Skip to main content

Advertisement

SpringerLink
Log in

Effects of urea on cell growth and physiological response in pigment biosynthesis in mixotrophic Chromochloris zofingiensis

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

The mixotrophic cultivation of Chromochloris zofingiensis (Chlorophyta, Trebouxiophyceae) under various urea concentrations was investigated for biomass and pigment production. The results showed that urea was favorable for biomass production with the highest biomass concentration of 8.86 g L−1 at 3.81 mmol L−1 of urea. When urea concentration was lowered to 0.19 mmol L−1, the highest content (0.99 mg g−1) and yield (4.11 mg L−1) of total carotenoids was reached due to an extremely high C/N ratio. Principle component analysis revealed that urea concentrations could indeed affect biomass production and pigment biosynthesis involving intracellular nitrogen assimilation and catabolism associated with chloroplast degradation. Our present study evaluates the feasibility of using urea for C. zofingiensis cultivation and provides new insights for a better understanding of the close relationships between urea metabolism and pigment biosynthesis in mixotrophic C. zofingiensis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Aghaie P, Tafreshi SAH, Ebrahimi MA, Haerinasab M (2018) Tolerance evaluation and clustering of fourteen tomato cultivars grown under mild and severe drought conditions. Scient Hort 232:1–12

    Article  Google Scholar 

  • Akbar TA, Hassan QK, Achari G (2011) A methodology for clustering lakes in Alberta on the basis of water quality parameters. Acta Hydrochim Hydrobiol 39:916–924

    CAS  Google Scholar 

  • Bar E, Rise MM, Arad S (1995) Pigment and structural character in Chlorella zofingiensis upon light and nitrogen stress. J Plant Physiol 146:527–534

    Article  CAS  Google Scholar 

  • Batista AD, Rosa RM, Machado M, Magalhães AS, Shalaguti BA, Gomes PF, Covell L, Vaz MG, Araújo WL, Nunes-Nesi A (2019) Increased urea availability promotes adjustments in C/N metabolism and lipid content without impacting growth in Chlamydomonas reinhardtii. Metabolomics 15:31

    Article  Google Scholar 

  • Beatty PH, Klein MS, Fischer JJ, Lewis IA, Muench DG, Good AG (2016) Understanding plant nitrogen metabolism through metabolomics and computational approaches. Plants 5:1–16

    Article  Google Scholar 

  • Chen C-Y, Lu I-C, Nagarajan D, Chang C-H, Ng I-S, Lee D-J, Chang J-S (2018) A highly efficient two-stage cultivation strategy for lutein production using heterotrophic culture of Chlorella sorokiniana MB-1-M12. Bioresour Technol 253:141–147

    Article  CAS  Google Scholar 

  • Chen J-H, Liu L, Wei D (2017a) Enhanced production of astaxanthin by Chromochloris zofingiensis in a microplate-based culture system under high light irradiation. Bioresour Technol 245:518–529

    Article  CAS  Google Scholar 

  • Chen J, Wei D, Pohnert G (2017b) Rapid estimation of astaxanthin and the carotenoid-to-chlorophyll ratio in the green microalga Chromochloris zofingiensis using flow cytometry. Mar Drugs 15:231–253

    Article  Google Scholar 

  • Cheng P, Wang Y, Oseiwusu D, Wang Y, Liu T (2018) Development of nitrogen supply strategy for Scenedesmus rubescens attached cultivation toward growth and lipid accumulation. Bioprocess Biosyst Eng 41:435–442

    Article  CAS  Google Scholar 

  • Christaki E, Bonos E, Giannenas I, Florou-Paneri P (2013) Functional properties of carotenoids originating from algae. J Sci Food Agric 93:5–11

    Article  CAS  Google Scholar 

  • Dong HP, Huang KX, Wang HL, Lu SH, Cen JY, Dong YL (2014) Understanding strategy of nitrate and urea assimilation in a Chinese strain of Aureococcus anophagefferens through RNA-Seq analysis. PLoS One 9:e111069

    Article  Google Scholar 

  • Feng P, Xu Z, Qin L, Alam MA, Wang Z, Zhu S (2020) Effects of different nitrogen sources and light paths of flat plate photobioreactors on the growth and lipid accumulation of Chlorella sp. GN1 outdoors. Bioresour Technol 301:122762. https://doi.org/10.1016/j.biortech.2020.122762

  • Guerin M, Huntley ME, Olaizola M (2003) Haematococcus astaxanthin: applications for human health and nutrition. Trends Biotechnol 21:210–216

    Article  CAS  Google Scholar 

  • Ip PF, Wong KH, Chen F (2004) Enhanced production of astaxanthin by the green microalga Chlorella zofingiensis in mixotrophic culture. Process Biochem 39:1761–1766

    Article  CAS  Google Scholar 

  • Kleinegris DMM, van Es MA, Janssen M, Brandenburg WA, Wijffels RH (2010) Carotenoid fluorescence in Dunaliella salina. J Appl Phycol 22:645–649

    Article  CAS  Google Scholar 

  • Liu J, Mao X, Zhou W, Guarnieri MT (2016) Simultaneous production of triacylglycerol and high-value carotenoids by the astaxanthin-producing oleaginous green microalga Chlorella zofingiensis. Bioresour Technol 214:319–327

    Article  CAS  Google Scholar 

  • Liu J, Sun Z, Gerken H, Liu Z, Jiang Y, Chen F (2014) Chlorella zofingiensis as an alternative microalgal producer of astaxanthin: biology and industrial potential. Mar Drugs 12:3487–3515

    Article  Google Scholar 

  • Lorenz RT, Cysewski GR (2000) Commercial potential for Haematococcus microalgae as a natural source of astaxanthin. Trends Biotechnol 18:160–167

    Article  CAS  Google Scholar 

  • Maroneze MM, Jacob-Lopes E, Zepka LQ, Roca M, Pérez-Gálvez A (2019) Esterified carotenoids as new food components in cyanobacteria. Food Chem 287:295–302

    Article  Google Scholar 

  • Mulders KJM, Weesepoel Y, Bodenes P, Lamers PP, Vincken J-P, Martens DE, Gruppen H, Wijffels RH (2015) Nitrogen-depleted Chlorella zofingiensis produces astaxanthin, ketolutein and their fatty acid esters: a carotenoid metabolism study. J Appl Phycol 27:125–140

    Article  CAS  Google Scholar 

  • Orosa M, Franqueira D, Cid A, Abalde J (2005) Analysis and enhancement of astaxanthin accumulation in Haematococcus pluvialis. Bioresour Technol 96:373–378

    Article  CAS  Google Scholar 

  • Peng J, Xiang W, Tang Q, Sun N, Chen F, Yuan J (2008) Comparative analysis of astaxanthin and its esters in the mutant E1 of Haematococcus pluvialis and other green algae by HPLC with a C30 column. Sci China Ser C 51:1108–1115

    Article  CAS  Google Scholar 

  • Perez-Garcia O, Escalante FME, de Bashan LE, Bashan Y (2011) Heterotrophic cultures of microalgae: metabolism and potential products. Water Res 45:11–36

    Article  CAS  Google Scholar 

  • Pinton R, Tomasi N, Zanin L (2016) Molecular and physiological interactions of urea and nitrate uptake in plants. Plant Signal Behav 11:1–4

    Article  Google Scholar 

  • Raven JA, Giordano M (2016) Combined nitrogen. In: Borowitzka MA, Beardall J, Raven JA (eds) The physiology of microalgae. Springer, Dordrecht, pp 143–154

    Chapter  Google Scholar 

  • Ribeiro DM, Roncaratti LF, Possa GC, Garcia LC, Cançado LJ, Williams TCR, Brasil BSAF (2020) A low-cost approach for Chlorella sorokiniana production through combined use of urea, ammonia and nitrate based fertilizers. Bioresour Technol Rep 9:100354

    Article  Google Scholar 

  • Saini RK, Keum Y-S (2019) Microbial platforms to produce commercially vital carotenoids at industrial scale: an updated review of critical issues. J Ind Microbiol Biotechnol 46:657–674

    Article  CAS  Google Scholar 

  • Santos IC, Smuts J, Choi WS, Kim Y, Kim SB, Schug KA (2018) Analysis of bacterial FAMEs using gas chromatography – vacuum ultraviolet spectroscopy for the identification and discrimination of bacteria. Talanta 182:536–543

    Article  CAS  Google Scholar 

  • Sun N, Wang Y, Li YT, Huang JC, Chen F (2008) Sugar-based growth, astaxanthin accumulation and carotenogenic transcription of heterotrophic Chlorella zofingiensis (Chlorophyta). Process Biochem 43:1288–1292

    Article  CAS  Google Scholar 

  • Tekin HO (2016) Nitrogen source, an important determinant of fatty acid accumulation and profile in Scenedesmus obliquus. Acta Phys Polon 130:428–433

    Article  Google Scholar 

  • Veaudor T, Cassier-Chauvat C, Chauvat F (2019) Genomics of urea transport and catabolism in cyanobacteria: biotechnological implications. Front Microbiol 10:2052

    Article  Google Scholar 

  • Wang FF, Gao BY, Wu MM, Huang LD, Zhang CW (2019) A novel strategy for the hyper-production of astaxanthin from the newly isolated microalga Haematococcus pluvialis JNU35. Algal Res 39:1–9

    Google Scholar 

  • Witte CP (2011) Urea metabolism in plants. Plant Sci 180:431–438

    Article  CAS  Google Scholar 

  • Xue J, Lee C (2011) Using principal components analysis (PCA) with cluster analysis to study the organic geochemistry of sinking particles in the ocean. Org Geol 42:356–367

    CAS  Google Scholar 

  • Zanin L, Zamboni A, Monte R, Tomasi N, Varanini Z, Cesco S, Pinton R (2015) Transcriptomic analysis highlights reciprocal interactions of urea and nitrate for nitrogen acquisition by maize roots. Plant Cell Physiol 56:532–548

    Article  CAS  Google Scholar 

  • Zhang Z, Huang JJ, Sun DZ, Lee Y, Chen F (2017) Two-step cultivation for production of astaxanthin in Chlorella zofingiensis using a patented energy-free rotating floating photobioreactor (RFP). Bioresour Technol 224:515–522

    Article  CAS  Google Scholar 

Download references

Funding

This work was funded by the Key Project of Guangdong Basic and Applied Basic Research Fundation (Dongguan Joint Fund) (Grant No. 2019B1515120002), the District Joint Fund for Young Scientists of Guangdong Basic and Applied Basic Research Fundation (Grant No. 2019A1515110591), and the SinoPec Technology Development Program (Grant Nos. 218017-1 and 36100002-19-FW2099-0035).

Author information

Authors and Affiliations

  1. School of Food Science and Engineering, South China University of Technology, Guangzhou, 510641, People’s Republic of China

    Junhui Chen, Xiaoli Jiang & Dong Wei

Authors
  1. Junhui Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiaoli Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dong Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dong Wei.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, J., Jiang, X. & Wei, D. Effects of urea on cell growth and physiological response in pigment biosynthesis in mixotrophic Chromochloris zofingiensis. J Appl Phycol 32, 1607–1618 (2020). https://doi.org/10.1007/s10811-020-02114-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-020-02114-3

Keywords

Search

Navigation