Abstract
In this study, a new microalgal strain, Asterarcys quadricellulare R-56, was isolated for biomass and lipid production. The effects of carbon and nitrogen sources and initial pH on the cell growth and lipid accumulation of strain R-56 were investigated. At 10 g L−1 glucose, 0.6 g L−1 sodium nitrate, and pH 7, the highest biomass of 4.18 g L−1 and lipid content of 43.66% were obtained. Microalgae had a broad pH tolerance in the range of 5–11, and the pH of the culture medium was close to neutral at the end of cultivation. The maximum contents of chlorophyll, carbohydrate, and protein under the recommended culture conditions were 19.47 mg mL−1, 21.80%, and 29.94%, respectively. Palmitic and palmitoleic acid contents in strain R-56 accounted for as high as 83.73% of total fatty acids. This study suggested that strain R-56 was a promising lipid producer for high-quality biodiesel production.
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References
Anitha S, Shah AR, Ali BMJ (2018) Modulation of lipid productivity under nitrogen, salinity and temperature stress in microalgae Dunaliella sp. J Environ Biol 39(5):625–632. https://doi.org/10.22438/jeb/39/5/MRN-761
Anne-Marie K, Yee W, Loh SH, Aziz A, Cha TS (2020) Influence of nitrogen availability on biomass, lipid production, fatty acid profile, and the expression of fatty acid desaturase genes in Messastrum gracile SE-MC4. World J Microbiol Biotechnol 36(1):17. https://doi.org/10.1007/s11274-019-2790-y
Ansari FA, Guldhe A, Gupta SK, Rawat I, Bux F (2021) Improving the feasibility of aquaculture feed by using microalgae. Environ Sci Pollut Res 28(32):43234–43257. https://doi.org/10.1007/s11356-021-14989-x
Arunachalam Sivagurulingam AP, Sivanandi P, Pandian S (2022) Isolation, mass cultivation, and biodiesel production potential of marine microalgae identified from Bay of Bengal. Environ Sci Pollut Res 29(5):6646–6655. https://doi.org/10.1007/s11356-021-16163-9
Bameri L, Sourinejad I, Ghasemi Z, Fazelian N (2022) Toxicity of TiO2 nanoparticles to the marine microalga Chaetoceros muelleri Lemmermann, 1898 under long-term exposure. Environ Sci Pollut Res 29(20):30427–30440. https://doi.org/10.1007/s11356-021-17870-z
Bartley ML, Boeing WJ, Dungan BN, Holguin FO, Schaub T (2013) pH effects on growth and lipid accumulation of the biofuel microalgae Nannochloropsis salina and invading organisms. J Appl Phycol 26(3):1431–1437. https://doi.org/10.1007/s10811-013-0177-2
Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37(8):911–917. https://doi.org/10.1139/o59-099
Brindhadevi K, Mathimani T, Rene ER, Shanmugam S, Chi NTL, Pugazhendhi A (2021) Impact of cultivation conditions on the biomass and lipid in microalgae with an emphasis on biodiesel. Fuel 284:119058. https://doi.org/10.1016/j.fuel.2020.119058
Che R, Huang L, Xu JW, Zhao P, Li T, Ma H, Yu X (2017) Effect of fulvic acid induction on the physiology, metabolism, and lipid biosynthesis-related gene transcription of Monoraphidium sp. FXY-10. Bioresour Technol 227:324–334. https://doi.org/10.1016/j.biortech.2016.12.017
Chu FJ, Wan TJ, Pai TY, Lin HW, Liu SH, Huang CF (2020) Use of magnetic fields and nitrate concentration to optimize the growth and lipid yield of Nannochloropsis oculata. J Environ Manage 253:109680. https://doi.org/10.1016/j.jenvman.2019.109680
Cordeiro ECN, Mógor ÁF, Amatussi JO, Mógor G, Marques HMC, de Lara GB (2022) Microalga biofertilizer improves potato growth and yield, stimulating amino acid metabolism. J Appl Phycol 34(1):385–394. https://doi.org/10.1007/s10811-021-02656-0
Costa SS, Miranda AL, Andrade BB, Assis DJ, Souza CO, de Morais MG, Costa JAV, Druzian JI (2018) Influence of nitrogen on growth, biomass composition, production, and properties of polyhydroxyalkanoates (PHAs) by microalgae. Int J Biol Macromol 116:552–562. https://doi.org/10.1016/j.ijbiomac.2018.05.064
Dani N, Zare D, Assadi MM, Irani S, Soltani N (2021) Isolation, screening and medium optimization of native microalgae for lipid production using nutritional starvation strategy and statistical design. Int J Environ Sci Te 18(10):2997–3012. https://doi.org/10.1007/s13762-020-03037-9
Dar RA, Gupta RK, Phutela UG (2021) Enhancement of euryhaline Asterarcys quadricellulare biomass production for improving biogas generation through anaerobic co-digestion with carbon rich substrate. 3 Biotech 11(5):251. https://doi.org/10.1007/s13205-021-02792-x
Deshmukh S, Kumar R, Bala K (2019) Microalgae biodiesel: A review on oil extraction, fatty acid composition, properties and effect on engine performance and emissions. Fuel Process Technol 191:232–247. https://doi.org/10.1016/j.fuproc.2019.03.013
Dolganyuk V, Andreeva A, Budenkova E, Sukhikh S, Babich O, Ivanova S, Prosekov A, Ulrikh E (2020) Study of morphological features and determination of the fatty acid composition of the microalgae lipid complex. Biomolecules 10(11):1571. https://doi.org/10.3390/biom10111571
Fawzy MA, El-Otify AM, Adam MS, Moustafa SSA (2021) The impact of abiotic factors on the growth and lipid accumulation of some green microalgae for sustainable biodiesel production. Environ Sci Pollut Res 28(31):42547–42561. https://doi.org/10.1007/s11356-021-13781-1
Goswami RK, Agrawal K, Mehariya S, Verma P (2022) Current perspective on wastewater treatment using photobioreactor for Tetraselmis sp.: an emerging and foreseeable sustainable approach. Environ Sci Pollut Res 29(41):61905–61937. https://doi.org/10.1007/s11356-021-16860-5
Gupta PL, Choi HJ, Pawar RR, Jung SP, Lee SM (2016) Enhanced biomass production through optimization of carbon source and utilization of wastewater as a nutrient source. J Environ Manage 184(Pt 3):585–595. https://doi.org/10.1016/j.jenvman.2016.10.018
Gutierrez J, Kwan TA, Zimmerman JB, Peccia J (2016) Ammonia inhibition in oleaginous microalgae. Algal Res 19:123–127. https://doi.org/10.1016/j.algal.2016.07.016
Jazzar S, Quesada-Medina J, Olivares-Carrillo P, Marzouki MN, Acien-Fernandez FG, Fernandez-Sevilla JM, Molina-Grima E, Smaali I (2015) A whole biodiesel conversion process combining isolation, cultivation and in situ supercritical methanol transesterification of native microalgae. Bioresour Technol 190:281–288. https://doi.org/10.1016/j.biortech.2015.04.097
Ji B (2022) Towards environment-sustainable wastewater treatment and reclamation by the non-aerated microalgal-bacterial granular sludge process: Recent advances and future directions. Sci Total Environ 806(Pt 4):150707. https://doi.org/10.1016/j.scitotenv.2021.150707
Ju J-H, Ko D-J, Heo S-Y, Lee J-J, Kim Y-M, Lee B-S, Kim M-S, Kim C-H, Seo J-W, Oh B-R (2020) Regulation of lipid accumulation using nitrogen for microalgae lipid production in Schizochytrium sp. ABC101. Renew Energ 153:580–587. https://doi.org/10.1016/j.renene.2020.02.047
Kong F, Ren H-Y, Liu D, Wang Z, Nan J, Ren N-Q, Fu Q (2022) Improved decolorization and mineralization of azo dye in an integrated system of anaerobic bioelectrochemical modules and aerobic moving bed biofilm reactor. Bioresour Technol 353:127147. https://doi.org/10.1016/j.biortech.2022.127147
Kong F, Ren H-Y, Pavlostathis SG, Nan J, Ren N-Q, Wang A (2020) Overview of value-added products bioelectrosynthesized from waste materials in microbial electrosynthesis systems. Renew Sust Energ Rev 125:109816. https://doi.org/10.1016/j.rser.2020.109816
Liu X, Hong Y, Liu Y (2021) Cultivation of Chlorella sp. HQ in inland saline-alkaline water under different light qualities. Front Env Sci Eng 16(4):45. https://doi.org/10.1007/s11783-021-1479-2
Lu W, Liu S, Lin Z, Lin M (2020) Enhanced microalgae growth for biodiesel production and nutrients removal in raw swine wastewater by carbon sources supplementation. Waste Biomass Valori 12(4):1991–1999. https://doi.org/10.1007/s12649-020-01135-w
Ma X, Mi Y, Zhao C, Wei Q (2022) A comprehensive review on carbon source effect of microalgae lipid accumulation for biofuel production. Sci Total Environ 806(Pt 3):151387. https://doi.org/10.1016/j.scitotenv.2021.151387
Mandal MK, Chanu NK, Chaurasia N (2020) Exogenous addition of indole acetic acid and kinetin under nitrogen-limited medium enhances lipid yield and expression of glycerol-3-phosphate acyltransferase & diacylglycerol acyltransferase genes in indigenous microalgae: A potential approach for biodiesel production. Bioresour Technol 297:122439. https://doi.org/10.1016/j.biortech.2019.122439
Melo JM, Ribeiro MR, Telles TS, Amaral HF, Andrade DS (2022) Microalgae cultivation in wastewater from agricultural industries to benefit next generation of bioremediation: a bibliometric analysis. Environ Sci Pollut Res 29(15):22708–22720. https://doi.org/10.1007/s11356-021-17427-0
Mera R, Torres E, Abalde J (2016) Effects of sodium sulfate on the freshwater microalga Chlamydomonas moewusii: implications for the optimization of algal culture media. J Phycol 52(1):75–88. https://doi.org/10.1111/jpy.12367
Morowvat MH, Ghasemi Y (2019) Maximizing biomass and lipid production in heterotrophic culture of Chlorella vulgaris: Techno-economic assessment. Recent Pat Food Nutr Agric 10(2):115–123. https://doi.org/10.2174/2212798410666180911100034
Morsi H, Eladel H, Maher A (2021) Coupling nutrient removal and biodiesel production by the Chlorophyte Asterarcys quadricellulare grown in municipal wastewater. BioEnergy Res 15:193–201. https://doi.org/10.1007/s12155-021-10314-z
Nagappan S, Kumar G (2021) Investigation of four microalgae in nitrogen deficient synthetic wastewater for biorefinery based biofuel production. Environ Technol Inno 23:101572. https://doi.org/10.1016/j.eti.2021.101572
Pradhan B, Patra S, Nayak R, Swain SS, Jit BP, Behera C, Ragusa A, Ki JS, Jena M (2022) Low-dose priming of gamma radiation enhanced cadmium tolerance in Chlamydomonas reinhardtii by modulating physio-biochemical pathways. Environ Sci Pollut Res 29(53):80383–80398. https://doi.org/10.1007/s11356-022-21374-9
Ra CH, Kang CH, Jung JH, Jeong GT, Kim SK (2016) Effects of light-emitting diodes (LEDs) on the accumulation of lipid content using a two-phase culture process with three microalgae. Bioresour Technol 212:254–261. https://doi.org/10.1016/j.biortech.2016.04.059
Rahmani A, Zerrouki D, Tabchouche A, Djafer L (2022) Oilfield-produced water as a medium for the growth of Chlorella pyrenoidosa outdoor in an arid region. Environ Sci Pollut Res 29:87509–87518. https://doi.org/10.1007/s11356-022-21916-1
Ren H-Y, Wang X-W, Kong F, Zhao L, Xing D, Ren N-Q, Liu B-F (2022) Enhanced semi-continuous hydrogen production by addition of microplastics under mesophilic and thermophilic fermentation. Fuel 315:123247. https://doi.org/10.1016/j.fuel.2022.123247
Ren HY, Dai YQ, Kong F, Xing D, Zhao L, Ren NQ, Ma J, Liu BF (2020) Enhanced microalgal growth and lipid accumulation by addition of different nanoparticles under xenon lamp illumination. Bioresour Technol 297:122409. https://doi.org/10.1016/j.biortech.2019.122409
Ren HY, Liu BF, Ma C, Zhao L, Ren NQ (2013) A new lipid-rich microalga Scenedesmus sp. strain R-16 isolated using Nile red staining: effects of carbon and nitrogen sources and initial pH on the biomass and lipid production. Biotechnol Biofuels 6(1):143. https://doi.org/10.1186/1754-6834-6-143
Sakarika M, Kornaros M (2016) Effect of pH on growth and lipid accumulation kinetics of the microalga Chlorella vulgaris grown heterotrophically under sulfur limitation. Bioresour Technol 219:694–701. https://doi.org/10.1016/j.biortech.2016.08.033
Salbitani G, Bolinesi F, Affuso M, Carraturo F, Mangoni O, Carfagna S (2020) Rapid and positive effect of bicarbonate addition on growth and photosynthetic efficiency of the green microalgae Chlorella Sorokiniana (Chlorophyta, Trebouxiophyceae). Appl Sci 10(13):4515. https://doi.org/10.3390/app10134515
Shen XF, Gao LJ, Zhou SB, Huang JL, Wu CZ, Qin QW, Zeng RJ (2020) High fatty acid productivity from Scenedesmus obliquus in heterotrophic cultivation with glucose and soybean processing wastewater via nitrogen and phosphorus regulation. Sci Total Environ 708:134596. https://doi.org/10.1016/j.scitotenv.2019.134596
Singh DP, Khattar JS, Rajput A, Chaudhary R, Singh R (2019) High production of carotenoids by the green microalga Asterarcys quadricellulare PUMCC 5.1.1 under optimized culture conditions. PLoS One 14(9):e0221930. https://doi.org/10.1371/journal.pone.0221930
Song Q, Kong F, Liu B-F, Song X, Ren N-Q, Ren H-Y (2023a) Insights into the effect of rhamnolipids on the anaerobic fermentation and microalgae lipid production of waste activated sludge: Performance and mechanisms. ACS EST Engg. https://doi.org/10.1021/acsestengg.2c00372
Song X, Liu B-F, Kong F, Ren N-Q, Ren H-Y (2022) Overview on stress-induced strategies for enhanced microalgae lipid production: Application, mechanisms and challenges. Resour Conserv Recy 183:106355. https://doi.org/10.1016/j.resconrec.2022.106355
Song X, Liu B-F, Kong F, Song Q, Ren N-Q, Ren H-Y (2023) Lipid accumulation by a novel microalga Parachlorella kessleri R-3 with wide pH tolerance for promising biodiesel production. Algal Res 69:102925. https://doi.org/10.1016/j.algal.2022.102925
Song X, Liu B-F, Kong F, Song Q, Ren N-Q, Ren H-Y (2023) Simultaneous chromium removal and lipid accumulation by microalgae under acidic and low temperature conditions for promising biodiesel production. Bioresour Technol 370:128515. https://doi.org/10.1016/j.biortech.2022.128515
Song X, Zhao Y, Han B, Li T, Zhao P, Xu JW, Yu X (2020) Strigolactone mediates jasmonic acid-induced lipid production in microalga Monoraphidium sp. QLY-1 under nitrogen deficiency conditions. Bioresour Technol 306:123107. https://doi.org/10.1016/j.biortech.2020.123107
Song X, Zhao Y, Li T, Han B, Zhao P, Xu JW, Yu X (2019) Enhancement of lipid accumulation in Monoraphidium sp. QLY-1 by induction of strigolactone. Bioresour Technol 288:121607. https://doi.org/10.1016/j.biortech.2019.121607
Srinivasan R, Mageswari A, Subramanian P, Suganthi C, Chaitanyakumar A, Aswini V, Gothandam KM (2018) Bicarbonate supplementation enhances growth and biochemical composition of Dunaliella salina V-101 by reducing oxidative stress induced during macronutrient deficit conditions. Sci Rep 8(1):6972. https://doi.org/10.1038/s41598-018-25417-5
Sung YJ, Choi HI, Lee JS, Hong ME, Sim SJ (2019) Screening of oleaginous algal strains from Chlamydomonas reinhardtii mutant libraries via density gradient centrifugation. Biotechnol Bioeng 116(12):3179–3188. https://doi.org/10.1002/bit.27149
Tarazona Delgado R, Guarieiro MdS, Antunes PW, Cassini ST, Terreros HM, Fernandes VdO (2021) Effect of nitrogen limitation on growth, biochemical composition, and cell ultrastructure of the microalga Picocystis salinarum. J Appl Phycol 33(4):2083–2092. https://doi.org/10.1007/s10811-021-02462-8
Varshney P, Beardall J, Bhattacharya S, Wangikar PP (2019) Effect of elevated carbon dioxide and nitric oxide on the physiological responses of two green algae, Asterarcys quadricellulare and Chlorella sorokiniana. J Appl Phycol 32(1):189–204. https://doi.org/10.1007/s10811-019-01950-2
Verma R, Kumari KVLK, Srivastava A, Kumar A (2020) Photoautotrophic, mixotrophic, and heterotrophic culture media optimization for enhanced microalgae production. J Environ Chem Eng 8(5):104149. https://doi.org/10.1016/j.jece.2020.104149
Wang Z, Wen X, Xu Y, Ding Y, Geng Y, Li Y (2018) Maximizing CO2 biofixation and lipid productivity of oleaginous microalga Graesiella sp. WBG-1 via CO2-regulated pH in indoor and outdoor open reactors. Sci Total Environ 619–620:827–833. https://doi.org/10.1016/j.scitotenv.2017.10.127
Xiao B, Wang J, Liao B, Zheng H, Yang X, Xie Z, Li D, Li C (2022) Combined effects of copper and microplastics on physiological parameters of Tubastrea aurea corals. Environ Sci Pollut Res 29(10):14393–14399. https://doi.org/10.1007/s11356-021-16665-6
Xing W, Zhang R, Shao Q, Meng C, Wang X, Wei Z, Sun F, Wang C, Cao K, Zhu B, Gao Z (2021) Effects of laser mutagenesis on microalgae production and lipid accumulation in two economically important fresh Chlorella strains under heterotrophic conditions. Agronomy 11(5):961. https://doi.org/10.3390/agronomy11050961
Ye S, Gao L, Zhao J, An M, Wu H, Li M (2020) Simultaneous wastewater treatment and lipid production by Scenedesmus sp. HXY2. Bioresour Technol 302:122903. https://doi.org/10.1016/j.biortech.2020.122903
Yin D, Wang Z, Wen X, Ding Y, Hou X, Geng Y, Li Y (2019) Effects of carbon concentration, pH, and bubbling depth on carbon dioxide absorption ratio in microalgae medium. Environ Sci Pollut Res 26(32):32902–32910. https://doi.org/10.1007/s11356-019-06287-4
Yun HS, Kim YS, Yoon HS (2021) Effect of different cultivation modes (photoautotrophic, mixotrophic, and heterotrophic) on the growth of Chlorella sp. and biocompositions. Front Bioeng Biotechnol 9:774143. https://doi.org/10.3389/fbioe.2021.774143
Zhao L, Geng X, Zhang Y, Hu X, Zhang X, Xu H, Yang G, Pan K, Jiang Y (2022a) How do microalgae in response to biological pollution treat in cultivation? A case study investigating microalgal defense against ciliate predator Euplotes vannus. Environ Sci Pollut Res 29(21):32171–32179. https://doi.org/10.1007/s11356-021-18123-9
Zhao Y, Li D, Xu JW, Zhao P, Li T, Ma H, Yu X (2018) Melatonin enhances lipid production in Monoraphidium sp. QLY-1 under nitrogen deficiency conditions via a multi-level mechanism. Bioresour Technol 259:46–53. https://doi.org/10.1016/j.biortech.2018.03.014
Zhao Y, Ngo HH, Yu X (2022b) Phytohormone-like small biomolecules for microalgal biotechnology. Trends Biotechnol 40(9):1025–1028. https://doi.org/10.1016/j.tibtech.2022.06.008
Zhao Y, Qiao T, Gu D, Zhu L, Yu X (2022c) Stimulating biolipid production from the novel alga Ankistrodesmus sp. by coupling salt stress and chemical induction. Renew Energ 183:480–490. https://doi.org/10.1016/j.renene.2021.11.034
Zhu L, Li S, Hu T, Nugroho YK, Yin Z, Hu D, Chu R, Mo F, Liu C, Hiltunen E (2019) Effects of nitrogen source heterogeneity on nutrient removal and biodiesel production of mono- and mix-cultured microalgae. Energ Convers Manage 201:112144. https://doi.org/10.1016/j.enconman.2019.112144
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The authors thank the State Key Laboratory of Urban Water Resource and Environment (Harbin Institute of Technology) for providing the research facilities.
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This work was supported by the Key Research and Development Program of Heilongjiang Province (No. 2022ZX02C15), the Natural Science Foundation of Heilongjiang Province (No. YQ2022E008), the Academic Backbone Project of Northeast Agricultural University (No. 54917412), and the Heilongjiang Touyan Innovation Team Program.
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All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Xueting Song. Strain selection was performed by Hong-Yu Ren. The first draft of the manuscript was written by Hong-Yu Ren and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Ren, HY., Song, X., Kong, F. et al. Lipid production characteristics of a newly isolated microalga Asterarcys quadricellulare R-56 as biodiesel feedstock. Environ Sci Pollut Res 30, 48339–48350 (2023). https://doi.org/10.1007/s11356-023-25728-9
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DOI: https://doi.org/10.1007/s11356-023-25728-9