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Advanced Gene Technology and Synthetic Biology Approaches to Custom Design Microalgae for Biodiesel Production

  • Neha Arora
  • Shweta Tripathi
  • Krishna Mohan Poluri
  • Vikas Pruthi
Chapter

Abstract

Photosynthetic microalgae are being recognized as propitious source for sustainable production of bio-based fuels particularly biodiesel. Oleaginous microalgae possess inherent capability to accumulate high amounts of lipids (mostly as triacylglycerols) under adverse physiological conditions, which can be transesterified to form biodiesel. Since the last decade, research is being focused on finding targets to increase the biomass and lipid productivity of microalgae contributing to large-scale cultivation feasibility. In this regard, algal omics plays a vital role in categorizing regulatory pathways responsible for increasing the lipid accumulation in microalgae leading to identification of suitable targets for genetic engineering. Metabolic engineering of microalgal strains improves the control over growth and lipid pathways resulting in more reproducible and predictable systems compared to the wild-type strains. The present chapter is a comprehensive catalogue of algal omics including transcriptomics, proteomics and metabolomics studies carried out for augmenting lipid accumulation in different microalgal strains under various physiological conditions. The chapter substantiates the rationale for transgenic microalgae and the requisite of integrated genome editing and synthetic biology approach for custom designing of lipid accumulation in microalgae for biodiesel production.

Keywords

Microalgae Lipid Biodiesel Omics Genetic engineering 

Notes

Acknowledgements

Authors are thankful for financial support DBT-SRF to NA (Grant No.: 7001-35-44).

References

  1. Ajjawi I, Verruto J, Aqui M, et al. Lipid production in Nannochloropsis gaditana is doubled by decreasing expression of a single transcriptional regulator. Nat Biotechnol. 2017;35:647.  https://doi.org/10.1038/nbt.3865.CrossRefGoogle Scholar
  2. Akula SP, Miriyala RN, Thota H, et al. Bioinformation techniques for integrating –omics data. Bioinformation. 2009;3(6):284–6.PubMedPubMedCentralCrossRefGoogle Scholar
  3. Arenas EG, Rodriguez Palacio MC, Juantorena AU, et al. Microalgae as a potential source for biodiesel production: techniques, methods, and other challenges. Int J Energy Res. 2017;41:761–89.  https://doi.org/10.1002/er.3663.CrossRefGoogle Scholar
  4. Arora N, Gulati K, Patel A, et al. A hybrid approach integrating arsenic detoxification with biodiesel production using oleaginous microalgae. Algal Res. 2017a;24:29–39.  https://doi.org/10.1016/j.algal.2017.03.012.CrossRefGoogle Scholar
  5. Arora N, Patel A, Sharma M, et al. Insights into the enhanced lipid production characteristics of a fresh water microalga under high salinity conditions. Ind Eng Chem Res. 2017b;56:7413.  https://doi.org/10.1021/acs.iecr.7b00841.CrossRefGoogle Scholar
  6. Baek K, Kim DH, Jeong J, et al. DNA-free two-gene knockout in Chlamydomonas reinhardtii via CRISPR-Cas9 ribonucleoproteins. Sci Rep. 2016;6:1–7.  https://doi.org/10.1038/srep30620.CrossRefGoogle Scholar
  7. Bajhaiya AK, Dean AP, Zeef LAH, et al. PSR1 is a global transcriptional regulator of phosphorus deficiency responses and carbon storage metabolism in Chlamydomonas reinhardtii. Plant Physiol. 2015;170:1216–34.  https://doi.org/10.1104/pp.15.01907.PubMedPubMedCentralCrossRefGoogle Scholar
  8. Bajhaiya AK, Ziehe Moreira J, Pittman JK. Transcriptional engineering of microalgae: prospects for high-value chemicals. Trends Biotechnol. 2017;35:95–9.  https://doi.org/10.1016/j.tibtech.2016.06.001.CrossRefGoogle Scholar
  9. Baroukh C, Bernard O. Metabolic modeling of C. sorokiniana diauxic heterotrophic growth. IFAC-PapersOnLine. 2016;49:330–5.  https://doi.org/10.1016/j.ifacol.2016.12.148.CrossRefGoogle Scholar
  10. Beacham TA, Sweet JB, Allen MJ. Large scale cultivation of genetically modified microalgae: a new era for environmental risk assessment. Algal Res. 2017;25:90–100.  https://doi.org/10.1016/j.algal.2017.04.028.CrossRefGoogle Scholar
  11. Bellou S, Baeshen MN, Elazzazy AM, et al. Microalgal lipids biochemistry and biotechnological perspectives. Biotechnol Adv. 2014;32:1476–93.  https://doi.org/10.1016/j.biotechadv.2014.10.003.PubMedCrossRefGoogle Scholar
  12. Belshaw N, Grouneva I, Aram L, et al. Efficient CRISPR/Cas-mediated homologous recombination in the model diatom Thalassiosira pseudonana. bioRxiv. 2017. http://doi.org/10.1101/215582.
  13. Blaby IK, Glaesener AG, Mettler T, et al. Systems-level analysis of nitrogen starvation-induced modifications of carbon metabolism in a Chlamydomonas reinhardtii starchless mutant. Plant Cell. 2013;25:4305–23.  https://doi.org/10.1105/tpc.113.117580.PubMedPubMedCentralCrossRefGoogle Scholar
  14. Boyle NR, Morgan JA. Flux balance analysis of primary metabolism in Chlamydomonas reinhardtii. BMC Syst Biol. 2009;3:4.  https://doi.org/10.1186/1752-0509-3-4.PubMedPubMedCentralCrossRefGoogle Scholar
  15. Boyle NR, Page MD, Liu B, et al. Three acyltransferases and nitrogen-responsive regulator are implicated in nitrogen starvation-induced triacylglycerol accumulation in Chlamydomonas. J Biol Chem. 2012;287:15811–25.  https://doi.org/10.1074/jbc.M111.334052.PubMedCrossRefGoogle Scholar
  16. Bradnam KR, Fass JN, Alexandrov A, et al. Assemblathon 2: evaluating de novo methods of genome assembly in three vertebrate species. Gigascience. 2013;2:1–31.  https://doi.org/10.1186/2047-217X-2-10.CrossRefGoogle Scholar
  17. Brennan L, Owende P. Biofuels from microalgae — a review of technologies for production, processing, and extractions of biofuels and co-products. Renew Sustain Energ Rev. 2010;14:557–77.  https://doi.org/10.1016/j.rser.2009.10.009.CrossRefGoogle Scholar
  18. Carrier G, Garnier M, Le Cunff L, et al. 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. 2014;9:e86889.  https://doi.org/10.1371/journal.pone.0086889.PubMedPubMedCentralCrossRefGoogle Scholar
  19. Cerutti H. RNA interference: traveling in the cell and gaining functions? Trends Genet. 2003;19:39–46.  https://doi.org/10.1016/S0168-9525(02)00010-0.PubMedCrossRefGoogle Scholar
  20. Chang RL, Ghamsari L, Manichaikul A, et al. Metabolic network reconstruction of Chlamydomonas offers insight into light-driven algal metabolism. Mol Syst Biol. 2011;  https://doi.org/10.1038/msb.2011.52.CrossRefGoogle Scholar
  21. Cheng JS, Niu YH, Lu SH, Yuan YJ. Metabolome analysis reveals ethanolamine as potential marker for improving lipid accumulation of model photosynthetic organisms. J Chem Technol Biotechnol. 2012;87:1409–18.  https://doi.org/10.1002/jctb.3759.CrossRefGoogle Scholar
  22. Chia MA, Lombardi AT, da Graça Gama Melão M, Parrish CC. Combined nitrogen limitation and cadmium stress stimulate total carbohydrates, lipids, protein and amino acid accumulation in Chlorella vulgaris (Trebouxiophyceae). Aquat Toxicol. 2015;160:87–95.  https://doi.org/10.1016/j.aquatox.2015.01.002.PubMedCrossRefGoogle Scholar
  23. Choi G, Kim B, Ahn C. Effect of nitrogen limitation on oleic acid biosynthesis in Botryococcus braunii. J Appl Phycol. 2011;23:1031–7.  https://doi.org/10.1007/s10811-010-9636-1.CrossRefGoogle Scholar
  24. Choi JI, Yoon M, Joe M, et al. Development of microalga Scenedesmus dimorphus mutant with higher lipid content by radiation breeding. Bioprocess Biosyst Eng. 2014;37:2437–44.  https://doi.org/10.1007/s00449-014-1220-7.PubMedCrossRefGoogle Scholar
  25. Christian M, Cermak T, Doyle EL, et al. Targeting DNA double-strand breaks with TAL effector nucleases. Genetics. 2010;186:756–61.  https://doi.org/10.1534/genetics.110.120717.CrossRefGoogle Scholar
  26. Cogne G, Rügen M, Bockmayr A, et al. A model-based method for investigating bioenergetic processes in autotrophically growing eukaryotic microalgae: application to the green algae Chlamydomonas reinhardtii. Biotechnol Prog. 2011;27:631–40.  https://doi.org/10.1002/btpr.596.PubMedCrossRefGoogle Scholar
  27. Corteggiani E, Telatin A, Vitulo N, et al. Chromosome scale genome assembly and transcriptome profiling of Nannochloropsis gaditana in nitrogen depletion. Mol Plant. 2014;7:323–35.  https://doi.org/10.1093/mp/sst120.PubMedCrossRefGoogle Scholar
  28. Daboussi F, Leduc S, Maréchal A, et al. Genome engineering empowers the diatom Phaeodactylum tricornutum for biotechnology. Nat Commun. 2014;5:1–7.  https://doi.org/10.1038/ncomms4831.CrossRefGoogle Scholar
  29. Deng XD, Gu B, Li YJ, et al. The roles of acyl-CoA: diacylglycerol acyltransferase 2 genes in the biosynthesis of triacylglycerols by the green algae Chlamydomonas reinhardtii. Mol Plant. 2012;5:945–7.  https://doi.org/10.1093/mp/sss040.PubMedCrossRefGoogle Scholar
  30. Deng X, Cai J, Fei X. Involvement of phosphatidate phosphatase in the biosynthesis of triacylglycerols in Chlamydomonas reinhardtii. J Zhejiang Univ Sci B. 2013;14:1121–31.  https://doi.org/10.1631/jzus.B1300180.PubMedPubMedCentralCrossRefGoogle Scholar
  31. Deng X, Cai J, Li Y, Fei X. Expression and knockdown of the PEPC1 gene affect carbon flux in the biosynthesis of triacylglycerols by the green alga Chlamydomonas reinhardtii. Biotechnol Lett. 2014;36:2199–208.  https://doi.org/10.1007/s10529-014-1593-3.PubMedCrossRefGoogle Scholar
  32. Dhar S, Pathak M, Shukla PR. Transformation of India’s transport sector under global warming of 2 °C and 1.5 °C scenario. J Clean Prod. 2018;172:417–27.  https://doi.org/10.1016/j.jclepro.2017.10.076.CrossRefGoogle Scholar
  33. Dong H-P, Williams E, Wang D-Z, et al. Responses of Nannochloropsis oceanica IMET1 to long-term nitrogen starvation and recovery. Plant Physiol. 2013;162:1110–26.  https://doi.org/10.1104/pp.113.214320.PubMedPubMedCentralCrossRefGoogle Scholar
  34. Doshi A, Pascoe S, Coglan L, Rainey TJ. Economic and policy issues in the production of algae-based biofuels: a review. Renew Sustain Energ Rev. 2016;64:329–37.  https://doi.org/10.1016/j.rser.2016.06.027.CrossRefGoogle Scholar
  35. Dragosits M, Mattanovich D. Adaptive laboratory evolution – principles and applications for biotechnology TL – 12. Microb Cell Factories. 2013;12:64.  https://doi.org/10.1186/1475-2859-12-64.CrossRefGoogle Scholar
  36. Dunahay TG, Jarvls EE, Dais SS, Roessler PG. Manipulation of microalgal lipid production using genetic engineering. Appl Biochem Biotechnol. 1996;57:223–31.CrossRefGoogle Scholar
  37. Dunn WB, Ellis DI. Metabolomics: current analytical platforms and methodologies. TrAC Trends Anal Chem. 2005;24:285–94.  https://doi.org/10.1016/j.trac.2004.11.021.CrossRefGoogle Scholar
  38. Fan J, Xu H, Li Y. Transcriptome-based global analysis of gene expression in response to carbon dioxide deprivation in the green algae Chlorella pyrenoidosa. ALGAL. 2016;16:12–9.  https://doi.org/10.1016/j.algal.2016.02.032.CrossRefGoogle Scholar
  39. Fang L, Sun D, Xu Z, et al. Transcriptomic analysis of a moderately growing subisolate Botryococcus braunii 779 (Chlorophyta) in response to nitrogen deprivation. Biotechnol Biofuels. 2015;8:1–21.  https://doi.org/10.1186/s13068-015-0307-y.CrossRefGoogle Scholar
  40. Filiatrault MJ. Progress in prokaryotic transcriptomics. Curr Opin Microbiol. 2011;14:579–86.  https://doi.org/10.1016/j.mib.2011.07.023.PubMedCrossRefGoogle Scholar
  41. Foflonker F, Ananyev G, Qiu H, et al. The unexpected extremophile: tolerance to fluctuating salinity in the green alga Picochlorum. Algal Res. 2016;16:465–72.  https://doi.org/10.1016/j.algal.2016.04.003.CrossRefGoogle Scholar
  42. Garcia de Lomana AL, Baliga N. Transcriptional program for nitrogen starvation-induced lipid accumulation in Chlamydomonas reinhardtii. Biotechnol Biofuels. 2010;8:796–9.  https://doi.org/10.1126/science.1189003.CrossRefGoogle Scholar
  43. Garnier M, Carrier G, Rogniaux H, et al. Comparative proteomics reveals proteins impacted by nitrogen deprivation in wild-type and high lipid-accumulating mutant strains of Tisochrysis lutea. J Proteome. 2014;105:107–20.  https://doi.org/10.1016/j.jprot.2014.02.022.PubMedCrossRefGoogle Scholar
  44. Ghosh A, Khanra S, Mondal M, et al. Progress toward isolation of strains and genetically engineered strains of microalgae for production of biofuel and other value added chemicals: A review. Energy Convers Manag. 2016;113:104–18.  https://doi.org/10.1016/j.enconman.2016.01.050.CrossRefGoogle Scholar
  45. Gomes C, Dal DO, Quek L, et al. AlgaGEM – a genome-scale metabolic reconstruction of algae based on the Chlamydomonas reinhardtii genome. BMC Genomics. 2011;12:S5.Google Scholar
  46. Goncalves EC, Wilkie AC, Kirst M, Rathinasabapathi B. Metabolic regulation of triacylglycerol accumulation in the green algae: identification of potential targets for engineering to improve oil yield. Plant Biotechnol J. 2016;14:1649–60.  https://doi.org/10.1111/pbi.12523.PubMedPubMedCentralCrossRefGoogle Scholar
  47. Gordon GC, Korosh TC, Cameron JC, et al. CRISPR interference as a titratable, trans-acting regulatory tool for metabolic engineering in the cyanobacterium Synechococcus sp. strain PCC 7002. Metab Eng. 2016;38:170–9.  https://doi.org/10.1016/j.ymben.2016.07.007.PubMedPubMedCentralCrossRefGoogle Scholar
  48. Guarnieri MT, Nag A, Smolinski SL, et al. Examination of triacylglycerol biosynthetic pathways via de novo transcriptomic and proteomic analyses in an unsequenced microalga. PLoS One. 2011;6:e25851.  https://doi.org/10.1371/journal.pone.0025851.PubMedPubMedCentralCrossRefGoogle Scholar
  49. Guarnieri MT, Nag A, Yang S, Pienkos PT. Proteomic analysis of Chlorella vulgaris: potential targets for enhanced lipid accumulation. J Proteome. 2013;93:245–53.  https://doi.org/10.1016/j.jprot.2013.05.025.CrossRefGoogle Scholar
  50. Gupta V, Thakur RS, Reddy CRK, Jha B. Central metabolic processes of marine macrophytic algae revealed from NMR based metabolome analysis. RSC Adv. 2013;3:7037.  https://doi.org/10.1039/c3ra23017a.CrossRefGoogle Scholar
  51. Hannon M, Gimpel J, Tran M, et al. Biofuels from algae: challenges and potential. Biofuels. 2010;1:763–84.  https://doi.org/10.4155/bfs.10.44.PubMedPubMedCentralCrossRefGoogle Scholar
  52. Ho S-H, Nakanishi A, Ye X, et al. Optimizing biodiesel production in marine Chlamydomonas sp. JSC4 through metabolic profiling and an innovative salinity-gradient strategy. Biotechnol Biofuels. 2014a;7:97.  https://doi.org/10.1186/1754-6834-7-97.PubMedPubMedCentralCrossRefGoogle Scholar
  53. Ho S, Ye X, Hasunuma T, et al. Perspectives on engineering strategies for improving biofuel production from microalgae — a critical review. Biotechnol Adv. 2014b;32:1448–59.  https://doi.org/10.1016/j.biotechadv.2014.09.002.CrossRefGoogle Scholar
  54. Ho SH, Ye X, Hasunuma T, et al. Perspectives on engineering strategies for improving biofuel production from microalgae – a critical review. Biotechnol Adv. 2014c;32:1448–59.  https://doi.org/10.1016/j.biotechadv.2014.09.002.CrossRefGoogle Scholar
  55. Ho SH, Nakanishi A, Ye X, et al. Dynamic metabolic profiling of the marine microalga Chlamydomonas sp. JSC4 and enhancing its oil production by optimizing light intensity Luisa Gouveia. Biotechnol Biofuels. 2015;8:1–17.  https://doi.org/10.1186/s13068-015-0226-y.PubMedPubMedCentralCrossRefGoogle Scholar
  56. Hu Q, Sommerfeld M, Jarvis E, et al. Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J. 2008;54:621–39.  https://doi.org/10.1111/j.1365-313X.2008.03492.x.CrossRefGoogle Scholar
  57. Ikaran Z, Suárez-Alvarez S, Urreta I, Castañón S. The effect of nitrogen limitation on the physiology and metabolism of Chlorella vulgaris var L3. Algal Res. 2015;10:134–44.  https://doi.org/10.1016/j.algal.2015.04.023.CrossRefGoogle Scholar
  58. Ito T, Tanaka M, Shinkawa H, et al. Metabolic and morphological changes of an oil accumulating trebouxiophycean alga in nitrogen-deficient conditions. Metabolomics. 2013;9:178–87.  https://doi.org/10.1007/s11306-012-0463-z.PubMedCrossRefGoogle Scholar
  59. Jaeger D, Winkler A, Mussgnug JH, et al. 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. 2017;10:1–34.  https://doi.org/10.1186/s13068-017-0882-1.
  60. Jamers A, Blust R, De Coen W. Omics in algae: paving the way for a systems biological understanding of algal stress phenomena? Aquat Toxicol. 2009;92:114–21.  https://doi.org/10.1016/j.aquatox.2009.02.012.PubMedCrossRefGoogle Scholar
  61. Jiang WZ, Weeks DP. A gene-within-a-gene Cas9/sgRNA hybrid construct enables gene editing and gene replacement strategies in Chlamydomonas reinhardtii. Algal Res. 2017;26:474–80.  https://doi.org/10.1016/j.algal.2017.04.001.CrossRefGoogle Scholar
  62. Kajikawa M, Sawaragi Y, Shinkawa H, et al. Algal dual-specificity tyrosine phosphorylation-regulated kinase, triacylglycerol accumulation regulator1, regulates accumulation of triacylglycerol in nitrogen or sulfur deficiency. Plant Physiol. 2015;168:752–64.  https://doi.org/10.1104/pp.15.00319.PubMedPubMedCentralCrossRefGoogle Scholar
  63. Kang NK, Jeon S, Kwon S, et al. Effects of overexpression of a bHLH transcription factor on biomass and lipid production in Nannochloropsis salina. Biotechnol Biofuels. 2015;8:1–13. doi:  https://doi.org/10.1186/s13068-015-0386-9.
  64. Kang NK, Kim EK, Kim YU, et al. Increased lipid production by heterologous expression of AtWRI1 transcription factor in Nannochloropsis salina. Biotechnol Biofuels. 2017;10:1–14.  https://doi.org/10.1186/s13068-017-0919-5.
  65. Kao PH, Ng IS. CRISPRi mediated phosphoenolpyruvate carboxylase regulation to enhance the production of lipid in Chlamydomonas reinhardtii. Bioresour Technol. 2017;245:1527.  https://doi.org/10.1016/j.biortech.2017.04.111.PubMedPubMedCentralCrossRefGoogle Scholar
  66. Kato Y, Ho SH, Vavricka CJ, et al. Evolutionary engineering of salt-resistant Chlamydomonas sp. strains reveals salinity stress-activated starch-to-lipid biosynthesis switching. Bioresour Technol. 2017;245:1484–90.  https://doi.org/10.1016/j.biortech.2017.06.035.PubMedCrossRefGoogle Scholar
  67. Kim J, Fabris M, Baart G, et al. Flux balance analysis of primary metabolism in the diatom Phaeodactylum tricornutum. Plant J. 2016;85:161–76.  https://doi.org/10.1111/tpj.13081.PubMedCrossRefGoogle Scholar
  68. Klok AJ, Lamers PP, Martens DE, et al. Edible oils from microalgae: insights in TAG accumulation. Trends Biotechnol. 2014;32:521–8.  https://doi.org/10.1016/j.tibtech.2014.07.004.PubMedCrossRefGoogle Scholar
  69. Kurotani A, Yamada Y, Sakurai T. Alga-PrAS (Algal Protein Annotation Suite): a database of comprehensive annotation in algal proteomes. Plant Cell Physiol. 2017;58:e6.  https://doi.org/10.1093/pcp/pcw212.PubMedPubMedCentralCrossRefGoogle Scholar
  70. Kwak M, Park WK, Shin SE, et al. Improvement of biomass and lipid yield under stress conditions by using diploid strains of Chlamydomonas reinhardtii. Algal Res. 2017;26:180–9.  https://doi.org/10.1016/j.algal.2017.07.027.CrossRefGoogle Scholar
  71. Lenka SK, Carbonaro N, Park R, et al. Current advances in molecular, biochemical, and computational modeling analysis of microalgal triacylglycerol biosynthesis. Biotechnol Adv. 2016;34:1046–63.  https://doi.org/10.1016/j.biotechadv.2016.06.004.PubMedCrossRefGoogle Scholar
  72. Levering J, Broddrick J, Dupont CL, et al. Genome-scale model reveals metabolic basis of biomass partitioning in a model diatom. PLoS One. 2016;11:1–22.  https://doi.org/10.1371/journal.pone.0155038.CrossRefGoogle Scholar
  73. Li Y, Fei X, Deng X. Novel molecular insights into nitrogen starvation-induced triacylglycerols accumulation revealed by differential gene expression analysis in green algae Micractinium pusillum. Biomass Bioenergy. 2012;42:199–211.  https://doi.org/10.1016/j.biombioe.2012.03.010.CrossRefGoogle Scholar
  74. Li Y, Mu J, Chen D, et al. Production of biomass and lipid by the microalgae Chlorella protothecoides with heterotrophic-Cu(II) stressed (HCuS) coupling cultivation. Bioresour Technol. 2013a;148:283–92.  https://doi.org/10.1016/j.biortech.2013.08.153.PubMedCrossRefGoogle Scholar
  75. Li Y, Yuan Z, Mu J, et al. Proteomic analysis of lipid accumulation in Chlorella protothecoides cells by heterotrophic N deprivation coupling cultivation. Energy Fuel. 2013b;27:4031.CrossRefGoogle Scholar
  76. Li Y, Xu H, Han F, et al. Regulation of lipid metabolism in the green microalga Chlorella protothecoides by heterotrophy-photoinduction cultivation regime. Bioresour Technol. 2014;192:781–91.  https://doi.org/10.1016/j.biortech.2014.07.028.PubMedCrossRefGoogle Scholar
  77. Li Y, Mu J, Chen D, et al. Proteomics analysis for enhanced lipid accumulation in oleaginous Chlorella vulgaris under a heterotrophic-Na+ induction two-step regime. Biotechnol Lett. 2015;37:1021–30.  https://doi.org/10.1007/s10529-014-1758-0.PubMedCrossRefGoogle Scholar
  78. Li DW, Cen SY, Liu YH, et al. A type 2 diacylglycerol acyltransferase accelerates the triacylglycerol biosynthesis in heterokont oleaginous microalga Nannochloropsis oceanica. J Biotechnol. 2016a;229:65–71.  https://doi.org/10.1016/j.jbiotec.2016.05.005.PubMedCrossRefGoogle Scholar
  79. Li L, Zhang G, Wang Q. De novo transcriptomic analysis of Chlorella sorokiniana reveals differential genes expression in photosynthetic carbon fixation and lipid production. BMC Microbiol. 2016b;16:1–12.  https://doi.org/10.1186/s12866-016-0839-8.CrossRefGoogle Scholar
  80. Lim DKY, Schuhmann H, Thomas-Hall SR, et al. RNA-Seq and metabolic flux analysis of Tetraselmis sp. M8 during nitrogen starvation reveals a two-stage lipid accumulation mechanism. Bioresour Technol. 2017;244:1281–93.  https://doi.org/10.1016/j.biortech.2017.06.003.PubMedCrossRefGoogle Scholar
  81. Lohse M, Bolger AM, Nagel A, et al. RobiNA: a user-friendly, integrated software solution for RNA-Seq-based transcriptomics. Nucleic Acids Res. 2012;40:1–6.  https://doi.org/10.1093/nar/gks540.CrossRefGoogle Scholar
  82. Longworth J, Noirel J, Pandhal J, et al. HILIC- and SCX-based quantitative proteomics of Chlamydomonas reinhardtii during nitrogen starvation induced lipid and carbohydrate accumulation. J Proteome Res. 2012;11:5959–71.PubMedCrossRefGoogle Scholar
  83. Longworth J, Wu D, Huete-Ortega M, et al. Proteome response of Phaeodactylum tricornutum, during lipid accumulation induced by nitrogen depletion. Algal Res. 2016;18:213–24.  https://doi.org/10.1016/j.algal.2016.06.015.PubMedPubMedCentralCrossRefGoogle Scholar
  84. López García de Lomana A, Schäuble S, Valenzuela J, et al. Transcriptional program for nitrogen starvation-induced lipid accumulation in Chlamydomonas reinhardtii. Biotechnol Biofuels. 2015;8:207.  https://doi.org/10.1186/s13068-015-0391-z.PubMedPubMedCentralCrossRefGoogle Scholar
  85. Lü J, Sheahan C, Fu P. Metabolic engineering of algae for fourth generation biofuels production. Energy Environ Sci. 2011;4:2451.  https://doi.org/10.1039/c0ee00593b.CrossRefGoogle Scholar
  86. Lu S, Wang J, Niu Y, et al. Metabolic profiling reveals growth related FAME productivity and quality of Chlorella sorokiniana with different inoculum sizes. Biotechnol Bioeng. 2012;109:1651–62.  https://doi.org/10.1002/bit.24447.PubMedCrossRefGoogle Scholar
  87. Maheswari U, Mock T, Armbrust EV, Bowler C. Update of the diatom EST database: a new tool for digital transcriptomics. Nucleic Acids Res. 2009;37:1001–5.  https://doi.org/10.1093/nar/gkn905.CrossRefGoogle Scholar
  88. Maity JP, Bundschuh J, Chen CY, Bhattacharya P. Microalgae for third generation biofuel production, mitigation of greenhouse gas emissions and wastewater treatment: present and future perspectives – a mini review. Energy. 2014;78:104–13.  https://doi.org/10.1016/j.energy.2014.04.003.CrossRefGoogle Scholar
  89. Manuelle N, Courchesne D, Parisien A, et al. Enhancement of lipid production using biochemical, genetic and transcription factor engineering approaches. J Biotechnol. 2009;141:31–41.  https://doi.org/10.1016/j.jbiotec.2009.02.018.CrossRefGoogle Scholar
  90. Mastrobuoni G, Irgang S, Pietzke M, et al. Proteome dynamics and early salt stress response of the photosynthetic organism Chlamydomonas reinhardtii. BMC Genomics. 2012;13:1–13.  https://doi.org/10.1186/1471-2164-13-215.CrossRefGoogle Scholar
  91. Mclean TI. “Eco-omics”: a review of the application of genomics, transcriptomics, and proteomics for the study of the ecology of harmful algae. Microb Ecol. 2013;65:901–15.  https://doi.org/10.1007/s00248-013-0220-5.PubMedCrossRefGoogle Scholar
  92. Mehtani J, Arora N, Patel A, et al. Augmented lipid accumulation in ethyl methyl sulphonate mutants of oleaginous microalga for biodiesel production. Bioresour Technol. 2017;242:121.  https://doi.org/10.1016/j.biortech.2017.03.108.PubMedCrossRefGoogle Scholar
  93. Miller R, Wu G, Deshpande RR, et al. Changes in transcript abundance in Chlamydomonas reinhardtii following nitrogen deprivation predict diversion of metabolism. Plant Physiol. 2010;154:1737–52.  https://doi.org/10.1104/pp.110.165159.PubMedPubMedCentralCrossRefGoogle Scholar
  94. Mioso R, Marante FJT, González JEG, et al. Metabolite profiling of Schizochytrium sp. by GC-MS, an oleaginous microbial source of biodiesel. Braz J Microbiol. 2014;45:403–9.  https://doi.org/10.1590/S1517-83822014000200006.PubMedPubMedCentralCrossRefGoogle Scholar
  95. Morales-Sánchez D, Kyndt J, Ogden K, Martinez A. Toward an understanding of lipid and starch accumulation in microalgae: a proteomic study of Neochloris oleoabundans cultivated under N-limited heterotrophic conditions. Algal Res. 2016;20:22–34.  https://doi.org/10.1016/j.algal.2016.09.006.CrossRefGoogle Scholar
  96. Msanne J, Xu D, Konda AR, et al. Metabolic and gene expression changes triggered by nitrogen deprivation in the photoautotrophically grown microalgae Chlamydomonas reinhardtii and Coccomyxa sp. C-169. Phytochemistry. 2012;75:50–9.  https://doi.org/10.1016/j.phytochem.2011.12.007.PubMedCrossRefGoogle Scholar
  97. Murphy CF, Allen DT. Energy-water Nexus for mass cultivation of algae. Environ Sci Technol. 2011;45:5861–8.PubMedCrossRefGoogle Scholar
  98. Muthuraj M, Palabhanvi B, Misra S. Flux balance analysis of Chlorella sp. FC2 IITG under photoautotrophic and heterotrophic growth conditions. Photosynth Res. 2013a;118:167–79.  https://doi.org/10.1007/s11120-013-9943-x.PubMedCrossRefGoogle Scholar
  99. Muthuraj M, Palabhanvi B, Misra S, et al. Flux balance analysis of Chlorella sp. FC2 IITG under photoautotrophic and heterotrophic growth conditions. Photosynth Res. 2013b;118:167–79.  https://doi.org/10.1007/s11120-013-9943-x.PubMedCrossRefGoogle Scholar
  100. Muto M, Tanaka M, Liang Y, et al. Enhancement of glycerol metabolism in the oleaginous marine diatom Fistulifera solaris JPCC DA0580 to improve triacylglycerol productivity. Biotechnol Biofuels. 2015;8:1–7.  https://doi.org/10.1186/s13068-014-0184-9.PubMedPubMedCentralCrossRefGoogle Scholar
  101. Orth JD, Thiele I, Palsson BØ. Primer what is flux balance analysis? Nat Biotechnol. 2010;28:245–8.  https://doi.org/10.1038/nbt.1614.PubMedPubMedCentralCrossRefGoogle Scholar
  102. Perrineau MM, Gross J, Zelzion E, et al. Using natural selection to explore the adaptive potential of Chlamydomonas reinhardtii. PLoS One. 2014;9:e92533.  https://doi.org/10.1371/journal.pone.0092533.PubMedPubMedCentralCrossRefGoogle Scholar
  103. Poong SW, Lim PE, Phang SM, et al. Transcriptome sequencing of an Antarctic microalga, Chlorella sp. (Trebouxiophyceae, Chlorophyta) subjected to short-term ultraviolet radiation stress. J Appl Phycol. 2017;30:1–13.  https://doi.org/10.1007/s10811-017-1124-4.CrossRefGoogle Scholar
  104. Posewitz MC. Algal oil productivity gets a fat bonus. Nat Biotechnol. 2017;35:636–8.  https://doi.org/10.1038/nbt.3920.PubMedCrossRefGoogle Scholar
  105. Radakovits R, Jinkerson RE, Darzins A, Posewitz MC. Genetic engineering of algae for enhanced biofuel production. Eukaryot Cell. 2010;9:486–501.  https://doi.org/10.1128/EC.00364-09.PubMedPubMedCentralCrossRefGoogle Scholar
  106. Rai V, Muthuraj M, Gandhi MN, et al. Real-time iTRAQ-based proteome profiling revealed the central metabolism involved in nitrogen starvation induced lipid accumulation in microalgae. Sci Rep. 2017;7:1–16.  https://doi.org/10.1038/srep45732.CrossRefGoogle Scholar
  107. Rengel R, Smith RT, Haslam RP, et al. Overexpression of acetyl-CoA synthetase (ACS) enhances the biosynthesis of neutral lipids and starch in the green microalga Chlamydomonas reinhardtii. Algal Res. 2018;31:183–93.  https://doi.org/10.1016/j.algal.2018.02.009.CrossRefGoogle Scholar
  108. Rismani-Yazdi H, Haznedaroglu BZ, Hsin C, Peccia J. Transcriptomic analysis of the oleaginous microalga Neochloris oleoabundans reveals metabolic insights into triacylglyceride accumulation. Biotechnol Biofuels. 2012;5:74.PubMedPubMedCentralCrossRefGoogle Scholar
  109. Rodríguez-Moyá M, Gonzalez R. Systems biology approaches for the microbial production of biofuels. Biofuels. 2010;1:291–310. ISSN: 1759–7269.Google Scholar
  110. Sarayloo E, Tardu M, Unlu YS, et al. Understanding lipid metabolism in high-lipid-producing Chlorella vulgaris mutants at the genome-wide level. Algal Res. 2017;28:244–52.  https://doi.org/10.1016/j.algal.2017.11.009.CrossRefGoogle Scholar
  111. Schuhmann H, Lim DK, Schenk PM. Perspectives on metabolic engineering for increased lipid contents in microalgae. Biofuels. 2012;3:71–86.  https://doi.org/10.4155/bfs.11.147.CrossRefGoogle Scholar
  112. Serif M, Lepetit B, Weißert K, et al. A fast and reliable strategy to generate TALEN-mediated gene knockouts in the diatom Phaeodactylum tricornutum. Algal Res. 2017;23:186–95.  https://doi.org/10.1016/j.algal.2017.02.005.CrossRefGoogle Scholar
  113. Shang C, Bi G, Yuan Z, et al. Discovery of genes for production of biofuels through transcriptome sequencing of Dunaliella parva. Algal Res. 2016;13:318–26.  https://doi.org/10.1016/j.algal.2015.12.012.CrossRefGoogle Scholar
  114. Shang C, Zhu S, Wang Z, et al. Proteome response of Dunaliella parva induced by nitrogen limitation. Algal Res. 2017;23:196–202.  https://doi.org/10.1016/j.algal.2017.01.016.CrossRefGoogle Scholar
  115. Sharma YC, Singh V. Microalgal biodiesel: a possible solution for India’s energy security. Renew Sustain Energ Rev. 2017;67:72–88.  https://doi.org/10.1016/j.rser.2016.08.031.CrossRefGoogle Scholar
  116. Sharon-Gojman R, Leu S, Zarka A. Antenna size reduction and altered division cycles in self-cloned, marker-free genetically modified strains of Haematococcus pluvialis. Algal Res. 2017;28:172–83.  https://doi.org/10.1016/j.algal.2017.09.015.CrossRefGoogle Scholar
  117. Shin H, Hong S, Kim H, Yoo C, Lee H, Choi H, Lee C, Cho B. Elucidation of the growth delimitation of Dunaliella tertiolecta under nitrogen stress by integrating transcriptome and peptidome analysis. Bioresour Technol. 2015;194:57–66.  https://doi.org/10.1016/j.biortech.2015.07.002.PubMedCrossRefGoogle Scholar
  118. Shin SE, Koh HG, Kang NK, et al. Isolation, phenotypic characterization and genome wide analysis of a Chlamydomonas reinhardtii strain naturally modified under laboratory conditions: towards enhanced microalgal biomass and lipid production for biofuels. Biotechnol Biofuels. 2017;10:1–15.  https://doi.org/10.1186/s13068-017-1000-0.CrossRefGoogle Scholar
  119. Shinde Y, Dwivedi D, Khatri P, Sangwai JS. Biomass and solar: emerging energy resources for India. 2018.CrossRefGoogle Scholar
  120. Shrager J, Hauser C, Chang C, et al. Chlamydomonas reinhardtii. Society. 2003;131:401–8.  https://doi.org/10.1104/pp.016899.mants.CrossRefGoogle Scholar
  121. Song P, Li L, Liu J. Proteomic analysis in nitrogen-deprived Isochrysis galbana during lipid accumulation. PLoS One. 2013;8:1–13.  https://doi.org/10.1371/journal.pone.0082188.CrossRefGoogle Scholar
  122. Sui X, Niu X, Shi M, et al. Metabolomic analysis reveals mechanism of antioxidant butylated hydroxyanisole on lipid accumulation in Crypthecodinium cohnii. J Agric Food Chem. 2014;62:12477–84.PubMedCrossRefGoogle Scholar
  123. Sun D, Zhu J, Fang L, et al. De novo transcriptome profiling uncovers a drastic downregulation of photosynthesis upon nitrogen deprivation in the nonmodel green alga Botryosphaerella sudeticus. BMC Genomics. 2013;14:1–18.CrossRefGoogle Scholar
  124. Szyjka SJ, Mandal S, Schoepp NG, et al. Evaluation of phenotype stability and ecological risk of a genetically engineered alga in open pond production. Algal Res. 2017;24:378–86.  https://doi.org/10.1016/j.algal.2017.04.006.CrossRefGoogle Scholar
  125. Tan KWM, Lee YK. Expression of the heterologous Dunaliella tertiolecta fatty acyl-ACP thioesterase leads to increased lipid production in Chlamydomonas reinhardtii. J Biotechnol. 2017;247:60–7.  https://doi.org/10.1016/j.jbiotec.2017.03.004.PubMedCrossRefGoogle Scholar
  126. Tanaka T, Maeda Y, Veluchamy A, et al. Oil accumulation by the oleaginous diatom Fistulifera solaris as revealed by the genome and transcriptome. Plant Cell. 2015;27:162–76.  https://doi.org/10.1105/tpc.114.135194.CrossRefGoogle Scholar
  127. Tran NT, Padula MP, Evenhuis CR, et al. Proteomic and biophysical analyses reveal a metabolic shift in nitrogen deprived Nannochloropsis oculata. Algal Res. 2016;19:1–11.  https://doi.org/10.1016/j.algal.2016.07.009.CrossRefGoogle Scholar
  128. Tsai C-H, Warakanont J, Takeuchi T, et al. The protein Compromised Hydrolysis of Triacylglycerols 7 (CHT7) acts as a repressor of cellular quiescence in Chlamydomonas. Proc Natl Acad Sci. 2014;111:15833–8.  https://doi.org/10.1073/pnas.1414567111.CrossRefGoogle Scholar
  129. Valenzuela J, Mazurie A, Carlson RP, et al. Potential role of multiple carbon fixation pathways during lipid accumulation in Phaeodactylum tricornutum. Biotechnol Biofuels. 2012;5:40.  https://doi.org/10.1186/1754-6834-5-40.PubMedPubMedCentralCrossRefGoogle Scholar
  130. Velmurugan N, Sung M, Yim SS, et al. Systematically programmed adaptive evolution reveals potential role of carbon and nitrogen pathways during lipid accumulation in Chlamydomonas reinhardtii. Biotechnol Biofuels. 2014;7:117.  https://doi.org/10.1186/s13068-014-0117-7.PubMedPubMedCentralCrossRefGoogle Scholar
  131. Wang ST, Pan YY, Liu CC, et al. Characterization of a green microalga UTEX 2219-4: effects of photosynthesis and osmotic stress on oil body formation. Bot Stud. 2011;52:305–12.Google Scholar
  132. Wang DZ, Li C, Zhang Y, et al. Quantitative proteomic analysis of differentially expressed proteins in the toxicity-lost mutant of Alexandrium catenella (Dinophyceae) in the exponential phase. J Proteome. 2012;75:5564–77.  https://doi.org/10.1016/j.jprot.2012.08.001.CrossRefGoogle Scholar
  133. Wang L, Xue C, Wang L, et al. Strain improvement of Chlorella sp. for phenol biodegradation by adaptive laboratory evolution. Bioresour Technol. 2016;205:264–8.  https://doi.org/10.1016/j.biortech.2016.01.022.PubMedCrossRefGoogle Scholar
  134. Wang X, Wei W, Li NJ, et al. Heterogeneous expression of human PNPLA3 triggers algal lipid accumulation and lipid droplet enlargement. Algal Res. 2018;31:276–81.  https://doi.org/10.1016/j.algal.2018.02.019.CrossRefGoogle Scholar
  135. Wase N, Black PN, Stanley BA, Dirusso CC. Integrated quantitative analysis of nitrogen stress response in Chlamydomonas reinhardtii using metabolite and protein profiling. J Proteome Res. 2014a;13:1373–96.  https://doi.org/10.1021/pr400952z.PubMedCrossRefGoogle Scholar
  136. Wase N, Black PN, Stanley BA, Dirusso CC. Integrated quantitative analysis of nitrogen stress response in Chlamydomonas reinhardtii using metabolite and protein profiling. J Proteome Res. 2014b;13:1373–96.  https://doi.org/10.1021/pr400952z.PubMedCrossRefGoogle Scholar
  137. Wei L, Xin Y, Wang Q, et al. RNAi-based targeted gene knockdown in the model oleaginous microalgae Nannochloropsis oceanica. Plant J. 2017;89:1236–50.  https://doi.org/10.1111/tpj.13411.PubMedCrossRefGoogle Scholar
  138. Wobbe L, Remacle C. Improving the sunlight-to-biomass conversion efficiency in microalgal biofactories. J Biotechnol. 2014;201:28–42.  https://doi.org/10.1016/j.jbiotec.2014.08.021.PubMedCrossRefGoogle Scholar
  139. Wu C, Xiong W, Dai J, Wu Q. Genome-based metabolic mapping and 13C flux analysis reveal systematic properties of an oleaginous microalga Chlorella protothecoides. Plant Physiol. 2015;167:586–99.  https://doi.org/10.1104/pp.114.250688.PubMedPubMedCentralCrossRefGoogle Scholar
  140. Xie F, Liu T, Qian WJ, et al. Liquid chromatography-mass spectrometry-based quantitative proteomics. J Biol Chem. 2011;286:25443–9.  https://doi.org/10.1074/jbc.R110.199703.PubMedPubMedCentralCrossRefGoogle Scholar
  141. Xue J, Niu YF, Huang T, et al. Genetic improvement of the microalga Phaeodactylum tricornutum for boosting neutral lipid accumulation. Metab Eng. 2015;27:1–9.  https://doi.org/10.1016/j.ymben.2014.10.002.CrossRefGoogle Scholar
  142. Yang ZK, Niu YF, Ma YH, et al. Molecular and cellular mechanisms of neutral lipid accumulation in diatom following nitrogen deprivation. Biotechnol Biofuels. 2013;6:1–14.  https://doi.org/10.1186/1754-6834-6-67.PubMedPubMedCentralCrossRefGoogle Scholar
  143. Yang ZK, Ma YH, Zheng JW, et al. Proteomics to reveal metabolic network shifts towards lipid accumulation following nitrogen deprivation in the diatom Phaeodactylum tricornutum. J Appl Phycol. 2014;26:73–82.  https://doi.org/10.1007/s10811-013-0050-3.PubMedCrossRefGoogle Scholar
  144. Yang Y, Feng J, Li T, et al. CyanOmics: an integrated database of omics for the model cyanobacterium Synechococcus sp. PCC 7002. Database. 2015; 1–9. doi:  https://doi.org/10.1093/database/bau127.
  145. Yang J, Pan Y, Bowler C, et al. Knockdown of phosphoenolpyruvate carboxykinase increases carbon flux to lipid synthesis in Phaeodactylum tricornutum. Algal Res. 2016;15:50–8.  https://doi.org/10.1016/j.algal.2016.02.004.CrossRefGoogle Scholar
  146. Yang B, Liu J, Ma X, et al. Genetic engineering of the Calvin cycle toward enhanced photosynthetic CO2 fixation in microalgae. Biotechnol Biofuels. 2017;10:229.  https://doi.org/10.1186/s13068-017-0916-8.
  147. Yao L, Tan TW, Ng YK, et al. 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. 2015;8:1–16.  https://doi.org/10.1186/s13068-015-0382-0.CrossRefGoogle Scholar
  148. Yao L, Shen H, Wang N, et al. Elevated acetyl-CoA by amino acid recycling fuels microalgal neutral lipid accumulation in exponential growth phase for biofuel production. Plant Biotechnol J. 2017;15:497–509.  https://doi.org/10.1111/pbi.12648.PubMedCrossRefGoogle Scholar
  149. Yohn C, Brand A, Michael M, Behnke CA. Transformation of algae forincreasing lipid production. U.S. patent 9428779 B2, filed February 1, 2011, and issued August 30, 2016. (2016)Google Scholar
  150. Yu S, Zhao Q, Miao X, Shi J. Enhancement of lipid production in low-starch mutants Chlamydomonas reinhardtii by adaptive laboratory evolution. Bioresour Technol. 2013;147:499–507.  https://doi.org/10.1016/j.biortech.2013.08.069.CrossRefGoogle Scholar
  151. Zhang J, Hao Q, Bai L, et al. Overexpression of the soybean transcription factor GmDof4 significantly enhances the lipid content of Chlorella ellipsoidea. Biotechnol Biofuels. 2014;7:1–16.  https://doi.org/10.1186/s13068-014-0128-4.PubMedPubMedCentralCrossRefGoogle Scholar
  152. Zhang Y, Liu X, White MA, Colosi LM. Economic evaluation of algae biodiesel based on meta-analyses. Int J Sustain Energy. 2017;36:682–94.  https://doi.org/10.1080/14786451.2015.1086766.CrossRefGoogle Scholar
  153. Zhu Y, Huang Y. Use of flux balance analysis to promote lipid productivity in Chlorella sorokiniana. J Appl Phycol. 2017;29:889–902.  https://doi.org/10.1007/s10811-016-0973-6.CrossRefGoogle Scholar
  154. Zienkiewicz K, Du ZY, Ma W, et al. Stress-induced neutral lipid biosynthesis in microalgae??? Molecular, cellular and physiological insights. Biochim Biophys Acta Mol Cell Biol Lipids. 2016;1861:1269–81.  https://doi.org/10.1016/j.bbalip.2016.02.008.CrossRefGoogle Scholar
  155. Zuñiga C, Li C-T, Huelsman T, et al. Genome-scale metabolic model for the green alga Chlorella vulgaris UTEX 395 accurately predicts phenotypes under autotrophic, heterotrophic, and mixotrophic growth conditions. Plant Physiol. 2016;172:589–602.  https://doi.org/10.1104/pp.16.00593.PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Neha Arora
    • 1
  • Shweta Tripathi
    • 1
  • Krishna Mohan Poluri
    • 1
  • Vikas Pruthi
    • 1
  1. 1.Department of BiotechnologyIndian Institute of Technology RoorkeeRoorkeeIndia

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