Applied Microbiology and Biotechnology

, Volume 97, Issue 17, pp 7627–7637 | Cite as

Comprehensive model of microalgae photosynthesis rate as a function of culture conditions in photobioreactors

  • T. A. Costache
  • F. Gabriel Acién Fernández
  • M. M. Morales
  • J. M. Fernández-Sevilla
  • I. Stamatin
  • E. Molina
Biotechnological products and process engineering

Abstract

In this paper, the influence of culture conditions (irradiance, temperature, pH, and dissolved oxygen) on the photosynthesis rate of Scenedesmus almeriensis cultures is analyzed. Short-run experiments were performed to study cell response to variations in culture conditions, which take place in changing environments such as outdoor photobioreactors. Experiments were performed by subjecting diluted samples of cells to different levels of irradiance, temperature, pH, and dissolved oxygen concentration. Results demonstrate the existence of photoinhibition phenomena at irradiances higher than 1,000 μE/m2 s; in addition to reduced photosynthesis rates at inadequate temperatures or pH—the optimal values being 35 °C and 8, respectively. Moreover, photosynthesis rate reduction at dissolved oxygen concentrations above 20 mg/l is demonstrated. Data have been used to develop an integrated model based on considering the simultaneous influence of irradiance, temperature, pH, and dissolved oxygen. The model fits the experimental results in the range of culture conditions tested, and it was validated using data obtained by the simultaneous variation of two of the modified variables. Furthermore, the model fits experimental results obtained from an outdoor culture of S. almeriensis performed in an open raceway reactor. Results demonstrate that photosynthetic efficiency is modified as a function of culture conditions, and can be used to determine the proximity of culture conditions to optimal values. Optimal conditions found (T = 35 °C, pH = 8, dissolved oxygen concentration <20 mg/l) allows to maximize the use of light by the cells. The developed model is a powerful tool for the optimal design and management of microalgae-based processes, especially outdoors, where the cultures are subject to daily culture condition variations.

Keywords

Photosynthesis rate Irradiance pH Temperature Dissolved oxygen Microalgae 

References

  1. Acién FG, Garcia F, Sanchez JA, Fernández JM, Molina E (1998) Modelling of biomass productivity in tubular photobioreactors for microalgal cultures. Effects of dilution rate, tube diameter and solar irradiance. Biotechnol Bioeng 58(6):605–616CrossRefGoogle Scholar
  2. Acién FG, García F, Chisti Y (1999) Photobioreactors: light regime, mass transfer, and scaleup. Prog Ind Microbiol 35:231–247CrossRefGoogle Scholar
  3. Acien F, González-López CV, Fernández JM, Molina E (2012) Conversion of CO2 into biomass by microalgae: how realistic a contribution may it be to significant CO2 removal? Appl Microbiol Biotechnol 96:577–586CrossRefGoogle Scholar
  4. Acién FG, Fernández JM, Molina E (2013) Photobioreactors for the production of microalgae. Rev Env Sci Biotechnol 1–21Google Scholar
  5. Allen M, Arnon DI (1955) Studies on nitrogen-fixing blue-green algae. I. Growth and nitrogen-fixation by Anabaena cylindrica. Plant Physiol 30:366–372PubMedCrossRefGoogle Scholar
  6. Badger MR, Von Caemmerer S, Ruuska S, Nakano H, Laisk A, Allen JF, Asada K, Matthijs HCP, Griffiths H (2000) Electron flow to oxygen in higher plants and algae: rates and control of direct photoreduction (Mehler reaction) and rubisco oxygenase. Philos Trans R Soc B Biol Sci 355:1433–1446CrossRefGoogle Scholar
  7. Béchet Q, Shilton A, Park JBK, Craggs RJ, Guieysse B (2011) Universal temperature model for shallow algal ponds provides improved accuracy. Environ Sci Technol 45:3702–3709PubMedCrossRefGoogle Scholar
  8. Berenguel M, Rodríguez F, Acién FG, García JL (2004) Model predictive control of pH in tubular photobioreactors. J Process Control 14:377–387CrossRefGoogle Scholar
  9. Bernard O (2011) Hurdles and challenges for modelling and control of microalgae for CO2 mitigation and biofuel production. J Process Control 21:1378–1389CrossRefGoogle Scholar
  10. Bernard O, Rémond B (2012) Validation of a simple model accounting for light and temperature effect on microalgal growth. Bioresour Technol 123:520–527PubMedCrossRefGoogle Scholar
  11. Bitaubé E, Caro I, Pérez L (2008) Kinetic model for growth of Phaeodactylum tricornutum in intensive culture photobioreactor. Biochem Eng J 40:520–525CrossRefGoogle Scholar
  12. Blanchard GF, Guarini J, Richard P, Gros P, Mornet F (1996) Quantifying the short-term temperature effect on light-saturated photosynthesis of intertidal microphytobenthos. Mar Ecol Prog Ser 134:309–313CrossRefGoogle Scholar
  13. Brindley C, Acién FG, Fernández-Sevilla JM (2010) The oxygen evolution methodology affects photosynthetic rate measurements of microalgae in well-defined light regimes. Biotechnol Bioeng 106:228–237PubMedGoogle Scholar
  14. Brindley C, Acién FG, Fernández-Sevilla JM (2011) Analysis of light regime in continuous light distributions in photobioreactors. Bioresour Technol 102:3138–3148PubMedCrossRefGoogle Scholar
  15. Brune DE, Lundquist TJ, Benemann JR (2009) Microalgal biomass for greenhouse gas reductions: potential for replacement of fossil fuels and animal feeds. J Environ Eng 135:1136–1144CrossRefGoogle Scholar
  16. Butterwick C, Heaney SI, Talling JF (2005) Diversity in the influence of temperature on the growth rates of freshwater algae, and its ecological relevance. Freshw Biol 50:291–300CrossRefGoogle Scholar
  17. Camacho F, Acién FG, Sánchez JA, García F, Molina E (1999) Prediction of dissolved oxygen and carbon dioxide concentration profiles in tubular photobioreactors for microalgal culture. Biotechnol Bioeng 62:71–86PubMedCrossRefGoogle Scholar
  18. Camacho F, García F, Fernández JM, Chisti Y, Molina E (2003) A mechanistic model of photosynthesis in microalgae. Biotechnol Bioeng 81:459–473PubMedCrossRefGoogle Scholar
  19. Carvalho AP, Silva SO, Baptista JM, Malcata FX (2011) Light requirements in microalgal photobioreactors: an overview of biophotonic aspects. Appl Microbiol Biotechnol 89:1275–1288PubMedCrossRefGoogle Scholar
  20. Chisti Y (2010) A bioeconomy vision of sustainability. Biofuels Bioprod Bioref 4:359–361CrossRefGoogle Scholar
  21. Eilers PHC, Peeters JCH (1988) A model for the relationship between light intensity and the rate of photosynthesis in phytoplankton. Ecol Model 42:199–215CrossRefGoogle Scholar
  22. Falkowski PG, Owens TG (1978) Effects of light intensity on photosynthesis and dark respiration in six species of marine phytoplankton. Mar Biol 45:289–295CrossRefGoogle Scholar
  23. Falkowski PG, Oliver MJ (2007) Mix and match: how climate selects phytoplankton. Nat Rev Microbiol 5:813–819PubMedCrossRefGoogle Scholar
  24. Fernández I, Acién FG, Fernández JM, Guzmán JL, Magán JJ, Berenguel M (2012) Dynamic model of microalgal production in tubular photobioreactors. Bioresour Technol 126:172–181PubMedCrossRefGoogle Scholar
  25. García JL, Berenguel M, Rodríguez F, Fernández JM, Brindley C, Acién FG (2003) Minimization of carbon losses in pilot-scale outdoor photobioreactors by model-based predictive control. Biotechnol Bioeng 84:533–543CrossRefGoogle Scholar
  26. Goldman JC, Azov Y, Riley CB, Dennett MR (1982a) The effect of pH in intensive microalgal cultures. I. Biomass regulation. J Exp Mar Biol Ecol 57:1–13CrossRefGoogle Scholar
  27. Goldman JC, Riley CB, Dennett MR (1982b) The effect of pH in intensive microalgal cultures. II. Species competition. J Exp Mar Biol Ecol 57:15–24CrossRefGoogle Scholar
  28. Gordon JM, Polle JEW (2007) Ultrahigh bioproductivity from algae. Appl Microbiol Biotechnol 76:969–975PubMedCrossRefGoogle Scholar
  29. Han B (2001) Photosynthesis—irradiance response at physiological level: a mechanistic model. J Theor Biol 213:121–127PubMedCrossRefGoogle Scholar
  30. Jeon YC, Cho CW, Yun Y (2006) Oxygen evolution rate of photosynthetic microalga Haematococcus pluvialis depending on light intensity and quality. Stud Surf Sci Catal 159:157–160CrossRefGoogle Scholar
  31. 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
  32. MacIntyre HL, Kana TM, Anning T, Geider RJ (2002) Photoacclimation of photosynthesis irradiance response curves and photosynthetic pigments in microalgae and cyanobacteria. J Phycol 38:17–38CrossRefGoogle Scholar
  33. Marquez FJ, Sasaki K, Nishio N, Nagai S (1995) Inhibitory effect of oxygen accumulation on the growth of Spirulina platensis. Biotechnol Lett 17:225–228CrossRefGoogle Scholar
  34. Mazzuca T, Garcia F, Camacho F, Acién FG, Molina E (2000) Carbon dioxide uptake efficiency by outdoor microalgal cultures in tubular airlift photobioreactors. Biotechnol Bioeng 67:465–475CrossRefGoogle Scholar
  35. Mendoz JL, Granados MR, deGodos I, Acién FG, Molina E, Heaven S, Banks CJ (2013) Oxygen transfer and evolution in microalgal culture in open raceways. Bioresour Technol 37:188–195CrossRefGoogle Scholar
  36. Moisan JR, Moisan TA, Abbott MR (2002) Modelling the effect of temperature on the maximum growth rates of phytoplankton populations. Ecol Model 153:197–215CrossRefGoogle Scholar
  37. Molina E, Fernández JM, Sánchez JA, García F (1996a) A study on simultaneous photolimitation and photoinhibition in dense microalgal cultures taking into account incident and averaged irradiances. J Biotechnol 45:59–69CrossRefGoogle Scholar
  38. Molina E, García F, Sánchez JA, Acién FG, Fernández JM (1996b) Growth yield determination in a chemostat culture of the marine microalga Isochrysis galbana. J Appl Phycol 8:529–534CrossRefGoogle Scholar
  39. Muñoz R, Köllner C, Guieysse B (2009) Biofilm photobioreactors for the treatment of industrial wastewaters. J Hazard Mater 161:29–34PubMedCrossRefGoogle Scholar
  40. Nedbal L, Tichý V, Xiong F, Grobbelaar JU (1996) Microscopic green algae and cyanobacteria in high-frequency intermittent light. J Appl Phycol 8:325–333CrossRefGoogle Scholar
  41. Olaizola M, Duerr EO, Freeman DW (1991) Effect of CO2 enhancement in an outdoor algal production system using Tetraselmis. J Appl Phycol 3:363–366Google Scholar
  42. Papadakis IA, Kotzabasis K, Lika K (2005) A cell-based model for the photoacclimation and CO2-acclimation of the photosynthetic apparatus. Biochim Biophys Acta Bioenerg 1708:250–261CrossRefGoogle Scholar
  43. Posten C (2009) Design principles of photo-bioreactors for cultivation of microalgae. Eng Life Sci 9:165–177CrossRefGoogle Scholar
  44. Pulz O, Gross W (2004) Valuable products from biotechnology of microalgae. Appl Microbiol Biotechnol 65:635–648PubMedCrossRefGoogle Scholar
  45. Quinn JC, Catton KB, Johnson S, Bradley TH (2012) Geographical assessment of microalgae biofuels potential incorporating resource availability. Bioenergy Research 1–10Google Scholar
  46. Sánchez JF, Fernández-Sevilla JM, Acién FG, Cerón MC, Pérez-Parra J, Molina-Grima E (2008) Biomass and lutein productivity of Scenedesmus almeriensis: influence of irradiance, dilution rate and temperature. Appl Microbiol Biotechnol 79:719–729PubMedCrossRefGoogle Scholar
  47. Singh DP, Singh N, Verma K (1995) Photooxidative damage to the cyanobacterium Spirulina platensis mediated by singlet oxygen. Curr Microbiol 31:44–48CrossRefGoogle Scholar
  48. Slegers PM, van Beveren PJM, Wijffels RH, Van Straten G, Van Boxtel AJB (2013) Scenario analysis of large scale algae production in tubular photobioreactors. Appl Energy 105:395–406CrossRefGoogle Scholar
  49. Sousa C, de Winter L, Janssen M, Vermuë MH, Wijffels RH (2012) Growth of the microalgae Neochloris oleoabundans at high partial oxygen pressures and sub-saturating light intensity. Bioresour Technol 104:565–570PubMedCrossRefGoogle Scholar
  50. Takache H, Christophe G, Cornet J, Pruvost J (2010) Experimental and theoretical assessment of maximum productivities for the microalgae Chlamydomonas reinhardtii in two different geometries of photobioreactors. Biotechnol Prog 26:431–440PubMedGoogle Scholar
  51. Vejrazka C, Janssen M, Streefland M, Wijffels RH (2011) Photosynthetic efficiency of Chlamydomonas reinhardtii in flashing light. Biotechnol Bioeng 108:2905–2913PubMedCrossRefGoogle Scholar
  52. Vonshak A, Abeliovich A, Boussiba S, Arad S, Richmond A (1982) Production of Spirulina biomass: effects of environmental factors and population density. Biomass 2:175–185CrossRefGoogle Scholar
  53. Weissman JC, Goebel RP, Benemann JR (1988) Photobioreactor design: mixing, carbon utilization, and oxygen accumulation. Biotechnol Bioeng 31:336–344PubMedCrossRefGoogle Scholar
  54. Wigmosta MS, Coleman AM, Skaggs RJ, Huesemann MH, Lane LJ (2011) National microalgae biofuel production potential and resource demand. Water Resour Res 47:W00H04. doi:10.1029/2010WR009966 CrossRefGoogle Scholar
  55. Yun Y, Park JM (2003) Kinetic modeling of the light-dependent photosynthetic activity of the green microalga Chlorella vulgaris. Biotechnol Bioeng 83:303–311PubMedCrossRefGoogle Scholar
  56. Zijffers J-F, Schippers KJ, Zheng K, Janssen M, Tramper J, Wijffels RH (2010) Maximum photosynthetic yield of green microalgae in photobioreactors. Mar Biotechnol 12:708–718PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • T. A. Costache
    • 2
  • F. Gabriel Acién Fernández
    • 1
  • M. M. Morales
    • 1
  • J. M. Fernández-Sevilla
    • 1
  • I. Stamatin
    • 2
  • E. Molina
    • 1
  1. 1.Department of Chemical EngineeringUniversity of AlmeríaAlmeríaSpain
  2. 2.3Nano-SAE Research Centre, Faculty of PhysicsUniversity of BucharestBucharestRomania

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