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Comparative study on light attenuation models of Galdieria sulphuraria for efficient production of phycocyanin

  • Haohua Wang
  • Zhen Zhang
  • Minxi WanEmail author
  • Ruixuan Wang
  • Jianke Huang
  • Kaikai Zhang
  • Jiacai Guo
  • Wenmin Bai
  • Yuanguang LiEmail author
Article

Abstract

The thermo-acidophilic red microalga Galdieria sulphuraria is valuable especially for the intracellular thermostable phycocyanin with broad application prospects. Heterotrophy or photoinduction had been studied to enhance the production of phycocyanin at small-scale indoors. The aim of this study was to scale up the photoinduction process. The Cornet model could well describe and predict the light attenuation in G. sulphuraria suspension compared with the Lambert-Beer and hyperbolic models. Volume-averaged light intensity was the key parameter for photoinduction by testing respectively in 1-L column bioreactor, 3-L and 15-L flat plate photobioreactors indoors and outdoors, and supposed to be 600 μmol photons m−2 s−1. Accordingly, amplifying photoinduction in 1.35-m2 raceway pond outdoors was successfully carried out with the final cell dry weight of 2.37 g L−1 and phycocyanin up to 10.32%, which was comparable with that from Spirulina/Arthrospira and 3.82 times higher than that of heterotrophic cells of G. sulphuraria.

Keywords

Galdieria sulphuraria Rhodophyta Phycocyanin Scale-up Light attenuation Volume-averaged light intensity 

Notes

Funding information

This research was funded by the National High Technology Research and Development Program of China (2015AA020602).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Aiba S (1982) Growth kinetics of photosynthetic microorganisms. Adv Biochem Eng 23:85–156Google Scholar
  2. Barbier G, Oesterhelt C, Larson MD, Halgren RG, Wilkerson C, Garavito RM, Benning C, Weber AP (2005) Comparative genomics of two closely related unicellular thermo-acidophilic red algae, Galdieria sulphuraria and Cyanidioschyzon merolae, reveals the molecular basis of the metabolic flexibility of Galdieria sulphuraria and significant differences in carbohydrate metabolism of both algae. Plant Physiol 137:460–474CrossRefGoogle Scholar
  3. Chang CJ, Yang YH, Liang YC, Chiu CJ, Chu KH, Chou HN, Chiang BL (2011) A novel phycobiliprotein alleviates allergic airway inflammation by modulating immune responses. Am J Respir Crit Care Med 183:15–25CrossRefGoogle Scholar
  4. Cornet JF, Dussap CG, Dubertret G (1992) A structured model for simulation of cultures of the cyanobacterium Spirulina platensis in photobioreactors: I. Coupling between light transfer and growth kinetics. Biotechnol Bioeng 40:817-825CrossRefGoogle Scholar
  5. Cornet J-F, Dussap C-G, Gros J-B (1994) Conversion of radiant light energy in photobioreactors. AICHE J 40:1055–1066CrossRefGoogle Scholar
  6. Cornet JF, Dussap CG, Gros JB, Binois C, Lasseur C (1995) A simplified monodimensional approach for modeling coupling between radiant light transfer and growth kinetics in photobioreactors. Chem Eng Sci 50:1489–1500CrossRefGoogle Scholar
  7. Darvehei P, Bahri PA, Moheimani NR (2018) Model development for the growth of microalgae: a review. Renew Sust Energ Rev 97:233–258CrossRefGoogle Scholar
  8. Eriksen NT (2008) Production of phycocyanin--a pigment with applications in biology, biotechnology, foods and medicine. Appl Microbiol Biotechnol 80:1–14CrossRefGoogle Scholar
  9. Fan M, Wang XQ, Duan KH, Pang GC (2008) Progress of the studies on photosensitization from Spirulina phycocyanin. Chin Bull Life Sci 20:283–286Google Scholar
  10. Fan J, Huang J, Li Y, Han F, Wang J, Li X, Wang W, Li S (2012) Sequential heterotrophy–dilution–photoinduction cultivation for efficient microalgal biomass and lipid production. Bioresour Technol 112:206–211CrossRefGoogle Scholar
  11. Fernandez FG, Camacho FG, Perez JA, Sevilla JM, Grima EM (1997) A model for light distribution and average solar irradiance inside outdoor tubular photobioreactors for the microalgal mass culture. Biotechnol Bioeng 55:701–714CrossRefGoogle Scholar
  12. Graverholt OS, Eriksen NT (2007) Heterotrophic high-cell-density fed-batch and continuous-flow cultures of Galdieria sulphuraria and production of phycocyanin. Appl Microbiol Biotechnol 77:69–75CrossRefGoogle Scholar
  13. Graziani G, Schiavo S, Nicolai MA, Buono S, Fogliano V, Pinto G, Pollio A (2013) Microalgae as human food: chemical and nutritional characteristics of the thermo-acidophilic microalga Galdieria sulphuraria. Food Funct 4:144–152CrossRefGoogle Scholar
  14. Grima EM, Camacho FG, Pérez JAS, Fernández FGA, Sevilla JMF (1997) Evaluation of photosynthetic efficiency in microalgal cultures using averaged irradiance. Enzym Microb Technol 21:375–381CrossRefGoogle Scholar
  15. Gross W, Schnarrenberger C (1995) Heterotrophic growth of two strains of the acido-thermophilic red alga Galdieria sulphuraria. Plant Cell Physiol 36:633–638Google Scholar
  16. Henkanatte-Gedera SM, Selvaratnam T, Karbakhshravari M, Myint M, Nirmalakhandan N, Van Voorhies W, Lammers PJ (2017) Removal of dissolved organic carbon and nutrients from urban wastewaters by Galdieria sulphuraria: laboratory to field scale demonstration. Algal Res 24:450–456CrossRefGoogle Scholar
  17. 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 110:1583–1594CrossRefGoogle Scholar
  18. Jiang L, Wang Y, Yin Q, Liu G, Liu H, Huang Y, Li B (2017) Phycocyanin: a potential drug for cancer treatment. J Cancer 8:3416–3429CrossRefGoogle Scholar
  19. Kuddus M, Singh P, Thomas G, Alhazimi A (2013) Recent developments in production and biotechnological applications of C-phycocyanin. Biomed Res Int 2013:742859CrossRefGoogle Scholar
  20. Leifer A (1988) The kinetics of environmental aquatic photochemistry, theory and practice. American Chemical Society, Washington, DCGoogle Scholar
  21. Moon M, Mishra SK, Kim CW, Suh WI, Park MS, Yang JW (2014) Isolation and characterization of thermostable phycocyanin from Galdieria sulphuraria. Korean J Chem Eng 31:490–495CrossRefGoogle Scholar
  22. Morcos NC, Berns M, Henry WL (1988) Phycocyanin: laser activation, cytotoxic effects, and uptake in human atherosclerotic plaque. Lasers Surg Med 8:10–17CrossRefGoogle Scholar
  23. Oesterhelt C, Schmalzlin E, Schmitt JM, Lokstein H (2007) Regulation of photosynthesis in the unicellular acidophilic red alga Galdieria sulphuraria. Plant J 51:500–511CrossRefGoogle Scholar
  24. Pleonsil P, Soogarun S, Suwanwong Y (2013) Anti-oxidant activity of holo- and apo-C-phycocyanin and their protective effects on human erythrocytes. Int J Biol Macromol 60:393–398CrossRefGoogle Scholar
  25. Pottier L, Pruvost J, Derernetz J, Cornet JF, Legrand J, Dussap CG (2001) A fully predictive model for one-dimensional light attenuation by Chlamydomonas reinhardtii in a torus photobioreactor. Biotechnol Bioeng 91:569–582CrossRefGoogle Scholar
  26. Rahman DY, Sarian FD, van Wijk A, Martinez-Garcia M, van der Maarel MJEC (2017) Thermostable phycocyanin from the red microalga Cyanidioschyzon merolae, a new natural blue food colorant. J Appl Phycol 29:1233–1239CrossRefGoogle Scholar
  27. Romay C, Armesto J, Remirez D, Gonzalez R, Ledon N, Garcia I (1998) Antioxidant and anti-inflammatory properties of C-phycocyanin from blue-green algae. Inflamm Res 47:36–41CrossRefGoogle Scholar
  28. Sarada R, Pillai MG, Ravishankar GA (1999) Phycocyanin from Spirulina sp: influence of processing of biomass on phycocyanin yield, analysis of efficacy of extraction methods and stability studies on phycocyanin. Process Biochem 34:795–801CrossRefGoogle Scholar
  29. Schmidt RA, Wiebe MG, Eriksen NT (2005) Heterotrophic high cell-density fed-batch cultures of the phycocyanin-producing red alga Galdieria sulphuraria. Biotechnol Bioeng 90:77–84CrossRefGoogle Scholar
  30. Sloth JK, Wiebe MG, Eriksen NT (2006) Accumulation of phycocyanin in heterotrophic and mixotrophic cultures of the acidophilic red alga Galdieria sulphuraria. Enzym Microb Technol 38:168–175CrossRefGoogle Scholar
  31. Sorensen L, Hantke A, Eriksen NT (2013) Purification of the photosynthetic pigment C-phycocyanin from heterotrophic Galdieria sulphuraria. J Sci Food Agric 93:2933–2938CrossRefGoogle Scholar
  32. Stramigioli C, Spiga G, Santarelli F (1982) Radiative transfer and batch photochemical reaction in a plan slab. Ind Eng Chem Fundam 21:119–123CrossRefGoogle Scholar
  33. Wan M, Zhang Z, Wang J, Huang J, Fan J, Yu A, Wang W, Li Y (2015) Sequential heterotrophy-dilution-photoinduction cultivation of Haematococcus pluvialis for efficient production of astaxanthin. Bioresour Technol 198:557–563CrossRefGoogle Scholar
  34. Wan M, Wang Z, Zhang Z, Wang J, Li S, Yu A, Li Y (2016) A novel paradigm for the high-efficient production of phycocyanin from Galdieria sulphuraria. Bioresour Technol 218:272–278CrossRefGoogle Scholar
  35. Weber A, Oesterhelt C, Gross W, Bräutigam A, Imboden L, Krassovskaya I, Linka N, Truchina J, Schneidereit J, Voll H, Voll L, Zimmermann M, Jamai A, Riekhof W, Yu B, Garavito R, Benning C (2004) EST-analysis of the thermo-acidophilic red microalga Galdieria sulphuraria reveals potential for lipid A biosynthesis and unveils the pathway of carbon export from rhodoplasts. Plant Mol Biol 55:17–32CrossRefGoogle Scholar
  36. Xie Y, Jin Y, Zeng X, Chen J, Lu Y, Jing K (2015) Fed-batch strategy for enhancing cell growth and C-phycocyanin production of Arthrospira (Spirulina) platensis under phototrophic cultivation. Bioresour Technol 180:281–287CrossRefGoogle Scholar
  37. Yun Y-S, Park JM (2001) Attenuation of monochromatic and polychromatic lights in Chlorella vulgaris suspensions. Appl Microbiol Biotechnol 55:765–770CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Haohua Wang
    • 1
  • Zhen Zhang
    • 1
  • Minxi Wan
    • 1
    Email author
  • Ruixuan Wang
    • 1
  • Jianke Huang
    • 1
  • Kaikai Zhang
    • 1
  • Jiacai Guo
    • 1
  • Wenmin Bai
    • 2
  • Yuanguang Li
    • 1
    Email author
  1. 1.State Key Laboratory of Bioreactor EngineeringEast China University of Science and TechnologyShanghaiPeople’s Republic of China
  2. 2.Jiaxing Zeyuan Bio-Products Company Ltd.ZhejiangChina

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