Skip to main content

Advertisement

SpringerLink
Log in

Current perspectives on integrated approaches to enhance lipid accumulation in microalgae

  • Review Article
  • Published:
3 Biotech Aims and scope Submit manuscript

Abstract

In recent years, research initiatives on renewable bioenergy or biofuels have been gaining momentum, not only due to fast depletion of finite reserves of fossil fuels but also because of the associated concerns for the environment and future energy security. In the last few decades, interest is growing concerning microalgae as the third-generation biofuel feedstock. The CO2 fixation ability and conversion of it into value-added compounds, devoid of challenging food and feed crops, make these photosynthetic microorganisms an optimistic producer of biofuel from an environmental point of view. Microalgal-derived fuels are currently being considered as clean, renewable, and promising sustainable biofuel. Therefore, most research targets to obtain strains with the highest lipid productivity and a high growth rate at the lowest cultivation costs. Different methods and strategies to attain higher biomass and lipid accumulation in microalgae have been extensively reported in the previous research, but there are fewer inclusive reports that summarize the conventional methods with the modern techniques for lipid enhancement and biodiesel production from microalgae. Therefore, the current review focuses on the latest techniques and advances in different cultivation conditions, the effect of different abiotic and heavy metal stress, and the role of nanoparticles (NPs) in the stimulation of lipid accumulation in microalgae. Techniques such as genetic engineering, where particular genes associated with lipid metabolism, are modified to boost lipid synthesis within the microalgae, the contribution of “Omics” in metabolic pathway studies. Further, the contribution of CRISPR/Cas9 system technique to the production of microalgae biofuel is also briefly described.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ahmad I, Sharma AK, Daniell H, Kumar S (2015) Altered lipid composition and enhanced lipid production in green microalga by introduction of brassica diacylglycerol acyltransferase 2. Plant Biotechnol J 13:540–550

    CAS  PubMed  Google Scholar 

  • Ajjawi I, Verruto J, Aqui M, Soriaga LB, Coppersmith J, Kwok K, Peach L, Orchard E, Kalb R, Xu W (2017) Lipid production in Nannochloropsis gaditana is doubled by decreasing expression of a single transcriptional regulator. Nat Biotechnol 35:647–652

    CAS  PubMed  Google Scholar 

  • Alishah H, Pourseyedi S, Mahani SE, Ebrahimipour SY (2016a) Extract-mediated synthesis of Ag@ AgCl nanoparticles using Conium maculatum seeds: characterization, antibacterial activity and cytotoxicity effect against MCF-7 cell line. R Sci Chem Adv 6:73197–73202

    CAS  Google Scholar 

  • Alishah H, Seyedi SP, Ebrahimipour SY, Esmaeili-Mahani S (2016b) A green approach for the synthesis of silver nanoparticles using root extract of Chelidonium majus: characterization and antibacterial evaluation. J Cluster Sci 27:421–429

    CAS  Google Scholar 

  • Alishah H, Pourseyedi S, Ebrahimipour SY, Mahani SE, Rafiei N (2017) Green synthesis of starch-mediated CuO nanoparticles: preparation, characterization, antimicrobial activities and in vitro MTT assay against MCF-7 cell line. Rendiconti Lincei 28:65–71

    Google Scholar 

  • Aratboni HA, Rafiei N, Garcia-Granados R, Alemzadeh A, Morones-Ramirez JR (2019) Biomass and lipid induction strategies in microalgae for biofuel production and other applications. Microb Cell Fact 18:178

    Google Scholar 

  • Arisz SA, van Himbergen JAJ, Musgrave A, van den Ende H, Munnik T (2000) Polar glycerolipids of Chlamydomonas moewusii. Phytochem 53:265–270

    CAS  Google Scholar 

  • Arora N, Pienkos PT, Pruthi V, Poluri KM, Guarnieri MT (2018) Leveraging algal omics to reveal potential targets for augmenting TAG accumulation. Biotechnol Adv 36:1274–1292

    CAS  PubMed  Google Scholar 

  • Artamonova EY, Vasskog T, Eilertsen HC (2017) Lipid content and fatty acid composition of Porosira glacialis and Attheya longicornis in response to carbon dioxide (CO2) aeration. PLoS ONE 12(5):e0177703

    CAS  PubMed  PubMed Central  Google Scholar 

  • Banerjee C, Dubey KK, Shukla P (2016) Metabolic engineering of microalgal based biofuel production: prospects and challenges. Front Microbiol 7:432

    PubMed  PubMed Central  Google Scholar 

  • Barreiro DL, Prins W, Ronsse F, Brilman W (2013) Hydrothermal liquefaction (HTL) of microalgae for biofuel production: state of the art review and future prospects. Biomass Bioener 53:113–127

    Google Scholar 

  • Bartley ML, Boeing WJ, Corcoran AA, Holguin FO, Schaub T (2013) Effects of salinity on growth and lipid accumulation of biofuel microalga Nannochloropsis salina and invading organisms. Biomass Bioener 54:83–88

    CAS  Google Scholar 

  • Battah M, El-Ayoty Y, Abomohra AEF, Abd El-Ghany S, Esmael A (2015) Effect of Mn2+, Co2+ and H2O2 on biomass and lipids of the green microalga Chlorella vulgaris as a potential candidate for biodiesel production. Ann Microbiol 65:155–162

    CAS  Google Scholar 

  • Beacham TA, Sweet JB, Allen MJ (2017) Large scale cultivation of genetically modified microalgae: a new era for environmental risk assessment. Algal Res 25:90–100

    Google Scholar 

  • Bharadwaj SV, Ram S, Pancha I, Mishra S (2020) Recent trends in strain improvement for production of biofuels from microalgae. Microalgae cultivation for biofuels production. Academic Press, New York, pp 211–225

    Google Scholar 

  • Blaby IK, Glaesener AG, Mettler T, Fitz-Gibbon ST, Gallaher SD, Liu B, Boyle NR, Kropat J, Stitt M, Johnson S, Benning C, Pellegrini M, Casero D, Merchant SS (2013) Systems-level analysis of nitrogen starvation-induced modifications of carbon metabolism in a Chlamydomonas reinhardtii starchless mutant. Plant Cell 25:4305–4323

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bogen C, Klassen V, Wichmann J, Russa ML, Doebbe A, Grundmann MM et al (2013) Identification of Monoraphidium contortum as a promising species for liquid biofuel production. Bioresour Technol 133:622–626

    CAS  PubMed  Google Scholar 

  • Bohnenberger JE, Crossetti LO (2014) Influence of temperature and nutrient content on lipid production in freshwater microalgae cultures. Ann Braz Aca Sci 86:1239–1248

    CAS  Google Scholar 

  • Borowitzka MA (2013) High-value products from microalgae—their development and commercialisation. J Appl Phycol 25:743–756

    CAS  Google Scholar 

  • Boyle NR, Page MD, Liu B, Blaby IK, Casero D, Kropat J, Cokus SJ, Hong-hermesdorf A, Shaw J, Karpowicz SJ, Gallaher SD, Johnson S, Benning C, Pellegrini M, Grossman A, Merchant SS (2012) Three acyltransferases and nitrogen-responsive regulator are implicated in nitrogen starvation-induced triacylglycerol accumulation in Chlamydomonas. J Biol Chem 287:15811–15825

    CAS  PubMed  PubMed Central  Google Scholar 

  • Breuer G, de Jaeger L, Artus VG, Martens DE, Springer J, Draaisma RB, Lamers PP (2014) Superior triacylglycerol (TAG) accumulation in starchless mutants of Scenedesmus obliquus: (II) evaluation of TAG yield and productivity in controlled photobioreactors. Biotechnol Biofuels 7:70

    PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Carpinelli CE, Telatin A, Vitulo N, Forcato C, Angelo MD, Schiavon R, Vezzi A, Mario G, Morosinotto T (2014) Chromosome scale genome assembly and transcriptome profiling of Nannochloropsis gaditana in nitrogen depletion. Mol Plant 7:323–335

    Google Scholar 

  • Carrier G, Garnier M, Cunff LL, Bougaran G, Probert I, De Vargas C, Corre E, Cadoret JP, Saint-Jean B (2014) Comparative transcriptome of wild type and selected strains of the microalgae Tisochrysis lutea provides insights into the genetic basis, lipid metabolism and the life cycle. PLoS ONE 9:e86889

    PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Cheirsilp B, Kitcha S, Torpee S (2012) Co-culture of an oleaginous yeast Rhodotorula glutinis and a microalga Chlorella vulgaris for biomass and lipid production using pure and crude glycerol as a sole carbon source. Ann Microbiol 62:987–993

    CAS  Google Scholar 

  • Cheng JS, Niu YH, Lu SH, Yuan YJ (2012) Metabolome analysis reveals ethanolamine as potential marker for improving lipid accumulation of model photosynthetic organisms. J Chem Technol Biotechnol 87:1409–1418

    CAS  Google Scholar 

  • Chia MA, Lombardi AT, Melao MDGG, Parrish CC (2013) Effects of cadmium and nitrogen on lipid composition of Chlorella vulgaris (Trebouxiophyceae, Chlorophyta). Eur J Phycol 48:1–11

    CAS  Google Scholar 

  • Choi WY, Lee HY (2016) Effective production of bioenergy from marine Chlorella sp. by high-pressure homogenization. Biotechnol Biotechnol Equ 30:81–89

    CAS  Google Scholar 

  • Chokshi K, Pancha I, Ghosh A, Mishra S (2017) Salinity induced oxidative stress alters the physiological responses and improves the biofuel potential of green microalgae Acutodesmus dimorphus. Biores Technol 244:1376–1383

    CAS  Google Scholar 

  • Cuellar-Bermudez SP, Romero-Ogawa MA, Vannela R, Lai YS, Rittmann BE, Parra-Saldivar R (2015) Effects of light intensity and carbon dioxide on lipids and fatty acids produced by Synechocystis sp. PCC6803 during continuous flow. Algal Res 12:10–16

    Google Scholar 

  • Daboussi F, Leduc S, Maréchal A, Dubois G, Guyot V, Perez-Michaut C, Voytas DF (2014) Genome engineering empowers the diatom Phaeodactylum tricornutum for biotechnology. Nat Commun 5:1–7

    Google Scholar 

  • Damiani MC, Popovich CA, Constenla D, Leonardi PI (2010) Lipid analysis in Haematococcus pluvialis to assess its potential use as biodiesel feedstock. Bioresour Technol 101:38013807

    Google Scholar 

  • De Jaeger L, Carreres BM, Springer J, Schaap PJ, Eggink G, Martins Dos Santos VAP, Wijffels RH, Martens DE (2018) Neochloris oleoabundans is worth its salt: transcriptomic analysis under salt and nitrogen stress. PLoS ONE 13:e0194834

    PubMed  PubMed Central  Google Scholar 

  • De-Bashan LE, Bashan Y, Moreno M, Lebsky VK, Bustillos JJ (2002) Increased pigment and lipid content, lipid variety, and cell and population size of the microalgae Chlorella spp. when co-immobilized in alginate beads with the microalgae-growth-promoting bacterium Azospirillum brasilense. Canad J Microbiol 48:514–521

    CAS  Google Scholar 

  • Del Pozo JC, Lopez Mataz MA, Ramirez-Parra E, Gutierrez C (2005) Hormonal control of the plant cell cycle. Physiol Plant 123:173–183

    Google Scholar 

  • Deng X, Cai J, Fei X (2013) Effect of the expression and knockdown of citrate synthase gene on carbon flux during triacylglycerol biosynthesis by green algae Chlamydomonas reinhardtii. BMC Biochem 14:1–11

    Google Scholar 

  • Deng X, Fan X, Li P, Fei X (2015) A photoperiod-regulating gene CONSTANS is correlated to lipid biosynthesis in Chlamydomonas reinhardtii. BioMed Res Int 2015:715020

  • Diao J, Song X, Cui J, Liu L, Shi M, Wang F, Zhang W (2019) Rewiring metabolic network by chemical modulator-based laboratory evolution doubles lipid production in Crypthecodinium cohnii. Metabol Eng 51:88–98

    CAS  Google Scholar 

  • Dickinson S, Mientus M, Frey D, Amini-Hajibashi A, Ozturk S, Shaikh F, El-Halwagi MM (2017) A review of biodiesel production from microalgae. Clean Technol Environ Poll 19:637–668

    CAS  Google Scholar 

  • Dunahay TG, Jarvis EE, Dais SS, Roessler PG (1996) Manipulation of microalgal lipid production using genetic engineering. Appl Biochem Biotechnol 57:223

    Google Scholar 

  • Fan J, Cui Y, Wan M, Wang W, Li Y (2014) Lipid accumulation and biosynthesis genes response of the oleaginous Chlorella pyrenoidosa under three nutrition stressors. Biotechnol Biofuel 7:17

    Google Scholar 

  • Fan J, Ning K, Zeng X, Luo Y, Wang D, Hu J, Li J, Xu H (2015) Genomic foundation of starch-to-lipid switch in Oleaginous Chlorella spp. Plant Physiol 1:2444–2461

    Google Scholar 

  • Fan J, Xu H, Li Y (2016) Transcriptome-based global analysis of gene expression in response to carbon dioxide deprivation in the green algae Chlorella pyrenoidosa. Algal Res 16:12–19

    Google Scholar 

  • Fang L, Sun D, Xu Z, He J, Qi S, Chen X, Chew W, Liu J (2015) Transcriptomic analysis of a moderately growing sub isolate Botryococcus braunii 779 (Chlorophyta) in response to nitrogen deprivation. Biotechnol Biofuels 8:130

    PubMed  PubMed Central  Google Scholar 

  • Farrokheh A, Tahvildari K, Nozari M (2020) Biodiesel production from the Chlorella vulgaris and Spirulina platensis microalgae by electrolysis using CaO/KOH-Fe3O4 and KF/KOH-Fe3O4 as magnetic nanocatalysts. Biomass Conv Bioref. https://doi.org/10.1007/s13399-020-00688-z

  • Fei X, Li X, Li P, Deng X (2017) Involvement of Chlamydomonas DNA damage tolerance gene UBC2 in lipid accumulation. Algal Res 22:148–159

    Google Scholar 

  • Ferenczi A, Pyott DE, Xipnitou A, Molnar A (2017) Efficient targeted DNA editing and replacement in Chlamydomonas reinhardtii using Cpf1 ribonucleoproteins and single-stranded DNA. Proc Nat Acad Sci 114:13567–13572

    CAS  PubMed  Google Scholar 

  • Foflonker F, Ananyev G, Qiu H, Morrison A, Palenik B, Dismukes GC, Bhattacharya D (2016) The unexpected extremophile: tolerance to fluctuating salinity in the green alga Picochlorum. Algal Res 16:465–472

    Google Scholar 

  • Freire I, Cortina-Burgueno A, Grille P, Arizcun MA, Abellán E, Segura M, Otero A (2016) Nannochloropsis limnetica: a freshwater microalga for marine aquaculture. Aquaculture 459:124–130

    Google Scholar 

  • Garcia de Lomana AL, Baliga N (2010) Transcriptional program for nitrogen starvation-induced lipid accumulation in Chlamydomonas reinhardtii. Biotechnol Biofuels 8:207

    Google Scholar 

  • Gen Q, Wang Q, Chi ZM (2014) Direct conversion of cassava starch into single cell oil by co-cultures of the oleaginous yeast Rhodosporidium toruloides and immobilized amylases-producing yeast Saccharomycopsis fibuligera. Ren Energy 62:522–526

    Google Scholar 

  • Gonzalez-Fernandez C, Ballesteros M (2012) Linking microalgae and cyanobacteria culture conditions and key-enzymes for carbohydrate accumulation. Biotechnol Adv 30:1655–1661

    CAS  PubMed  Google Scholar 

  • Guarnieri MT, Pienkos PT (2015) Algal omics: unlocking bioproduct diversity in algae cell factories. Photosynth Res 123:255–263

    CAS  PubMed  Google Scholar 

  • Guo DS, Ji XJ, Ren LJ, Li GL, Huang H (2017) Improving docosahexaenoic acid production by Schizochytrium sp. using a newly designed high-oxygen-supply bioreactor. AIChE. J Biomolecular Eng Bioeng Biochem Biofuels Food 63:4278–4286

    CAS  Google Scholar 

  • Hannon M, Gimpel J, Tran M, Rasala B, Mayfield S (2010) Biofuels from algae: challenges and potential. Biofuels 1:763–784

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hashimoto K, Yoshizawa AC, Okuda S, Kuma K, Goto S, Kanehisa M (2008) The repertoire of desaturases and elongases reveals fatty acid variations in 56 eukaryotic genomes. J Lipid Res 49:183–191

    CAS  PubMed  Google Scholar 

  • He M, Yan Y, Pei F, Wu M, Gebreluel T, Zou S, Wang C (2017) Improvement on lipid production by Scenedesmus obliquus triggered by low dose exposure to nanoparticles. Sci Rep 7:1–12

    Google Scholar 

  • Ho S, Chen C, Chang J (2012) Effect of light intensity and nitrogen starvation on CO2 fixation and lipid/ carbohydrate production of an indigenous microalga Scenedesmus obliquus CNW-N. Bioresour Technol 113:244–252

    CAS  PubMed  Google Scholar 

  • Ho SH, Chan MC, Liu CC, Chen CY, Lee WL, Lee DJ, Chang JS (2014a) Enhancing lutein productivity of an indigenous microalga Scenedesmus obliquus FSP-3 using light-related strategies. Bioresour Technol 152:275–282

    CAS  PubMed  Google Scholar 

  • Ho SH, Nakanishi A, Ye X, Chang JS, Hara K, Hasunuma T, Kondo A (2014b) Optimizing biodiesel production in marine Chlamydomonas sp. JSC4 through metabolic profiling and an innovative salinity-gradient strategy. Biotechnol Biofuels 7:97

    PubMed  PubMed Central  Google Scholar 

  • Hopes A, Nekrasov V, Kamoun S, Mock T (2016) Editing of the urease gene by CRISPR–Cas in the diatom Thalassiosira pseudonana. Plant Meth 12:49

    Google Scholar 

  • Hu YR, Wang F, Wang SK, Liu CZ, Guo C (2013) Efficient harvesting of marine microalgae Nannochloropsis maritima using magnetic nanoparticles. Bioresour Technol 138:387–390

    CAS  PubMed  Google Scholar 

  • Huang Y, Su C (2014) High lipid content and productivity of microalgae cultivating under elevated carbon dioxide. Int J Environ Sci Technol 11:703–710

    CAS  Google Scholar 

  • Ikaran Z, Urreta I, Castañón S (2015) The effect of nitrogen limitation on the physiology and metabolism of Chlorella vulgaris var L3. Algal Res 10:134–144

    Google Scholar 

  • Iwai M, Ikeda K, Shimojima M, Ohta H (2014) Enhancement of extraplastidic oil synthesis in Chlamydomonas reinhardtii using a type-2 diacylglycerol acyltransferase with a phosphorus starvation-inducible promoter. Plant Biotechnol J 12:808–819

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jaeger D, Winkler A, Mussgnug JH, Kalinowski J, Goesmann A, Kruse O (2017) Time-resolved transcriptome analysis and lipid pathway reconstruction of the oleaginous green microalga Monoraphidium neglectum reveal a model for triacylglycerol and lipid hyperaccumulation. Biotechnol Biofuels 10:197

    PubMed  PubMed Central  Google Scholar 

  • Jayakumar S, Bhuyar P, Pugazhendhi A, Rahim MHA, Maniam GP, Govindan N (2021) Effects of light intensity and nutrients on the lipid content of marine microalga (diatom) Amphiprora sp. for promising biodiesel production. Sci Total Environ 768:145471

    CAS  PubMed  Google Scholar 

  • Jeon HS, Park SE, Ahn B, Kim YK (2017) Enhancement of biodiesel production in Chlorella vulgaris cultivation using silica nanoparticles. Biotechnol Biop Eng 22:136–141

    CAS  Google Scholar 

  • Ji J, Long Z, Lin D (2011) Toxicity of oxide nanoparticles to the green algae Chlorella sp. Chem Eng J 170:525–530

    CAS  Google Scholar 

  • Jiang W, Brueggeman AJ, Horken KM, Plucinak TM, Weeks DP (2014) Successful transient expression of Cas9 and single guide RNA genes in Chlamydomonas reinhardtii. Eukar Cell 13:1465–1469

    Google Scholar 

  • Johnson X, Alric J (2013) Central carbon metabolism and electron transport in Chlamydomonas reinhardtii: metabolic constraints for carbon partitioning between oil and starch. Eukary Cell 12:776–793

    CAS  Google Scholar 

  • Kalita N, Baruah G, Goswami RCD, Talukdar J, Kalita MC (2011) Ankistrodesmus falcatus: a promising candidate for lipid production, its biochemical analysis and strategies to enhance lipid productivity. J Microbiol Biotechnol Res 1:148–157

    CAS  Google Scholar 

  • Kan G, Shi C, Wang X, Xie Q, Wang M, Wang X, Miao J (2012) Acclimatory responses to high-salt stress in Chlamydomonas (Chlorophyta, Chlorophyceae) from Antarctica. Acta Oceanol Sinica 31:116–124

    Google Scholar 

  • Kang NK, Lee B, Choi GG, Moon M, Park MS, Lim J, Yang JW (2014) Enhancing lipid productivity of Chlorella vulgaris using oxidative stress by TiO2 nanoparticles. Kor J Chem Eng 31:861–867

    CAS  Google Scholar 

  • Kang NK, Kim EK, Kim YU, Lee B, Jeong WJ, Jeong B, Chang YK (2017) Increased lipid production by heterologous expression of AtWRI1 transcription factor in Nannochloropsis salina. Biotechnol Biofuels 10:231

    PubMed  PubMed Central  Google Scholar 

  • Kao PH, Ng IS (2017) CRISPRi mediated phosphoenolpyruvate carboxylase regulation to enhance the production of lipid in Chlamydomonas reinhardtii. Bioresour Technol 245:1527–1537

    CAS  PubMed  Google Scholar 

  • Kasai Y, Oshima K, Ikeda F, Abe J, Yoshimitsu Y, Harayama S (2015) Construction of a self-cloning system in the unicellular green alga Pseudochoricystis ellipsoidea. Biotechnol Biofuels 8:94

    PubMed  PubMed Central  Google Scholar 

  • Khan AZ, Shahid A, Cheng H, Mahboob S, Al-Ghanim KA, Bilal M, Nawaz MZ (2018a) Omics technologies for microalgae-based fuels and chemicals: challenges and opportunities. Protein Pept Lett 25:99–107

    CAS  PubMed  Google Scholar 

  • Khan MI, Shin JH, Kim JD (2018b) The promising future of microalgae: current status, challenges, and optimization of a sustainable and renewable industry for biofuels, feed, and other products. Microb Cell Fact 17:36

    PubMed  PubMed Central  Google Scholar 

  • Khan MJ, Bawra N, Verma A, Kumar V, Pugazhendhi A, Joshi KB, Vinayak V (2021) Cultivation of diatom Pinnularia saprophila for lipid production: a comparison of methods for harvesting the lipid from the cells. Bioresour Technol 319:124129

    CAS  PubMed  Google Scholar 

  • Khotimchenko SV, Yakovleva IM (2005) Lipid composition of the red alga Tichocarpus crinitus exposed to different levels of photon irradiance. Phytochem 66:73–79

    CAS  Google Scholar 

  • Khozin-Goldberg I, Cohen Z (2011) Unraveling algal lipid metabolism: recent advances in gene identification. Biochimie 93:91–100

    CAS  PubMed  Google Scholar 

  • Kim S, Kim D, Cho SW, Kim J, Kim JS (2014) Highly efficient RNA-guided genome editing in human cells via delivery of purified Cas9 ribonucleoproteins. Genome Res 24:1012–1019

    CAS  PubMed  PubMed Central  Google Scholar 

  • Knothe G (2009) Improving biodiesel fuel properties by modifying fatty ester composition. Energy Environ Sci 2:759–766

    CAS  Google Scholar 

  • Kwak M, Park WK, Shin SE, Koh HG, Lee B, Jeong B, Chang YK (2017) Improvement of biomass and lipid yield under stress conditions by using diploid strains of Chlamydomonas reinhardtii. Algal Res 26:180–189

    Google Scholar 

  • Lam MK, Lee KT (2012) Microalgae biofuels: a critical review of issues, problems and the way forward. Biotechnol Adv 30:673–690

    CAS  PubMed  Google Scholar 

  • Lamers PP, Janssen M, De Vos RCH, Bino RJ, Wijffels RH (2012) Carotenoid and fatty acid metabolism in nitrogen starved Dunaliella salina, a unicellular green microalga. J Biotechnol 162:21–27

    CAS  PubMed  Google Scholar 

  • Lei A, Chen H, Shen G, Hu Z, Chen L, Wang J (2012) Expression of fatty acid synthesis genes and fatty acid accumulation in Haematococcus pluvialis under different stressors. Biotechnol Biofuels 5:18

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lenka SK, Carbonaro N, Park R, Miller SM, Thorpe I, Li Y (2016) Current advances in molecular, biochemical, and computational modeling analysis of microalgal triacylglycerol biosynthesis. Biotechnol Adv 34:1046–1063

    CAS  PubMed  Google Scholar 

  • Li Y, Han D, Hu G, Dauvillee D, Sommerfeld M, Ball S, Hu Q (2010) Chlamydomonas starchless mutant defective in ADP-glucose pyrophosphorylase hyper-accumulates triacylglycerol. Metabol Eng 12:387–391

    Google Scholar 

  • Li Y, Fei X, Deng X (2012) Novel molecular insights into nitrogen starvation-induced triacylglycerols accumulation revealed by differential gene expression analysis in green algae Micractinium pusillum. Biomass Bioener 42:199–211

    CAS  Google Scholar 

  • Li J, Han D, Wang D, Ning K, Jia J, Wei L, Hu Q (2014a) Choreography of transcriptomes and lipidomes of Nannochloropsis reveals the mechanisms of oil synthesis in microalgae. Plant Cell 26:1645–1665

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Han F, Xu H, Mu J, Chen D, Feng B, Zeng H (2014b) Potential lipid accumulation and growth characteristic of the green alga Chlorella with combination cultivation mode of nitrogen (N) and phosphorus (P). Bioresour Technol 174:24–32

    CAS  PubMed  Google Scholar 

  • Li L, Zhang G, Wang Q (2016) De novo transcriptomic analysis of Chlorella sorokiniana reveals differential genes expression in photosynthetic carbon fixation and lipid production. BMC Microbiol 16:223

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li DW, Balamurugan S, Yang YF, Zheng JW, Huang D, Zou LG, Li HY (2019) Transcriptional regulation of microalgae for concurrent lipid overproduction and secretion. Sci Adv 5:3795

    Google Scholar 

  • Liang MH, Jiang JG (2013) Advancing oleaginous microorganisms to produce lipid via metabolic engineering technology. Prog Lipid Res 52:395–408

    CAS  PubMed  Google Scholar 

  • Liang Y, Sarkany N, Cui Y (2009) Biomass and lipid productivities of Chlorella vulgaris under autotrophic, heterotrophic and mixotrophic growth conditions. Biotechnol Lett 31:1043–1049

    CAS  PubMed  Google Scholar 

  • Lim DK, Schenk PM (2017) Microalgae selection and improvement as oil crops: GM vs non-GM strain engineering. AIMS Bioeng 4:151–161

    Google Scholar 

  • Lin IP, Jiang PL, Chen CS, Tzen JTC (2012) A unique caleosin serving as the major integral protein in oil bodies isolated from Chlorella sp. cells cultured with limited nitrogen. Plant Physiol Biochem 61:80–87

    CAS  PubMed  Google Scholar 

  • Lin H, Wang Q, Shen Q, Zhan J, Zhao Y (2013) Genetic engineering of microorganisms for biodiesel production. Bioeng 4(5):292–304

    Google Scholar 

  • Liu ZY, Wang GC, Zhou BC (2008) Effect of iron on growth and lipid accumulation in Chlorella vulgaris. Bioresour Technol 99:4717–4722

    CAS  PubMed  Google Scholar 

  • Liu J, Wen QW, Yunmeng SY (2016) Stimulatory effect of auxins on the growth and lipid productivity of Chlorella pyrenoidosa and Scenedesmus quadricauda. Algal Res 18:273–280

    Google Scholar 

  • Lu Y, Xu J (2015) Phytohormones in microalgae: a new opportunity for microalgal biotechnology. Trends Plant Sci 20:273–282

    CAS  PubMed  Google Scholar 

  • Luo SS, Dong ZJ, Wu XD, Liu YH, Ruan R (2013) Pelletization behavior of fungal Chlorella sp. symbiosis system. Res J Biotechnol 8:56–59

    CAS  Google Scholar 

  • Lv H, Qu G, Qi X, Lu L, Tian C, Ma Y (2013) Transcriptome analysis of Chlamydomonas reinhardtii during the process of lipid accumulation. Genome 101:229–237

    CAS  Google Scholar 

  • Lynn SG, Kilham SS, Kreeger DA, Interlandi SJ (2000) Effect of nutrient availability on the biochemical and elemental stoichiometry in the freshwater diatom Stephanodiscus minutulus (Bacillariophyceae). J Phycol 36:510–522

    CAS  PubMed  Google Scholar 

  • Ma X, Yao L, Yang B, Lee YK, Chen F, Liu J (2017) RNAi-mediated silencing of a pyruvate dehydrogenase kinase enhances triacylglycerol biosynthesis in the oleaginous marine alga Nannochloropsis salina. Sci Rep 7:11485

    PubMed  PubMed Central  Google Scholar 

  • Mata TM, Almeidab R, Caetanoa NS (2013) Effect of the culture nutrients on the biomass and lipid productivities of microalgae Dunaliella tertiolecta. Chem Eng 32:973

    Google Scholar 

  • Matsuzaki M, Misumi O, Shin-I T (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae. Nature 428:653–657

    CAS  PubMed  Google Scholar 

  • Mendes LBB, Vermelho AB (2013) Allelopathy as a potential strategy to improve microalgae cultivation. Biotechnol Biofuels 6:152–166

    CAS  Google Scholar 

  • Menegol T, Diprat AB, Rodrigues E, Rech R (2017) Effect of temperature and nitrogen concentration on biomass composition of Heterochlorella luteoviridis. Food Sci Technol 37:28–37

    Google Scholar 

  • Miao XL, Wu QY (2006) Biodiesel production from heterotrophic microalgal oil. Biores Technol 97:841–846

    CAS  Google Scholar 

  • Miller R, Wu G, Deshpande RR, Vieler A, Gärtner K, Li X, Moellering ER, Zäuner S, Cornish AJ, Liu B, Bullard B, Sears BB, Kuo MHMH, Hegg EL, Shachar Hill Y, Shiu SHSH, Benning C, Gartner K, Li X, Moellering ER, Zauner S, Cornish AJ, Liu B, Bullard B, Sears BB, Kuo MHMH, Hegg EL, Shachar Hill Y, Shiu SHSH, Benning C (2010) Changes in transcript abundance in Chlamydomonas reinhardtii following nitrogen deprivation predict diversion of metabolism. Plant Physiol 154:1737–1752

    CAS  PubMed  PubMed Central  Google Scholar 

  • Min SK, Yoon GH, Joo JH, Sim SJ, Shin HS (2014) Mechanosensitive physiology of Chlamydomonas reinhardtii under direct membrane distortion. Sci Rep 4:4675

    PubMed  PubMed Central  Google Scholar 

  • Mishra A, Medhi K, Malaviya P, Thakur IS (2019) Omics approaches for microalgal applications: prospects and challenges. Bioresour Technol 291:121890

    CAS  PubMed  Google Scholar 

  • Misra N, Panda PK, Parida BK (2013) Agrigenomics for microalgal biofuel production: an overview of various bioinformatics resources and recent studies to link OMICS to bioenergy and bioeconomy. Omics A J Int Biol 17:537–549

    CAS  Google Scholar 

  • Moellering ER, Benning C (2010) RNA interference silencing of a major lipid droplet protein affects lipid droplet size in Chlamydomonas reinhardtii. Eukary Cell 9:97–106

    CAS  Google Scholar 

  • Msanne J, Xu D, Konda AR, Casas-Mollano JA, Awada T, Cahoon EB, Cerutti H (2012) Metabolic and gene expression changes triggered by nitrogen deprivation in the photoautotrophically grown microalgae Chlamydomonas reinhardtii and Coccomyxa sp. C-169. Phytochem 75:50–59

    CAS  Google Scholar 

  • Naduthodi MIS, Barbosa MJ, van der Oost J (2018) Progress of CRISPR-Cas based genome editing in photosynthetic microbes. Biotechnol J 13:e1700591

    PubMed  Google Scholar 

  • Nakanishi A, Aikawa S, Ho SH, Chen CY, Chang JS, Hasunuma T et al (2014) Development of lipid productivities under different CO2 conditions of marine microalgae Chlamydomonas sp. JSC4. Bioresour Technol 152:247–252

    CAS  PubMed  Google Scholar 

  • Nordin N, Yusof N, Maeda T, Mustapha NA, Yusoff MZM, Khairuddin RFR (2020) Mechanism of carbon partitioning towards starch and triacylglycerol in Chlorella vulgaris under nitrogen stress through whole-transcriptome analysis. Biomass Bioenergy 138:105600

    CAS  Google Scholar 

  • Nymark M, Sharma AK, Sparstad T, Bones AM, Winge P (2016) A CRISPR/Cas9 system adapted for gene editing in marine algae. Sci Rep 6:24951

    CAS  PubMed  PubMed Central  Google Scholar 

  • Oh HM, Ahn CY, Lee YK, Kim HS, Ko SR (2014) Novel microorganism rhizobium sp. publication classification KB 10 having properties of promoting growth of Botryococcus braunii and increased fatty acid content, 2014 March. US patent no. US20140087420

  • Osada K, Maeda Y, Yoshino T, Nojima D, Bowler C, Tanaka T (2017) Enhanced NADPH production in the pentose phosphate pathway accelerates lipid accumulation in the oleaginous diatom Fistulifera solaris. Algal Res 23:126–134

    Google Scholar 

  • Osorio H, Jara C, Fuenzalida K, Rey-Jurado E, Vasquez M (2019) High-efficiency nuclear transformation of the microalgae Nannochloropsis oceanica using Tn5 Transposome for the generation of altered lipid accumulation phenotypes. Biotechnol Biofuel 12:134

    Google Scholar 

  • Ota M, Kato Y, Watanabe H, Watanabe M, Sato Y, Smith RL Jr, Inomata H (2009) Fatty acid production from a highly CO2 tolerant alga, Chlorocuccum littorale, in the presence of inorganic carbon and nitrate. Bioresour Technol 100:5237–5242

    CAS  PubMed  Google Scholar 

  • Pandit PR, Fulekar MH, Karuna MSL (2017) Effect of salinity stress on growth, lipid productivity, fatty acid composition, and biodiesel properties in Acutodesmus obliquus and Chlorella vulgaris. Environ Sci Poll Res 24:13437–13451

    CAS  Google Scholar 

  • Park JC, Choi SP, Hong ME, Sim SJ (2014) Enhanced astaxanthin production from microalga, Haematococcus pluvialis by two-stage perfusion culture with stepwise light irradiation. Bioproc Biosyst Eng 37:2039–2047

    CAS  Google Scholar 

  • Piotrowska-Niczyporuk A, Bajguz A (2014) The effect of natural and synthetic auxins on the growth, metabolite content and antioxidant response of green alga Chlorella vulgaris (Trebouxiophyceae). Plant Growth Reg 73:57–66

    CAS  Google Scholar 

  • Poliner E, Takeuchi T, Du ZY, Benning C, Farre EM (2018) Nontransgenic marker-free gene disruption by an episomal CRISPR system in the oleaginous microalga, Nannochloropsis oceanica CCMP1779. ACS Synth Biol 7:962–968

    CAS  PubMed  Google Scholar 

  • Poong SW, Lim PE, Phang SM, Wong CY, Pai TW, Chen CM, Yang CH, Liu CC (2017) Transcriptome sequencing of an Antarctic microalga, Chlorella sp. (Trebouxiophyceae, Chlorophyta) subjected to short-term ultraviolet radiation stress. J Appl Phycol 30:87–99

    Google Scholar 

  • Ra CH, Kang CH, Na KK, Lee CG, Kim SK (2015) Cultivation of four microalgae for biomass and oil production using a two-stage culture strategy with salt stress. Ren Energy 80:117–122

    CAS  Google Scholar 

  • Radakovits R, Jinkerson RE, Darzins A, Posewitz MC (2010) Genetic engineering of algae for enhanced biofuel production. Eukary Cell 9:486–501

    CAS  Google Scholar 

  • Radakovits R, Jinkerson RE, Fuerstenberg SI, Tae H, Settlage RE, Boore JL, Posewitz MC (2012) Draft genome sequence and genetic transformation of the oleaginous alga Nannochloropsis gaditana. Nat Commun 3:1–11

    Google Scholar 

  • Ramazanov A, Ramazanov Z (2006) Isolation and characterization of a starchless mutant of Chlorella pyrenoidosa STL-PI with a high growth rate, and high protein and polyunsaturated fatty acid content. Phycol Res 54:255–259

    CAS  Google Scholar 

  • Reichelt KV, Hoffmann-Luecke P, Hartmann B, Weber B, Ley JP, Krammer GE, Engel KH (2012) Phytochemical characterization of South African bush tea (Athrixia phylicoides DC.). South Afr J Bot 83:1–8

    CAS  Google Scholar 

  • Ren HY, Liu BF, Kong F, Zhao L, Xie GJ, Ren NQ (2014) Enhanced lipid accumulation of green microalga Scenedesmus sp. by metal ions and EDTA addition. Bioresour Technol 169:763–767

    CAS  PubMed  Google Scholar 

  • Renaud SM, Thinh LV, Lambrinidis G, Parry DL (2002) Effect of temperature on growth, chemical composition and fatty acid composition of tropical Australian microalgae grown in batch cultures. Aquaculture 211:195–214

    CAS  Google Scholar 

  • Rengel R, Smith RT, Haslam RP, Sayanova O, Vila M, León R (2018) Overexpression of acetyl-CoA synthetase (ACS) enhances the biosynthesis of neutral lipids and starch in the green microalga Chlamydomonas reinhardtii. Algal Res 31:183–193

    Google Scholar 

  • Rismani-Yazdi H, Haznedaroglu BZ, Hsin C, Peccia J (2012) Transcriptomic analysis of the oleaginous microalga Neochloris oleoabundans reveals metabolic insights into triacylglyceride accumulation. Biotechnol Biofuels 5:74

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rivas MO, Vargas P, Riquelme CE (2010) Interactions of Botryococcus braunii cultures with bacterial biofilms. Microb Ecol 60:628–635

    CAS  PubMed  Google Scholar 

  • Rodriguez-moya M, Gonzalez R (2017) Systems biology approaches for the microbial production of biofuels systems biology approaches for the microbial production of biofuels. Biofuels 2:291–310

    Google Scholar 

  • Ryu BG, Kim J, Farooq W, Han JI, Yang JW, Kim W (2014) Algal-bacterial process for the simultaneous detoxification of thiocyanate-containing wastewater and maximized lipid production under photoautotrophic/photoheterotrophic conditions. Bioresour Technol 162:70–79

    CAS  PubMed  Google Scholar 

  • Salama ES, Kim HC, Abou-Shanab RA, Ji MK, Oh YK, Kim SH, Jeon BH (2013) Biomass, lipid content, and fatty acid composition of freshwater Chlamydomonas mexicana and Scenedesmus obliquus grown under salt stress. Bioproc Biosyst Eng 36:827–833

    CAS  Google Scholar 

  • Salama ES, Kabra AN, Ji MK, Kim JR, Min B, Jeon BH (2014) Enhancement of microalgae growth and fatty acid content under the influence of phytohormones. Bioresour Technol 172:97–103

    CAS  PubMed  Google Scholar 

  • Sarma H, Forid N, Prasad R, Prasad MNV, Ma LQ, Rinklebe J (2021) Enhancing phytoremediation of hazardous metal(loid)s using genome engineering CRISPR–Cas9 technology. J Hazard Mater. https://doi.org/10.1016/j.jhazmat.2021.125493

    Article  PubMed  Google Scholar 

  • Sasso S, Pohnert G, Lohr M, Mittag M, Hertweck C (2011) Microalgae in the postgenomic era: a blooming reserviour for new natural products. Microbiol Mol Biol Rev 36:761–785

    Google Scholar 

  • Schuhmann H, Lim DK, Schenk PM (2012) Perspectives on metabolic engineering for increased lipid contents in microalgae. Biofuels 3:71–86

    CAS  Google Scholar 

  • Serrano G et al (2009) Chlamydomonas CONSTANS and the evolution of plant photoperiodic signaling. Current Biol 19:359–368

    CAS  Google Scholar 

  • Shahid A, Rehman AU, Usman M, Ashraf MUF, Javed MR, Khan AZ, Mehmood MA (2020) Engineering the metabolic pathways of lipid biosynthesis to develop robust microalgal strains for biodiesel production. Biotechnol Appl Biochem 67:41–51

    CAS  PubMed  Google Scholar 

  • Shanmugam S, Mathimani T, Anto S, Sudhakar MP, Kumar SS, Pugazhendhi A (2020) Cell density, lipidomic profile, and fatty acid characterization as selection criteria in bioprospecting of microalgae and cyanobacterium for biodiesel production. Bioresour Technol 304:123061

    CAS  PubMed  Google Scholar 

  • Sharma KK, Schuhmann H, Schenk PM (2012) High lipid induction in microalgae for biodiesel production. Energy 5:1532–1553

    CAS  Google Scholar 

  • Sharmin N, Hasan MS, Parsons AJ, Furniss D, Scotchford CA, Ahmed I, Rudd CD (2013) Effect of boron addition on the thermal, degradation, and cytocompatibility properties of phosphate-based glasses. BioMed Res Int 2013:902427

    PubMed  PubMed Central  Google Scholar 

  • Shin H, Hong S, Kim H, Yoo C, Lee H, Choi H, Lee C, Cho B (2015) Elucidation of the growth delimitation of Dunaliella tertiolecta under nitrogen stress by integrating transcriptome and peptidome analysis. Bioresour Technol 194:57–66

    CAS  PubMed  Google Scholar 

  • Shin SE, Lim JM, Koh HG, Kim EK, Kang NK, Jeon S, Kim J (2016) CRISPR/Cas9-induced knockout and knock-in mutations in Chlamydomonas reinhardtii. Sci Rep 6:1–15

    Google Scholar 

  • Shrestha A, Khan A, Dey N (2018) Cis-trans engineering: advances and perspectives on customized transcriptional regulation in Plants. Mol Plant 11:886–898

    CAS  PubMed  Google Scholar 

  • Sibi G, Ananda KD, Gopal T, Harinath K, Banupriya S, Chaitra S (2017) Metal nanoparticle triggered growth and lipid production in Chlorella vulgaris. Int J Sci Res Environ Sci Toxicol 2:1–8

    Google Scholar 

  • Singh P, Guldhe A, Kumari S, Rawat I, Bux F (2016) Combined metals and EDTA control: an integrated and scalable lipid enhancement strategy to alleviate biomass constraints in microalgae under nitrogen limited conditions. Energy Conv Manag 114:100–109

    CAS  Google Scholar 

  • Sirikhachornkit A, Suttangkakul A, Vuttipongchaikij S, Juntawong P (2018) De novo transcriptome analysis and gene expression profiling of an oleaginous microalga Scenedesmus acutus TISTR8540 during nitrogen deprivation-induced lipid accumulation. Sci Rep 8:1–12

    CAS  Google Scholar 

  • Slattery SS, Diamond A, Wang H, Therrien JA, Lant JT, Jazey T et al (2018) An expanded plasmid-based genetic toolbox enables Cas9 genome editing and stable maintenance of synthetic pathways in Phaeodactylum tricornutum. ACS Synth Biol 7:328–338

    CAS  PubMed  Google Scholar 

  • Smith SR, Glé C, Abbriano RMJ, Traller C, Davis A, Trentacoste E, Vernet M, Allen AE, Hildebrand M (2016) Transcript level coordination of carbon pathways during silicon starvation-induced lipid accumulation in the diatom Thalassiosira pseudonana. New Phytol 210:890–904

    CAS  PubMed  PubMed Central  Google Scholar 

  • Song CW, Lee J, Lee SY (2015) Genome engineering and gene expression control for bacterial strain development. Biotechnol J 10:56–68

    CAS  PubMed  Google Scholar 

  • Srivastava G, Goud VV (2017) Salinity induced lipid production in microalgae and cluster analysis (ICCB 16-BR_047). Bioresour Technol 242:244–252

    CAS  PubMed  Google Scholar 

  • Srivastava V, Gupta SK, Singh P, Sharma B, Singh RP (2018) Biochemical, physiological, and yield responses of lady’s finger (Abelmoschus esculentus L.) grown on varying ratios of municipal solid waste vermicompost. Int J Recycl Org Waste Agric 7:241–250

    Google Scholar 

  • Sturme MH, Gong Y, Heinrich JM, Klok AJ, Eggink G, Wang D, Wijffels RH (2018) Transcriptome analysis reveals the genetic foundation for the dynamics of starch and lipid production in Ettlia oleoabundans. Algal Res 33:142–155

    Google Scholar 

  • Su CH, Chien LJ, Gomes J, Lin YS, Yu YK, Liou JS, Syu RJ (2011) Factors affecting lipid accumulation by Nannochloropsis oculata in a two-stage cultivation process. J Appl Phycol 23:903–908

    CAS  Google Scholar 

  • Sun D, Zhu J, Fang L, Zhang X, Chow Y, Liu J (2013) De novo transcriptome profiling uncovers a drastic downregulation of photosynthesis upon nitrogen deprivation in the nonmodel green alga Botryosphaerella sudeticus. BMC Genom 14:1–18

    CAS  Google Scholar 

  • Sun H, Liu B, Lu X, Cheng KW, Chen F (2017) Staged cultivation enhances biomass accumulation in the green growth phase of Haematococcus pluvialis. Bioresour Technol 233:326–331

    CAS  PubMed  Google Scholar 

  • Sun XM, Ren LJ, Zhao QY, Ji XJ, Huang H (2018) Microalgae for the production of lipid and carotenoids: a review with focus on stress regulation and adaptation. Biotechnol Biofuels 11:272

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sun XM, Ren LJ, Zhao QY, Zhang LH, Huang H (2019) Application of chemicals for enhancing lipid production in microalgae-a short review. Bioresour Technol 293:122135

    CAS  PubMed  Google Scholar 

  • Sushchik NN, Kalacheva GS, Zhila NO, Gladyshev MI, Volova TG (2003) A temperature dependence of the intra- and extracellular fatty-acid composition of green algae ad Cyanobacterium. Russ J Plant Physiol 50:374–380

    CAS  Google Scholar 

  • Tabatabaei M, Masoud T, Salehi JG, Mohammadreza S, Mohammad P (2011) Biodiesel production from genetically engineered microalgae: future of bioenergy in Iran. Ren Sustain Energy Rev 15:1918–1927

    CAS  Google Scholar 

  • Tan KWM, Lee YK (2016) The dilemma for lipid productivity in green microalgae: importance of substrate provision in improving oil yield without sacrificing growth. Biotechnol Biofuels 9:1–14

    Google Scholar 

  • Tanwar A, Sharma S, Kumar S (2018) Targeted genome editing in algae using CRISPR/Cas9. Ind J Plant Physiol 23:653–669

    Google Scholar 

  • Tate JJ, Wing MTG, Rusch KA, Benton MG (2013) The effects of plant growth substances and mixed cultures on growth and metabolite production of green algae Chlorella sp.: a review. J Plant Grow Reg 32:417–428

    CAS  Google Scholar 

  • Tibocha-Bonilla JD, Zuniga C, Godoy-Silva RD, Zengler K (2018) Advances in metabolic modeling of oleaginous microalgae. Biotechnol Biofuels 11:241

    PubMed  PubMed Central  Google Scholar 

  • Toor SS, Rosendahl L, Rudolf A (2011) Hydrothermal liquefaction of biomass: a review of subcritical water technologies. Energy 36:2328–2342

    CAS  Google Scholar 

  • Trentacoste EM, Shrestha RP, Smith SR, Gle C, Hartmann AC, Hildebrand M, Gerwick WH (2013) Metabolic engineering of lipid catabolism increases microalgal lipid accumulation without compromising growth. Proc Nat Acad Sci 110:19748–19753

    CAS  PubMed  Google Scholar 

  • Valenzuela J, Mazurie A, Carlson RP, Gerlach R, Cooksey KE, Peyton BM, Fields MW (2012) Potential role of multiple carbon fixation pathways during lipid accumulation in Phaeodactylum tricornutum. Biotechnol Biofuels 5:40

    CAS  PubMed  PubMed Central  Google Scholar 

  • Verruto J, Francis K, Wang Y, Low MC, Greiner J, Tacke S et al (2018) Unrestrained markerless trait stacking in Nannochloropsis gaditana through combined genome editing and marker recycling technologies. Proc Nat Acad Sci 115:E7015–E7022

    CAS  PubMed  Google Scholar 

  • Vlaskin MS, Grigorenko AV, Chernova NI, Kiseleva SV (2018) Hydrothermal liquefaction of microalgae after different pre-treatments. Energy Expl Exploit 36:1546–1555

    Google Scholar 

  • Wang C, Li Y, Lu J, Deng X, Li H, Hu Z (2018) Effect of overexpression of LPAAT and GPD1 on lipid synthesis and composition in green microalga Chlamydomonas reinhardtii. J App Phycol 30:1711–1719

    CAS  Google Scholar 

  • Wayne Orr A, Helmke BP, Blackman BR, Schwatz MA (2006) Mechanism of mechanotransduction. Dev Cell 10:11–20

    PubMed  Google Scholar 

  • Wei L, Huang X, Huang Z (2015) Temperature effects on lipid properties of microalgae Tetraselmis subcordiformis and Nannochloropsis oculate as biofuel resources. Chin J Oceanol Limnol 33:99106

    Google Scholar 

  • Wei L, Xin Y, Wang Q, Yang J, Hu H, Xu J (2017) RNAi-based targeted gene knockdown in the model oleaginous microalgae Nannochloropsis oceanica. Plant J 89:1236–1250

    CAS  PubMed  Google Scholar 

  • Wensel P, Helms G, Hiscox B, Davis WC, Kirchhoff H, Bule M, Yu L, Chen S (2014) Isolation, characterization, and validation of oleaginous, multi-trophic, and haloalkaline-tolerant microalgae for two-stage cultivation. Algal Res 4:2–11

    Google Scholar 

  • Work VH, Radakovits R, Jinkerson RE, Meuser JE, Elliott LG, Vinyard DJ, Posewitz MC (2010) Increased lipid accumulation in the Chlamydomonas reinhardtii sta7-10 starchless isoamylase mutant and increased carbohydrate synthesis in complemented strains. Eukary Cell 9:1251–1261

    CAS  Google Scholar 

  • Wrede D, Taha M, Miranda AF, Kadali K, Stevenson T, Ball AS et al (2014) Cocultivation of fungal and microalgal cells as an efficient system for harvesting microalgal cells, lipid production and wastewater treatment. PLoS ONE 9:e113497

    PubMed  PubMed Central  Google Scholar 

  • Xia CJ, Zhang JG, Zhang WD, Hu B (2011) A new cultivation method for microbial oil production: cell pelletization and lipid accumulation by Mucor circinelloides. Biotechnol Biofuels 4:15

    PubMed  PubMed Central  Google Scholar 

  • Xie SX, Sun S, Dai SY, Yuan JS (2013) Efficient coagulation of microalgae in cultures with filamentous fungi. Algal Res Biomass Biofuels Bioproc 2:28–33

    Google Scholar 

  • Xin L, Hu HY, Ke G, Sun YX (2010) Effects of different nitrogen and phosphorus concentrations on the growth, nutrient uptake, and lipid accumulation of a freshwater microalga Scenedesmus sp. Bioresour Technol 101:5494–5500

    CAS  PubMed  Google Scholar 

  • Xin Y, Lu Y, Lee YY, Wei L, Jia J, Wang Q, Liu J (2017) Producing designer oils in industrial microalgae by rational modulation of co-evolving type-2 diacylglycerol acyltransferases. Mol Plant 10:1523–1539

    CAS  PubMed  Google Scholar 

  • Xin Y, Shen C, She Y, Chen H, Wang C, Wei L, Xu J (2019) Biosynthesis of triacylglycerol molecules with a tailored PUFA profile in industrial microalgae. Mol Plant 12:474–488

    CAS  PubMed  Google Scholar 

  • Xue F, Miao J, Zhang X, Tan T (2010) A new strategy for lipid production by mix cultivation of Spirulina platensis and Rhodotorula glutinis. Appl Biochem Biotechnol 160:498–503

    CAS  PubMed  Google Scholar 

  • Xue J, Niu YF, Huang T, Yang WD, Liu JS, Li HY (2015) Genetic improvement of the microalga Phaeodactylum tricornutum for boosting neutral lipid accumulation. Metabol Eng 27:1–9

    Google Scholar 

  • Yadav G, Sekar M, Kim SH, Geo VE, Bhatia SK, Sabir JS, Chi NTL, Brindadevi K, Pugazhendhi A (2021) Lipid content, biomass density, fatty acid as selection markers for evaluating the suitability of four fast growing cyanobacterial strains for biodiesel production. Bioresour Technol 325:124654

    CAS  PubMed  Google Scholar 

  • Yang D, Song D, Kind T, Ma Y, Hoefkens J, Fiehn O (2015a) Lipidomic analysis of Chlamydomonas reinhardtii under nitrogen and sulfur deprivation. PLoS ONE 10:e0137948

    PubMed  PubMed Central  Google Scholar 

  • Yang Y, Feng J, Li T, Ge F, Zhao J (2015b) CyanOmics: an integrated database of omics for the model cyanobacterium Synechococcus sp. PCC 7002. Database, 2015, 2015

  • Yang B, Liu J, Jiang Y, Chen F (2016) Chlorella species as hosts for genetic engineering and expression of heterologous proteins: progress, challenge and perspective. Biotechnol J 11:1244–1261

    CAS  PubMed  Google Scholar 

  • Yang L, Chen J, Qin S, Zeng M, Jiang Y, Hu L, Wang J (2018) Growth and lipid accumulation by different nutrients in the microalga Chlamydomonas reinhardtii. Biotechnol Biofuels 11(1):40

    PubMed  PubMed Central  Google Scholar 

  • Yao L, Tan TW, Ng YK, Hon K, Ban K, Shen H, Lin H, Lee YK (2015) RNA-Seq transcriptomic analysis with Bag2D software identifies key pathways enhancing lipid yield in a high lipid producing mutant of the non-model green alga Dunaliella tertiolecta. Biotechnol Biofuels 8:191

    PubMed  PubMed Central  Google Scholar 

  • Yoo C, Jun SY, Lee JY, Ahn CY, Oh HM (2010) Selection of microalgae for lipid production under high levels carbon dioxide. Bioresour Technol 101:S71–S74

    CAS  PubMed  Google Scholar 

  • Zalogin TR, Pick U (2014) Inhibition of nitrate reductase by azide in microalgae results in triglycerides accumulation. Algal Res 3:17–23

    Google Scholar 

  • Zhao CH, Chi Z, Zhang F, Guo FJ, Li M, Song WB (2011) Direct conversion of inulin and extract of tubers of Jerusalem artichoke into single cell oil by cocultures of Rhodotorula mucilaginosa TJY15a and immobilized inulinase producing yeast cells. Bioresour Technol 102(10):6128–6133

    CAS  PubMed  Google Scholar 

  • Zhao P, Yu X, Li J, Tang X, Huang Z (2014) Enhancing lipid productivity by cocultivation of Chlorella sp. U4341 and Monoraphidium sp. FXY-10. J Biosci Bioeng 118:1–6

    Google Scholar 

  • Zhao B, Li Y, Li C, Yang H, Wang W (2018) Enhancement of Schizochytrium DHA synthesis by plasma mutagenesis aided with malonic acid and zeocin screening. Appl Microbiol Biotechnol 102:2351–2361

    CAS  PubMed  Google Scholar 

  • Zoller S, Lutzoni F (2003) Slow algae, fast fungi: exceptionally high nucleotide substitution rate differences between lichenized fungi Omphalina and their symbiotic green algae Coccomyxa. Mol Phylogen Evol 29:629–640

    CAS  Google Scholar 

Download references

Acknowledgements

Prof. Veena Pande is thankful to the Department of Biotechnology, Kumaun University, Nainital for providing infrastructure and facilities for research.

Author information

Authors and Affiliations

  1. Department of Biotechnology, Sir J. C. Bose Technical Campus Bhimtal, Kumaun University, Nainital, Uttarakhand, 263136, India

    Jyoti Rawat & Veena Pande

  2. Department of Life Sciences, School of Basic Sciences and Research, Sharda University, Knowledge Park III, Greater Noida, Uttar Pradesh, 201310, India

    Piyush Kumar Gupta & Soumya Pandit

  3. Department of Botany, Mahatma Gandhi Central University, Motihari, Bihar, 845801, India

    Ram Prasad

Authors
  1. Jyoti Rawat
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Piyush Kumar Gupta
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Soumya Pandit
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ram Prasad
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Veena Pande
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

JR contributed to the collection of the literature, writing, and editing the manuscript drafts. PKG contributed to drawing the figures and editing the draft and also provided the critical inputs in the review discussion. VP and RP conceptualized, planned, and finalized the manuscript.

Corresponding authors

Correspondence to Ram Prasad or Veena Pande.

Ethics declarations

Conflict of interest

Authors declare no competing interest concerning the work performed in the manuscript.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rawat, J., Gupta, P.K., Pandit, S. et al. Current perspectives on integrated approaches to enhance lipid accumulation in microalgae. 3 Biotech 11, 303 (2021). https://doi.org/10.1007/s13205-021-02851-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s13205-021-02851-3

Keywords

Search

Navigation