Fluorometric determination of the neutral lipid content of microalgal cells using nile red. J Microbiol Meth 6:333–345CrossRefGoogle Scholar
  207. 207.
    Elsey D, Jameson D, Raleigh B, Cooney MJ (2007) Fluorescent measurement of microalgal neutral lipids. J Microbiol Meth 68:639–642CrossRefGoogle Scholar
  208. 208.
    Chen W, Zhang CW, Song LR, Sommerfeld M, Hu Q (2009) A high throughput Nile red method for quantitative measurement of neutral lipids in microalgae. J Microbiol Meth 77:41–47CrossRefGoogle Scholar
  209. 209.
    Doan T-TY, Obbard JP (2011) Improved nile red staining of Nannochloropsis sp. J Appl Phycol 23:895–901CrossRefGoogle Scholar
  210. 210.
    Broger T, Odermatt RP, Huber P, Sonnleitner B (2011) Real-time on-line flow cytometry for bioprocess monitoring. J Biotechnol 154:240–247CrossRefGoogle Scholar
  211. 211.
    Sitton G, Srienc F (2008) Mammalian cell culture scale-up and fed-batch control using automated flow cytometry. J Biotechnol 135:174–180CrossRefGoogle Scholar
  212. 212.
    Pomati F, Jokela J, Simona M, Veronesi M, Ibelings BW (2011) An automated platform for phytoplankton ecology and aquatic ecosystem monitoring. Environ Sci Technol 45:9658–9665CrossRefGoogle Scholar
  213. 213.
    Erickson RA, Jimenez R (2013) Microfluidic cytometer for high-throughput measurement of photosynthetic characteristics and lipid accumulation in individual algal cells. Lab Chip 13:2893–2901CrossRefGoogle Scholar
  214. 214.
    Huang YY, Beal CM, Cai WW, Ruoff RS, Terentjev EM (2010) Micro-Raman spectroscopy of algae: composition analysis and fluorescence background behavior. Biotechnol Bioeng 105:889–898Google Scholar
  215. 215.
    Fu D, Yu Y, Folick A, Currie E, Farese RV, Tsai TH, Xie XS, Wang MC (2014) In vivo metabolic fingerprinting of neutral lipids with hyperspectral stimulated raman scattering microscopy. J Am Chem Soc 136:8820–8828CrossRefGoogle Scholar
  216. 216.
    Parab NDT, Tomar V (2012) Raman spectroscopy of algae: a review. J Nanomedic Nanotechnol 3:131–137Google Scholar
  217. 217.
    Wei X, Jie DF, Cuello JJ, Johnson DJ, Qiu ZJ, He Y (2014) Microalgal detection by raman microspectroscopy. TrAC-Trend Anal Chem 53:33–40CrossRefGoogle Scholar
  218. 218.
    Collins AM, Jones HDT, Han DX, Hu Q, Beechem TE, Timlin JA (2011) Carotenoid distribution in living cells of Haematococcus pluvialis (Chlorophyceae). PLoS One 6:e24302CrossRefGoogle Scholar
  219. 219.
    Pilat Z, Bernatova S, Jezek J, Sery M, Samek O, Zemanek P, Nedbal L, Trtilek M (2012) Raman microspectroscopy of algal lipid bodies: beta-carotene quantification. J Appl Phycol 24:541–546CrossRefGoogle Scholar
  220. 220.
    Dementjev A, Kostkeviciene J (2013) Applying the method of Coherent Anti-stokes Raman microscopy for imaging of carotenoids in microalgae and cyanobacteria. J Raman Spectrosc 44:973–979CrossRefGoogle Scholar
  221. 221.
    Pilat Z, Bernatova S, Jezek J, Sery M, Samek O, Zemanek P, Nedbal L, Trtilek M (2011) Raman microspectroscopy of algal lipid bodies: beta-carotene as a volume sensor. In: Tomanek P, Senderakova D, Pata P (eds) Photonics, devices, and systems V, Proceedings of SPIE 8306. doi:10.1117/12.912264
  222. 222.
    Samek O, Jonas A, Pilat Z, Zemanek P, Nedbal L, Triska J, Kotas P, Trtilek M (2010) Raman microspectroscopy of individual algal cells: sensing unsaturation of storage lipids in vivo. Sensors 10:8635–8651CrossRefGoogle Scholar
  223. 223.
    Wu HW, Volponi JV, Oliver AE, Parikh AN, Simmons BA, Singh S (2011) In vivo lipidomics using single-cell Raman spectroscopy. Proc Natl Acad Sci USA 108:3809–3814CrossRefGoogle Scholar
  224. 224.
    Kaczor A, Baranska M (2011) Structural changes of carotenoid astaxanthin in a single algal cell monitored in situ by Raman spectroscopy. Anal Chem 83:7763–7770CrossRefGoogle Scholar
  225. 225.
    Davis RW, Wu HW, Singh S (2014) Multispectral sorter for rapid, nondestructive optical bioprospecting for algae biofuels. In: Farkas DL, Nicolau DV, Leif RC (eds) Imaging, manipulation, and analysis of biomolecules, cells, and tissues XII, Proceedings SPIE 8947, 89471E. doi:10.1117/12.2040538
  226. 226.
    Lee TH, Chang JS, Wang HY (2013) Rapid and in vivo quantification of cellular lipids in chlorella vulgaris using near-infrared Raman spectrometry. Anal Chem 85:2155–2160CrossRefGoogle Scholar
  227. 227.
    Oh SK, Yoo SJ, Jeong DH, Lee JM (2013) Real-time estimation of glucose concentration in algae cultivation system using Raman spectroscopy. Bioresour Technol 142:131–137CrossRefGoogle Scholar
  228. 228.
    Gao CF, Xiong W, Zhang YL, Yuan WQ, Wu QY (2008) Rapid quantitation of lipid in microalgae by time-domain nuclear magnetic resonance. J Microbiol Meth 75:437–440CrossRefGoogle Scholar
  229. 229.
    Beal CM, Webber ME, Ruoff RS, Hebner RE (2010) Lipid analysis of Neochloris oleoabundans by liquid state NMR. Biotechnol Bioeng 106:573–583CrossRefGoogle Scholar
  230. 230.
    Schor AR, Buie CR (2013) Non-invasive sorting of lipid producing microalgae with dielectrophoresis using microelectrodes. In: Proceedings of the ASME 2012 international mechanical engineering congress and exposition IMECE2012, vol 9, Pts A and B, Houston, Texas, USA, pp 701–707Google Scholar
  231. 231.
    Deng YL, Chang JS, Juang YJ (2013) Separation of microalgae with different lipid contents by dielectrophoresis. Bioresour Technol 135:137–141CrossRefGoogle Scholar
  232. 232.
    Gallo-Villanueva RC, Jesus-Perez NM, Martinez-Lopez JI, Pacheco A, Lapizco-Encinas BH (2011) Assessment of microalgae viability employing insulator-based dielectrophoresis. Microfluid Nanofluid 10:1305–1315CrossRefGoogle Scholar
  233. 233.
    Michael KA, Hiibel SR, Geiger EJ (2014) Dependence of the dielectrophoretic upper crossover frequency on the lipid content of microalgal cells. Algal Res 6:17–21CrossRefGoogle Scholar
  234. 234.
    Wu YF, Huang CJ, Wang L, Miao XL, Xing WL, Cheng J (2005) Electrokinetic system to determine differences of electrorotation and traveling-wave electrophoresis between autotrophic and heterotrophic algal cells. Colloids Surf A Physicochem Eng Aspects 262:57–64CrossRefGoogle Scholar
  235. 235.
    Sun T, Gawad S, Bernabini C, Green NG, Morgan H (2007) Broadband single cell impedance spectroscopy using maximum length sequences: theoretical analysis and practical considerations. Meas Sci Technol 18:2859–2868CrossRefGoogle Scholar
  236. 236.
    Gitelson AA, Grits YA, Etzion D, Ning Z, Richmond A (2000) Optical properties of Nannochloropsis sp. and their application to remote estimation of cell mass. Biotechnol Bioeng 69:516–525CrossRefGoogle Scholar
  237. 237.
    Flynn KJ, Davidson K, Cunningham A (1993) Relations between carbon and nitrogen during growth of Nannochloropsis oculata (Droop) Hibberd under continuous illumination. New Phytol 125:717–722CrossRefGoogle Scholar
  238. 238.
    Lubian LM, Montero O, Moreno-Garrido I, Huertas IE, Sobrino C, Gonzalez-del Valle M, Pares G (2000) Nannochloropsis (Eustigmatophyceae) as source of commercially valuable pigments. J Appl Phycol 12:249–255CrossRefGoogle Scholar
  239. 239.
    Pal D, Khozin-Goldberg I, Cohen Z, Boussiba S (2011) The effect of light, salinity, and nitrogen availability on lipid production by Nannochloropsis sp. Appl Microbiol Biotechnol 90:1429–1441CrossRefGoogle Scholar
  240. 240.
    Reichardt TA, Collins AM, Garcia OF, Ruffing AM, Jones HDT, Timlin JA (2012) Spectroradiometric monitoring of Nannochloropsis salina growth. Algal Res 1:22–31CrossRefGoogle Scholar
  241. 241.
    Ohnuki S, Nogami S, Ota S, Watanabe K, Kawano S, Ohya Y (2013) Image-Based monitoring system for green algal Haematococcus pluvialis (Chlorophyceae) cells during culture. Plant Cell Physiol 54:1917–1929CrossRefGoogle Scholar
  242. 242.
    Cordoba-Matson MV, Gutierrez J, Porta-Gandara MA (2010) Evaluation of Isochrysis galbana (clone T-ISO) cell numbers by digital image analysis of color intensity. J Appl Phycol 22:427–434CrossRefGoogle Scholar
  243. 243.
    Uyar B (2013) A novel non-invasive digital imaging method for continuous biomass monitoring and cell distribution mapping in photobioreactors. J Chem Technol Biotechnol 88:1144–1149CrossRefGoogle Scholar
  244. 244.
    Jung SK, Lee SB (2003) Image analysis of light distribution in a photobioreactor. Biotechnol Bioeng 84:394–397CrossRefGoogle Scholar
  245. 245.
    Jung SK, Lee SB (2006) In situ monitoring of cell concentration in a photobioreactor using image analysis: comparison of uniform light distribution model and artificial neural networks. Biotechnol Prog 22:1443–1450CrossRefGoogle Scholar
  246. 246.
    Song YX, Li MQ, Yang JD, Wang JS, Pan XX, Sun YQ, Li DQ (2014) Capacitive detection of living microalgae in a microfluidic chip. Sensor Actuat B-Chem 194:164–172CrossRefGoogle Scholar
  247. 247.
    Prediger A, Lindner P, Bluma A, Reardon KF, Scheper T (2013) In situ microscopy. In: Morgan PS, Rose FR, Matcher SJ (eds) Optical techniques in regenerative medicine. CRC Press, Taylor & Francis, Boca Raton, pp 114–141Google Scholar
  248. 248.
    Komives C, Parker RS (2003) Bioreactor state estimation and control. Curr Opin Biotech 14:468–474CrossRefGoogle Scholar
  249. 249.
    Odman P, Johansen CL, Olsson L, Gernaey KV, Lantz AE (2009) On-line estimation of biomass, glucose and ethanol in Saccharomyces cerevisiae cultivations using in-situ multi-wavelength fluorescence and software sensors. J Biotechnol 144:102–112CrossRefGoogle Scholar
  250. 250.
    Simutis R, Havlik I, Lubbert A (1993) Fuzzy-aided neural network for real-time state estimation and process prediction in the alcohol formation step of production-scale beer brewing. J Biotechnol 27:203–215CrossRefGoogle Scholar
  251. 251.
    Beluhan D, Beluhan S (2000) Hybrid modeling approach to on-line estimation of yeast biomass concentration in industrial bioreactor. Biotechnol Lett 22:631–635CrossRefGoogle Scholar
  252. 252.
    Zhang DM, Yan F, Sun ZL, Zhang QH, Xue SZ, Cong W (2014) On-line modeling intracellular carbon and energy metabolism of Nannochloropsis sp. in nitrogen-repletion and nitrogen-limitation cultures. Bioresour Technol 164:86–92CrossRefGoogle Scholar
  253. 253.
    Merrett MJ, Nimer NA, Dong LF (1996) The utilization of bicarbonate ions by the marine microalga Nannochloropsis oculata (Droop) Hibberd. Plant Cell Environ 19:478–484CrossRefGoogle Scholar
  254. 254.
    Su WW, Li J, Xu NS (2003) State and parameter estimation of microalgal photobioreactor cultures based on local irradiance measurement. J Biotechnol 105:165–178CrossRefGoogle Scholar
  255. 255.
    Goffaux G, Wouwer AV, Bernard O (2009) Continuous—discrete interval observers for monitoring microalgae cultures. Biotechnol Prog 25:667–675CrossRefGoogle Scholar
  256. 256.
    Obeid J, Flaus JM, Adrot O, Magnin JP, Willison JC (2010) State estimation of a batch hydrogen production process using the photosynthetic bacteria Rhodobacter capsulatus. Int J Hydrogen Energ 35:10719–10724CrossRefGoogle Scholar
  257. 257.
    Nuñez S, Garelli F, De Battista H (2012) Sliding mode observer for biomass estimation in a biohydrogen production process. Int J Hydrogen Energ 37:10089–10094CrossRefGoogle Scholar
  258. 258.
    Rocha-Cozatl E, Wouwer AV (2011) State and input estimation in phytoplanktonic cultures using quasi-unknown input observers. Chem Eng J 175:39–48CrossRefGoogle Scholar
  259. 259.
    Martin de la Cruz MC, Gonzalez Vilas L, Yarovenko N, Spyrakos E, Torres Palenzuela JM (2013) Spectral fluorescence signature techniques and absorption measurements for continuous monitoring of biofuel-producing microalgae cultures. In: Hadjimitsis DG, Themistocleous K, Michaelides S, Papadavid G (eds) First international conference on remote sensing and geoinformation of the environment (Rscy2013), Proc. SPIE 8795. doi:10.1117/12.2028345
  260. 260.
    Merzlyak MN, Chivkunova OB, Gorelova OA, Reshetnikova IV, Solovchenko AE, Khozin-Goldberg I, Cohen Z (2007) Effect of nitrogen starvation on optical properties, pigments, and arachidonic acid content of the unicellular green alga Parietochloris incisa (Trebouxiophyceae, Chlorophyta). J Phycol 43:833–843CrossRefGoogle Scholar
  261. 261.
    Solovchenko A, Merzlyak MN, Khozin-Goldberg I, Cohen Z, Boussiba S (2010) Coordinated carotenoid and lipid syntheses induced in Parietochloris incisa (Chlorophyta, Trebouxiophyceae) mutant deficient in delta 5 desaturase by nitrogen starvation and high light. J Phycol 46:763–772CrossRefGoogle Scholar
  262. 262.
    Solovchenko A, Solovchenko O, Khozin-Goldberg I, Didi-Cohen S, Pal D, Cohen Z, Boussiba S (2013) Probing the effects of high-light stress on pigment and lipid metabolism in nitrogen-starving microalgae by measuring chlorophyll fluorescence transients: studies with a delta 5 desaturase mutant of Parietochloris incisa (Chlorophyta, Trebouxiophyceae). Algal Res 2:175–182CrossRefGoogle Scholar
  263. 263.
    Mairet F, Moisan M, Bernard O (2014) Estimation of neutral lipid and carbohydrate quotas in microalgae using adaptive interval observers. Bioprocess Biosyst Eng 37:51–61CrossRefGoogle Scholar
  264. 264.
    Mairet F, Moisan M, Bernard O (2014) Interval observer with near optimal adaptation dynamics. Application to the estimation of lipid quota in microalgae. Int J Robust Nonlin 24:1142–1157CrossRefGoogle Scholar
  265. 265.
    Beutel S, Henkel S (2011) In situ sensor techniques in modern bioprocess monitoring. Appl Microbiol Biotechnol 91:1493–1505CrossRefGoogle Scholar
  266. 266.
    Meiser A, Schmid-Staiger U, Trosch W (2004) Optimization of eicosapentaenoic acid production by Phaeodactylum tricornutum in the flat panel airlift (FPA) reactor. J Appl Phycol 16:215–225CrossRefGoogle Scholar
  267. 267.
    Wu Y-H, Yu Y, Li X, Hu H-Y, Su Z-F (2012) Biomass production of a Scenedesmus sp. under phosphorous-starvation cultivation condition. Bioresour Technol 112:193–198CrossRefGoogle Scholar
  268. 268.
    Masojidek J, Koblizek M, Torzillo G (2007) Photosynthesis in Microalgae. In: Richmond A (ed) Handbook of microalgal culture: biotechnology and applied phycology. Blackwell Science, Oxford, pp 20–39Google Scholar
  269. 269.
    Ritchie RJ (2013) The use of solar radiation by the photosynthetic bacterium, Rhodopseudomonas palustris: model simulation of conditions found in a shallow pond or a flatbed reactor. Photochem Photobiol 89:1143–1162CrossRefGoogle Scholar
  270. 270.
    Guzman HM, Valido AD, Presmanes KF, Duarte LC (2012) Quick estimation of intraspecific variation of fatty acid composition in Dunaliella salina using flow cytometry and Nile Red. J Appl Phycol 24:1237–1243CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Ivo Havlik
    • 1
  • Thomas Scheper
    • 1
  • Kenneth F. Reardon
    • 2
  1. 1.Institute of Technical ChemistryLeibniz University HannoverHannoverGermany
  2. 2.Colorado State UniversityFort CollinsUSA

Personalised recommendations