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

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.

Graphical abstract

Keywords

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

References

[1] Abou-Shanab R A I, Ji M K, Kim H C, Paeng K J, Jeon B H (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

[2] Abreu A P, Fernandes B, Vicente A A, Teixeira J, Dragone G (2012). Mixotrophic cultivation of Chlorella vulgaris using industrial dairy waste as organic carbon source. Bioresource Technology, 118: 61–66

[3] Biddanda B, Benner R (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

[4] Bligh E G, Dyer W J (1959). A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology, 37(8): 911–917

[5] Bohutskyi P, Liu K, Kessler B A, Kula T, Hong Y, Bouwer E J, Betenbaugh M J, Allnutt F C T (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

[6] Campos H, Boeing W J, Dungan B N, Schaub T (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

[7] Chinnasamy S, Bhatnagar A, Hunt R W, Das K C (2010). Microalgae cultivation in a wastewater dominated by carpet mill effluents for biofuel applications. Bioresource Technology, 101(9): 3097–3105

[8] Chisti Y (2007). Biodiesel from microalgae. Biotechnology Advances, 25(3): 294–306

[9] Deng X, Li Y, Fei X (2009). Microalgae: A promising feedstock for biodiesel. African Journal of Microbiological Research, 3(13): 1008–1014

[10] Escapa C, Coimbra R N, Paniagua S, García A I, Otero M (2017). Paracetamol and salicylic acid removal from contaminated water by microalgae. Journal of Environmental Management, 203(Pt 2): 799–806

[11] Farooq W, Lee Y C, Ryu B G, Kim B H, Kim H S, Choi Y E, Yang J W (2013). Two-stage cultivation of two Chlorella sp. strains by simultaneous treatment of brewery wastewater and maximizing lipid productivity. Bioresource Technology, 132: 230–238

[12] Gopalakrishnan K, Roostaei J, Zhang Y (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

[13] Griffiths M J, Harrison S T L (2009). Lipid productivity as a key characteristic for choosing algal species for biodiesel production. Journal of Applied Phycology, 21(5): 493–507

[14] Guldhe A, Kumari S, Ramanna L, Ramsundar P, Singh P, Rawat I, Bux F (2017). Prospects, recent advancements and challenges of different wastewater streams for microalgal cultivation. Journal of Environmental Management, 203(Pt 1): 299–315

[15] Gupta P L, Choi H J, Pawar R R, Jung S P, Lee S M (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

[16] Han F, Huang J, Li Y, Wang W, Wan M, Shen G, Wang J (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

[17] Hong Y, Hu H Y, Li F M (2008). Physiological and biochemical effects of allelochemical ethyl 2-methyl acetoacetate (EMA) on cyanobacterium Microcystis aeruginosa. Ecotoxicology and Environmental Safety, 71(2): 527–534

[18] Hu Q, Sommerfeld M, Jarvis E, Ghirardi M, Posewitz M, Seibert M, Darzins A (2008). Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J, 54(4): 621–639

[19] Iasimone F, Panico A, De Felice V, Fantasma F, Iorizzi M, Pirozzi F (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

[20] Jebali A, Acién F G, Sayadi S, Molina-Grima E (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

[21] Jeffryes C, Rosenberger J, Rorrer G L (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

[22] Li X, Hu H Y, Gan K, Sun Y X (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] Li X, Hu H Y, Yang J (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] Li X, Hu H Y, Yang J, Wu Y H (2010c). Enhancement effect of ethyl-2-methyl acetoacetate on triacylglycerols production by a freshwater microalga, Scenedesmus sp. LX1. Bioresource Technology, 101: 9819–9821

[25] Lin Q, Gu N, Li G, Lin J, Huang L, Tan L L (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

[26] Liu J, Huang J C, Sun Z, Zhong Y J, Jiang Y, Chen F (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

[27] Maceiras R, Rodrı´guez M, Cancela A, Urréjola S, Sánchez A (2011). Macroalgae: Raw material for biodiesel production. Applied Energy, 88(10): 3318–3323

[28] Ranjbar R, Inoue R, Shiraishi H, Katsuda T, Katoh S (2008). High efficiency production of astaxanthin by autotrophic cultivation of Haematococcus pluvialis in a bubble column photobioreactor. Biochemical Engineering Journal, 39(3): 575–580

[29] Ren H, Tuo J, Addy M M, Zhang R, Lu Q, Anderson E, Chen P, Ruan R (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

[30] Roleda M Y, Slocombe S P, Leakey R J, Day J G, Bell E M, Stanley M S (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

[31] Salama E S, Kurade M B, Abou-Shanab R A I, El-Dalatony M M, Yang I S, Min B, Jeon B H (2017). Recent progress in microalgal biomass production coupled with wastewater treatment for biofuel generation. Renewable & Sustainable Energy Reviews, 79: 1189–1211

[32] Tan Y, Lin J (2011). Biomass production and fatty acid profile of a Scenedesmus rubescens-like microalga. Bioresource Technology, 102(21): 10131–10135

[33] Wang H, Zhou W, Shao H, Liu T (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

[34] Wang K, Yang J, Zhuang S (1999). Improving the biomass of Dunaliella salina by fed-batch culture. Marine Science Bulletin 18:64–69 (in Chinese with English abstract)

[35] Wang X, Lin L, Lu H, Liu Z, Duan N, Dong T, Xiao H, Li B, Xu P (2018). Microalgae cultivation and culture medium recycling by a two-stage cultivation system. Frontiers of Environmental Science & Engineering, 12(6): 14

[36] Wu Y H, Yu Y, Hu H Y, Zhuang L L (2016). Effects of cultivation conditions on the production of soluble algal products (SAPs) of Scenedesmus sp. LX1. Algal Research, 16: 376–382

[37] Wu Z, Shi X (2007). Optimization for high-density cultivation of heterotrophic Chlorella based on a hybrid neural network model. Letters in Applied Microbiology, 44(1): 13–18

[38] Yang J, Li X, Hu H Y, Zhang X, Yu Y, Chen Y S (2011). Growth and lipid accumulation properties of a freshwater microalga, Chlorella ellipsoidea YJ1, in domestic secondary effluents. Applied Energy, 88(10): 3295–3299

[39] Yoon K, Han D, Li Y, Sommerfeld M, Hu Q (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

[40] Yu Z, Pei H, Hou Q, Nie C, Zhang L, Yang Z, Wang X (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

[41] Zhan J J, Zhang Q, Qin M M, Hong Y (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

[42] Zhang Q, Hong Y (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

[43] Zhang Q, Hong Y (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

[44] Zhang Q, Wang T, Hong Y (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

[45] Zheng Y, Li T, Yu X C, Bates P D, Dong T, Chen S L (2013). High-density fed-batch culture of a thermotolerant microalga Chlorella sorokiniana for biofuel production. Applied Energy, 108: 281–287

[46] Zhou W G, Li Y C, Min M, Hu B, Zhang H, Ma X C, Li L, Cheng Y L, Chen P, Ruan R (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

[47] Zhou W G, Min M, Li Y C, Hu B, Ma X C, Cheng Y L, Liu Y H, Chen P, Ruan R (2012b). A hetero-photoautotrophic two-stage cultivation process to improve wastewater nutrient removal and enhance algal lipid accumulation. Bioresource Technology, 110: 448–455

RIGHTS & PERMISSIONS

Higher Education Press and Springer-Verlag GmbH Germany, part of Springer Nature