Abstract

This study presents experimental measurements of the absorption and scattering cross sections and the spectral complex index of refraction of filamentous cyanobacteria. Filamentous heterocystous cyanobacterium Anabaena cylindrica was chosen as a model organism. Its filaments consisted of long chains of polydisperse cells. Their average mass scattering and absorption cross sections were measured from 400 to 750 nm at four different times during their batch growth in medium BG-11(-N) under 3000 lux of white fluorescent light. The effective real (or refraction index) and imaginary (or absorption index) parts of the complex index of refraction were retrieved using an inverse method based on a genetic algorithm. The microorganisms were modeled as infinitely long and randomly oriented volume-equivalent cylinders. The absorption index featured peaks corresponding to chlorophyll a (Chl a) at 436 and 676 nm and phycocyanin (PCCN) at 630 nm and a shoulder around 480 nm, corresponding to photoprotective carotenoids. The absorption peaks of Chl a and PCCN concentrations increased and the shoulder due to carotenoids decreased in response to photolimitation caused by biomass growth. Subsequent nitrogen limitation caused the PCCN absorption peak to decrease significantly due to degradation of PCCN as an endogenous source of nitrogen for nitrogenase maintenance and synthesis, as confirmed by increasing heterocyst differentiation. The results can be used for predicting and optimizing light transfer in photobioreactors for wastewater treatment and ammonia or biofuel production.

© 2014 Optical Society of America

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2013 (3)

E. Lee, R.-L. Heng, and L. Pilon, “Spectral optical properties of selected photosynthetic microalgae producing biofuels,” J. Quant. Spectrosc. Radiat. Transfer 114, 112–135 (2013).

R. Kandilian, E. Lee, and L. Pilon, “Radiation and optical properties of Nannochloropsis oculata grown under different irradiances and spectra,” Bioresour. Technol. 137, 63–73 (2013).
[Crossref]

E. Lee and L. Pilon, “Light scattering by long and randomly oriented linear chains of spheres,” J. Opt. Soc. Am. A 30, 1892–1900 (2013).
[Crossref]

2011 (4)

O. Zhernovaya, O. Sydoruk, V. Tuchin, and A. Douplik, “The refractive index of human hemoglobin in the visible range,” Phys. Med. Biol. 56, 4013–4021 (2011).
[Crossref]

P. M. Slegers, R. H. Wijffels, G. van Straten, and A. J. B. van Boxtel, “Design scenarios for flat panel photobioreactors,” Appl. Energy 88, 3342–3353 (2011).
[Crossref]

L. Pilon, H. Berberoğlu, and R. Kandilian, “Radiation transfer in photobiological carbon dioxide fixation and fuel production by microalgae,” J. Quant. Spectrosc. Radiat. Transfer 112, 2639–2660 (2011).
[Crossref]

M. J. Griffiths, C. Garcin, R. P. van Hille, and S. T. Harrison, “Interference by pigment in the estimation of microalgal biomass concentration by optical density,” J. Microbiol. Methods 85, 119–123 (2011).
[Crossref]

2010 (1)

P. J. l. B. Williams and L. M. L. Laurens, “Microalgae as biodiesel and biomass feedstocks: review and analysis of the biochemistry, energetics and economics,” Energ. Environ. Sci. 3, 554–590 (2010).
[Crossref]

2009 (2)

Z. Dubinsky and N. Stambler, “Photoacclimation processes in phytoplankton: mechanisms, consequences, and applications,” Aquat. Microb. Ecol. 56, 163–176 (2009).
[Crossref]

H. Berberoğlu, P. S. Gomez, and L. Pilon, “Radiation characteristics of Botryococcus braunii, Chlorococcum littorale, and Chlorella sp. used for CO2 fixation and biofuel production,” J. Quant. Spectrosc. Radiat. Transfer 110, 1879–1893 (2009).
[Crossref]

2008 (1)

H. Berberoğlu, L. Pilon, and A. Melis, “Radiation characteristics of Chlamydomonas reinhardtii CC125 and its truncated chlorophyll antenna transformants tla1, tlaX, and tla1-CW+,” Int. J. Hydrogen Energy 33, 6467–6483 (2008).
[Crossref]

2007 (3)

H. Berberoğlu and L. Pilon, “Experimental measurement of the radiation characteristics of Anabaena variabilis ATCC 29413-U and Rhodobacter sphaeroides ATCC 49419,” Int. J. Hydrogen Energy 32, 4772–4785 (2007).
[Crossref]

Y. Chisti, “Biodiesel from microalgae,” Biotechnol. Adv. 25, 294–306 (2007).
[Crossref]

R. Kitamura, L. Pilon, and M. Jonasz, “Optical constants of silica glass from extreme ultraviolet to far infrared at near room temperature,” Appl. Opt. 46, 8118–8133 (2007).
[Crossref]

2005 (1)

L. Pottier, J. Pruvost, J. Deremetz, J. F. Cornet, J. Legrand, and C. G. Dussap, “A fully predictive model for one-dimensional light attenuation by Chlamydomonas reinhardtii in a torous photobioreactor,” Biotechnol. Bioeng. 91, 569–582 (2005).
[Crossref]

2004 (1)

A. Quirantes and S. Bernard, “Light scattering by marine algae: two-layer spherical and nonspherical models,” J. Quant. Spectrosc. Radiat. Transfer 89, 311–321 (2004).
[Crossref]

2001 (1)

D. Das and T. N. Veziroğlu, “Hydrogen production by biological processes: a survey of literature,” Int. J. Hydrogen Energy 26, 13–28 (2001).
[Crossref]

1999 (1)

D. C. Sigee, J. Teper, and E. Levado, “Elemental composition of the cyanobacterium Anabaena flos-aquae collected from different depths within a stratified lake,” Eur. J. Phycol. 34, 477–485 (1999).
[Crossref]

1997 (1)

D. Stramski and C. D. Mobley, “Effect of microbial particles on oceanic optics: a database of single-particle optical properties,” Limnol. Oceanogr. 42, 538–549 (1997).
[Crossref]

1992 (1)

J.-F. Cornet, C. G. Dussap, and G. Dubertret, “A structured model for simulation of cultures of the cyanobacterium Spirulina platensis in photobioreactors: I. Coupling between light transfer and growth kinetics,” Biotechnol. Bioeng. 40, 817–825 (1992).
[Crossref]

1991 (1)

P. G. Falkowski and J. LaRoche, “Acclimation to spectral irradiance in algae,” J. Phycol. 27, 8–14 (1991).
[Crossref]

1990 (1)

R. Bidigare, M. Ondrusek, J. Morrow, and D. Kiefer, “In vivo absorption properties of algal pigments,” Proc. SPIE 1302, 290–302 (1990).
[Crossref]

1987 (1)

I. Canto de Loura, J. P. Dubacq, and J. C. Thomas, “The effects of nitrogen deficiency on pigments and lipids of cyanobacteria,” Plant Physiol. 83, 838–843 (1987).
[Crossref]

1986 (2)

P. A. Roger, A. Tirol, S. Ardales, and I. Watanabe, “Chemical composition of cultures and natural samples of N2-fixing blue-green algae from rice fields,” Biol. Fertil. Soils 2, 131–146 (1986).

A. Morel and A. Bricaud, “Inherent optical properties of algal cells including picoplankton: theoretical and experimental results,” Can. Bull. Fish. Aquat. Sci. 214, 521–560 (1986).

1983 (1)

R. J. Davies-Colley, R. D. Pridmore, and J. E. Hewitt, “Optical properties and reflectance spectra of 3 shallow lakes obtained from a spectrophotometric study,” New Zeal. J. Mar. Freshwater Res. 17, 445–459 (1983).
[Crossref]

1980 (1)

M. M. Allen and F. Hutchison, “Nitrogen limitation and recovery in the cyanobacterium Aphanocapsa 6308,” Arch. Microbiol. 128, 1–7 (1980).
[Crossref]

1979 (1)

J. R. Benemann, “Production of nitrogen fertilizer with nitrogen-fixing blue-green algae,” Enzyme Microb. Technol. 1, 83–90 (1979).
[Crossref]

1978 (1)

K. G. Privoznik, K. J. Daniel, and F. P. Incropera, “Absorption, extinction and phase function measurements for algal suspensions of Chlorella pyrenoidosa,” J. Quant. Spectrosc. Radiat. Transfer 20, 345–352 (1978).
[Crossref]

1977 (1)

M. J. Griffiths and S. Harrison, “Lipid productivity as a key characteristic for choosing algal species for biodiesel production,” Appl. Environ. Microbiol. 33, 123–131 (1977).

1975 (1)

W. D. P. Stewart and P. Rowell, “Effects of l-methionine-dl-sulphoximine on the assimilation of newly fixed NH3, acetylene reduction and heterocyst production in Anabaena cylindrica,” Biochem. Biophys. Res. Commun. 65, 846–856 (1975).
[Crossref]

1974 (1)

L. Vasconcelos and P. Fay, “Nitrogen metabolism and ultrastructure in Anabaena cylindrica,” Arch. Microbiol. 96, 271–279 (1974).
[Crossref]

1973 (1)

N. M. Weare and J. R. Benemann, “Nitrogen fixation by Anabaena cylindrica,” Arch. Microbiol. 90, 323–332 (1973).

1970 (1)

P. Fay, “Photostimulation of nitrogen fixation in Anabaena cylindrica,” Biochim. Biophys. Acta. Bioenerg. 216, 353–356 (1970).
[Crossref]

1969 (3)

P. Fay, “Cell differentiation and pigment composition in Anabaena cylindrica,” Arch. Microbiol. 67, 62–70 (1969).

C. P. Wolk and R. D. Simon, “Pigments and lipids of heterocysts,” Planta 86, 92–97 (1969).
[Crossref]

M. M. Allen and A. J. Smith, “Nitrogen chlorosis in blue-green algae,” Arch. Microbiol. 69, 114–120 (1969).

1967 (1)

P. F. Brownell and D. J. D. Nicholas, “Some effects of sodium on nitrate assimilation and N2 fixation in Anabaena cylindrica,” Plant Physiol. 42, 915–921 (1967).
[Crossref]

1965 (1)

1961 (1)

T. R. Parsons, K. Stephens, and J. D. H. Strickland, “On the chemical composition of eleven species of marine phytoplanktons,” J. Fish. Res. Board Can. 18, 1001–1016 (1961).
[Crossref]

Allen, M. M.

M. M. Allen and F. Hutchison, “Nitrogen limitation and recovery in the cyanobacterium Aphanocapsa 6308,” Arch. Microbiol. 128, 1–7 (1980).
[Crossref]

M. M. Allen and A. J. Smith, “Nitrogen chlorosis in blue-green algae,” Arch. Microbiol. 69, 114–120 (1969).

Ardales, S.

P. A. Roger, A. Tirol, S. Ardales, and I. Watanabe, “Chemical composition of cultures and natural samples of N2-fixing blue-green algae from rice fields,” Biol. Fertil. Soils 2, 131–146 (1986).

Benemann, J. R.

J. R. Benemann, “Production of nitrogen fertilizer with nitrogen-fixing blue-green algae,” Enzyme Microb. Technol. 1, 83–90 (1979).
[Crossref]

N. M. Weare and J. R. Benemann, “Nitrogen fixation by Anabaena cylindrica,” Arch. Microbiol. 90, 323–332 (1973).

Berberoglu, H.

L. Pilon, H. Berberoğlu, and R. Kandilian, “Radiation transfer in photobiological carbon dioxide fixation and fuel production by microalgae,” J. Quant. Spectrosc. Radiat. Transfer 112, 2639–2660 (2011).
[Crossref]

H. Berberoğlu, P. S. Gomez, and L. Pilon, “Radiation characteristics of Botryococcus braunii, Chlorococcum littorale, and Chlorella sp. used for CO2 fixation and biofuel production,” J. Quant. Spectrosc. Radiat. Transfer 110, 1879–1893 (2009).
[Crossref]

H. Berberoğlu, L. Pilon, and A. Melis, “Radiation characteristics of Chlamydomonas reinhardtii CC125 and its truncated chlorophyll antenna transformants tla1, tlaX, and tla1-CW+,” Int. J. Hydrogen Energy 33, 6467–6483 (2008).
[Crossref]

H. Berberoğlu and L. Pilon, “Experimental measurement of the radiation characteristics of Anabaena variabilis ATCC 29413-U and Rhodobacter sphaeroides ATCC 49419,” Int. J. Hydrogen Energy 32, 4772–4785 (2007).
[Crossref]

Bernard, S.

A. Quirantes and S. Bernard, “Light scattering by marine algae: two-layer spherical and nonspherical models,” J. Quant. Spectrosc. Radiat. Transfer 89, 311–321 (2004).
[Crossref]

Bidigare, R.

R. Bidigare, M. Ondrusek, J. Morrow, and D. Kiefer, “In vivo absorption properties of algal pigments,” Proc. SPIE 1302, 290–302 (1990).
[Crossref]

Bohren, C. F.

C. F. Bohren and D. R. Huffman, Absorption and Scattering of Light by Small Particles (Wiley, 1998).

Bricaud, A.

A. Morel and A. Bricaud, “Inherent optical properties of algal cells including picoplankton: theoretical and experimental results,” Can. Bull. Fish. Aquat. Sci. 214, 521–560 (1986).

Brownell, P. F.

P. F. Brownell and D. J. D. Nicholas, “Some effects of sodium on nitrate assimilation and N2 fixation in Anabaena cylindrica,” Plant Physiol. 42, 915–921 (1967).
[Crossref]

Canto de Loura, I.

I. Canto de Loura, J. P. Dubacq, and J. C. Thomas, “The effects of nitrogen deficiency on pigments and lipids of cyanobacteria,” Plant Physiol. 83, 838–843 (1987).
[Crossref]

Charbonneau, P.

P. Charbonneau and B. Knapp, “A user’s guide to PIKAIA 1.0,” (National Center for Atmospheric Research, 1995).

Chisti, Y.

Y. Chisti, “Biodiesel from microalgae,” Biotechnol. Adv. 25, 294–306 (2007).
[Crossref]

Cornet, J. F.

L. Pottier, J. Pruvost, J. Deremetz, J. F. Cornet, J. Legrand, and C. G. Dussap, “A fully predictive model for one-dimensional light attenuation by Chlamydomonas reinhardtii in a torous photobioreactor,” Biotechnol. Bioeng. 91, 569–582 (2005).
[Crossref]

Cornet, J.-F.

J.-F. Cornet, C. G. Dussap, and G. Dubertret, “A structured model for simulation of cultures of the cyanobacterium Spirulina platensis in photobioreactors: I. Coupling between light transfer and growth kinetics,” Biotechnol. Bioeng. 40, 817–825 (1992).
[Crossref]

Daniel, K. J.

K. G. Privoznik, K. J. Daniel, and F. P. Incropera, “Absorption, extinction and phase function measurements for algal suspensions of Chlorella pyrenoidosa,” J. Quant. Spectrosc. Radiat. Transfer 20, 345–352 (1978).
[Crossref]

Das, D.

D. Das and T. N. Veziroğlu, “Hydrogen production by biological processes: a survey of literature,” Int. J. Hydrogen Energy 26, 13–28 (2001).
[Crossref]

Dauchet, J.

J. Dauchet, “Analyse Radiative des Photobioréacteurs,” Ph.D. dissertation, (Université Blaise Pascal, Clermont Ferrand II, France, 2012).

Davies-Colley, R. J.

R. J. Davies-Colley, R. D. Pridmore, and J. E. Hewitt, “Optical properties and reflectance spectra of 3 shallow lakes obtained from a spectrophotometric study,” New Zeal. J. Mar. Freshwater Res. 17, 445–459 (1983).
[Crossref]

Deremetz, J.

L. Pottier, J. Pruvost, J. Deremetz, J. F. Cornet, J. Legrand, and C. G. Dussap, “A fully predictive model for one-dimensional light attenuation by Chlamydomonas reinhardtii in a torous photobioreactor,” Biotechnol. Bioeng. 91, 569–582 (2005).
[Crossref]

Douplik, A.

O. Zhernovaya, O. Sydoruk, V. Tuchin, and A. Douplik, “The refractive index of human hemoglobin in the visible range,” Phys. Med. Biol. 56, 4013–4021 (2011).
[Crossref]

Dubacq, J. P.

I. Canto de Loura, J. P. Dubacq, and J. C. Thomas, “The effects of nitrogen deficiency on pigments and lipids of cyanobacteria,” Plant Physiol. 83, 838–843 (1987).
[Crossref]

Dubertret, G.

J.-F. Cornet, C. G. Dussap, and G. Dubertret, “A structured model for simulation of cultures of the cyanobacterium Spirulina platensis in photobioreactors: I. Coupling between light transfer and growth kinetics,” Biotechnol. Bioeng. 40, 817–825 (1992).
[Crossref]

Dubinsky, Z.

Z. Dubinsky and N. Stambler, “Photoacclimation processes in phytoplankton: mechanisms, consequences, and applications,” Aquat. Microb. Ecol. 56, 163–176 (2009).
[Crossref]

Dussap, C. G.

L. Pottier, J. Pruvost, J. Deremetz, J. F. Cornet, J. Legrand, and C. G. Dussap, “A fully predictive model for one-dimensional light attenuation by Chlamydomonas reinhardtii in a torous photobioreactor,” Biotechnol. Bioeng. 91, 569–582 (2005).
[Crossref]

J.-F. Cornet, C. G. Dussap, and G. Dubertret, “A structured model for simulation of cultures of the cyanobacterium Spirulina platensis in photobioreactors: I. Coupling between light transfer and growth kinetics,” Biotechnol. Bioeng. 40, 817–825 (1992).
[Crossref]

Falkowski, P. G.

P. G. Falkowski and J. LaRoche, “Acclimation to spectral irradiance in algae,” J. Phycol. 27, 8–14 (1991).
[Crossref]

Fay, P.

L. Vasconcelos and P. Fay, “Nitrogen metabolism and ultrastructure in Anabaena cylindrica,” Arch. Microbiol. 96, 271–279 (1974).
[Crossref]

P. Fay, “Photostimulation of nitrogen fixation in Anabaena cylindrica,” Biochim. Biophys. Acta. Bioenerg. 216, 353–356 (1970).
[Crossref]

P. Fay, “Cell differentiation and pigment composition in Anabaena cylindrica,” Arch. Microbiol. 67, 62–70 (1969).

Fournier, G. R.

M. Jonasz and G. R. Fournier, Light Scattering by Particles in Water: Theoretical and Experimental Foundations (Academic, 2007).

Garcin, C.

M. J. Griffiths, C. Garcin, R. P. van Hille, and S. T. Harrison, “Interference by pigment in the estimation of microalgal biomass concentration by optical density,” J. Microbiol. Methods 85, 119–123 (2011).
[Crossref]

Gomez, P. S.

H. Berberoğlu, P. S. Gomez, and L. Pilon, “Radiation characteristics of Botryococcus braunii, Chlorococcum littorale, and Chlorella sp. used for CO2 fixation and biofuel production,” J. Quant. Spectrosc. Radiat. Transfer 110, 1879–1893 (2009).
[Crossref]

Griffiths, M. J.

M. J. Griffiths, C. Garcin, R. P. van Hille, and S. T. Harrison, “Interference by pigment in the estimation of microalgal biomass concentration by optical density,” J. Microbiol. Methods 85, 119–123 (2011).
[Crossref]

M. J. Griffiths and S. Harrison, “Lipid productivity as a key characteristic for choosing algal species for biodiesel production,” Appl. Environ. Microbiol. 33, 123–131 (1977).

Harrison, S.

M. J. Griffiths and S. Harrison, “Lipid productivity as a key characteristic for choosing algal species for biodiesel production,” Appl. Environ. Microbiol. 33, 123–131 (1977).

Harrison, S. T.

M. J. Griffiths, C. Garcin, R. P. van Hille, and S. T. Harrison, “Interference by pigment in the estimation of microalgal biomass concentration by optical density,” J. Microbiol. Methods 85, 119–123 (2011).
[Crossref]

Heng, R.-L.

E. Lee, R.-L. Heng, and L. Pilon, “Spectral optical properties of selected photosynthetic microalgae producing biofuels,” J. Quant. Spectrosc. Radiat. Transfer 114, 112–135 (2013).

Hewitt, J. E.

R. J. Davies-Colley, R. D. Pridmore, and J. E. Hewitt, “Optical properties and reflectance spectra of 3 shallow lakes obtained from a spectrophotometric study,” New Zeal. J. Mar. Freshwater Res. 17, 445–459 (1983).
[Crossref]

Huffman, D. R.

C. F. Bohren and D. R. Huffman, Absorption and Scattering of Light by Small Particles (Wiley, 1998).

Hutchison, F.

M. M. Allen and F. Hutchison, “Nitrogen limitation and recovery in the cyanobacterium Aphanocapsa 6308,” Arch. Microbiol. 128, 1–7 (1980).
[Crossref]

Incropera, F. P.

K. G. Privoznik, K. J. Daniel, and F. P. Incropera, “Absorption, extinction and phase function measurements for algal suspensions of Chlorella pyrenoidosa,” J. Quant. Spectrosc. Radiat. Transfer 20, 345–352 (1978).
[Crossref]

Jonasz, M.

R. Kitamura, L. Pilon, and M. Jonasz, “Optical constants of silica glass from extreme ultraviolet to far infrared at near room temperature,” Appl. Opt. 46, 8118–8133 (2007).
[Crossref]

M. Jonasz and G. R. Fournier, Light Scattering by Particles in Water: Theoretical and Experimental Foundations (Academic, 2007).

Kandilian, R.

R. Kandilian, E. Lee, and L. Pilon, “Radiation and optical properties of Nannochloropsis oculata grown under different irradiances and spectra,” Bioresour. Technol. 137, 63–73 (2013).
[Crossref]

L. Pilon, H. Berberoğlu, and R. Kandilian, “Radiation transfer in photobiological carbon dioxide fixation and fuel production by microalgae,” J. Quant. Spectrosc. Radiat. Transfer 112, 2639–2660 (2011).
[Crossref]

Ke, B.

B. Ke, Photosynthesis, Photobiochemistry and Photobiophysics (Kluwer Academic, 2001).

Kerker, M.

M. Kerker, The Scattering of Light, and Other Electromagnetic Radiation (Academic, 1969).

Kiefer, D.

R. Bidigare, M. Ondrusek, J. Morrow, and D. Kiefer, “In vivo absorption properties of algal pigments,” Proc. SPIE 1302, 290–302 (1990).
[Crossref]

Kitamura, R.

Knapp, B.

P. Charbonneau and B. Knapp, “A user’s guide to PIKAIA 1.0,” (National Center for Atmospheric Research, 1995).

LaRoche, J.

P. G. Falkowski and J. LaRoche, “Acclimation to spectral irradiance in algae,” J. Phycol. 27, 8–14 (1991).
[Crossref]

Laurens, L. M. L.

P. J. l. B. Williams and L. M. L. Laurens, “Microalgae as biodiesel and biomass feedstocks: review and analysis of the biochemistry, energetics and economics,” Energ. Environ. Sci. 3, 554–590 (2010).
[Crossref]

Lee, E.

E. Lee, R.-L. Heng, and L. Pilon, “Spectral optical properties of selected photosynthetic microalgae producing biofuels,” J. Quant. Spectrosc. Radiat. Transfer 114, 112–135 (2013).

E. Lee and L. Pilon, “Light scattering by long and randomly oriented linear chains of spheres,” J. Opt. Soc. Am. A 30, 1892–1900 (2013).
[Crossref]

R. Kandilian, E. Lee, and L. Pilon, “Radiation and optical properties of Nannochloropsis oculata grown under different irradiances and spectra,” Bioresour. Technol. 137, 63–73 (2013).
[Crossref]

Legrand, J.

L. Pottier, J. Pruvost, J. Deremetz, J. F. Cornet, J. Legrand, and C. G. Dussap, “A fully predictive model for one-dimensional light attenuation by Chlamydomonas reinhardtii in a torous photobioreactor,” Biotechnol. Bioeng. 91, 569–582 (2005).
[Crossref]

Levado, E.

D. C. Sigee, J. Teper, and E. Levado, “Elemental composition of the cyanobacterium Anabaena flos-aquae collected from different depths within a stratified lake,” Eur. J. Phycol. 34, 477–485 (1999).
[Crossref]

Malitson, I. H.

Melis, A.

H. Berberoğlu, L. Pilon, and A. Melis, “Radiation characteristics of Chlamydomonas reinhardtii CC125 and its truncated chlorophyll antenna transformants tla1, tlaX, and tla1-CW+,” Int. J. Hydrogen Energy 33, 6467–6483 (2008).
[Crossref]

Mobley, C. D.

D. Stramski and C. D. Mobley, “Effect of microbial particles on oceanic optics: a database of single-particle optical properties,” Limnol. Oceanogr. 42, 538–549 (1997).
[Crossref]

Modest, M. F.

M. F. Modest, Radiative Heat Transfer, 2nd edition (Academic, 2003).

Morel, A.

A. Morel and A. Bricaud, “Inherent optical properties of algal cells including picoplankton: theoretical and experimental results,” Can. Bull. Fish. Aquat. Sci. 214, 521–560 (1986).

Morrow, J.

R. Bidigare, M. Ondrusek, J. Morrow, and D. Kiefer, “In vivo absorption properties of algal pigments,” Proc. SPIE 1302, 290–302 (1990).
[Crossref]

Nicholas, D. J. D.

P. F. Brownell and D. J. D. Nicholas, “Some effects of sodium on nitrate assimilation and N2 fixation in Anabaena cylindrica,” Plant Physiol. 42, 915–921 (1967).
[Crossref]

Ondrusek, M.

R. Bidigare, M. Ondrusek, J. Morrow, and D. Kiefer, “In vivo absorption properties of algal pigments,” Proc. SPIE 1302, 290–302 (1990).
[Crossref]

Parsons, T. R.

T. R. Parsons, K. Stephens, and J. D. H. Strickland, “On the chemical composition of eleven species of marine phytoplanktons,” J. Fish. Res. Board Can. 18, 1001–1016 (1961).
[Crossref]

Pilon, L.

E. Lee and L. Pilon, “Light scattering by long and randomly oriented linear chains of spheres,” J. Opt. Soc. Am. A 30, 1892–1900 (2013).
[Crossref]

R. Kandilian, E. Lee, and L. Pilon, “Radiation and optical properties of Nannochloropsis oculata grown under different irradiances and spectra,” Bioresour. Technol. 137, 63–73 (2013).
[Crossref]

E. Lee, R.-L. Heng, and L. Pilon, “Spectral optical properties of selected photosynthetic microalgae producing biofuels,” J. Quant. Spectrosc. Radiat. Transfer 114, 112–135 (2013).

L. Pilon, H. Berberoğlu, and R. Kandilian, “Radiation transfer in photobiological carbon dioxide fixation and fuel production by microalgae,” J. Quant. Spectrosc. Radiat. Transfer 112, 2639–2660 (2011).
[Crossref]

H. Berberoğlu, P. S. Gomez, and L. Pilon, “Radiation characteristics of Botryococcus braunii, Chlorococcum littorale, and Chlorella sp. used for CO2 fixation and biofuel production,” J. Quant. Spectrosc. Radiat. Transfer 110, 1879–1893 (2009).
[Crossref]

H. Berberoğlu, L. Pilon, and A. Melis, “Radiation characteristics of Chlamydomonas reinhardtii CC125 and its truncated chlorophyll antenna transformants tla1, tlaX, and tla1-CW+,” Int. J. Hydrogen Energy 33, 6467–6483 (2008).
[Crossref]

H. Berberoğlu and L. Pilon, “Experimental measurement of the radiation characteristics of Anabaena variabilis ATCC 29413-U and Rhodobacter sphaeroides ATCC 49419,” Int. J. Hydrogen Energy 32, 4772–4785 (2007).
[Crossref]

R. Kitamura, L. Pilon, and M. Jonasz, “Optical constants of silica glass from extreme ultraviolet to far infrared at near room temperature,” Appl. Opt. 46, 8118–8133 (2007).
[Crossref]

Pottier, L.

L. Pottier, J. Pruvost, J. Deremetz, J. F. Cornet, J. Legrand, and C. G. Dussap, “A fully predictive model for one-dimensional light attenuation by Chlamydomonas reinhardtii in a torous photobioreactor,” Biotechnol. Bioeng. 91, 569–582 (2005).
[Crossref]

Pridmore, R. D.

R. J. Davies-Colley, R. D. Pridmore, and J. E. Hewitt, “Optical properties and reflectance spectra of 3 shallow lakes obtained from a spectrophotometric study,” New Zeal. J. Mar. Freshwater Res. 17, 445–459 (1983).
[Crossref]

Privoznik, K. G.

K. G. Privoznik, K. J. Daniel, and F. P. Incropera, “Absorption, extinction and phase function measurements for algal suspensions of Chlorella pyrenoidosa,” J. Quant. Spectrosc. Radiat. Transfer 20, 345–352 (1978).
[Crossref]

Pruvost, J.

L. Pottier, J. Pruvost, J. Deremetz, J. F. Cornet, J. Legrand, and C. G. Dussap, “A fully predictive model for one-dimensional light attenuation by Chlamydomonas reinhardtii in a torous photobioreactor,” Biotechnol. Bioeng. 91, 569–582 (2005).
[Crossref]

Quirantes, A.

A. Quirantes and S. Bernard, “Light scattering by marine algae: two-layer spherical and nonspherical models,” J. Quant. Spectrosc. Radiat. Transfer 89, 311–321 (2004).
[Crossref]

Richmond, A.

A. Richmond, Handbook of Microalgal Culture (Blackwell Science, 2004).

Roger, P. A.

P. A. Roger, A. Tirol, S. Ardales, and I. Watanabe, “Chemical composition of cultures and natural samples of N2-fixing blue-green algae from rice fields,” Biol. Fertil. Soils 2, 131–146 (1986).

Rowell, P.

W. D. P. Stewart and P. Rowell, “Effects of l-methionine-dl-sulphoximine on the assimilation of newly fixed NH3, acetylene reduction and heterocyst production in Anabaena cylindrica,” Biochem. Biophys. Res. Commun. 65, 846–856 (1975).
[Crossref]

Sigee, D. C.

D. C. Sigee, J. Teper, and E. Levado, “Elemental composition of the cyanobacterium Anabaena flos-aquae collected from different depths within a stratified lake,” Eur. J. Phycol. 34, 477–485 (1999).
[Crossref]

Simon, R. D.

C. P. Wolk and R. D. Simon, “Pigments and lipids of heterocysts,” Planta 86, 92–97 (1969).
[Crossref]

Slegers, P. M.

P. M. Slegers, R. H. Wijffels, G. van Straten, and A. J. B. van Boxtel, “Design scenarios for flat panel photobioreactors,” Appl. Energy 88, 3342–3353 (2011).
[Crossref]

Smith, A. J.

M. M. Allen and A. J. Smith, “Nitrogen chlorosis in blue-green algae,” Arch. Microbiol. 69, 114–120 (1969).

Stambler, N.

Z. Dubinsky and N. Stambler, “Photoacclimation processes in phytoplankton: mechanisms, consequences, and applications,” Aquat. Microb. Ecol. 56, 163–176 (2009).
[Crossref]

Stephens, K.

T. R. Parsons, K. Stephens, and J. D. H. Strickland, “On the chemical composition of eleven species of marine phytoplanktons,” J. Fish. Res. Board Can. 18, 1001–1016 (1961).
[Crossref]

Stewart, W. D. P.

W. D. P. Stewart and P. Rowell, “Effects of l-methionine-dl-sulphoximine on the assimilation of newly fixed NH3, acetylene reduction and heterocyst production in Anabaena cylindrica,” Biochem. Biophys. Res. Commun. 65, 846–856 (1975).
[Crossref]

Stramski, D.

D. Stramski and C. D. Mobley, “Effect of microbial particles on oceanic optics: a database of single-particle optical properties,” Limnol. Oceanogr. 42, 538–549 (1997).
[Crossref]

Strickland, J. D. H.

T. R. Parsons, K. Stephens, and J. D. H. Strickland, “On the chemical composition of eleven species of marine phytoplanktons,” J. Fish. Res. Board Can. 18, 1001–1016 (1961).
[Crossref]

Sydoruk, O.

O. Zhernovaya, O. Sydoruk, V. Tuchin, and A. Douplik, “The refractive index of human hemoglobin in the visible range,” Phys. Med. Biol. 56, 4013–4021 (2011).
[Crossref]

Teper, J.

D. C. Sigee, J. Teper, and E. Levado, “Elemental composition of the cyanobacterium Anabaena flos-aquae collected from different depths within a stratified lake,” Eur. J. Phycol. 34, 477–485 (1999).
[Crossref]

Thomas, J. C.

I. Canto de Loura, J. P. Dubacq, and J. C. Thomas, “The effects of nitrogen deficiency on pigments and lipids of cyanobacteria,” Plant Physiol. 83, 838–843 (1987).
[Crossref]

Tirol, A.

P. A. Roger, A. Tirol, S. Ardales, and I. Watanabe, “Chemical composition of cultures and natural samples of N2-fixing blue-green algae from rice fields,” Biol. Fertil. Soils 2, 131–146 (1986).

Tuchin, V.

O. Zhernovaya, O. Sydoruk, V. Tuchin, and A. Douplik, “The refractive index of human hemoglobin in the visible range,” Phys. Med. Biol. 56, 4013–4021 (2011).
[Crossref]

van Boxtel, A. J. B.

P. M. Slegers, R. H. Wijffels, G. van Straten, and A. J. B. van Boxtel, “Design scenarios for flat panel photobioreactors,” Appl. Energy 88, 3342–3353 (2011).
[Crossref]

van de Hulst, H. C.

H. C. van de Hulst, Light Scattering by Small Particles (Courier Dover, 2012).

van Hille, R. P.

M. J. Griffiths, C. Garcin, R. P. van Hille, and S. T. Harrison, “Interference by pigment in the estimation of microalgal biomass concentration by optical density,” J. Microbiol. Methods 85, 119–123 (2011).
[Crossref]

van Straten, G.

P. M. Slegers, R. H. Wijffels, G. van Straten, and A. J. B. van Boxtel, “Design scenarios for flat panel photobioreactors,” Appl. Energy 88, 3342–3353 (2011).
[Crossref]

Vasconcelos, L.

L. Vasconcelos and P. Fay, “Nitrogen metabolism and ultrastructure in Anabaena cylindrica,” Arch. Microbiol. 96, 271–279 (1974).
[Crossref]

Veziroglu, T. N.

D. Das and T. N. Veziroğlu, “Hydrogen production by biological processes: a survey of literature,” Int. J. Hydrogen Energy 26, 13–28 (2001).
[Crossref]

Watanabe, I.

P. A. Roger, A. Tirol, S. Ardales, and I. Watanabe, “Chemical composition of cultures and natural samples of N2-fixing blue-green algae from rice fields,” Biol. Fertil. Soils 2, 131–146 (1986).

Weare, N. M.

N. M. Weare and J. R. Benemann, “Nitrogen fixation by Anabaena cylindrica,” Arch. Microbiol. 90, 323–332 (1973).

Wijffels, R. H.

P. M. Slegers, R. H. Wijffels, G. van Straten, and A. J. B. van Boxtel, “Design scenarios for flat panel photobioreactors,” Appl. Energy 88, 3342–3353 (2011).
[Crossref]

Williams, P. J. l. B.

P. J. l. B. Williams and L. M. L. Laurens, “Microalgae as biodiesel and biomass feedstocks: review and analysis of the biochemistry, energetics and economics,” Energ. Environ. Sci. 3, 554–590 (2010).
[Crossref]

Wolk, C. P.

C. P. Wolk and R. D. Simon, “Pigments and lipids of heterocysts,” Planta 86, 92–97 (1969).
[Crossref]

Zhernovaya, O.

O. Zhernovaya, O. Sydoruk, V. Tuchin, and A. Douplik, “The refractive index of human hemoglobin in the visible range,” Phys. Med. Biol. 56, 4013–4021 (2011).
[Crossref]

Appl. Energy (1)

P. M. Slegers, R. H. Wijffels, G. van Straten, and A. J. B. van Boxtel, “Design scenarios for flat panel photobioreactors,” Appl. Energy 88, 3342–3353 (2011).
[Crossref]

Appl. Environ. Microbiol. (1)

M. J. Griffiths and S. Harrison, “Lipid productivity as a key characteristic for choosing algal species for biodiesel production,” Appl. Environ. Microbiol. 33, 123–131 (1977).

Appl. Opt. (1)

Aquat. Microb. Ecol. (1)

Z. Dubinsky and N. Stambler, “Photoacclimation processes in phytoplankton: mechanisms, consequences, and applications,” Aquat. Microb. Ecol. 56, 163–176 (2009).
[Crossref]

Arch. Microbiol. (5)

L. Vasconcelos and P. Fay, “Nitrogen metabolism and ultrastructure in Anabaena cylindrica,” Arch. Microbiol. 96, 271–279 (1974).
[Crossref]

P. Fay, “Cell differentiation and pigment composition in Anabaena cylindrica,” Arch. Microbiol. 67, 62–70 (1969).

N. M. Weare and J. R. Benemann, “Nitrogen fixation by Anabaena cylindrica,” Arch. Microbiol. 90, 323–332 (1973).

M. M. Allen and A. J. Smith, “Nitrogen chlorosis in blue-green algae,” Arch. Microbiol. 69, 114–120 (1969).

M. M. Allen and F. Hutchison, “Nitrogen limitation and recovery in the cyanobacterium Aphanocapsa 6308,” Arch. Microbiol. 128, 1–7 (1980).
[Crossref]

Biochem. Biophys. Res. Commun. (1)

W. D. P. Stewart and P. Rowell, “Effects of l-methionine-dl-sulphoximine on the assimilation of newly fixed NH3, acetylene reduction and heterocyst production in Anabaena cylindrica,” Biochem. Biophys. Res. Commun. 65, 846–856 (1975).
[Crossref]

Biochim. Biophys. Acta. Bioenerg. (1)

P. Fay, “Photostimulation of nitrogen fixation in Anabaena cylindrica,” Biochim. Biophys. Acta. Bioenerg. 216, 353–356 (1970).
[Crossref]

Biol. Fertil. Soils (1)

P. A. Roger, A. Tirol, S. Ardales, and I. Watanabe, “Chemical composition of cultures and natural samples of N2-fixing blue-green algae from rice fields,” Biol. Fertil. Soils 2, 131–146 (1986).

Bioresour. Technol. (1)

R. Kandilian, E. Lee, and L. Pilon, “Radiation and optical properties of Nannochloropsis oculata grown under different irradiances and spectra,” Bioresour. Technol. 137, 63–73 (2013).
[Crossref]

Biotechnol. Adv. (1)

Y. Chisti, “Biodiesel from microalgae,” Biotechnol. Adv. 25, 294–306 (2007).
[Crossref]

Biotechnol. Bioeng. (2)

J.-F. Cornet, C. G. Dussap, and G. Dubertret, “A structured model for simulation of cultures of the cyanobacterium Spirulina platensis in photobioreactors: I. Coupling between light transfer and growth kinetics,” Biotechnol. Bioeng. 40, 817–825 (1992).
[Crossref]

L. Pottier, J. Pruvost, J. Deremetz, J. F. Cornet, J. Legrand, and C. G. Dussap, “A fully predictive model for one-dimensional light attenuation by Chlamydomonas reinhardtii in a torous photobioreactor,” Biotechnol. Bioeng. 91, 569–582 (2005).
[Crossref]

Can. Bull. Fish. Aquat. Sci. (1)

A. Morel and A. Bricaud, “Inherent optical properties of algal cells including picoplankton: theoretical and experimental results,” Can. Bull. Fish. Aquat. Sci. 214, 521–560 (1986).

Energ. Environ. Sci. (1)

P. J. l. B. Williams and L. M. L. Laurens, “Microalgae as biodiesel and biomass feedstocks: review and analysis of the biochemistry, energetics and economics,” Energ. Environ. Sci. 3, 554–590 (2010).
[Crossref]

Enzyme Microb. Technol. (1)

J. R. Benemann, “Production of nitrogen fertilizer with nitrogen-fixing blue-green algae,” Enzyme Microb. Technol. 1, 83–90 (1979).
[Crossref]

Eur. J. Phycol. (1)

D. C. Sigee, J. Teper, and E. Levado, “Elemental composition of the cyanobacterium Anabaena flos-aquae collected from different depths within a stratified lake,” Eur. J. Phycol. 34, 477–485 (1999).
[Crossref]

Int. J. Hydrogen Energy (3)

D. Das and T. N. Veziroğlu, “Hydrogen production by biological processes: a survey of literature,” Int. J. Hydrogen Energy 26, 13–28 (2001).
[Crossref]

H. Berberoğlu and L. Pilon, “Experimental measurement of the radiation characteristics of Anabaena variabilis ATCC 29413-U and Rhodobacter sphaeroides ATCC 49419,” Int. J. Hydrogen Energy 32, 4772–4785 (2007).
[Crossref]

H. Berberoğlu, L. Pilon, and A. Melis, “Radiation characteristics of Chlamydomonas reinhardtii CC125 and its truncated chlorophyll antenna transformants tla1, tlaX, and tla1-CW+,” Int. J. Hydrogen Energy 33, 6467–6483 (2008).
[Crossref]

J. Fish. Res. Board Can. (1)

T. R. Parsons, K. Stephens, and J. D. H. Strickland, “On the chemical composition of eleven species of marine phytoplanktons,” J. Fish. Res. Board Can. 18, 1001–1016 (1961).
[Crossref]

J. Microbiol. Methods (1)

M. J. Griffiths, C. Garcin, R. P. van Hille, and S. T. Harrison, “Interference by pigment in the estimation of microalgal biomass concentration by optical density,” J. Microbiol. Methods 85, 119–123 (2011).
[Crossref]

J. Opt. Soc. Am. (1)

J. Opt. Soc. Am. A (1)

J. Phycol. (1)

P. G. Falkowski and J. LaRoche, “Acclimation to spectral irradiance in algae,” J. Phycol. 27, 8–14 (1991).
[Crossref]

J. Quant. Spectrosc. Radiat. Transfer (5)

E. Lee, R.-L. Heng, and L. Pilon, “Spectral optical properties of selected photosynthetic microalgae producing biofuels,” J. Quant. Spectrosc. Radiat. Transfer 114, 112–135 (2013).

L. Pilon, H. Berberoğlu, and R. Kandilian, “Radiation transfer in photobiological carbon dioxide fixation and fuel production by microalgae,” J. Quant. Spectrosc. Radiat. Transfer 112, 2639–2660 (2011).
[Crossref]

H. Berberoğlu, P. S. Gomez, and L. Pilon, “Radiation characteristics of Botryococcus braunii, Chlorococcum littorale, and Chlorella sp. used for CO2 fixation and biofuel production,” J. Quant. Spectrosc. Radiat. Transfer 110, 1879–1893 (2009).
[Crossref]

A. Quirantes and S. Bernard, “Light scattering by marine algae: two-layer spherical and nonspherical models,” J. Quant. Spectrosc. Radiat. Transfer 89, 311–321 (2004).
[Crossref]

K. G. Privoznik, K. J. Daniel, and F. P. Incropera, “Absorption, extinction and phase function measurements for algal suspensions of Chlorella pyrenoidosa,” J. Quant. Spectrosc. Radiat. Transfer 20, 345–352 (1978).
[Crossref]

Limnol. Oceanogr. (1)

D. Stramski and C. D. Mobley, “Effect of microbial particles on oceanic optics: a database of single-particle optical properties,” Limnol. Oceanogr. 42, 538–549 (1997).
[Crossref]

New Zeal. J. Mar. Freshwater Res. (1)

R. J. Davies-Colley, R. D. Pridmore, and J. E. Hewitt, “Optical properties and reflectance spectra of 3 shallow lakes obtained from a spectrophotometric study,” New Zeal. J. Mar. Freshwater Res. 17, 445–459 (1983).
[Crossref]

Phys. Med. Biol. (1)

O. Zhernovaya, O. Sydoruk, V. Tuchin, and A. Douplik, “The refractive index of human hemoglobin in the visible range,” Phys. Med. Biol. 56, 4013–4021 (2011).
[Crossref]

Plant Physiol. (2)

P. F. Brownell and D. J. D. Nicholas, “Some effects of sodium on nitrate assimilation and N2 fixation in Anabaena cylindrica,” Plant Physiol. 42, 915–921 (1967).
[Crossref]

I. Canto de Loura, J. P. Dubacq, and J. C. Thomas, “The effects of nitrogen deficiency on pigments and lipids of cyanobacteria,” Plant Physiol. 83, 838–843 (1987).
[Crossref]

Planta (1)

C. P. Wolk and R. D. Simon, “Pigments and lipids of heterocysts,” Planta 86, 92–97 (1969).
[Crossref]

Proc. SPIE (1)

R. Bidigare, M. Ondrusek, J. Morrow, and D. Kiefer, “In vivo absorption properties of algal pigments,” Proc. SPIE 1302, 290–302 (1990).
[Crossref]

Other (10)

M. Jonasz and G. R. Fournier, Light Scattering by Particles in Water: Theoretical and Experimental Foundations (Academic, 2007).

P. Charbonneau and B. Knapp, “A user’s guide to PIKAIA 1.0,” (National Center for Atmospheric Research, 1995).

M. L. Parry, ed., Climate Change 2007: Impacts, Adaptation and Vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (IPPC) (Cambridge University, 2007), Vol. 4.

A. Richmond, Handbook of Microalgal Culture (Blackwell Science, 2004).

M. F. Modest, Radiative Heat Transfer, 2nd edition (Academic, 2003).

B. Ke, Photosynthesis, Photobiochemistry and Photobiophysics (Kluwer Academic, 2001).

H. C. van de Hulst, Light Scattering by Small Particles (Courier Dover, 2012).

M. Kerker, The Scattering of Light, and Other Electromagnetic Radiation (Academic, 1969).

C. F. Bohren and D. R. Huffman, Absorption and Scattering of Light by Small Particles (Wiley, 1998).

J. Dauchet, “Analyse Radiative des Photobioréacteurs,” Ph.D. dissertation, (Université Blaise Pascal, Clermont Ferrand II, France, 2012).

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Figures (7)

Fig. 1.
Fig. 1.

Micrograph image of A. cylindrica showing vegetative cells and heterocysts 2.5–3 μm in diameter. Reproduced with permission from Prof. Yuuji Tsukii, Hosei University, Protist Information Server http://protist.i.hosei.ac.jp.

Fig. 2.
Fig. 2.

Block diagram of the procedure used to retrieve the refraction index, nλ, and absorption index, kλ, from the measured absorption and scattering cross sections per unit length C¯abs,λ and C¯sca,λ at a given wavelength, λ, for volume-equivalent diameter distribution f(dc,eq). Here, P=100 individuals per generation for a maximum of 500 generations.

Fig. 3.
Fig. 3.

Histograms of volume-equivalent diameter distribution f(dc,eq) of A. cylindrica filaments for Samples 1, 2, 3, and 4 at concentrations (a) X1=0.086kg/m3, (b) X2=0.108kg/m3, (c) X3=0.151kg/m3, and (d) X4=0.171kg/m3 obtained from more than 1120 cells for each sample.

Fig. 4.
Fig. 4.

Scattering phase function of A. cylindrica at 633 nm measured experimentally using a polar nephelometer and predicted using the retrieved values of n633 and k633 for Sample 3 with xw=0.75.

Fig. 5.
Fig. 5.

(a) Absorption coefficient, κλ, (b) scattering coefficient, σs,λ, (c) average mass absorption cross section, A¯abs,λ=κλ/X, and (d) average mass scattering cross section, S¯sca,λ=σs,λ/X, from 400 to 750 nm of A. cylindrica in Sample 3 for mass concentrations, X3,1=0.431, X3,2=0.296, and X3,3=0.202kg/m3.

Fig. 6.
Fig. 6.

Average mass (a) absorption, A¯abs,λ, and (b) scattering cross sections S¯sca,λ from 400 to 750 nm of A. cylindrica for Samples 1, 2, 3, and 4 collected after day 6, 9, 12, and 14, respectively.

Fig. 7.
Fig. 7.

Retrieved (a) refraction, nλ, and (b) absorption, kλ, indices between 400 to 750 nm for A. cylindrica assuming water mass fraction to be xw=0.75 or 0.85 for Samples 1, 2, 3, and 4 collected after day 6, 9, 12, and 14, respectively.

Equations (9)

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s^·Iλ(r,s^)=κλIλ(r,s^)σs,λIλ(r,s^)+σs,λ4π4πIλ(r,s^)ΦT,λ(s^i,s^)dΩi,
κλ=A¯abs,λXandσs,λ=S¯sca,λX,
14π4πΦT,λ(s^i,s^)dΩi=1.
gλ=120πΦT,λ(θ)cosθsinθdθ,
X=0.816OD750
dc,eq,i2=j=1Nc23ds,i,j3j=1Ncds,i,jwithi=1,2,,Nf.
C¯abs,λ=A¯abs,λρdm(1xw)(π6Nfi=1Nfj=1Ncds,i,j2),andC¯sca,λ=S¯sca,λρdm(1xw)(π6Nfi=1Nfj=1Ncds,i,j2).
δλ=(C¯abs,λ,predC¯abs,λC¯abs,λ)2+(C¯sca,λ,predC¯sca,λC¯sca,λ)2.
nλ2=1+0.6961663λ2λ2(0.0684043)2+0.4079426λ2λ2(0.1162414)2+0.8974794λ2λ2(9.896161)2,

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