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Improved Carotenoid Productivity and COD Removal Efficiency by Co-culture of Rhodotorula glutinis and Chlorella vulgaris Using Starch Wastewaters as Raw Material

  • Zhiping ZhangEmail author
  • Zhengjun Pang
  • Suyue Xu
  • Tao Wei
  • Lili Song
  • Guanglu Wang
  • Jingnan Zhang
  • Xu Yang
Article
  • 24 Downloads

Abstract

Utilization of low-cost raw materials for the bio-based chemical production, such as carotenoids, by the co-culture of Rhodotorula glutinis and Chlorella vulgaris has recently become an attractive option. In this study, the primary nutrients of starch wastewater were analyzed, which were used for carotenoid production by the co-culture strategy in a 5-L fermenter around 4000 Lux light intensity. Synergistic effect of gas utilization revealed that the two species could build up the beneficial balance on mutualism. The maximum carotenoid productivity and COD removal efficiency were 12.34 mg/L and 79.6%, respectively, which were higher than those of monoculture yeast (8.31 mg/L and 54.1%). The organic acids, amino acids, and sugar removal efficiencies were increased by 85%, 31%, and 44%, respectively, and more than three kinds of carotenoids were identified compared with those of monoculture yeast. The results demonstrated that the co-culture strategy of two different nutritional microorganisms could significantly improve carotenoid productivity and COD removal efficiency.

Keywords

Rhodotorula glutinis Chlorella vulgaris Co-culture Starch wastewater Carotenoids 

Notes

Funding information

This work was supported by the National Nature Science Foundation of China (No. 21706244), the Key Research Projects of the Science and Technology Department of Henan Province (No. 172102310700; 152102110104), and the Scientific Research Funds of Zhengzhou university of Light Industry (No. 2014BSJJ033).

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no competing interests.

References

  1. 1.
    Saini, R. K., & Keum, Y. S. (2018). Microbial platforms to produce commercially vital carotenoids at industrial scale: an updated review of critical issues. Journal of Industrial Microbiology & Biotechnology.  https://doi.org/10.1007/s10295-018-2104-7.
  2. 2.
    Ligia, A. D. C. C., Karen, Y. F. K., & Susan, G. K. (2017). Microbial production of carotenoids-a review. African Journal of Biotechnology, 16(4), 139–146.CrossRefGoogle Scholar
  3. 3.
    Nigam, P. S., & Luke, J. S. (2016). Food additives: production of microbial pigments and their antioxidant properties. Current Opinion in Food Science, 7, 93–100.CrossRefGoogle Scholar
  4. 4.
    Zhou, Q., Zhang, P. Y., & Zhang, G. M. (2014). Biomass and carotenoid production in photosynthetic bacteria wastewater treatment: effects of light intensity. Bioresource Technology, 171, 330–335.CrossRefGoogle Scholar
  5. 5.
    Panesar, R., Kaur, S., & Panesar, P. S. (2015). Production of microbial pigments utilizing agro-industrial waste: a review. Current Opinion in Food Science, 1(1), 70–76.CrossRefGoogle Scholar
  6. 6.
    Hernández-Almanza, A., Montanez, J. C., Aguilar-González, M. A., Martínez-Ávila, C., Rodríguez-Herrera, R., & Aguilar, C. N. (2014). Rhodotorula glutinis, as source of pigments and metabolites for food industry. Food Bioscience, 5, 64–72.CrossRefGoogle Scholar
  7. 7.
    Mannazzu, I., Landolfo, S., Silva, T. L. D., & Buzzini, P. (2015). Red yeasts and carotenoid production: outlining a future for non-conventional yeasts of biotechnological interest. World Journal of Microbiology and Biotechnology, 31(11), 1665–1673.CrossRefGoogle Scholar
  8. 8.
    Marova, I., Carnecka, M., Halienova, A., Certik, M., Dvorakova, T., & Haronikova, A. (2012). Use of several waste substrates for carotenoid-rich yeast biomass production. Journal of Environmental Management, 95, S338–S342.CrossRefGoogle Scholar
  9. 9.
    Zhang, Z. P., Zhang, X., & Tan, T. W. (2014). Lipid and carotenoid production by Rhodotorula glutinis under irradiation/high-temperature and dark/low-temperature cultivation. Bioresource Technology, 157, 149–153.CrossRefGoogle Scholar
  10. 10.
    Zhang, Z. P., Ji, H. R., Gong, G. P., Zhang, X., & Tan, T. W. (2014). Synergistic effects of oleaginous yeast Rhodotorula glutinis and microalga Chlorella vulgaris for enhancement of biomass and lipid yields. Bioresource Technology, 164, 93–99.CrossRefGoogle Scholar
  11. 11.
    Patias, L. D., Fernandes, A. S., Petry, F. C., Mercadante, A. Z., Jacoblopes, E., & Zepka, L. Q. (2017). Carotenoid profile of three microalgae/cyanobacteria species with peroxyl radical scavenger capacity. Food Research International, 100(Pt 1), 260–266.CrossRefGoogle Scholar
  12. 12.
    Gateau, H., Solymosi, K., Marchand, J., & Schoefs, B. (2017). Carotenoids of microalgae used in food industry and medicine. Mini Reviews in Medicinal Chemistry, 16(999), 1140–1172.Google Scholar
  13. 13.
    Li, X., Hu, H. Y., Gan, K., & Sun, Y. X. (2010). Effects of different nitrogen and phosphorus concentrations on the growth nutrient uptake, and lipid accumulation of a freshwater microalga Scenedesmus sp. Bioresource Technology, 101, 5494–5500.CrossRefGoogle Scholar
  14. 14.
    Manowattana, A., Techapun, C., Watanabe, M., & Chaiyaso, T. (2017). Bioconversion of biodiesel-derived crude glycerol into lipids and carotenoids by an oleaginous red yeast, Sporidiobolus pararoseus KM281507 in an airlift bioreactor. Journal of Bioscience and Bioengineering, 125, 59–66.CrossRefGoogle Scholar
  15. 15.
    Inbaraj, B. S., Chien, J. T., & Chen, B. H. (2006). Improved high performance liquid chromatographic method for determination of carotenoids in the microalga Chlorella pyrenoidosa. Journal of Chromatography A, 1102(1-2), 193–199.CrossRefGoogle Scholar
  16. 16.
    Saini, R. K., & Keum, Y. S. (2017). Progress in microbial carotenoids production. Indian Journal Microbiology, 57, 1–2.CrossRefGoogle Scholar
  17. 17.
    Dias, C., Sousa, S., Caldeira, J., Reis, A., & Lopes, D. S. T. (2015). New dual-stage pH control fed-batch cultivation strategy for the improvement of lipids and carotenoids production by the red yeast Rhodosporidium toruloides NCYC 921. Bioresource Technology, 189, 309–318.CrossRefGoogle Scholar
  18. 18.
    Cardoso, L. A., Jäckel, S., Karp, S. G., Framboisier, X., Chevalot, I., & Marc, I. (2016). Improvement of Sporobolomyces ruberrimus carotenoids production by the use of raw glycerol. Bioresource Technology, 200, 374–379.CrossRefGoogle Scholar
  19. 19.
    Srinivasan, R., Babu, S., & Gothandam, K. M. (2017). Accumulation of phytoene, a colorless carotenoid by inhibition of phytoene desaturase (PDS) gene in Dunaliella salina V-101. Bioresource Technology, 242, 311–318.CrossRefGoogle Scholar
  20. 20.
    Magdouli, S., Brar, S. K., & Blais, J. F. (2016). Co-culture for lipid production: advances and challenges. Biomass & Bioenergy, 92, 20–30.CrossRefGoogle Scholar
  21. 21.
    Huang, C., Luo, M. T., Chen, X. F., Xiong, L., Li, X. M., & Chen, X. D. (2017). Recent advances and industrial viewpoint for biological treatment of wastewaters by oleaginous microorganisms. Bioresource Technology, 232, 398–407.CrossRefGoogle Scholar
  22. 22.
    Yen, H. W., Chen, P. W., & Chen, L. J. (2015). The synergistic effects for the co-cultivation of oleaginous yeast-Rhodotorula glutinis and microalgae-Scenedesmus obliquus on the biomass and total lipids accumulation. Bioresource Technology, 184, 148–152.CrossRefGoogle Scholar
  23. 23.
    Liu, M., Zhang, X., & Tan, T. W. (2016). The effect of amino acids on lipid production and nutrient removal by Rhodotorula glutinis cultivation in starch wastewater. Bioresource Technology, 218, 712–717.CrossRefGoogle Scholar
  24. 24.
    Braunwald, T., Schwemmlein, L., Graeff-Hönninger, S., French, W., Hernandez, R., Holmes, W., & Claupein, W. (2013). Effect of different C/N ratios on carotenoid and lipid production by Rhodotorula glutinis. Apply Microbiology and Biotechnology, 97(14), 6581–6588.CrossRefGoogle Scholar
  25. 25.
    Karthikeyan, O. P., Hao, H. T. N., Razaghi, A., & Heimann, K. (2018). Recycling of food waste for fuel precursors using an integrated bio-refinery approach. Bioresource Technology, 248, 194–198.CrossRefGoogle Scholar
  26. 26.
    Cheirsilp, B., Suwannarat, W., & Niyomdecha, R. (2011). Mixed culture of oleaginous yeast Rhodotorula glutinis and microalga Chlorella vulgaris for lipid production from industrial wastes and its use as biodiesel feedstock. New Biotechnology, 28(4), 362–368.CrossRefGoogle Scholar
  27. 27.
    Xue, F. Y., Miao, J. X., Zhang, X., & Tan, T. W. (2010). A new strategy for lipid production by mix cultivation of Spirulina platensis and Rhodotorula glutinis. Applied Biochemistry and Biotechnology, 160(2), 498–503.CrossRefGoogle Scholar
  28. 28.
    Vera, L., Sun, W., Iftikhar, M., & Liu, J. T. (2015). LCA based comparative study of a microbial oil production starch wastewater treatment plant and its improvements with the combination of CHP system in Shandong, China. Resources, Conservation & Recycling, 96, 1–10.CrossRefGoogle Scholar
  29. 29.
    Ling, J., Nip, S., Cheok, W. L., Toledo, R. A., & Shim, H. (2014). Lipid production by a mixed culture of oleaginous yeast and microalga from distillery and domestic mixed wastewater. Bioresource Technology, 173, 132–139.CrossRefGoogle Scholar
  30. 30.
    Cai, S. Q., Hu, C. Q., & Du, S. B. (2007). Comparisons of growth and biochemical composition between mixed culture of alga and yeast and monocultures. Journal of Bioscience and Bioengineering, 104(5), 391–397.CrossRefGoogle Scholar
  31. 31.
    Yadav, J. S. S., Bezawada, J., Ajila, C. M., Yan, S., Tyagi, R. D., & Surampalli, R. Y. (2014). Mixed culture of Kluyveromyces marxianus and Candida krusei for single-cell protein production and organic load removal from whey. Bioresource Technology, 164, 119–127.CrossRefGoogle Scholar
  32. 32.
    Qin, L., Wei, D., Wang, Z. M., & Alam, M. A. (2018). Advantage assessment of mixed culture of Chlorella vulgaris and Yarrowia lipolytica for treatment of liquid digestate of yeast industry and cogeneration of biofuel feedstock. Applied Biochemistry and Biotechnology.  https://doi.org/10.1007/s12010-018-2854-8.
  33. 33.
    Schneider, T., Graeff-Hönninger, S., French, W. T., Hernandez, R., Merkt, N., Claupein, W., Hetrick, M., & Phamb, P. (2013). Lipid and carotenoid production by oleaginous red yeast Rhodotorula glutinis cultivated on brewery effluents. Energy, 61, 34–43.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.School of Food and BioengineeringZhengzhou University of Light IndustryZhengzhouPeople’s Republic of China
  2. 2.Collaborative Innovation Center of Food Production and SafetyZhengzhouPeople’s Republic of China

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