Abstract
The effects of various carbon sources on growth, photosynthetic pigments and lipid production of Chlorella vulgaris 31 were investigated under photoautotrophic, mixotrophic and heterotrophic cultivations. The results indicated that in two concentration gradients (2 and 10 g L−1), glucose, maltose and sodium acetate all significantly promoted the growth of C. vulgaris 31, while the effects of sucrose and glycerol were not significant. The alga could barely assimilate xylose. The biosynthesis of chlorophylls and carotenoids in algal cells was reduced under mixotrophic and heterotrophic cultivations; however, lipid production was promoted significantly. Moreover, this inhibition or promotion has significant concentration dependence of carbon source. The composition and proportion of fatty acids could also be regulated by different culture conditions and organic carbon sources. The finding suggests that the biomass, pigment and lipid production of C. vulgaris 31 could be regulated by controlling the trophic mode and carbon source.
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References
Andrade MR, Costa JAV (2007) Mixotrophic cultivation of microalga Spirulina platensis using molasses as organic substrate. Aquaculture 264:130–134
Baldisserotto C, Popovich C, Giovanardi M, Sabia A, Ferroni L, Constenla D, Leonardi P, Pancaldi S (2016) Photosynthetic aspects and lipid profiles in the mixotrophic alga Neochloris oleoabundans as useful parameters for biodiesel production. Algal Res 16:255–265
Basu S, Roy AS, Mohanty K, Ghoshal AK (2013) Enhanced CO2 sequestration by a novel microalga: Scenedesmus obliquus SA1 isolated from bio-diversity hotspot region of Assam, India. Bioresour Technol 143:369–377
Cheirsilp B, Torpee S (2012) Enhanced growth and lipid production of microalgae under mixotrophic culture condition: effect of light intensity, glucose concentration and fed-batch cultivation. Bioresour Technol 110:510–516
Chen F, Chen H, Gong X (1997) Mixotrophic and heterotrophic growth of Haematococcus lacustris and rheological behavior of the cell suspensions. Bioresour Technol 62:19–24
Dai C, He J, Wang G, Li S (2005) A review of ecological research on mixotrophic plankton. Acta Ecol Sin 25:2399–2405
Dourou M, Aggeli D, Papanikolaou S, Aggelis G (2018) Critical steps in carbon metabolism affecting lipid accumulation and their regulation in oleaginous microorganisms. Appl Microbiol Biotechnol 102:2509–2523
Enamala MK, Enamala S, Chavali M, Donepudi J, Yadavalli R, Kolapalli B, Aradhyula TV, Velpuri J, Kuppam C (2018) Production of biofuels from microalgae-a review on cultivation, harvesting, lipid extraction, and numerous applications of microalgae. Renew Sust Energ Rev 94:49–68
Gaurav N, Sivasankari S, Kiran G, Ninawe A, Selvin J (2017) Utilization of bioresources for sustainable biofuels: a review. Renew Sust Energ Rev 73:205–214
GB/T 17376 (2008) Preparation of fatty acid methyl ester from animal and vegetable oils. China National Standard
Gong M, Bassi A (2016) Carotenoids from microalgae: a review of recent developments. Biotechnol Adv 34:1396–1412
Gupta S, Pawar SB (2019) Strategic mixed substrate cultivation of microalgae: productivity, respiration, yield, and lipid quality. J Appl Phycol 31:1573–1588
Huang Y, Luo L, Xu K, Wang XC (2019) Characteristics of external carbon uptake by microalgae growth and associated effects on algal biomass composition. Bioresour Technol 292:121887
Kang RJ, Wang J, Shi DJ, Cong W, Cai ZL, Ouyang F (2004) Interactions between organic and inorganic carbon sources during mixotrophic cultivation of Synechococcus sp. Biotechnol Lett 26:1429–1432
Kim S, Park JE, Cho YB, Hwang SJ (2013) Growth rate, organic carbon and nutrient removal rates of Chlorella sorokiniana in autotrophic, heterotrophic and mixotrophic conditions. Bioresour Technol 144:8–13
Kong WB, Yang H, Cao YT, Song H, Hua SF, Xia CG (2013) Effect of glycerol and glucose on the enhancement of biomass, lipid and soluble carbohydrate production by Chlorella vulgaris in mixotrophic culture. Food Technol Biotechnol 51:62–69
Kumar V, Muthuraj M, Palabhanvi B, Ghoshal AK, Das D (2014) High cell density lipid rich cultivation of a novel microalgal isolate Chlorella sorokiniana FC6 IITG in a single-stage fed-batch mode under mixotrophic condition. Bioresour Technol 170:115–124
Lari Z, Moradi-Kheibari N, Ahmadzadeh H, Abrishamchi P, Moheimani NR, Murry MA (2016) Bioprocess engineering of microalgae to optimize lipid production through nutrient management. J Appl Phycol 28:3235–3250
Lari Z, Abrishamchi P, Ahmadzadeh H, Soltani N (2019) Differential carbon partitioning and fatty acid composition in mixotrophic and autotrophic cultures of a new marine isolate Tetraselmis sp. KY114885. J Appl Phycol 31:201–210
Leite GB, Paranjape K, Abdelaziz AEM, Hallenbeck PC (2015) Utilization of biodiesel-derived glycerol or xylose for increased growth and lipid production by indigenous microalgae. Bioresour Technol 184:123–130
Leite GB, Paranjape K, Hallenbeck PC (2016) Breakfast of champions: fast lipid accumulation by cultures of Chlorella and Scenedesmus induced by xylose. Algal Res 16:338–348
Li DJ, Wang L, Zhao QY, Wei W, Sun YH (2015) Improving high carbon dioxide tolerance and carbon dioxide fixation capability of Chlorella sp. by adaptive laboratory evolution. Bioresour Technol 185:269–275
Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembrane. Methods Enzymol 148:350–382
Lin TS, Wu JY (2015) Effect of carbon sources on growth and lipid accumulation of newly isolated microalgae cultured under mixotrophic condition. Bioresour Technol 184:100–107
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
Liu L, Zhao Y, Jiang X, Wang X, Liang W (2018) Lipid accumulation of Chlorella pyrenoidosa under mixotrophic cultivation using acetate and ammonium. Bioresour Technol 262:342–346
Lv JM, Cheng LH, Xu XH, Zhang L, Chen HL (2010) Enhanced lipid production of Chlorella vulgaris by adjustment of cultivation conditions. Bioresour Technol 101:6797–6804
Madeira M, Cardoso C, Lopes PA, Coelho D, Afonso C, Bandarra N, Prates JAM (2017) Microalgae as feed ingredients for livestock production and meat quality: a review. Livest Sci 205:111–121
Manirafasha E, Ndikubwimana T, Zeng X, Lu Y, Jing K (2016) Phycobiliprotein: potential microalgae derived pharmaceutical and biological reagent. Biochem Eng J 109:282–296
Menegol T, Romero-Villegas GI, López-Rodríguez M, Navarro-López E, López-Rosales L, Chisti Y, Cerón-García MC, Molina-Grima E (2019) Mixotrophic production of polyunsaturated fatty acids and carotenoids by the microalga Nannochloropsis gaditana. J Appl Phycol 31:2823–2832
Mondal M, Ghosh A, Sharma AS, Tiwari ON, Gayen K, Mandal MK, Halder GN (2016) Mixotrophic cultivation of Chlorella sp. BTA 9031 and Chlamydomonas sp. BTA 9032 isolated from coal field using various carbon sources for biodiesel production. Energ Convers Manage 124:297–304
Paranjape K, Leite GB, Hallenbeck PC (2016) Effect of nitrogen regime on microalgal lipid production during mixotrophic growth with glycerol. Bioresour Technol 214:778–786
Rai MP, Nigam S, Sharma R (2013) Response of growth and fatty acid compositions of Chlorella pyrenoidosa under mixotrophic cultivation with acetate and glycerol for bioenergy application. Biomass Bioenergy 58:251–257
Ratledge C, Wynn JP (2002) The biochemistry and molecular biology of lipid accumulation in oleaginous microorganisms. Adv Appl Microbiol 51:1–51
Razzak SA, Ali SAM, Hossain MM, Delasa H (2017) Biological CO2 fixation with production of microalgae in wastewater–a review. Renew Sust Energ Rev 76:379–390
Shin YS, Choi HI, Choi JW, Lee JS, Sung YJ, Sim SJ (2018) Multilateral approach on enhancing economic viability of lipid production from microalgae: a review. Bioresour Technol 258:335–344
Song M, Pei H (2018) The growth and lipid accumulation of Scenedesmus quadricauda during batch mixotrophic/heterotrophic cultivation using xylose as a carbon source. Bioresour Technol 263:525–531
Stadnichuk IN, Rakhimberdieva MG, Bolychevtseva YV, Yurina NP, Karapetyan NV, Selyakh IO (1998) Inhibition by glucose of chlorophyll a, and phycocyanobilin biosynthesis in the unicellular red alga Galdieria partita, at the stage of coproporphyrinogen III formation. Plant Sci 136:11–23
Shen X-F, Qin Q-W, Yan S-K, Huang J-L, Liu K, Zhou S-B (2019) Biodiesel production from Chlorella vulgaris under nitrogen starvation in autotrophic, heterotrophic, and mixotrophic cultures. J Appl Phycol 31:1589–1596
Stoecker DK (1998) Conceptual models of mixotrophy in planktonic protists and some ecological and evolutionary implications. Eur J Protistol 34:281–290
Tan XB, Zhao XC, Yang LB, Liao JY, Zhou YY (2018) Enhanced biomass and lipid production for cultivating Chlorella pyrenoidosa in anaerobically digested starch wastewater using various carbon sources and up-scaling culture outdoors. Biochem Eng J 135:105–114
Tu ZM, Liu LT, Lin WT, Xie ZZ, Luo JF (2018) Potential of using sodium bicarbonate as external carbon source to cultivate microalga in non-sterile condition. Bioresour Technol 266:109–115
Vaz BDS, Moreira JB, Morais MGD, Costa JAV (2016) Microalgae as a new source of bioactive compounds in food supplements. Curr Opin Food Sci 7:73–77
Yeh KL, Chang JS (2012) Effects of cultivation conditions and media composition on cell growth and lipid productivity of indigenous microalga Chlorella vulgaris EPS-31. Bioresour Technol 105:120–127
Yeh KL, Chen CY, Chang JS (2012) pH-stat photoheterotrophic cultivation of indigenous Chlorella vulgaris ESP-31 for biomass and lipid production using acetic acid as the carbon source. Biochem Eng J 64:1–7
Yu GC, Shi DJ, Cai ZL, Cong W, Ouyang F (2011) Growth and physiological features of Cyanobacterium Anabaena sp. strain PCC 7120 in a glucose mixotrophic culture. Chin J Chem Eng 19:108–115
Zhang H, Wang W, Li Y, Yang W, Shen G (2011) Mixotrophic cultivation of Botryococcus braunii. Biomass Bioenergy 35:1710–1715
Zhang W, Zhang P, Sun H, Chen M, Lu S, Li P (2014) Effects of various organic carbon sources on the growth and biochemical composition of Chlorella pyrenoidosa. Bioresour Technol 173:52–58
Zili F, Bouzidi N, Ammar J, Zakhama W, Ghoul M, Sayadi S, Ouada HB (2017) Mixotrophic cultivation promotes growth, lipid productivity, and PUFA production of a thermophilic Chlorophyta strain related to the genus Graesiella. J Appl Phycol 29:35–43
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This work was financially supported by National Natural Science Foundation of China (No. 31360192) and Longyuan Youth Innovation & Entrepreneurship Team Project (2018).
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Kong, W., Yang, S., Wang, H. et al. Regulation of biomass, pigments, and lipid production by Chlorella vulgaris 31 through controlling trophic modes and carbon sources. J Appl Phycol 32, 1569–1579 (2020). https://doi.org/10.1007/s10811-020-02089-1
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DOI: https://doi.org/10.1007/s10811-020-02089-1