Astaxanthin accumulation difference between non-motile cells and akinetes of Haematococcus pluvialis was affected by pyruvate metabolism

Lei Fang , Jingkui Zhang , Zhongnan Fei , Minxi Wan

Bioresources and Bioprocessing ›› 2020, Vol. 7 ›› Issue (1) : 5

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Bioresources and Bioprocessing ›› 2020, Vol. 7 ›› Issue (1) : 5 DOI: 10.1186/s40643-019-0293-1
Research

Astaxanthin accumulation difference between non-motile cells and akinetes of Haematococcus pluvialis was affected by pyruvate metabolism

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Abstract

Background

Haematococcus pluvialis is the best source of natural astaxanthin, known as the king of antioxidants. H. pluvialis have four cell forms: spore, motile cell, non-motile cell and akinete. Spores and motile cells are susceptible to photoinhibition and would die under photoinduction conditions. Photoinduction using non-motile cells as seeds could result in a higher astaxanthin production than that using akinetes. However, the mechanism of this phenomenon has not been clarified.

Results

Transcriptome was sequenced and annotated to illustrate the mechanism of this phenomenon. All differentially expressed genes involved in astaxanthin biosynthesis were up-regulated. Particularly, chyb gene was up-regulated by 16-fold, improving the conversion of β-carotene into astaxanthin. Pyruvate was the precursor of carotenoids biosynthesis. Pyruvate kinase gene expression level was increased by 2.0-fold at the early stage of akinetes formation. More changes of gene transcription occurred at the early stage of akinetes formation, 52.7% and 51.9% of total DEGs in control group and treatment group, respectively.

Conclusions

Genes transcription network was constructed and the synthesis mechanism of astaxanthin was clarified. The results are expected to further guide the in-depth optimization of the astaxanthin production process in H. pluvialis by improving pyruvate metabolism.

Keywords

Astaxanthin / Haematococcus pluvialis / Pyruvate / Transcriptome

Cite this article

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Lei Fang, Jingkui Zhang, Zhongnan Fei, Minxi Wan. Astaxanthin accumulation difference between non-motile cells and akinetes of Haematococcus pluvialis was affected by pyruvate metabolism. Bioresources and Bioprocessing, 2020, 7(1): 5 DOI:10.1186/s40643-019-0293-1

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References

[1]

Borowitzka MA, Huisman JM, Osborn A. Culture of the astaxanthin-producing green alga Haematococcus pluvialis 1. Effects of nutrients on growth and cell type. J Appl Phycol, 1991, 3: 295-304.

[2]

Chen T, Wei D, Chen G, Wang Y, Chen F. Employment of organic acids to enhance astaxanthin formation in heterotrophic Chlorella zofingiensis. J Food Process Preserv, 2009, 33: 271-284.

[3]

Chen G, Wang B, Han D, Sommerfeld M, Lu Y, Chen F, Hu Q. Molecular mechanisms of the coordination between astaxanthin and fatty acid biosynthesis in Haematococcus pluvialis (Chlorophyceae). Plant J, 2015, 81: 95-107.

[4]

Cheng J, Li K, Zhu Y, Yang W, Zhou J, Cen K. Transcriptome sequencing and metabolic pathways of astaxanthin accumulated in Haematococcus pluvialis mutant under 15% CO2. Bioresour Technol, 2017, 228: 99-105.

[5]

Choi YE, Yun YS, Park JM, Yang JW. Determination of the time transferring cells for astaxanthin production considering two-stage process of Haematococcus pluvialis cultivation. Bioresour Technol, 2011, 102: 11249-11253.

[6]

Gao Z, Meng C, Zhang X, Xu D, Miao X, Wang Y, Yang L, Lv H, Chen L, Ye N. Induction of salicylic acid (SA) on transcriptional expression of eight carotenoid genes and astaxanthin accumulation in Haematococcus pluvialis. Enzyme Microb Technol, 2012, 51: 225-230.

[7]

Gao Z, Meng C, Zhang X, Xu D, Zhao Y, Wang Y, Lv H, Liming Y, Chen L, Ye N. Differential expression of carotenogenic genes, associated changes on astaxanthin production and photosynthesis features induced by JA in H. pluvialis. PLoS ONE, 2012, 7: e42243.

[8]

Gao Z, Meng C, Gao H, Li Y, Zhang X, Xu D, Zhou S, Liu B, Su Y, Ye N. Carotenoid genes transcriptional regulation for astaxanthin accumulation in fresh water unicellular alga Haematococcus pluvialis by gibberellin A3 (GA3). Indian J Biochem Biophys, 2013, 50: 548-553.

[9]

Gao Z, Miao X, Zhang X, Wu G, Guo Y, Wang M, Li B, Li X, Gao Y, Hu S, Sun J, Cui J, Meng C, Li Y. Comparative fatty acid transcriptomic test and iTRAQ-based proteomic analysis in Haematococcus pluvialis upon salicylic acid (SA) and jasmonic acid (JA) inductions. Algal Res, 2016, 17: 277-284.

[10]

García-Malea MC, Acién FG, Fernández JM, Cerón MC, Molina E. Continuous production of green cells of Haematococcus pluvialis: modeling of the irradiance effect. Enzyme Microb Technol, 2006, 38: 981-989.

[11]

Gu W, Xie X, Gao S, Zhou W, Pan G, Wang G. Comparison of different cells of Haematococcus pluvialis reveals an extensive acclimation mechanism during its aging process: from a perspective of photosynthesis. PLoS ONE, 2013, 8: e67028.

[12]

Hata N, Ogbonna JC, Hasegawa Y, Taroda H, Tanaka H. Production of astaxanthin by Haematococcus pluvialis in a sequential heterotrophic-photoautotrophic culture. J Appl Phycol, 2001, 13: 395-402.

[13]

He P, Duncan J, Barber J. Astaxanthin accumulation in the green alga Haematococcus pluvialis: effects of cultivation parameters. J Integr Plant Biol, 2007, 49: 447-451.

[14]

He B, Hou L, Dong M, Shi J, Huang X, Ding Y, Cong X, Zhang F, Zhang X, Zang X. Transcriptome analysis in Haematococcus pluvialis: astaxanthin induction by high light with acetate and Fe(2). Int J Mol Sci, 2018, 19: 175-193.

[15]

Huang JC, Chen F, Sandmann G. Stress-related differential expression of multiple β-carotene ketolase genes in the unicellular green alga Haematococcus pluvialis. J Biotechnol, 2006, 122: 176-185.

[16]

Huerlimann R, Heimann K. Comprehensive guide to acetyl-carboxylases in algae. Crit Rev Biotechnol, 2013, 33: 49-65.

[17]

Kang CD, Lee JS, Park TH, Sim SJ. Comparison of heterotrophic and photoautotrophic induction on astaxanthin production by Haematococcus pluvialis. Appl Microbiol Biotechnol, 2005, 68: 237-241.

[18]

Karsten H, Maximilian K, Jens R, Paul S, Graeme N, Klaus A. Determination of astaxanthin and astaxanthin esters in the microalgae Haematococcus pluvialis by LC-(APCI)MS and characterization of predominant carotenoid isomers by NMR spectroscopy. Anal Bioanal Chem, 2009, 395: 1613-1622.

[19]

Lee C, Choi YE, Yun YS. A strategy for promoting astaxanthin accumulation in Haematococcus pluvialis by 1-aminocyclopropane-1-carboxylic acid application. J Biotechnol, 2016, 236: 120-127.

[20]

Levitan O, Dinamarca J, Zelzion E, Lun DS, Guerra LT, Kim MK, Kim J, Van Mooy BA, Bhattacharya D, Falkowski PG. Remodeling of intermediate metabolism in the diatom Phaeodactylum tricornutum under nitrogen stress. Proc Natl Acad Sci USA, 2015, 112: 412-417.

[21]

Li J, Han D, Wang D, Ning K, Jia J, Wei L, Jing X, Huang S, Chen J, Li Y. Choreography of transcriptomes and lipidomes of Nannochloropsis reveals the mechanisms of oil synthesis in microalgae. Plant Cell, 2014, 26: 1645-1665.

[22]

Li K, Cheng J, Lu H, Yang W, Zhou J, Cen K. Transcriptome-based analysis on carbon metabolism of Haematococcus pluvialis mutant under 15% CO2. Bioresour Technol, 2017, 233: 313-321.

[23]

Li F, Cai M, Lin M, Huang X, Wang J, Zheng X, Wu S, An Y. Accumulation of astaxanthin was improved by the nonmotile cells of Haematococcus pluvialis. Biomed Res Int, 2019, 2019: 8101762.

[24]

Li Q, Zhang L, Liu J. Comparative transcriptome analysis at seven time points during Haematococcus pluvialis motile cell growth and astaxanthin accumulation. Aquaculture, 2019, 503: 304-311.

[25]

Lichtenthaler HK. The 1-deoxy-d-xylulose-5-phosphate pathway of isoprenoid biosynthesis in plants. Annu Rev Plant Physiol Plant Mol Biol, 1999, 50: 47-65.

[26]

Linden H. Carotenoid hydroxylase from Haematococcus pluvialis: cDNA sequence, regulation and functional complementation. Biochim Biophys Acta, 1999, 1446: 203-212.

[27]

Livak K, Schmittgen T. Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−△△Ct Method. Methods, 2000, 25: 402-408.

[28]

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

[29]

Lv H, Xia F, Liu M, Cui X, Wahid F, Jia S. Metabolomic profiling of the astaxanthin accumulation process induced by high light in Haematococcus pluvialis. Algal Res, 2016, 20: 35-43.

[30]

Melis A. Photosynthesis-to-fuels: from sunlight to hydrogen, isoprene, and botryococcene production. Energy Environ Sci, 2012, 5: 5531-5539.

[31]

Olaizola M. Commercial production of astaxanthin from Haematococcus pluvialis using 25,000-liter outdoor photobioreactors. J Appl Phycol, 2000, 12: 499-506.

[32]

Ranjbar R, Inoue R, Shiraishi H, Katsuda T, Katoh S. High efficiency production of astaxanthin by autotrophic cultivation of Haematococcus pluvialis in a bubble column photobioreactor. Biochem Eng J, 2008, 39: 575-580.

[33]

Saakov VS. Pools of 14 C-malic acid as a substrate for pyruvate production for the DOXP/MEP pathway of biosynthesis of carotenoids in chloroplasts. Dokl Biochem Biophys, 2005, 400: 7-13.

[34]

Sarada R, Tripathi U, Ravishankar GA. Influence of stress on astaxanthin production in Haematococcus pluvialis grown under different culture conditions. Process Biochem, 2002, 37: 623-627.

[35]

Schoefs B, Rmiki N, Rachadi J, Lemoine Y. Astaxanthin accumulation in Haematococcus requires a cytochrome P450 hydroxylase and an active synthesis of fatty acids. FEBS Lett, 2001, 500: 125-128.

[36]

Shtaida N, Khozin-Goldberg I, Boussiba S. The role of pyruvate hub enzymes in supplying carbon precursors for fatty acid synthesis in photosynthetic microalgae. Photosynthesis Res, 2015, 125: 407-422.

[37]

Wan M, Hou D, Li Y, Fan J, Huang J, Liang S, Wang W, Pan R, Wang J, Li S. The effective photoinduction of Haematococcus pluvialis for accumulating astaxanthin with attached cultivation. Bioresour Technol, 2014, 163: 26-32.

[38]

Wan M, Zhang J, Hou D, Fan J, Li Y, Huang J, Wang J. The effect of temperature on cell growth and astaxanthin accumulation of Haematococcus pluvialis during a light-dark cyclic cultivation. Bioresour Technol, 2014, 167: 276-283.

[39]

Wan M, Zhang Z, Wang J, Huang J, Fan J, Yu A, Wang W, Li Y. Sequential Heterotrophy–Dilution–Photoinduction Cultivation of Haematococcus pluvialis for efficient production of astaxanthin. Bioresour Technol, 2015, 198: 557-563.

[40]

Wang J, Sommerfeld MR, Lu C, Hu Q. Combined effect of initial biomass density and nitrogen concentration on growth and astaxanthin production of Haematococcus pluvialis (Chlorophyta) in outdoor cultivation. Algae, 2013, 28: 193-202.

[41]

Wen Z, Liu Z, Hou Y, Liu C, Gao F, Zheng Y, Chen F. Ethanol induced astaxanthin accumulation and transcriptional expression of carotenogenic genes in Haematococcus pluvialis. Enzyme Microb Technol, 2015, 78: 10-17.

[42]

Ye ZW, Jiang JG, Wu GH. Biosynthesis and regulation of carotenoids in Dunaliella: progresses and prospects. Biotechnol Adv, 2008, 26: 352-360.

[43]

Yu X, Niu X, Zhang X, Pei G, Liu J, Chen L, Zhang W. Identification and mechanism analysis of chemical modulators enhancing astaxanthin accumulation in Haematococcus pluvialis. Algal Res, 2015, 11: 284-293.

[44]

Zhang BY, Geng YH, Li ZK, Hu HJ, Li YG. Production of astaxanthin from Haematococcus in open pond by two-stage growth one-step process. Aquaculture, 2009, 295: 275-281.

[45]

Zhong YJ, Huang JC, Liu J, Li Y, Jiang Y, Xu ZF, Sandmann G, Chen F. Functional characterization of various algal carotenoid ketolases reveals that ketolating zeaxanthin efficiently is essential for high production of astaxanthin in transgenic Arabidopsis. J Exp Bot, 2011, 62: 3659-3669.

Funding

National Natural Science Foundation of China (CN)(31500062)

Post Doctoral Science Foundation(2013M530183)

Fundamental Research Funds for the Central Universities(222201414024)

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