Effects of cultivation strategies on the cultivation of Chlorella sp. HQ in photoreactors

doi:10.1007/s11783-019-1162-z

Front. Environ. Sci. Eng.

2019, Vol. 13

Issue (5) : 78 https://doi.org/10.1007/s11783-019-1162-z

RESEARCH ARTICLE

Effects of cultivation strategies on the cultivation of Chlorella sp. HQ in photoreactors

Xiaoya Liu, Yu Hong(

), Peirui Liu, Jingjing Zhan, Ran Yan

Beijing Key Laboratory for Source Control Technology of Water Pollution, College of Environmental Science and Engineering, Beijing Forestry University, Beijing 100083, China

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Abstract

Heterotrophic cultivation caused high level of ROS and high lipids accumulation.

HMTC is the best culture strategy for improving the microalgal biomass.

Chlorella sp. HQ had great nutrient removal capacity under five culture strategies.

The effects of cultivation strategies (including autotrophic cultivation (AC), heterotrophic cultivation (HC), fed-batch cultivation (FC), heterotrophic+ autotrophic two-stage cultivation (HATC), and heterotrophic+ mixotrophic two-stage cultivation (HMTC)) on the growth and lipid accumulation of Chlorella sp. HQ and its total nitrogen (TN) and total phosphorus (TP) removal in secondary effluent were investigated in column photoreactors. The results showed that the TN and TP removal rates ranged between 93.72%–95.82% and 92.73%–100%, respectively, under the five different strategies. The microalgal growth potential evaluated by the maximal growth rate (R_max) was in the order of HMTC>HC>FC>AC>HATC. The values of biomass, total lipid yield, triacylglycerols (TAGs) yield, and total lipid content of the microalga cultivated in the last 5 d increased significantly, but the TAGs productivities of the five strategies were lower than those in the first 7 d. Compared with all the other cultivation strategies, the TAGs productivity and yield after 12 d of cultivation under the heterotrophic condition reached the highest values accompanying the highest level of intracellular reactive oxygen species (ROS), in which the TAGs yield reached 40.81 mg/L at the end of the cultivation period. The peaks in TAGs yield and ROS level suggested that HC was beneficial for lipids accumulation via regulating the cellular redox status and exerting ROS stress on microalgal cells. In summary, HMTC was the best cultivation strategy for improving the microalgal biomass and HC was the best strategy for microalgal TAGs accumulation to produce biodiesel.

Keywords Chlorella sp. HQ Cultivation strategy lipids Nitrogen removal Phosphorus removal Reactive oxygen species

Corresponding Author(s): Yu Hong

Issue Date: 29 September 2019

Cite this article:

Xiaoya Liu,Yu Hong,Peirui Liu, et al. Effects of cultivation strategies on the cultivation of Chlorella sp. HQ in photoreactors[J]. Front. Environ. Sci. Eng., 2019, 13(5): 78.

URL:

https://academic.hep.com.cn/fese/EN/10.1007/s11783-019-1162-z
https://academic.hep.com.cn/fese/EN/Y2019/V13/I5/78

Tab.1 The design of five cultivation strategies

Tab.2 The daily flow rate of fed-batch cultivation

Fig.1 Growth curves of Chlorella sp. HQ under five different cultivation strategies (AC: autotrophic cultivation; HC: heterotrophic cultivation; FC: fed-batch cultivation; HATC: heterotrophic+ autotrophic two-stage cultivation; HMTC: heterotrophic+ mixotrophic two-stage cultivation).

Tab.3 The logistic parameters of Chlorella sp. HQ under different cultivation strategies

Fig.2 Biomass of Chlorella sp. HQ under different cultivation strategies (AC: autotrophic cultivation; HC: heterotrophic cultivation; FC: fed-batch cultivation; HATC: heterotrophic+ autotrophic two-stage cultivation; HMTC: heterotrophic+ mixotrophic two-stage cultivation).

Fig.3 Total lipid yield (a), triacylglycerols (TAGs) yield (b), lipid content per biomass (c), and TAGs content per biomass (d) of Chlorella sp. HQ under different cultivation strategies throughout the cultivation period (AC: autotrophic cultivation; HC: heterotrophic cultivation; FC: fed-batch cultivation; HATC: heterotrophic+ autotrophic two-stage cultivation; HMTC: heterotrophic+ mixotrophic two-stage cultivation).

Tab.4 The effects of prolonged culture time on biomass productivity, lipid productivity, and triacylglycerols (TAGs) productivity of Chlorella sp. HQ under different cultivation strategies

Fig.4 Total phosphorus (TP) concentration (a) and total nitrogen (TN) concentration (b) of the culture medium under different cultivation strategies throughout the cultivation period (AC: autotrophic cultivation; HC: heterotrophic cultivation; FC: fed-batch cultivation; HATC: heterotrophic+ autotrophic two-stage cultivation; HMTC: heterotrophic+ mixotrophic two-stage cultivation).

Tab.5 Lipid production and nutrient removal rates of Chlorella sp. HQ under five different cultivation strategies after 12 d of cultivation

Fig.5 Effects of cultivation strategies on the relative reactive oxygen species (ROS) level of Chlorella sp. HQ (AC: autotrophic cultivation; HC: heterotrophic cultivation; FC: fed-batch cultivation; HATC: heterotrophic+ autotrophic two-stage cultivation; HMTC: heterotrophic+ mixotrophic two-stage cultivation).

Tab.6 Abbreviations

1	R A I Abou-Shanab, M K Ji, H C Kim, K J Paeng, B H Jeon (2013). Microalgal species growing on piggery wastewater as a valuable candidate for nutrient removal and biodiesel production. Journal of Environmental Management, 115(3): 257–264 https://doi.org/10.1016/j.jenvman.2012.11.022 pmid: 23270891
2	A P Abreu, B Fernandes, A A Vicente, J Teixeira, G Dragone (2012). Mixotrophic cultivation of Chlorella vulgaris using industrial dairy waste as organic carbon source. Bioresource Technology, 118: 61–66 https://doi.org/10.1016/j.biortech.2012.05.055 pmid: 22705507
3	B Biddanda, R Benner (1997). Carbon, nitrogen, and carbohydrate fluxes during the production of particulate and dissolved organic matter by marine phytoplankton. Limnology and Oceanography, 42(3): 506–518 https://doi.org/10.4319/lo.1997.42.3.0506
4	E G Bligh, W J Dyer (1959). A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology, 37(8): 911–917 https://doi.org/10.1139/o59-099 pmid: 13671378
5	P Bohutskyi, K Liu, B A Kessler, T Kula, Y Hong, E J Bouwer, M J Betenbaugh, F C T Allnutt (2014). Mineral and non-carbon nutrient utilization and recovery during sequential phototrophic-heterotrophic growth of lipid-rich algae. Applied Microbiology and Biotechnology, 98(11): 5261–5273 https://doi.org/10.1007/s00253-014-5655-1 pmid: 24839256
6	H Campos, W J Boeing, B N Dungan, T Schaub (2014). Cultivating the marine microalga Nannochloropsis salina under various nitrogen sources: Effect on biovolume yields, lipid content and composition, and invasive organisms. Biomass and Bioenergy, 66: 301–307 https://doi.org/10.1016/j.biombioe.2014.04.005
7	S Chinnasamy, A Bhatnagar, R W Hunt, K C Das (2010). Microalgae cultivation in a wastewater dominated by carpet mill effluents for biofuel applications. Bioresource Technology, 101(9): 3097–3105 https://doi.org/10.1016/j.biortech.2009.12.026 pmid: 20053551
8	Y Chisti (2007). Biodiesel from microalgae. Biotechnology Advances, 25(3): 294–306 https://doi.org/10.1016/j.biotechadv.2007.02.001 pmid: 17350212
9	X Deng, Y Li, X Fei (2009). Microalgae: A promising feedstock for biodiesel. African Journal of Microbiological Research, 3(13): 1008–1014
10	C Escapa, R N Coimbra, S Paniagua, A I García, M Otero (2017). Paracetamol and salicylic acid removal from contaminated water by microalgae. Journal of Environmental Management, 203(Pt 2): 799–806 https://doi.org/10.1016/j.jenvman.2016.06.051 pmid: 27421699
11	W Farooq, Y C Lee, B G Ryu, B H Kim, H S Kim, Y E Choi, J W Yang (2013). Two-stage cultivation of two Chlorella sp. strains by simultaneous treatment of brewery wastewater and maximizing lipid productivity. Bioresource Technology, 132: 230–238 https://doi.org/10.1016/j.biortech.2013.01.034 pmid: 23411453
12	K Gopalakrishnan, J Roostaei, Y Zhang (2018). Mixed culture of Chlorella sp. and wastewater wild algae for enhanced biomass and lipid accumulation in artificial wastewater medium. Frontiers of Environmental Science & Engineering, 12(4): 14 https://doi.org/10.1007/s11783-018-1075-2
13	M J Griffiths, S T L Harrison (2009). Lipid productivity as a key characteristic for choosing algal species for biodiesel production. Journal of Applied Phycology, 21(5): 493–507 https://doi.org/10.1007/s10811-008-9392-7
14	A Guldhe, S Kumari, L Ramanna, P Ramsundar, P Singh, I Rawat, F Bux (2017). Prospects, recent advancements and challenges of different wastewater streams for microalgal cultivation. Journal of Environmental Management, 203(Pt 1): 299–315 https://doi.org/10.1016/j.jenvman.2017.08.012 pmid: 28803154
15	P L Gupta, H J Choi, R R Pawar, S P Jung, S M Lee (2016). Enhanced biomass production through optimization of carbon source and utilization of wastewater as a nutrient source. Journal of Environmental Management, 184(Pt 3): 585–595 https://doi.org/10.1016/j.jenvman.2016.10.018 pmid: 27789093
16	F Han, J Huang, Y Li, W Wang, M Wan, G Shen, J Wang (2013). Enhanced lipid productivity of Chlorella pyrenoidosa through the culture strategy of semi-continuous cultivation with nitrogen limitation and pH control by CO2. Bioresource Technology, 136: 418–424 https://doi.org/10.1016/j.biortech.2013.03.017 pmid: 23567711
17	Y Hong, H Y Hu, F M Li (2008). Physiological and biochemical effects of allelochemical ethyl 2-methyl acetoacetate (EMA) on cyanobacterium Microcystis aeruginosa. Ecotoxicology and Environmental Safety, 71(2): 527–534 https://doi.org/10.1016/j.ecoenv.2007.10.010 pmid: 18054385
18	Q Hu, M Sommerfeld, E Jarvis, M Ghirardi, M Posewitz, M Seibert, A Darzins (2008). Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J, 54(4): 621–639 https://doi.org/10.1111/j.1365-313X.2008.03492.x pmid: 18476868
19	F Iasimone, A Panico, V De Felice, F Fantasma, M Iorizzi, F Pirozzi (2018). Effect of light intensity and nutrients supply on microalgae cultivated in urban wastewater: Biomass production, lipids accumulation and settleability characteristics. Journal of Environmental Management, 223: 1078–1085 https://doi.org/10.1016/j.jenvman.2018.07.024 pmid: 30096748
20	A Jebali, F G Acién, S Sayadi, E Molina-Grima (2018). Utilization of centrate from urban wastewater plants for the production of Scenedesmus sp. in a raceway-simulating reactor. Journal of Environmental Management, 211: 112–124 https://doi.org/10.1016/j.jenvman.2018.01.043 pmid: 29408060
21	C Jeffryes, J Rosenberger, G L Rorrer (2013). Fed-batch cultivation and bioprocess modeling of Cyclotella sp. for enhanced fatty acid production by controlled silicon limitation. Algal Research, 2(1): 16–27 https://doi.org/10.1016/j.algal.2012.11.002
22	X Li, H Y Hu, K Gan, Y X Sun (2010a). 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
23	X Li, H Y Hu, J Yang (2010b). Lipid accumulation and nutrient removal properties of a newly isolated freshwater microalga, Scenedesmus sp. LX1, growing in secondary effluent. New Biotechnology, 27: 59–63
24	X Li, H Y Hu, J Yang, Y H Wu (2010c). Enhancement effect of ethyl-2-methyl acetoacetate on triacylglycerols production by a freshwater microalga, Scenedesmus sp. LX1. Bioresource Technology, 101: 9819–9821
25	Q Lin, N Gu, G Li, J Lin, L Huang, L L Tan (2012). Effects of inorganic carbon concentration on carbon formation, nitrate utilization, biomass and oil accumulation of Nannochloropsis oculata CS 179. Bioresource Technology, 111: 353–359 https://doi.org/10.1016/j.biortech.2012.02.008 pmid: 22386465
26	J Liu, J C Huang, Z Sun, Y J Zhong, Y Jiang, F Chen (2011). Differential lipid and fatty acid profiles of photoautotrophic and heterotrophic Chlorella zofingiensis: Assessment of algal oils for biodiesel production. Bioresource Technology, 102(1): 106–110 https://doi.org/10.1016/j.biortech.2010.06.017 pmid: 20591657
27	R Maceiras, M Rodrı´guez, A Cancela, S Urréjola, A Sánchez (2011). Macroalgae: Raw material for biodiesel production. Applied Energy, 88(10): 3318–3323 https://doi.org/10.1016/j.apenergy.2010.11.027
28	R Ranjbar, R Inoue, H Shiraishi, T Katsuda, S Katoh (2008). High efficiency production of astaxanthin by autotrophic cultivation of Haematococcus pluvialis in a bubble column photobioreactor. Biochemical Engineering Journal, 39(3): 575–580 https://doi.org/10.1016/j.bej.2007.11.010
29	H Ren, J Tuo, M M Addy, R Zhang, Q Lu, E Anderson, P Chen, R Ruan (2017). Cultivation of Chlorella vulgaris in a pilot-scale photobioreactor using real centrate wastewater with waste glycerol for improving microalgae biomass production and wastewater nutrients removal. Bioresource Technology, 245(Pt A): 1130–1138 https://doi.org/10.1016/j.biortech.2017.09.040 pmid: 28962086
30	M Y Roleda, S P Slocombe, R J Leakey, J G Day, E M Bell, M S Stanley (2013). Effects of temperature and nutrient regimes on biomass and lipid production by six oleaginous microalgae in batch culture employing a two-phase cultivation strategy. Bioresource Technology, 129: 439–449 https://doi.org/10.1016/j.biortech.2012.11.043 pmid: 23262022
31	E S Salama, M B Kurade, R A I Abou-Shanab, M M El-Dalatony, I S Yang, B Min, B H Jeon (2017). Recent progress in microalgal biomass production coupled with wastewater treatment for biofuel generation. Renewable & Sustainable Energy Reviews, 79: 1189–1211 https://doi.org/10.1016/j.rser.2017.05.091
32	Y Tan, J Lin (2011). Biomass production and fatty acid profile of a Scenedesmus rubescens-like microalga. Bioresource Technology, 102(21): 10131–10135 https://doi.org/10.1016/j.biortech.2011.07.091 pmid: 21903386
33	H Wang, W Zhou, H Shao, T Liu (2017). A comparative analysis of biomass and lipid content in five Tribonema sp. strains at autotrophic, heterotrophic and mixotrophic cultivation. Algal Research, 24: 284–289 https://doi.org/10.1016/j.algal.2017.04.020
34	K Wang, J Yang, S Zhuang (1999). Improving the biomass of Dunaliella salina by fed-batch culture. Marine Science Bulletin 18:64–69 (in Chinese with English abstract)
35	X Wang, L Lin, H Lu, Z Liu, N Duan, T Dong, H Xiao, B Li, P Xu (2018). Microalgae cultivation and culture medium recycling by a two-stage cultivation system. Frontiers of Environmental Science & Engineering, 12(6): 14 https://doi.org/10.1007/s11783-018-1078-z
36	Y H Wu, Y Yu, H Y Hu, L L Zhuang (2016). Effects of cultivation conditions on the production of soluble algal products (SAPs) of Scenedesmus sp. LX1. Algal Research, 16: 376–382 https://doi.org/10.1016/j.algal.2016.04.006
37	Z Wu, X Shi (2007). Optimization for high-density cultivation of heterotrophic Chlorella based on a hybrid neural network model. Letters in Applied Microbiology, 44(1): 13–18 https://doi.org/10.1111/j.1472-765X.2006.02038.x pmid: 17209808
38	J Yang, X Li, H Y Hu, X Zhang, Y Yu, Y S Chen (2011). Growth and lipid accumulation properties of a freshwater microalga, Chlorella ellipsoidea YJ1, in domestic secondary effluents. Applied Energy, 88(10): 3295–3299 https://doi.org/10.1016/j.apenergy.2010.11.029
39	K Yoon, D Han, Y Li, M Sommerfeld, Q Hu (2012). Phospholipid:diacylglycerol acyltransferase is a multifunctional enzyme involved in membrane lipid turnover and degradation while synthesizing triacylglycerol in the unicellular green microalga Chlamydomonas reinhardtii. Plant Cell, 24(9): 3708–3724 https://doi.org/10.1105/tpc.112.100701 pmid: 23012436
40	Z Yu, H Pei, Q Hou, C Nie, L Zhang, Z Yang, X Wang (2018). The effects of algal extracellular substances on algal growth, metabolism and long-term medium recycle, and inhibition alleviation through ultrasonication. Bioresource Technology, 267: 192–200 https://doi.org/10.1016/j.biortech.2018.07.019 pmid: 30025314
41	J J Zhan, Q Zhang, M M Qin, Y Hong (2016). Selection and characterization of eight freshwater green algae strains for synchronous water purification and lipid production. Frontiers of Environmental Science & Engineering, 10(3): 548–558 https://doi.org/10.1007/s11783-016-0831-4
42	Q Zhang, Y Hong (2014a). Comparison in growth, lipid accumulation, and nutrient removal capacities of Chlorella sp. in secondary effluents under sterile and non-sterile conditions. Water Sci Technol, 69(3): 573–579 https://doi.org/10.2166/wst.2013.748 pmid: 24552730
43	Q Zhang, Y Hong (2014b). Effects of stationary phase elongation and initial nitrogen and phosphorus concentrations on the growth and lipid-producing potential of Chlorella sp. HQ. Journal of Applied Phycology, 26(1): 141–149 https://doi.org/10.1007/s10811-013-0091-7
44	Q Zhang, T Wang, Y Hong (2014). Investigation of initial pH effects on growth of an oleaginous microalgae Chlorella sp. HQ for lipid production and nutrient uptake. Water Sci Technol, 70(4): 712–719 https://doi.org/10.2166/wst.2014.285 pmid: 25116503
45	Y Zheng, T Li, X C Yu, P D Bates, T Dong, S L Chen (2013). High-density fed-batch culture of a thermotolerant microalga Chlorella sorokiniana for biofuel production. Applied Energy, 108: 281–287 https://doi.org/10.1016/j.apenergy.2013.02.059
46	W G Zhou, Y C Li, M Min, B Hu, H Zhang, X C Ma, L Li, Y L Cheng, P Chen, R Ruan (2012a). Growing wastewater-born microalga Auxenochlorella protothecoides UMN280 on concentrated municipal wastewater for simultaneous nutrient removal and energy feedstock production. Applied Energy, 98: 433–440 https://doi.org/10.1016/j.apenergy.2012.04.005
47	W G Zhou, M Min, Y C Li, B Hu, X C Ma, Y L Cheng, Y H Liu, P Chen, R Ruan (2012b). A hetero-photoautotrophic two-stage cultivation process to improve wastewater nutrient removal and enhance algal lipid accumulation. Bioresource Technology, 110: 448–455 https://doi.org/10.1016/j.biortech.2012.01.063 pmid: 22326332

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