Advertisement

Applied Microbiology and Biotechnology

, Volume 103, Issue 21–22, pp 8863–8874 | Cite as

The growth and lutein accumulation in heterotrophic Chlorella protothecoides provoked by waste Monascus fermentation broth feeding

  • Zhenyao Wang
  • Rong Zhou
  • Yufang Tang
  • Ziting Wang
  • Bo Feng
  • Yuqin LiEmail author
Biotechnological products and process engineering
  • 52 Downloads

Abstract

Although the potential of heterotrophic microalgae served as a sustainable source for lutein, it was still crucial to formulate a suitable medium to offset the cost involved in algal biomass cultivation while improve inherent lutein productivity. The objective of this study was to investigate the feasibilities of waste Monascus fermentation broth medium (MFBM) toward heterotrophic Chlorella protothecoides-enriched lutein. The results indicated that C. protothecoides subjected to MFBM batch feeding achieved 7.1 g/L biomass and 7.27 mg/g lutein. The resulting lutein productivity (7.34 mg/L/day) represented 1.54-fold more than that of frequently used Basal medium. Concurrently, the effective metabolism and absorption of carbon, nitrogen, and phosphorus in MFBM by C. subellipsoidea cultivation make it easily complied with the permissible dischargeable limits for fermentation broth. When response to fed-batch culture mode, the biomass and lutein productivity peaked 20.4 g/L and 9.11 mg/L/day with concentrated MFBM feeding. Transcriptomics data hinted that MFBM feeding manipulated lutein biosynthesis key checkpoints (e.g., lycopene β-cyclase and lycopene ε-cyclase) while accelerated energy pathways (e.g., glycolysis and TCA cycle) to contribute such high lutein productivity in C. protothecoides. These encouraging findings not only provided indications in applying nutrient-rich fermentation broth for affordable microalgae cultivation but also presented possibilities in linking algal high value-added products like lutein with high-efficient biological nutrition removal from industrial fermentation processing.

Keywords

Chlorella protothecoides Monascus fermentation broth Heterotrophic Lutein productivity Transcriptomics 

Notes

Funding information

This work was supported by National Natural Science Foundation of China (21676228, 21777135), Hunan Provincial Natural Science Foundation of China (2017JJ3300), Scientific Research Fund of Hunan Provincial Education Department (18A068), and Collaborative Innovation Center of New Chemical Technologies for Environmental Benignity and Efficient Resource Utilization.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical statement

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

Supplementary material

253_2019_10150_MOESM1_ESM.xlsx (997 kb)
ESM 1 (XLSX 3212 kb)
253_2019_10150_MOESM2_ESM.pdf (997 kb)
ESM 2 (PDF 295 kb)

References

  1. Araya B, Gouveia L, Nobre B, Reis A, Chamy R, Poirrier P (2014) Evaluation of the simultaneous production of lutein and lipids using a vertical alveolar panel bioreactor for three Chlorella species. Algal Res 6:218–222.  https://doi.org/10.1016/j.algal.2014.06.003 CrossRefGoogle Scholar
  2. Bermejo E, Ruiz-Domínguez MC, Cuaresma M, Vaquero I, Ramos-Merchante A, Vega JM, Vílchez C, Garbayo I (2018) Production of lutein, and polyunsaturated fatty acids by the acidophilic eukaryotic microalga Coccomyxa onubensis under abiotic stress by salt or ultraviolet light. J Biosci Bioeng 125:669–675.  https://doi.org/10.1016/j.jbiosc.2017.12.025 CrossRefPubMedGoogle Scholar
  3. Campenni' L, Nobre BP, Santos CA, Oliveira AC, Aires-Barros MR, Palavra AM, Gouveia L (2013) Carotenoid and lipid production by the autotrophic microalga chlorella protothecoides under nutritional, salinity, and luminosity stress conditions. Appl microbiol Biotechnol 97:1383–1393.  https://doi.org/10.1007/s00253-012-4570-6 CrossRefPubMedGoogle Scholar
  4. Chen CY, Jesisca HC, Lee DJ, Chang CH, Chang JS (2016) Production, extraction and stabilization of lutein from microalga Chlorella sorokiniana MB-1. Bioresource Technol 200:500–505.  https://doi.org/10.1016/j.biortech.2015.10.071 CrossRefGoogle Scholar
  5. Chen CY, Lu IC, Nagarajan D, Chang CH, Ng IS, Lee DJ, Chang JS (2018) A highly efficient two-stage cultivation strategy for lutein production using heterotrophic culture of Chlorella sorokiniana MB-1-M12. Bioresource Technol 253:141–147.  https://doi.org/10.1016/j.biortech.2018.01.027 CrossRefGoogle Scholar
  6. Chen JH, Chen CY, Hasunuma T, Kondo A, Chang CH, Ng IS, Chang JS (2019) Enhancing lutein production with mixotrophic cultivation of Chlorella sorokiniana MB-1-M12 using different bioprocess operation strategies. Bioresource Technol 278:17–25.  https://doi.org/10.1016/j.biortech.2019.01.041 CrossRefGoogle Scholar
  7. Flórez-Miranda L, Cañizares-Villanueva RO, Melchy-Antonio O, Martínez-Jerónimo F, Flores-Ortíz CM (2017) Two stage heterotrophy/photoinduction culture of Scenedesmus incrassatulus: potential for lutein production. J Biotechnol 262:67–74.  https://doi.org/10.1016/j.jbiotec.2017.09.002 CrossRefPubMedGoogle Scholar
  8. Heo J, Shin DS, Cho K, Cho DH, Lee YJ, Kim HS (2018) Indigenous microalga Parachlorella sp. JD-076 as a potential source for lutein production: optimization of lutein productivity via regulation of light intensity and carbon source. Algal RES 33:1–7.  https://doi.org/10.1016/j.algal.2018.04.029 CrossRefGoogle Scholar
  9. Ho SH, Chan MC, Liu CC, Chen CY, Lee WL, Lee DJ, Chang JS (2014) Enhancing lutein productivity of an indigenous microalga Scenedesmus obliquus FSP-3 using light-related strategies. Bioresource Technol 152:275–282.  https://doi.org/10.1016/j.biortech.2013.11.031 CrossRefGoogle Scholar
  10. Ho SH, Xie YP, Chan MC, Liu CC, Chen CY, Lee DJ, Huang CC, Chang JS (2015) Effects of nitrogen source availability and bioreactor operating strategies on lutein production with Scenedesmus obliquus FSP-3. Bioresource Technol 184:131–138.  https://doi.org/10.1016/j.biortech.2014.10.062 CrossRefGoogle Scholar
  11. Hu JJ, Nagarajan D, Zhang QG, Chang JS, Lee DJ (2018) Heterotrophic cultivation of microalgae for pigment production: A review. Biotechnol Adv 36:54–67.  https://doi.org/10.1016/j.biotechadv.2017.09.009 CrossRefPubMedGoogle Scholar
  12. Huo SH, Kong M, Zhu FF, Zou B, Wang F, Xu L, Zhang CS, Huang DM (2018) Mixotrophic Chlorella sp. UJ-3 cultivation in the typical anaerobic fermentation effluents. Bioresource Technol 249:219–225.  https://doi.org/10.1016/j.biortech.2017.10.042 CrossRefGoogle Scholar
  13. Jeon JY, Kwon JS, Kang ST, Kim BR, Jung Y, Han JG, Park JH, Hwang JK (2014) Optimization of culture media for large-scale lutein production by heterotrophic Chlorella vulgaris. Biotechnol Progr 30:736–743.  https://doi.org/10.1002/btpr.1889 CrossRefGoogle Scholar
  14. Lin JH, Lee DJ, Chang JS (2015) Lutein production from biomass: Marigold flowers versus microalgae. Bioresource Technol 184:421–428.  https://doi.org/10.1016/j.biortech.2014.09.099 CrossRefGoogle Scholar
  15. Liu CH, Chang CY, Liao Q, Zhu X, Chang JS (2013) Photoheterotrophic growth of Chlorella vulgaris ESP6 on organic acids from dark hydrogen fermentation effluents. Bioresource Technol 145:331–336.  https://doi.org/10.1016/j.biortech.2012.12.111 CrossRefGoogle Scholar
  16. Ma RJ, Zhao XR, Xie YP, Ho SH, Chen JF (2019) Enhancing lutein productivity of Chlamydomonas sp. via high-intensity light exposure with corresponding carotenogenic genes expression profiles. Bioresource Technol 275:416–420.  https://doi.org/10.1016/j.biortech.2018.12.109 CrossRefGoogle Scholar
  17. Perez-Garcia O, Escalante FME, de Bashan LE, Bashan Y (2011) Heterotrophic cultures of microalgae: metabolism and potential products. Water Res 45:11–36.  https://doi.org/10.1016/j.watres.2010.08.037 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Ren HY, Kong FY, Ma J, Zhao L, Xie GJ, Xing DF, Guo WQ, Liu BF, Ren NQ (2018) Continuous energy recovery and nutrients removal from molasses wastewater by synergistic system of dark fermentation and algal culture under various fermentation types. Bioresource Technol 252:110–117.  https://doi.org/10.1016/j.biortech.2017.12.092 CrossRefGoogle Scholar
  19. Shi XM, Chen F (2002) High-yield production of lutein by the green microalga Chlorella protothecoidesin heterotrophic fed-batch culture. Biotechnol Progr 18:723–727.  https://doi.org/10.1021/bp0101987 CrossRefGoogle Scholar
  20. Wei D, Chen F, Chen G, Zhang XW, Liu LJ, Zhang H (2008) Enhanced production of lutein in heterotrophic Chlorella protothecoides by oxidative stress. Sci China Ser C 51:1088–1093.  https://doi.org/10.1007/s11427-008-0145-2 CrossRefGoogle Scholar
  21. Wu ZY, Wu SM, Shi XM (2007) Supercritical fluid extraction and determination of lutein in heterotrophically cultivated Chlorella pyrenoidosa. J Food Process Eng 30:174–185.  https://doi.org/10.1111/j.1745-4530.2007.00102.x CrossRefGoogle Scholar
  22. Xie Y, Zhao X, Chen J, Yang X, Ho SH, Wang B, Chang JS, Shen Y (2017) Enhancing cell growth and lutein productivity of Desmodesmus sp. F51 by optimal utilization of inorganic carbon sources and ammonium salt. Bioresource Technol 244:664–671.  https://doi.org/10.1016/j.biortech.2017.08.022 CrossRefGoogle Scholar
  23. Yeh TJ, Tseng YF, Chen YC, Hsiao Y, Lee PC, Chen TJ, Chen CY, Kao CY, Chang JS, Chen JC (2017) Transcriptome and physiological analysis of a lutein-producing alga Desmodesmus sp. reveals the molecular mechanisms for high lutein productivity. Algal Res 21:103–119.  https://doi.org/10.1016/j.algal.2016.11.013 CrossRefGoogle Scholar
  24. Zhao XR, Ma RJ, Liu XT, Ho SH, Xie YP, Chen JF (2019) Strategies related to light quality and temperature to improve lutein production of marine microalga Chlamydomonas sp. Bioproc Biosyst Eng 42:435–443.  https://doi.org/10.1007/s00449-018-2047-4 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Zhenyao Wang
    • 1
  • Rong Zhou
    • 1
  • Yufang Tang
    • 1
  • Ziting Wang
    • 1
  • Bo Feng
    • 1
  • Yuqin Li
    • 1
    Email author
  1. 1.Food Science and Engineering, School of Chemical EngineeringXiangtan UniversityXiangtanChina

Personalised recommendations