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Algal Reactor Design Based on Comprehensive Modeling of Light and Mixing

  • Alexandra D. HollandEmail author
  • Joseph M. Dragavon
Chapter

Abstract

The prospect of autotrophic (or light-driven) algal biomass production as a sustainable substitute for fossil feedstocks has yet to fulfill its potential. As a likely cause, the inability to robustly account for algal biomass production rates has prevented the derivation of satisfactory mass balances for the simple parameterization of bioreactors. The methodology presented here aims at resolving this shortcoming. Treating photons as a substrate continuously fed to algae provides the grounds to define an autotrophic yield ФDW, in grams of dry weight per mole of photons absorbed, as an operating parameter. Under low irradiances, the rate of algal biomass synthesis is the product of the yield ФDW and the flux of photons absorbed by the culture, modeled using a scatter-corrected polychromatic Beer-Lambert law. This work addresses the broad misconception that Photosynthesis-Irradiance curves, or the equivalent use of specific growth rate expressions independent of the biomass concentration, can be extended to adequately model biomass production under light-limitation. Since low photon fluxes per cell maximize ФDW, the photosynthetic units mechanistic model was adapted to determine a corresponding maximum residence time under high light. Such high speeds in the photic zone, which call for fundamental changes in bioreactor design, enable the use of ФDW to describe biomass productivity under otherwise inhibitory irradiances. Nitrogen limitation-induced lipid accumulation corresponds to a photon flux excess with respect to the rate of nitrogen uptake, such that continuous lipid production can be achieved using the ФDW and nitrogen quotient parameters. Additionally, energy to photon-counts conversion factors are derived.

Keywords

Algal chemostat parameterization Algal growth autotrophic yield Continuous algal lipid production Photic zone target speed Photosynthetic units mechanistic model Scatter-corrected polychromatic Beer-Lambert law 

Abbreviations and Nomeclature

A. Abbreviations

AM

Air-mass

AU

Absorbance unit

CARPT

Computer-automated radioactive particle tracking

Chl a

Chlorophyll a

DW

Dry weight

ELT

Exponential-to-linear

LHS

Left hand side

NPQ

Non-photochemical quenching

NREL

National Renewable Energy Laboratory

PAR

Photosynthetically active radiation (400-700 nm)

PI

Photosynthesis-irradiance

PPFD

Photosynthesis photon flux density

PQ

Plastoquinone

PSI

Photosystem I

PSII

Photosystem II

PSU

Photosynthetic unit

REC

Reduced carrier

QA

Quinone A

SC

Scatter-corrected

B. Variables and Corresponding Units

a [molPSII]

Number of open of PSII centers (or oxidized)

a* [molPSII]

Number of closed of PSII centers (or reduced)

a0 [molPSII]

Total number of PSII centers

AbsRAW(λ) [AU]

Raw algal absorption at wavelength λ

AbsSC(λ) [AU]

Scatter-corrected algal absorption at wavelength λ

AbsSCATTER(λ) [AU]

Scatter contribution to algal absorption at wavelength λ

Ac [m2]

Area of the culture perpendicular to the light source

C [gDW m−3]

Algal culture biomass concentration in the bioreactor

c [m s−1]

Celerity of light

C0 [gDW m−3]

Algal culture biomass concentration at inoculation time t 0

CE, [gDW m−3]

Culture biomass concentration during spectrum acquisition

cEJ [E J−1]

Einstein-to-Joules conversion factor

CPI [gDW m−3]

Algal biomass concentration in the PI chamber

d [m]

Depth of the photic zone, where light is > 99 % I 0

EP(λ) [W m−2 nm−1]

Photon energy reported for each wavelength increment dλ

EF(x) µE gDW−1 h−1

Specific energy flux at depth x

EFT µE gDW−1 h−1

Threshold specific energy flux at onset of light limitation

ELIGHT(λ) [counts nm−1]

Light source emission spectrum at λ

FCHEM [m3 h−1]

Chemostat volumetric flow rate (bioreactor)

F [molPSII gDW−1]

Weight fraction of PSII

FIN [m3 h−1]

Inlet stream volumetric flow rate (bioreactor)

FOUT [m3 h−1]

Outlet stream volumetric flow rate (bioreactor)

FPAR [-]

Fraction of energy in the PAR region

h [SI Units]

Planck’s constant

I(x) [µE m−2 h−1]

Local PPFD at a given depth x

I0 [µE m−2 h−1] or [µE m−2 s−1]

Incident photosynthesis photon flux density (PPFD)

IABS [µE m−2 h−1]

Absorbed PPFD by the algal culture

IH [µE m−2 s−1]

Highest possible direct normal solar irradiance

IOUT [µE m−2 h−1]

PPFD transmitted through the algal culture

IT [µE m−2 s−1]

Threshold irradiance at which NPQ becomes significant

k1 [s−1]

Rate of PSII excitation

k2 [s−1]

Rate of PSII relaxation

L [m]

Depth of the culture

LE [m]

Pathlength of the light through the spectrophotometer

LPI [m]

Depth of the PI chamber

mP [µE gDW−1 h−1]

Maintenance parameter

\(\dot n(\lambda )\) [E s−1 m−2 nm−1]

Photon flux reported for each wavelength increment at λ

Na [mol−1]

Avogadro’s constant

OD [AU]

Algae culture absorbance at 680 nm

P [gDW m−2 h−1]

Algal biomass area productivity

P(λ) [cps]

Spectrometer reading (in counts per second)

PBIOREACTOR [gDW m−3 h−1]

Bioreactor productivity

Pi [gDW h−1]

Zone i contribution to the algal biomass productivity

\(P_i^V\) [gDW m−3 h−1]

Local volumetric biomass production rate in zone i

PLIGHT(λ) [nm−1]

Normalized light-source photon fraction at λ

PLIPIDS [gLIPIDS h−1]

Lipid productivity

PMAX [gDW m−2 h−1]

Maximum algal biomass area productivity (light-limited)

PSUN(λ) [nm−1]

Normalized solar spectrum photon fraction at λ

qL [-]

Fraction of open PSII centers

qN [-]

Fraction of closed PSII centers

QN [gN gDW−1]

Nitrogen weight fraction (or nitrogen quotient)

S [gS m−3]

Substrate S concentration in the bioreactor

S0 [gS m−3]

Inlet stream substrate S concentration

t [h]

Time in the light phase, truncated for duration in the dark

t [s]

Time scale for the PSU model

t0 [h]

Reference inoculation time

u [-]

PSU model integrating factor (L or S subscript indicates linear or sinusoidal trajectory submodel respectively)

VC [m3]

Culture volume in bioreactor

vT [m s−1]

Target velocity in the photic zone for near maximum ФPSII (additional L or S subscript indicates linear or sinusoidal trajectory submodel respectively)

x [m]

Distance from the light incidence surface

xT [m]

Threshold depth (onset of light limitation in poorly-mixed reactor)

YC/S [gDW gS−1]

Biomass yield on the substrate S

YC/N [gDW gN−1]

Biomass yield on nitrogen substrate

β [-]

Proportionality constant between the spectrometer count reading and the incident photon flux

λ [nm]

Wavelength

µ [h−1]

Specific growth rate

µMAX [h−1]

Maximum specific growth rate

σ [m2 gDW−1]

Monochromatic absorption cross section

σDW [m2 gDW−1]

Scatter-corrected algae-specific light source-dependent absorption cross section

τ [s]

Time for the incident light to excite half the threshold PSII fraction

ψ(λ) [m2 gDW m−2]

Hyperbolic model parameter

ω(λ) [m2 gDW−1]

Hyperbolic model parameter

ФAPP [molCO2 E−1]

Apparent efficiency parameter in mole CO2 fixed per mole incident photons

ФCO2 [molCO2 E−1]

Quantum yield

ΦDW [gDW µE−1]

Autotrophic yield

ФC2 [molOZ E−1]

Quantum yield

ФPSII [-]

Photon fraction used to excite the QA pool, or PSII operating efficiency

Notes

Acknowledgements

We would like to acknowledge Dr. Agnieszka Kawska at IlluScientia.com for help in creating the Figs. 2, 3, 13 and 14.

References

  1. Aiba S (1982) Growth kinetics of photosynthetic microorganisms. Microbial Reactions. Springer, BerlinGoogle Scholar
  2. Anon (2009) Malaysian Palm Oil Industry Performance 2008. Global oils & fats business magazine. [online] Available at: http://theoilpalm.org/magazine/. Accessed 15 Sept 2012
  3. ASTM (2003) Reference solar spectral irradiances: direct normal and hemispherical on 37° tilted surface, ASTM G173-03. [online] Available at: http://www.astm.org/DATABASE.CART/HISTORICAL/G173-03E1.htm. Accessed 15 Oct 2012
  4. Bailey Green F, Bernstone LS, Lundquist TJ, Oswald WJ (1996) Advanced integrated wastewater pond systems for nitrogen removal. Water Sci Technol 33:207–217Google Scholar
  5. Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113PubMedCrossRefGoogle Scholar
  6. Barbosa MJ, Hoogakker J, Wijffels RH (2003a) Optimisation of cultivation parameters in photobioreactors for microalgae cultivation using the A-stat technique. Biomol Eng 20:115–123CrossRefGoogle Scholar
  7. Barbosa MJ, Janssen M, Ham N, Tramper J, Wijffels RH (2003b) Microalgae cultivation in air-lift reactors: modeling biomass yield and growth rate as a function of mixing frequency. Biotechnol Bioeng 82:170–179CrossRefGoogle Scholar
  8. Barbosa MJ, Hadiyanto, Wijffels RH (2004) Overcoming shear stress of microalgae cultures in sparged photobioreactors. Biotechnol Bioeng 85:78–85PubMedCrossRefGoogle Scholar
  9. Beckmann J, Lehr F, Finazzi G, Hankamer B, Posten C, Wobbe L, Kruse O (2009) Improvement of light to biomass conversion by de-regulation of light-harvesting protein translation in Chlamydomonas reinhardtii. J Biotechnol 142:70–77PubMedCrossRefGoogle Scholar
  10. Bernard O, Gouzé J-L (1999) Non-linear qualitative signal processing for biological systems: application to the algal growth in bioreactors. Math Biosci 157:357–372PubMedCrossRefGoogle Scholar
  11. Blanch HW, Clark DS (1997) Biochemical engineering. CRC Press, USAGoogle Scholar
  12. Camacho Rubio F, García Camacho F, Fernández Sevilla JM, Chisti Y, Molina Grima E (2003) A mechanistic model of photosynthesis in microalgae. Biotechnol Bioeng 81:459–473PubMedCrossRefGoogle Scholar
  13. Campbell D, Hurry V, Clarke AK, Gustafsson P, Oquist G (1998) Chlorophyll fluorescence analysis of cyanobacterial photosynthesis and acclimation. Microbiol Mol Microbiol Rev 62:667–683Google Scholar
  14. Capo TR, Jaramillo JC, Boyd AE, Lapointe BE, Serafy JE (1999) Sustained high yields of Gracilaria (Rhodophyta) grown in intensive large-scale culture. J Appl Phycol 11:143CrossRefGoogle Scholar
  15. Cleveland JS, Perry MJ, Kiefer DA, Talbot MC (1989) Maximal quantum yield of photosynthesis in the northwestern Sargasso Sea. J Mar Res 47:869–886CrossRefGoogle Scholar
  16. Cunningham FXJ, Dennenberg RJ, Jursinic PA, Gantt E (1990) Growth under Red Light Enhances Photosystem II Relative to Photosystem I and Phycobilisomes in the Red Alga Porphyridium cruentum. Plant Physiol 93:888–895PubMedCrossRefGoogle Scholar
  17. De Wijn R, Van Gorkom HJ (2002) The rate of charge recombination in Photosystem II. Biochimica et Biophysica Acta (BBA)—Bioenergetics 1553:302–308CrossRefGoogle Scholar
  18. Divakaran R, Sivasankara Pillai VN (2002) Flocculation of algae using chitosan. J Appl Phycol 14:419–422CrossRefGoogle Scholar
  19. Droop MR (1973) Some thoughts on nutrients limitation in algae. Journal of Phycology 9:264–272Google Scholar
  20. Dubinsky Z, Falkowski PG, Wyman K (1986) Light harvesting and utilization by phytoplankton. Plant Cell Physiol 27:1335–1349Google Scholar
  21. Falkowski PG, Owens TG, Ley AC, Mauzerall DC (1981) Effects of Growth Irradiance Levels on the Ratio of Reaction Centers in Two Species of Marine Phytoplankton. Plant Physiol 68:969–973PubMedCrossRefGoogle Scholar
  22. Farnsworth RK, Thompson ES. (1982) Mean monthly, seasonal, and annual pan evaporation for the United States. NOAA technical Report NWS 34. US Department of Commerce. [pdf] Available at: www.nws.noaa.gov/oh/hdsc/PMP_related_studies/TR34.pdf Accessed 15 Oct 2012
  23. Ferrari GM, Tassan S (1999) A method using chemical oxidation to remove light absorption by phytoplankton pigments. J Phycol 35:1090–1098CrossRefGoogle Scholar
  24. Finazzi G, Rappaport F (1998) In vivo characterization of the electrochemical proton gradient generated in darkness in green algae and its kinetic effects on the cytochrome b6f complex. BioChemistry 37:9999–10005PubMedCrossRefGoogle Scholar
  25. Fischer E, Sauer U (2005) Large-scale in vivo flux analysis shows rigidity and suboptimal performance of Bacillus subtilis metabolism. Nat Genet 37:636–640PubMedCrossRefGoogle Scholar
  26. Frost-Christensen H, Sand-Jensen K (1992) The quantum efficiency of photosynthesis in macroalgae and submerged angiosperms. Oecologia 91:377–384CrossRefGoogle Scholar
  27. Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta (BBA)—General Subjects 990:87–92CrossRefGoogle Scholar
  28. Gerbens-Leenes W, Hoekstra AY, Van Der Meer TH. (2009) The water footprint of bioenergy. Proc Natl Acad Sci 106:10219–10223PubMedCrossRefGoogle Scholar
  29. Gluz MD, Merchuk JC (1996) Modified airlift reactors: The helical flow promoters. Chem Eng Sci 51:2915–2920CrossRefGoogle Scholar
  30. Golueke CG, Oswald WJ (1959) Biological conversion of light energy to the chemical energy of methane. Appl Environ Microbiol 7:219–227Google Scholar
  31. Golueke CG, Oswald WJ, Gotaas HB (1957) Anaerobic digestion of Algae. Appl Microbiol 5:47–55PubMedGoogle Scholar
  32. Gressel J (2008) Transgenics are imperative for biofuel crops. Plant Sci 174:246–263CrossRefGoogle Scholar
  33. Griffiths M, Harrison S (2009) Lipid productivity as a key characteristic for choosing algal species for biodiesel production. J Appl Phycol 21:493–507CrossRefGoogle Scholar
  34. Grobbelaar JU. (2006) Photosynthetic response and acclimation of microalgae to light fluctuations. In: Rao DVS (ed) Algal cultures analogues of blooms and applications. Science Publishers, EnfieldGoogle Scholar
  35. Grobbelaar JU, Nedbal L, Tichy V (1996) Influence of high frequency light/dark fluctuations on photosynthetic characteristics of microalgae photoacclimated to different light intensities and implications for mass algae cultivation. J Appl Phycol 8:335–343CrossRefGoogle Scholar
  36. Guckert JB, Cooksey KE (1990) Triglyceride accumulation and fatty acid profile changes in Chlorella (Chlorophyta) during high pH-induced cell cycle inhibition. J Phycol 26:72CrossRefGoogle Scholar
  37. Hall DO, Acién Fernández FG, Guerrero EC, Rao KK, Molina Grima E (2003) Outdoor helical tubular photobioreactors for microalgal production: Modeling of fluid-dynamics and mass transfer and assessment of biomass productivity. Biotechnol Bioeng 82:62–73PubMedCrossRefGoogle Scholar
  38. Holland AD, Wheeler DR (2011) Intrinsic autotrophic biomass yield and productivity in algae: Modeling spectral and mixing-rate dependence. Biotechnol J 6:584–599PubMedCrossRefGoogle Scholar
  39. Holland AD, Dragavon JM, Sigee DC (2011) Intrinsic autotrophic biomass yield and productivity in algae: Experimental methods for strain selection. Biotechnol J 6:572–583PubMedCrossRefGoogle Scholar
  40. Holmes JJ, Weger HG, Turpin DH (1989) Chlorophyll a fluorescence predicts total photosynthetic electron flow to CO2 or NO3 /NO2 under transient conditions. Plant Physiol 91:331–337PubMedCrossRefGoogle Scholar
  41. Hu D, Li M, Zhou R, Sun Y (2012) Design and optimization of photo bioreactor for O2 regulation and control by system dynamics and computer simulation. Bioresour Technol 104:608–615PubMedCrossRefGoogle Scholar
  42. Huesemann M, Hausmann T, Bartha R, Aksoy M, Weissman J, Benemann J (2009) Biomass Productivities in Wild Type and Pigment Mutant of Cyclotella sp. (Diatom). Appl Biochem Biotechnol 157:507–526PubMedCrossRefGoogle Scholar
  43. Huesemann MH, Van Wagenen J, Miller T, Chavis A, Hobbs S, Crowe B (2013) A screening model to predict microalgae biomass growth in photobioreactors and raceway ponds. Biotechnol Bioeng. doi: 10.1002/bit.24814.Google Scholar
  44. Kania S, Giacomelli G (2001) Solar radiation availability for plant growth in Arizona controlled environment agriculture systems. University of Arizona. [pdf] Available at: http://ag.arizona.edu/ceac/sites/ag.arizona.edu.ceac/files/ASP%20Steve%20Solar%20Radiation%20paper%20v.2011.pdf. Accessed 15 Oct 2012
  45. Kilham SS, Kreeger DA, Goulden CE, Lynn SG (1997) Effects of nutrient limitation on biochemical constituents of Ankistrodesmus falcatus. Freshw Biol 38:591–596CrossRefGoogle Scholar
  46. Koizumi J-I, Aiba S (1980) Significance of the estimation light-absorption rate in the analysis of growth of Rhodopseudomonas spheroides. Appl Microbiol Biotechnol 10:113–123CrossRefGoogle Scholar
  47. Kramer D, Johnson G, Kiirats O, Edwards G (2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth Res 79:209–218PubMedCrossRefGoogle Scholar
  48. Kroon BMA, Thoms S (2006) From electron to biomass: a mechanistic model to describe phytoplankton photosynthesis and steady-state growth rates. J Phycol 42:593–609CrossRefGoogle Scholar
  49. Kurane R, Takeda K, Suzuki T (1986) Screening for and characteristics of microbial flocculants. Agric Biol Chem 50:2301–2307CrossRefGoogle Scholar
  50. Lal A, Edwards GE (1995) Maximum quantum yields of O2 evolution in C4 plants under high CO2. Plant Cell Physiol 36:1311–1317Google Scholar
  51. Lansche J, Müller J (2009) Life cycle assessment of energy generation of biogas fed combined heat and power plants: environmental impact of different agricultural substrates. Eng Life Sci 12:313–320.Google Scholar
  52. Lazar D (2003) Chlorophyll a fluorescence rise induced by high light illumination of dark-adapted plant tissue studied by means of a model of photosystem II and considering photosystem II heterogeneity. J theor biol 220:469–503PubMedCrossRefGoogle Scholar
  53. Lazar D (2006) The polyphasic chlorophyll a fluorescence rise measured under high intensity of exciting light. Funct Plant Biol 33:9–30CrossRefGoogle Scholar
  54. Lazar D, Pospisil P (1999) Mathematical simulation of chlorophyll a fluorescence rise measured with 3-(3†²,4†²-dichlorophenyl)-1,1-dimethylurea-treated barley leaves at room and high temperatures. Eur Biophys J 28:468–477PubMedCrossRefGoogle Scholar
  55. Liang Y, Sarkany N, Cui Y (2009) Biomass and lipid productivities of Chlorella vulgaris under autotrophic, heterotrophic and mixotrophic growth conditions. Biotechnol Lett 31:1043–1049PubMedCrossRefGoogle Scholar
  56. Lundquist TJ, Woertz IC, Quinn NWT, Benemann JR. (2010) A realistic technology and engineering assessment of algae biofuel production. Energy Biosciences Institute. [pdf] Available at: http://www.ascension-publishing.com/BIZ/Algae-EBI.pdf. Accessed 15 Oct 2012
  57. Luo H-P, Al-Dahhan MH (2004) Analyzing and modeling of photobioreactors by combining first principles of physiology and hydrodynamics. Biotechnol Bioeng 85:382–393PubMedCrossRefGoogle Scholar
  58. Luo H-P, Al-Dahhan MH (2011) Verification and validation of CFD simulations for local flow dynamics in a draft tube airlift bioreactor. Chem Eng Sci 66:907–923CrossRefGoogle Scholar
  59. Luo H-P, Kemoun A, Al-Dahhan MH, Sevilla JMF, Sanchez JLG, Camacho FG, Molina Grima E (2003) Analysis of photobioreactors for culturing high-value microalgae and cyanobacteria via an advanced diagnostic technique: CARPT. Chem Eng Sci 58:2519–2527CrossRefGoogle Scholar
  60. Macedo MF, Ferreira JG, Duarte P (1998) Dynamic behaviour of photosynthesis-irradiance curves determined from oxygen production during variable incubation periods. Mar Ecol Prog Ser 165:31–42CrossRefGoogle Scholar
  61. Mailleret L, Gouzé J, Bernard O (2005) Nonlinear control for algae growth models in the chemostat. Bioprocess Biosyst Eng 27:319–327PubMedCrossRefGoogle Scholar
  62. Mata-Alvarez J, Macé S, Llabrés P (2000) Anaerobic digestion of organic solid wastes. an overview of research achievements and perspectives. Bioresour Technol 74:3–16CrossRefGoogle Scholar
  63. Mecherikunnel AT, Gatlin JA, Richmond JC (1983) Data on total and spectral solar irradiance. Appl Optics 22:1354–1359CrossRefGoogle Scholar
  64. Merchuk JC, Garcia-Camacho F, Molina-Grima E (2007) Photobioreactor Design and Fluid Dynamics. Chem Biochem Eng Q 21:345–355Google Scholar
  65. Molina-Grima E, Fernandez J, Acien FG, Chisti Y (2001) Tubular photobioreactor design for algal cultures. J Biotechnol 92:113–131CrossRefGoogle Scholar
  66. Möller K, Müller T 2012 Effects of anaerobic digestion on digestate nutrient availability and crop growth: a review. Eng Life Sci 12:242–257Google Scholar
  67. Mulbry W, Westhead EK, Pizarro C, Sikora L (2005) Recycling of manure nutrients: use of algal biomass from dairy manure treatment as a slow release fertilizer. Bioresour Technol 96:451–458PubMedCrossRefGoogle Scholar
  68. Nasir IM, Mohd Ghazi TI, Omar R 2012 Anaerobic digestion technology in livestock manure treatment for biogas production: a review. Eng Life Sci 12:258–269Google Scholar
  69. Nedbal L, Tichy V, Xiong F, Grobbelaar JU (1996) Microscopic green algae and cyanobacteria in high-frequency intermittent light. Journal of Applied Phycology 8:325–333CrossRefGoogle Scholar
  70. Nedbal L, Trtilek M, Kaftan D (1999) Flash fluorescence induction: a novel method to study regulation of Photosystem II. J Photochem Photobiol B: Biol 48:154–157CrossRefGoogle Scholar
  71. Oberhuber W, Edwards GE (1993) Temperature dependence of the linkage of quantum yield of Photosystem II to CO2 fixation in C4 and C3 plants. Plant Physiol 101:507–512PubMedGoogle Scholar
  72. Oh H-M, Lee SJ, Park M-H, Kim H-S, Kim H-C, Yoon J-H, Kwon G-S, Yoon B-D (2001) Harvesting of Chlorella vulgaris using a bioflocculant from Paenibacillus sp. AM49. Biotechnol Lett 23:1229–1234CrossRefGoogle Scholar
  73. Oswald WJ, Golueke CG (1960) Biological transformation of solar energy. Adv Appl Microbiol 2:223–262PubMedCrossRefGoogle Scholar
  74. Pal S, Mal D, Singh RP (2005) Cationic starch: an effective flocculating agent. Carbohydr Polym 59:417–423CrossRefGoogle Scholar
  75. Ragonese FP, Williams JA (1968) A mathematical model for the batch reactor kinetics of algae growth. Biotechnol Bioeng 10:83–88CrossRefGoogle Scholar
  76. Rebolloso-Fuentes MM, Navarro-Perez A, Garcia-Camacho F, Ramos-Miras JJ, Guil-Guerrero JL (2001) Biomass nutrient profiles of the microalga Nannochloropsis. J Agric Food Chem 49:2966–2972PubMedCrossRefGoogle Scholar
  77. Reitan KI, Rainuzzo JR, Olsen Y (1994) Effect of nutrient limitation on fatty acid and lipid content of marine microalgae. J Phycol 30:972–979CrossRefGoogle Scholar
  78. Rodolfi L, Chini Zittelli G, 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 102:100–112PubMedCrossRefGoogle Scholar
  79. Rusch KA, Malone RF (1998) Microalgal production using a hydraulically integrated serial turbidostat algal reactor (HISTAR): a conceptual model. Aquac Eng 18:251–264CrossRefGoogle Scholar
  80. Sakshaug E, Johnsen G (2006) Absorption, fluorescence, excitation and photoacclimation. In: Rao DVS (ed) Algal cultures analogues of blooms and applications. Science Publishers, EnfieldGoogle Scholar
  81. Sánchez Mirón A, Molina Grima E, Fernández Sevilla JM, Chisti Y, García Camacho F (2000) Assessment of the photosynthetically active incident radiation on outdoor photobioreactors using oxalic acid/uranyl sulfate chemical actinometer. Journal of Applied Phycology 12:385–394CrossRefGoogle Scholar
  82. Sanders R (2005) Chemical engineer John Prausnitz awarded National Medal of Science. UC Berkeley News. [online] Available at: http://berkeley.edu/news/media/releases/2005/02/16_NMS.shtml. Accessed 16 Oct 2012
  83. Schreiber U (2004) Pulse-Amplitude-Modulation (PAM) fluorometry and saturation pulse method: an overview. In: Papageorgiou G (ed) Chlorophyll a fluorescence: a signature of photosynthesis. Springer, DordrechtGoogle Scholar
  84. Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10:51–62CrossRefGoogle Scholar
  85. Sheehan J, Dunahay T, Benemann J, Roessler P (1998) A look back at the U.S. department of energy’s aquatic species program—biodiesel from algae. National Renewable Energy Laboratory. [pdf] Available at: www.nrel.gov/docs/legosti/fy98/24190.pdf. Accessed 15 Oct 2012
  86. Shifrin NS, Chisholm SW (1981) Phytoplankton lipids: interspecific differences and effects of nitrate, silicate and light-dark cycles. J Phycol 17:374–384CrossRefGoogle Scholar
  87. Surisetty K (2009) Non-linear reparameterization of complex models with applications to a microalgal heterotrophic fed-batch bioreactor. Department of Chemical and Materials Engineering. University of Alberta. [pdf] Available at: http://en.scientificcommons.org/56516812. Accessed 15 Oct 2012
  88. Takache H, Christophe G, Cornet J-F, Pruvost J (2009) Experimental and theoretical assessment of maximum productivities for the microalgae Chlamydomonas reinhardtii in two different geometries of photobioreactors. Biotechnol Prog 26:431–440Google Scholar
  89. Thomas WH, Gibson CH (1990) Effects of small-scale turbulence on microalgae. J Appl Phycol 2:71–77CrossRefGoogle Scholar
  90. Thuillier G, Hersé M, Labs D, Foujols T, Peetermans W, Gillotay D, Simon PC, Mandel H (2003) The Solar Spectral Irradiance from 200 to 2400 nm as Measured by the SOLSPEC Spectrometer from the Atlas and Eureca Missions. Solar Physics 214:1–22CrossRefGoogle Scholar
  91. Tornabene TG (1983) Lipid composition of the nitrogen starved green alga Neochloris oleoabundans. Enzym Microb Technol 5:435–440CrossRefGoogle Scholar
  92. Van Wagenen J, Miller TW, Hobbs S, Hook P, Crowe B, Huesemann M (2012) Effects of light and temperature on fatty acid production in Nannochloropsis salina. Energies 5:731–740CrossRefGoogle Scholar
  93. Vunjak-Novakovic G, Kim Y, Wu X, Berzin I, Merchuk JC (2005) Air-lift bioreactors for algal growth on flue gas: Mathematical modeling and pilot-plant studies. Ind Eng Chem Res 44:6154–6163CrossRefGoogle Scholar
  94. Welschmeyer NA, Lorenzen CJ (1981) Chlorophyll-specific photosynthesis and quantum efficiency at subsaturating light intensities. J Phycol 17:283–293CrossRefGoogle Scholar
  95. Wilhelm C, Jakob T (2011) From photons to biomass and biofuels: evaluation of different strategies for the improvement of algal biotechnology based on comparative energy balances. Appl Microbiol and Biotechnol 92:909–919Google Scholar
  96. Wilkie AC, Mulbry WW (2002) Recovery of dairy manure nutrients by benthic freshwater algae. Bioresour Technol 84:81–91PubMedCrossRefGoogle Scholar
  97. Wong WW, Tran LM, Liao JC (2009) A hidden square-root boundary between growth rate and biomass yield. Biotechnol Bioeng 102:73–80PubMedCrossRefGoogle Scholar
  98. Wu X, Merchuk JC (2001) A model integrating fluid dynamics in photosynthesis and photoinhibition processes. Chem Eng Sci 56:3527–3538CrossRefGoogle Scholar
  99. Xu H, Miao X, Wu Q (2006) High quality biodiesel production from a microalga Chlorella protothecoides by heterotrophic growth in fermenters. J Biotechnol 126:499PubMedCrossRefGoogle Scholar
  100. Yamanè T, Shimizu S (1984) Fed-batch techniques in microbial processes. Bioprocess Parameter Control 30:147–194CrossRefGoogle Scholar
  101. Yang J, Xu M, Zhang X, Hu Q, Sommerfeld M, Chen Y (2010) Life-cycle analysis on biodiesel production from microalgae: Water footprint and nutrients balance. Bioresour Technol 102:159–165PubMedCrossRefGoogle Scholar
  102. Yun Y-S, Park JM (2003) Kinetic modeling of the light-dependent photosynthetic activity of the green microalga Chlorella vulgaris. Biotechnol Bioeng 83:303–311PubMedCrossRefGoogle Scholar
  103. Yun YS, Park JM (2001) Attenuation of monochromatic and polychromatic lights in Chlorella vulgaris suspensions. Appl Microbiol Biotechnol 55:765–770PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  1. 1.2 Les LétumièresMoussonvilliersFrance

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