Influence of light absorption rate on the astaxanthin production by the microalga Haematococcus pluvialis during nitrogen starvation

Khadija Samhat, Antoinette Kazbar, Hosni Takache, Ali Ismail, Jeremy Pruvost

Bioresources and Bioprocessing ›› 2023, Vol. 10 ›› Issue (1) : 78.

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Bioresources and Bioprocessing ›› 2023, Vol. 10 ›› Issue (1) : 78. DOI: 10.1186/s40643-023-00700-0
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Influence of light absorption rate on the astaxanthin production by the microalga Haematococcus pluvialis during nitrogen starvation

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Abstract

Large amounts of astaxanthin (about 4% DW) can be produced under nitrogen starvation of Haematococcus pluvialis in photobioreactors (PBRs) exposed to high light conditions to induce a light stress. However, in PBR, the large biomass concentration usually achieved leads to strong light attenuation conditions, which makes complex the analysis of this “light stress”. This study aims to elucidate the role of light transfer in astaxanthin cell content and productivity from the microalga Haematococcus pluvialis during nitrogen starvation. Haematococcus pluvialis was cultivated in a flat-panel PBR in a batch mode with sudden nitrogen starvation conditions and an incident photon flux density (PFD) of 250 µmol m−2 s−1. Different initial biomass concentrations (Missing superscript or subscript argument) were evaluated, 0.21, 0.52, 1.39 and 2.21 kg m−3. As a result, spectral mass absorption cross-sections of Haematococcus pluvialis were measured at different times during nitrogen starvation, and were used to relate the mean rate of photon absorption (MRPA) to the astaxanthin productivity. A minimum initial MRPA of 7000 ± 500 µmol kgx −1 s−1 was found necessary to trigger large accumulation of astaxanthin in Haematococcus pluvialis cells (up to 3.21% DW) during nitrogen starvation conditions. The results also demonstrated the link between the MRPA and the daily astaxanthin productivity of Haematococcus pluvialis cultures, introducing then the MRPA as a physical quantity of interest for a rational optimization of the light culture conditions in PBRs.

Keywords

Haematococcus pluvialis / Photobioreactor / Photosynthesis / Light transfer / Astaxanthin accumulation / Nitrogen starvation

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Khadija Samhat, Antoinette Kazbar, Hosni Takache, Ali Ismail, Jeremy Pruvost. Influence of light absorption rate on the astaxanthin production by the microalga Haematococcus pluvialis during nitrogen starvation. Bioresources and Bioprocessing, 2023, 10(1): 78 https://doi.org/10.1186/s40643-023-00700-0

References

Béchet Q, Shilton A, Guieysse B. Modeling the effects of light and temperature on algae growth: state of the art and critical assessment for productivity prediction during outdoor cultivation. Biotechnol Adv, 2013, 31: 1648-1663.
CrossRef Google scholar
Berges JA, Charlebois DO, Mauzerall DC, Falkowski PG. Differential effects of nitrogen limitation on photosynthetic efficiency of photosystems I and II in microalgae. Plant Physiol, 1996, 110: 689-696.
CrossRef Google scholar
Boussiba S. Carotenogenesis in the green alga Haematococcus pluvialis: cellular physiology and stress response. Physiol Plant, 2000, 108: 111-117.
CrossRef Google scholar
Boussiba S, Vonshak A. Astaxanthin accumulation in the Green Alga Haematococcus pluvialis. Plant Cell Physiol, 1991, 32: 1077-1082.
CrossRef Google scholar
Boussiba S, Fan L, Vonshak A. Enhancement and determination of astaxanthin accumulation in green alga Haematococcus pluvialis. Methods Enzymol, 1992, 213: 386-391.
CrossRef Google scholar
Cakmak T, Angun P, Demiray YE, . Differential effects of nitrogen and sulfur deprivation on growth and biodiesel feedstock production of Chlamydomonas reinhardtii. Biotechnol Bioeng, 2012, 109: 1947-1957.
CrossRef Google scholar
Cassano AE, Martin CA, Brandi RJ, Alfano OM. Photoreactor analysis and design: fundamentals and applications. Ind Eng Chem Res, 1995, 34: 2155-2201.
CrossRef Google scholar
Chekanov K, Schastnaya E, Neverov K, . Non-photochemical quenching in the cells of the carotenogenic chlorophyte Haematococcus lacustris under favorable conditions and under stress. Biochimica Et Biophysica Acta (BBA) General Subjects, 2019, 1863: 1429-1442.
CrossRef Google scholar
Cornet J-F, Dussap C-G. A Simple and reliable formula for assessment of maximum volumetric productivities in photobioreactors. Biotechnol Progress, 2009, 25: 424-435.
CrossRef Google scholar
Cornet JF, Dussap CG, Cluzel P, Dubertret G. A structured model for simulation of cultures of the cyanobacterium Spirulina platensis in photobioreactors: II. Identification of kinetic parameters under light and mineral limitations. Biotechnol Bioeng, 1992, 40: 826-834.
CrossRef Google scholar
Fábregas J, Otero A, Maseda A, Domínguez A. Two-stage cultures for the production of Astaxanthin from Haematococcus pluvialis. J Biotechnol, 2001, 89: 65-71.
CrossRef Google scholar
Fábregas J, Domínguez A, Maseda A, Otero A. Interactions between irradiance and nutrient availability during astaxanthin accumulation and degradation in Haematococcus pluvialis. Appl Microbiol Biotechnol, 2003, 61: 545-551.
CrossRef Google scholar
Fan L, Vonshak A, Zarka A, Boussiba S. Does astaxanthin protect Haematococcus against light damage?. Zeitschrift Für Naturforschung C, 1998, 53: 93-100.
CrossRef Google scholar
Ferrel Ballestas FR, Titica M, Legrand J, . Prediction of the radiation characteristics and the light absorption rate of Chlamydomonas reinhardtii cultivated under a progressive nitrogen starvation and accumulating carbon reserves. J Quant Spectrosc Radiat Transfer, 2023, 309.
CrossRef Google scholar
Flynn KJ, Davidson K, Cunningham A. Relations between carbon and nitrogen during growth of Nannochloropsis oculata (Droop) Hibberd under continuous illumination. New Phytol, 1993, 125: 717-722.
CrossRef Google scholar
Grima EM, Camacho FG, Pérez JAS, . A mathematical model of microalgal growth in light-limited chemostat culture. J Chem Technol Biotechnol, 1994, 61: 167-173.
CrossRef Google scholar
Guerin M, Huntley ME, Olaizola M. Haematococcus astaxanthin: applications for human health and nutrition. Trends Biotechnol, 2003, 21: 210-216.
CrossRef Google scholar
Han D, Li Y, Hu Q. Richmond A, Hu Q. Biology and commercial aspects of Haematococcus pluvialis. Handbook of microalgal culture, 2013, Oxford: John Wiley & Sons Ltd, 388-405.
CrossRef Google scholar
Harker M, Tsavalos AJ, Young AJ. Factors responsible for astaxanthin formation in the Chlorophyte Haematococcus pluvialis. Biores Technol, 1996, 55: 207-214.
CrossRef Google scholar
Hu Z, Li Y, Sommerfeld M, . Enhanced protection against oxidative stress in an astaxanthin-overproduction Haematococcus mutant (Chlorophyceae). Eur J Phycol, 2008, 43: 365-376.
CrossRef Google scholar
Jonasz M, Fournier G. Light scattering by particles in water: theoretical and experimental foundations, 2007, 1, Amsterdam: Elsevier/Academic Press.
Kandilian R, Pruvost J, Legrand J, Pilon L. Influence of light absorption rate by Nannochloropsis oculata on triglyceride production during nitrogen starvation. Biores Technol, 2014, 163: 308-319.
CrossRef Google scholar
Kandilian R, Soulies A, Pruvost J, . Simple method for measuring the spectral absorption cross-section of microalgae. Chem Eng Sci, 2016, 146: 357-368.
CrossRef Google scholar
Kandilian R, Taleb A, Heredia V, . Effect of light absorption rate and nitrate concentration on TAG accumulation and productivity of Parachlorella kessleri cultures grown in chemostat mode. Algal Res, 2019, 39.
CrossRef Google scholar
Kang CD, Lee JS, Park TH, Sim SJ. Comparison of heterotrophic and photoautotrophic induction on astaxanthin production by Haematococcus pluvialis. Appl Microbiol Biotechnol, 2005, 68: 237-241.
CrossRef Google scholar
Kobayashi M, Kakizono T, Nishio N, . Antioxidant role of astaxanthin in the green alga Haematococcus pluvialis. Appl Microbiol Biotechnol, 1997, 48: 351-356.
CrossRef Google scholar
le Williams PJB, Laurens LML. Microalgae as biodiesel & biomass feedstocks: review & analysis of the biochemistry, energetics & economics. Energy Environ Sci, 2010, 3: 554.
CrossRef Google scholar
Lee HY, Erickson LE, Yang SS. Kinetics and bioenergetics of light-limited photoautotrophic growth of Spirulina platensis. Biotechnol Bioeng, 1987, 29: 832-843.
CrossRef Google scholar
Lee E, Pruvost J, He X, . Design tool and guidelines for outdoor photobioreactors. Chem Eng Sci, 2014, 106: 18-29.
CrossRef Google scholar
Li Y, Sommerfeld M, Chen F, Hu Q. Effect of photon flux densities on regulation of carotenogenesis and cell viability of Haematococcus pluvialis (Chlorophyceae). J Appl Phycol, 2010, 22: 253-263.
CrossRef Google scholar
Liu H, Huang W-C, Guo N, Mao X. Application of secondary amine switchable hydrophilicity solvents for astaxanthin extraction from wet Haematococcus pluvialis. Algal Res, 2020, 48: 101892.
CrossRef Google scholar
Lorenz RT, Cysewski GR. Commercial potential for Haematococcus microalgae as a natural source of astaxanthin. Trends Biotechnol, 2000, 18: 160-167.
CrossRef Google scholar
Nichols HW, Bold HC. Trichosarcina polymorpha Gen. et Sp. Nov J Phycol, 1965, 1: 34-38.
CrossRef Google scholar
Olaizola M. No title found. J Appl Phycol, 2000, 12: 499-506.
CrossRef Google scholar
Pottier L, Pruvost J, Deremetz J, . A fully predictive model for one-dimensional light attenuation by Chlamydomonas reinhardtii in a torus photobioreactor. Biotechnol Bioeng, 2005, 91: 569-582.
CrossRef Google scholar
Pruvost J, Cornet J-F. Posten C, Walter C. Knowledge models for the engineering and optimization of photobioreactors. Microalgal biotechnology: potential and production, 2012, Berlin: De Gruyter, 181-224.
CrossRef Google scholar
Pruvost J, Van Vooren G, Cogne G, Legrand J. Investigation of biomass and lipids production with Neochloris oleoabundans in photobioreactor. Biores Technol, 2009, 100: 5988-5995.
CrossRef Google scholar
Qiu N, Wang X, Zhou F. A new method for fast extraction and determination of chlorophylls in natural water. Zeitschrift Für Naturforschung C, 2018, 73: 77-86.
CrossRef Google scholar
Ranjbar R, Inoue R, Katsuda T, . High efficiency production of astaxanthin in an airlift photobioreactor. J Biosci Bioeng, 2008, 106: 204-207.
CrossRef Google scholar
Recht L, Töpfer N, Batushansky A, . Metabolite profiling and integrative modeling reveal metabolic constraints for carbon partitioning under nitrogen starvation in the green algae Haematococcus pluvialis. J Biol Chem, 2014, 289: 30387-30403.
CrossRef Google scholar
Rizzo A, Ross ME, Norici A, Jesus B. A two-step process for improved biomass production and non-destructive Astaxanthin and carotenoids accumulation in Haematococcus pluvialis. Appl Sci, 2022, 12: 1261.
CrossRef Google scholar
Schmollinger S, Mühlhaus T, Boyle NR, . Nitrogen-sparing mechanisms in Chlamydomonas affect the transcriptome, the proteome, and photosynthetic metabolism. Plant Cell, 2014, 26: 1410-1435.
CrossRef Google scholar
Scibilia L, Girolomoni L, Berteotti S, . Photosynthetic response to nitrogen starvation and high light in Haematococcus pluvialis. Algal Res, 2015, 12: 170-181.
CrossRef Google scholar
Solovchenko AE, Chivkunova OB, Maslova IP. Pigment composition, optical properties, and resistance to photodamage of the microalga Haematococcus pluvialis cultivated under high light. Russ J Plant Physiol, 2011, 58: 9-17.
CrossRef Google scholar
Strickland JDH, Parsons TR (1968) A practical handbook of seawater analysis. Bulletin of Fisheries Research Board of Canada
Takache H, Christophe G, Cornet J-F, Pruvost J. Experimental and theoretical assessment of maximum productivities for the microalgae Chlamydomonas reinhardtii in two different geometries of photobioreactors. Biotechnol Progress, 2009
CrossRef Google scholar
Takache H, Pruvost J, Cornet J-F. Kinetic modeling of the photosynthetic growth of Chlamydomonas reinhardtii in a photobioreactor. Biotechnol Progress, 2012, 28: 681-692.
CrossRef Google scholar
Taleb A, Pruvost J, Legrand J, . Development and validation of a screening procedure of microalgae for biodiesel production: Application to the genus of marine microalgae Nannochloropsis. Biores Technol, 2015, 177: 224-232.
CrossRef Google scholar
Taleb A, Kandilian R, Touchard R, . Screening of freshwater and seawater microalgae strains in fully controlled photobioreactors for biodiesel production. Biores Technol, 2016, 218: 480-490.
CrossRef Google scholar
Van Vooren G, Le Grand F, Legrand J, . Investigation of fatty acids accumulation in Nannochloropsis oculata for biodiesel application. Biores Technol, 2012, 124: 421-432.
CrossRef Google scholar
Wang J, Han D, Sommerfeld MR, . Effect of initial biomass density on growth and astaxanthin production of Haematococcus pluvialis in an outdoor photobioreactor. J Appl Phycol, 2013, 25: 253-260.
CrossRef Google scholar
Wang J, Sommerfeld MR, Lu C, Hu Q. Combined effect of initial biomass density and nitrogen concentration on growth and astaxanthin production of Haematococcus pluvialis (Chlorophyta) in outdoor cultivation. Algae, 2013, 28: 193-202.
CrossRef Google scholar
Zhang W, Zhou X, Zhang Y, . Enhancing astaxanthin accumulation in Haematococcus pluvialis by coupled light intensity and nitrogen starvation in column photobioreactors. J Microbiol Biotechnol, 2018, 28: 2019-2028.
CrossRef Google scholar
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