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Chlamydomonas: Biotechnology and Biomedicine pp 193–217Cite as

Chlamydomonas: Triacylglycerol Accumulation

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Part of the book series: Microbiology Monographs ((MICROMONO,volume 31))

Abstract

The unicellular microalga Chlamydomonas reinhardtii exhibits immense metabolic flexibility, adjusting to changes in the environment and nutrient availability. One metabolic response under stress conditions is the synthesis of the neutral lipid triacylglycerol (TAG), accumulating as intracellular lipid droplets in the cytosol and chloroplast. With increased industrial interest in microalgal production of biofuels, feed, food, and chemicals, research on lipid metabolism using C. reinhardtii as a model system has accelerated in recent years. Conditions in which C. reinhardtii accumulates TAG have been identified, with nitrogen starvation as one of the most commonly used methods for induction. Genome, transcriptome, proteome, and lipidome analyses have provided information on the pathways involved in TAG synthesis and degradation. These studies have demonstrated that although a multitude of stress conditions induce TAG accumulation, there are differential response and regulatory mechanisms occurring under various induction conditions. Studies utilizing mutants have further led to the identification of pathways and regulatory components contributing to TAG synthesis and degradation. TAG metabolism is a multifaceted process in C. reinhardtii, and induction of TAG accumulation is accompanied by major reorganization of metabolic pathways, adjustments of photosynthetic complexes, membrane lipid recycling, and changes in carbon partitioning.

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References

  • Bajhaiya AK, Dean AP, Driver T, Trivedi DK, Rattray NJ, Allwood JW, Goodacre R, Pittman JK (2016) High-throughput metabolic screening of microalgae genetic variation in response to nutrient limitation. Metabolomics 12(1):9. doi:10.1007/s11306-015-0878-4

    Article  PubMed  CAS  Google Scholar 

  • Ball S, Marianne T, Dirick L, Fresnoy M, Delrue B, Decq A (1991) A Chlamydomonas-reinhardtii low-starch mutant is defective for 3-phosphoglycerate activation and orthophosphate inhibition of Adp-glucose pyrophosphorylase. Planta 185(1):17–26

    Article  CAS  PubMed  Google Scholar 

  • Benning C (2009) Mechanisms of lipid transport involved in organelle biogenesis in plant cells. Annu Rev Cell Dev Biol 25:71–91. doi:10.1146/annurev.cellbio.042308.113414

    Article  CAS  PubMed  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(11):4305–4323. doi:10.1105/tpc.113.117580

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blaby IK, Blaby-Haas CE, Tourasse N, Hom EF, Lopez D, Aksoy M, Grossman A, Umen J, Dutcher S, Porter M, King S, Witman GB, Stanke M, Harris EH, Goodstein D, Grimwood J, Schmutz J, Vallon O, Merchant SS, Prochnik S (2014) The Chlamydomonas genome project: a decade on. Trends Plant Sci 19(10):672–680. doi:10.1016/j.tplants.2014.05.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Block MA, Jouhet J (2015) Lipid trafficking at endoplasmic reticulum-chloroplast membrane contact sites. Curr Opin Cell Biol 35:21–29. doi:10.1016/j.ceb.2015.03.004

    Article  CAS  PubMed  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(19):15811–15825. doi:10.1074/jbc.M111.334052

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cagnon C, Mirabella B, Nguyen HM, Beyly-Adriano A, Bouvet S, Cuine S, Beisson F, Peltier G, Li-Beisson Y (2013) Development of a forward genetic screen to isolate oil mutants in the green microalga Chlamydomonas reinhardtii. Biotechnol Biofuels 6(1):178. doi:10.1186/1754-6834-6-178

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chochois V, Constans L, Dauvillee D, Beyly A, Soliveres M, Ball S, Peltier G, Cournac L (2010) Relationships between PSII-independent hydrogen bioproduction and starch metabolism as evidenced from isolation of starch catabolism mutants in the green alga Chlamydomonas reinhardtii. Int J Hydrog Energy 35(19):10731–10740. doi:10.1016/j.ijhydene.2010.03.052

    Article  CAS  Google Scholar 

  • Cirulis JT, Strasser BC, Scott JA, Ross GM (2012) Optimization of staining conditions for microalgae with three lipophilic dyes to reduce precipitation and fluorescence variability. Cytometry A 81(7):618–626. doi:10.1002/cyto.a.22066

    Article  PubMed  CAS  Google Scholar 

  • Davey MP, Horst I, Duong GH, Tomsett EV, Litvinenko AC, Howe CJ, Smith AG (2014) Triacylglyceride production and autophagous responses in Chlamydomonas reinhardtii depend on resource allocation and carbon source. Eukaryot Cell 13(3):392–400. doi:10.1128/EC.00178-13

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Deng XD, Gu B, Li YJ, Hu XW, Guo JC, Fei XW (2012) The roles of acyl-CoA: diacylglycerol acyltransferase 2 genes in the biosynthesis of triacylglycerols by the green algae Chlamydomonas reinhardtii. Mol Plant 5(4):945–947. doi:10.1093/mp/sss040

    Article  CAS  PubMed  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 14:38. doi:10.1186/1471-2091-14-38

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Doan TTY, Obbard JP (2011) Improved Nile Red staining of Nannochloropsis sp. J Appl Phycol 23(5):895–901. doi:10.1007/s10811-010-9608-5

    Article  CAS  Google Scholar 

  • Doan TTY, Obbard JP (2012) Enhanced intracellular lipid in Nannochloropsis sp via random mutagenesis and flow cytometric cell sorting. Algal Res Biomass Biofuels Bioprod 1(1):17–21. doi:10.1016/j.algal.2012.03.001

    CAS  Google Scholar 

  • Engel BD, Schaffer M, Kuhn Cuellar L, Villa E, Plitzko JM, Baumeister W (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ cryo-electron tomography. Elife 4. doi:10.7554/eLife.04889

  • Fan J, Andre C, Xu C (2011) A chloroplast pathway for the de novo biosynthesis of triacylglycerol in Chlamydomonas reinhardtii. FEBS Lett 585(12):1985–1991. doi:10.1016/j.febslet.2011.05.018

    Article  CAS  PubMed  Google Scholar 

  • Fan J, Yan C, Andre C, Shanklin J, Schwender J, Xu C (2012) Oil accumulation is controlled by carbon precursor supply for fatty acid synthesis in Chlamydomonas reinhardtii. Plant Cell Physiol 53(8):1380–1390. doi:10.1093/pcp/pcs082

    Article  CAS  PubMed  Google Scholar 

  • Flatt JP (1995) Use and storage of carbohydrate and fat. Am J Clin Nutr 61(4):952s–959s

    CAS  PubMed  Google Scholar 

  • Gao Q, Goodman JM (2015) The lipid droplet-a well-connected organelle. Front Cell Dev Biol 3(Aug):49. doi:10.3389/fcell.2015.00049

    PubMed  PubMed Central  Google Scholar 

  • Gardner RD, Lohman E, Gerlach R, Cooksey KE, Peyton BM (2013) Comparison of CO(2) and bicarbonate as inorganic carbon sources for triacylglycerol and starch accumulation in Chlamydomonas reinhardtii. Biotechnol Bioeng 110(1):87–96. doi:10.1002/bit.24592

    Article  CAS  PubMed  Google Scholar 

  • Gargouri M, Park JJ, Holguin FO, Kim MJ, Wang H, Deshpande RR, Shachar-Hill Y, Hicks LM, Gang DR (2015) Identification of regulatory network hubs that control lipid metabolism in Chlamydomonas reinhardtii. J Exp Bot 66(15):4551–4566. doi:10.1093/jxb/erv217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goncalves EC, Wilkie AC, Kirst M, Rathinasabapathi B (2016) Metabolic regulation of triacylglycerol accumulation in the green algae: identification of potential targets for engineering to improve oil yield. Plant Biotechnol J:1–12. doi:10.1111/pbi.12523

  • Goodenough U, Blaby I, Casero D, Gallaher SD, Goodson C, Johnson S, Lee JH, Merchant SS, Pellegrini M, Roth R, Rusch J, Singh M, Umen JG, Weiss TL, Wulan T (2014) The path to triacylglyceride obesity in the sta6 strain of Chlamydomonas reinhardtii. Eukaryot Cell 13(5):591–613. doi:10.1128/EC.00013-14

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Goodson C, Roth R, Wang ZT, Goodenough U (2011) Structural correlates of cytoplasmic and chloroplast lipid body synthesis in Chlamydomonas reinhardtii and stimulation of lipid body production with acetate boost. Eukaryot Cell 10(12):1592–1606. doi:10.1128/EC.05242-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goold H, Beisson F, Peltier G, Li-Beisson Y (2015) Microalgal lipid droplets: composition, diversity, biogenesis and functions. Plant Cell Rep 34(4):545–555. doi:10.1007/s00299-014-1711-7

    Article  CAS  PubMed  Google Scholar 

  • Greenspan P, Mayer EP, Fowler SD (1985) Nile red: a selective fluorescent stain for intracellular lipid droplets. J Cell Biol 100(3):965–973

    Article  CAS  PubMed  Google Scholar 

  • Grenier G, Guyon D, Roche O, Dubertret G, Tremolieres A (1991) Modification of the membrane fatty-acid composition of Chlamydomonas-reinhardtii cultured in the presence of liposomes. Plant Physiol Biochem 29(5):429–440

    CAS  Google Scholar 

  • Hemschemeier A, Casero D, Liu B, Benning C, Pellegrini M, Happe T, Merchant SS (2013) Copper response regulator1-dependent and -independent responses of the Chlamydomonas reinhardtii transcriptome to dark anoxia. Plant Cell 25(9):3186–3211. doi:10.1105/tpc.113.115741

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hernandez-Torres A, Zapata-Morales AL, Ochoa Alfaro AE, Soria-Guerra RE (2016) Identification of gene transcripts involved in lipid biosynthesis in Chlamydomonas reinhardtii under nitrogen, iron and sulfur deprivation. World J Microbiol Biotechnol 32(4):55. doi:10.1007/s11274-016-2008-5

    Article  PubMed  CAS  Google Scholar 

  • Hu Q, Sommerfeld M, Jarvis E, Ghirardi M, Posewitz M, Seibert M, Darzins A (2008) Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J 54(4):621–639. doi:10.1111/j.1365-313X.2008.03492.x

    Article  CAS  PubMed  Google Scholar 

  • Huang AHC (1992) Oil bodies and oleosins in seeds. Annu Rev Plant Physiol Plant Mol Biol 43:177–200

    Article  CAS  Google Scholar 

  • Huang NL, Huang MD, Chen TL, Huang AH (2013) Oleosin of subcellular lipid droplets evolved in green algae. Plant Physiol 161(4):1862–1874. doi:10.1104/pp.112.212514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hung CH, Ho MY, Kanehara K, Nakamura Y (2013) Functional study of diacylglycerol acyltransferase type 2 family in Chlamydomonas reinhardtii. FEBS Lett 587(15):2364–2370. doi:10.1016/j.febslet.2013.06.002

    Article  CAS  PubMed  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(6):808–819. doi:10.1111/pbi.12210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jacquier N, Choudhary V, Mari M, Toulmay A, Reggiori F, Schneiter R (2011) Lipid droplets are functionally connected to the endoplasmic reticulum in Saccharomyces cerevisiae. J Cell Sci 124(Pt 14):2424–2437. doi:10.1242/jcs.076836

    Article  CAS  PubMed  Google Scholar 

  • James GO, Hocart CH, Hillier W, Chen H, Kordbacheh F, Price GD, Djordjevic MA (2011) Fatty acid profiling of Chlamydomonas reinhardtii under nitrogen deprivation. Bioresour Technol 102(3):3343–3351. doi:10.1016/j.biortech.2010.11.051

    Article  CAS  PubMed  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. Eukaryot Cell 12(6):776–793. doi:10.1128/EC.00318-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Juergens MT, Deshpande RR, Lucker BF, Park JJ, Wang H, Gargouri M, Holguin FO, Disbrow B, Schaub T, Skepper JN, Kramer DM, Gang DR, Hicks LM, Shachar-Hill Y (2015) The regulation of photosynthetic structure and function during nitrogen deprivation in Chlamydomonas reinhardtii. Plant Physiol 167(2):558–573. doi:10.1104/pp.114.250530

    Article  CAS  PubMed  Google Scholar 

  • Kajikawa M, Sawaragi Y, Shinkawa H, Yamano T, Ando A, Kato M, Hirono M, Sato N, Fukuzawa H (2015) Algal dual-specificity tyrosine phosphorylation-regulated kinase, triacylglycerol accumulation regulator1, regulates accumulation of triacylglycerol in nitrogen or sulfur deficiency. Plant Physiol 168(2):752–764. doi:10.1104/pp.15.00319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim S, Kim H, Ko D, Yamaoka Y, Otsuru M, Kawai-Yamada M, Ishikawa T, Oh HM, Nishida I, Li-Beisson Y, Lee Y (2013) Rapid induction of lipid droplets in Chlamydomonas reinhardtii and Chlorella vulgaris by Brefeldin A. PLoS One 8(12):e81978. doi:10.1371/journal.pone.0081978

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim H, Jang S, Kim S, Yamaoka Y, Hong D, Song WY, Nishida I, Li-Beisson Y, Lee Y (2015) The small molecule fenpropimorph rapidly converts chloroplast membrane lipids to triacylglycerols in Chlamydomonas reinhardtii. Front Microbiol 6(February):54. doi:10.3389/fmicb.2015.00054

    PubMed  PubMed Central  Google Scholar 

  • Klok AJ, Lamers PP, Martens DE, Draaisma RB, Wijffels RH (2014) Edible oils from microalgae: insights in TAG accumulation. Trends Biotechnol 32(10):521–528. doi:10.1016/j.tibtech.2014.07.004

    Article  CAS  PubMed  Google Scholar 

  • Krishnan A, Kumaraswamy GK, Vinyard DJ, Gu H, Ananyev G, Posewitz MC, Dismukes GC (2015) Metabolic and photosynthetic consequences of blocking starch biosynthesis in the green alga Chlamydomonas reinhardtii sta6 mutant. Plant J 81(6):947–960. doi:10.1111/tpj.12783

    Article  CAS  PubMed  Google Scholar 

  • La Russa M, Bogen C, Uhmeyer A, Doebbe A, Filippone E, Kruse O, Mussgnug JH (2012) Functional analysis of three type-2 DGAT homologue genes for triacylglycerol production in the green microalga Chlamydomonas reinhardtii. J Biotechnol 162(1):13–20. doi:10.1016/j.jbiotec.2012.04.006

    Article  PubMed  CAS  Google Scholar 

  • Legeret B, Schulz-Raffelt M, Nguyen HM, Auroy P, Beisson F, Peltier G, Blanc G, Li-Beisson Y (2016) Lipidomic and transcriptomic analyses of Chlamydomonas reinhardtii under heat stress unveil a direct route for the conversion of membrane lipids into storage lipids. Plant Cell Environ 39(4):834–847. doi:10.1111/pce.12656

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Han D, Hu G, Dauvillee D, Sommerfeld M, Ball S, Hu Q (2010a) Chlamydomonas starchless mutant defective in ADP-glucose pyrophosphorylase hyper-accumulates triacylglycerol. Metab Eng 12(4):387–391. doi:10.1016/j.ymben.2010.02.002

    Article  PubMed  CAS  Google Scholar 

  • Li Y, Han D, Hu G, Sommerfeld M, Hu Q (2010b) Inhibition of starch synthesis results in overproduction of lipids in Chlamydomonas reinhardtii. Biotechnol Bioeng 107(2):258–268. doi:10.1002/bit.22807

    Article  CAS  PubMed  Google Scholar 

  • Li X, Benning C, Kuo MH (2012a) Rapid triacylglycerol turnover in Chlamydomonas reinhardtii requires a lipase with broad substrate specificity. Eukaryot Cell 11(12):1451–1462. doi:10.1128/EC.00268-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li X, Moellering ER, Liu B, Johnny C, Fedewa M, Sears BB, Kuo MH, Benning C (2012b) A galactoglycerolipid lipase is required for triacylglycerol accumulation and survival following nitrogen deprivation in Chlamydomonas reinhardtii. Plant Cell 24(11):4670–4686. doi:10.1105/tpc.112.105106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li X, Umen JG, Jonikas MC (2014) Waking sleeping algal cells. Proc Natl Acad Sci U S A 111(44):15610–15611. doi:10.1073/pnas.1418295111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li N, Xu C, Li-Beisson Y, Philippar K (2016a) Fatty acid and lipid transport in plant cells. Trends Plant Sci 21(2):145–158. doi:10.1016/j.tplants.2015.10.011

    Article  CAS  PubMed  Google Scholar 

  • Li X, Zhang R, Patena W, Gang SS, Blum SR, Ivanova N, Yue R, Robertson JM, Lefebvre PA, Fitz-Gibbon ST, Grossman AR, Jonikas MC (2016b) An indexed, mapped mutant library enables reverse genetics studies of biological processes in Chlamydomonas reinhardtii. Plant Cell 28(2):367–387. doi:10.1105/tpc.15.00465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li-Beisson Y, Beisson F, Riekhof W (2015) Metabolism of acyl-lipids in Chlamydomonas reinhardtii. Plant J 82(3):504–522. doi:10.1111/tpj.12787

    Article  CAS  PubMed  Google Scholar 

  • Liu B, Benning C (2013) Lipid metabolism in microalgae distinguishes itself. Curr Opin Biotechnol 24(2):300–309. doi:10.1016/j.copbio.2012.08.008

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Clarens AF, Colosi LM (2012) Algae biodiesel has potential despite inconclusive results to date. Bioresour Technol 104:803–806. doi:10.1016/j.biortech.2011.10.077

    Article  CAS  PubMed  Google Scholar 

  • Liu B, Vieler A, Li C, Jones AD, Benning C (2013a) Triacylglycerol profiling of microalgae Chlamydomonas reinhardtii and Nannochloropsis oceanica. Bioresour Technol 146:310–316. doi:10.1016/j.biortech.2013.07.088

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Zhang C, Shen X, Zhang X, Cichello S, Guan H, Liu P (2013b) Microorganism lipid droplets and biofuel development. BMB Rep 46(12):575–581

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J, Han D, Yoon K, Hu Q, Li Y (2016) Characterization of type 2 diacylglycerol acyltransferases in Chlamydomonas reinhardtii reveals their distinct substrate specificities and functions in triacylglycerol biosynthesis. Plant J. doi:10.1111/tpj.13143

  • Lopez Garcia de Lomana A, Schauble S, Valenzuela J, Imam S, Carter W, Bilgin DD, Yohn CB, Turkarslan S, Reiss DJ, Orellana MV, Price ND, Baliga NS (2015) Transcriptional program for nitrogen starvation-induced lipid accumulation in Chlamydomonas reinhardtii. Biotechnol Biofuels 8:207. doi:10.1186/s13068-015-0391-z

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Manandhar-Shrestha K, Hildebrand M (2013) Development of flow cytometric procedures for the efficient isolation of improved lipid accumulation mutants in a sp. microalga. J Appl Phycol 25:1643–1651. doi:10.1007/s10811-013-0021-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Merchant SS, Kropat J, Liu B, Shaw J, Warakanont J (2012) TAG, you’re it! Chlamydomonas as a reference organism for understanding algal triacylglycerol accumulation. Curr Opin Biotechnol 23(3):352–363. doi:10.1016/j.copbio.2011.12.001

    Article  CAS  PubMed  Google Scholar 

  • Miller R, Wu G, Deshpande RR, Vieler A, Gartner K, Li X, Moellering ER, Zauner S, Cornish AJ, Liu B, Bullard B, Sears BB, Kuo MH, Hegg EL, Shachar-Hill Y, Shiu SH, Benning C (2010) Changes in transcript abundance in Chlamydomonas reinhardtii following nitrogen deprivation predict diversion of metabolism. Plant Physiol 154(4):1737–1752. doi:10.1104/pp.110.165159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moellering ER, Benning C (2010) RNA interference silencing of a major lipid droplet protein affects lipid droplet size in Chlamydomonas reinhardtii. Eukaryot Cell 9(1):97–106. doi:10.1128/EC.00203-09

    Article  CAS  PubMed  Google Scholar 

  • Montero MF, Aristizabal M, Reina GG (2011) Isolation of high-lipid content strains of the marine microalga Tetraselmis suecica for biodiesel production by flow cytometry and single-cell sorting. J Appl Phycol 23(6):1053–1057. doi:10.1007/s10811-010-9623-6

    Article  CAS  Google Scholar 

  • Nguyen HM, Baudet M, Cuine S, Adriano JM, Barthe D, Billon E, Bruley C, Beisson F, Peltier G, Ferro M, Li-Beisson Y (2011) Proteomic profiling of oil bodies isolated from the unicellular green microalga Chlamydomonas reinhardtii: with focus on proteins involved in lipid metabolism. Proteomics 11(21):4266–4273. doi:10.1002/pmic.201100114

    Article  CAS  PubMed  Google Scholar 

  • Park JJ, Wang H, Gargouri M, Deshpande RR, Skepper JN, Holguin FO, Juergens MT, Shachar-Hill Y, Hicks LM, Gang DR (2015) The response of Chlamydomonas reinhardtii to nitrogen deprivation: a systems biology analysis. Plant J 81(4):611–624. doi:10.1111/tpj.12747

    Article  CAS  PubMed  Google Scholar 

  • Peltier G, Schmidt GW (1991) Chlororespiration: an adaptation to nitrogen deficiency in Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A 88(11):4791–4795

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Philipps G, Happe T, Hemschemeier A (2012) Nitrogen deprivation results in photosynthetic hydrogen production in Chlamydomonas reinhardtii. Planta 235(4):729–745. doi:10.1007/s00425-011-1537-2

    Article  CAS  PubMed  Google Scholar 

  • Plumley FG, Schmidt GW (1989) Nitrogen-dependent regulation of photosynthetic gene expression. Proc Natl Acad Sci U S A 86(8):2678–2682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pol A, Gross SP, Parton RG (2014) Review: Biogenesis of the multifunctional lipid droplet: lipids, proteins, and sites. J Cell Biol 204(5):635–646. doi:10.1083/jcb.201311051

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riekhof WR, Sears BB, Benning C (2005) Annotation of genes involved in glycerolipid biosynthesis in Chlamydomonas reinhardtii: discovery of the betaine lipid synthase BTA1Cr. Eukaryot Cell 4(2):242–252. doi:10.1128/EC.4.2.242-252.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roston RL, Gao J, Murcha MW, Whelan J, Benning C (2012) TGD1, -2, and -3 proteins involved in lipid trafficking form ATP-binding cassette (ABC) transporter with multiple substrate-binding proteins. J Biol Chem 287(25):21406–21415. doi:10.1074/jbc.M112.370213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sato A, Matsumura R, Hoshino N, Tsuzuki M, Sato N (2014) Responsibility of regulatory gene expression and repressed protein synthesis for triacylglycerol accumulation on sulfur-starvation in Chlamydomonas reinhardtii. Front Plant Sci 5(Sept):444. doi:10.3389/fpls.2014.00444

    PubMed  PubMed Central  Google Scholar 

  • Schmollinger S, Muhlhaus T, Boyle NR, Blaby IK, Casero D, Mettler T, Moseley JL, Kropat J, Sommer F, Strenkert D, Hemme D, Pellegrini M, Grossman AR, Stitt M, Schroda M, Merchant SS (2014) Nitrogen-sparing mechanisms in chlamydomonas affect the transcriptome, the proteome, and photosynthetic metabolism. Plant Cell 26(4):1410–1435. doi:10.1105/tpc.113.122523

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schulz-Raffelt M, Chochois V, Auroy P, Cuine S, Billon E, Dauvillee D, Li-Beisson Y, Peltier G (2016) Hyper-accumulation of starch and oil in a Chlamydomonas mutant affected in a plant-specific DYRK kinase. Biotechnol Biofuels 9:55. doi:10.1186/s13068-016-0469-2

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Scott SA, Davey MP, Dennis JS, Horst I, Howe CJ, Lea-Smith DJ, Smith AG (2010) Biodiesel from algae: challenges and prospects. Curr Opin Biotechnol 21(3):277–286. doi:10.1016/j.copbio.2010.03.005

    Article  CAS  PubMed  Google Scholar 

  • Shtaida N, Khozin-Goldberg I, Solovchenko A, Chekanov K, Didi-Cohen S, Leu S, Cohen Z, Boussiba S (2014) Downregulation of a putative plastid PDC E1alpha subunit impairs photosynthetic activity and triacylglycerol accumulation in nitrogen-starved photoautotrophic Chlamydomonas reinhardtii. J Exp Bot 65(22):6563–6576. doi:10.1093/jxb/eru374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Siaut M, Cuine S, Cagnon C, Fessler B, Nguyen M, Carrier P, Beyly A, Beisson F, Triantaphylides C, Li-Beisson Y, Peltier G (2011) Oil accumulation in the model green alga Chlamydomonas reinhardtii: characterization, variability between common laboratory strains and relationship with starch reserves. BMC Biotechnol 11(1):7. doi:10.1186/1472-6750-11-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Slade R, Bauen A (2013) Micro-algae cultivation for biofuels: cost, energy balance, environmental impacts and future prospects. Biomass Bioenergy 53:29–38. doi:10.1016/j.biombioe.2012.12.019

    Article  Google Scholar 

  • Tardif M, Atteia A, Specht M, Cogne G, Rolland N, Brugiere S, Hippler M, Ferro M, Bruley C, Peltier G, Vallon O, Cournac L (2012) PredAlgo: a new subcellular localization prediction tool dedicated to green algae. Mol Biol Evol 29(12):3625–3639. doi:10.1093/molbev/mss178

    Article  CAS  PubMed  Google Scholar 

  • Terashima M, Specht M, Naumann B, Hippler M (2010) Characterizing the anaerobic response of Chlamydomonas reinhardtii by quantitative proteomics. Mol Cell Proteomics 9(7):1514–1532. doi:10.1074/mcp.M900421-MCP200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Terashima M, Specht M, Hippler M (2011) The chloroplast proteome: a survey from the Chlamydomonas reinhardtii perspective with a focus on distinctive features. Curr Genet 57(3):151–168. doi:10.1007/s00294-011-0339-1

    Article  CAS  PubMed  Google Scholar 

  • Terashima M, Freeman ES, Jinkerson RE, Jonikas MC (2015) A fluorescence-activated cell sorting-based strategy for rapid isolation of high-lipid Chlamydomonas mutants. Plant J 81(1):147–159. doi:10.1111/tpj.12682

    Article  CAS  PubMed  Google Scholar 

  • Tsai CH, Warakanont J, Takeuchi T, Sears BB, Moellering ER, Benning C (2014) The protein compromised hydrolysis of triacylglycerols 7 (CHT7) acts as a repressor of cellular quiescence in Chlamydomonas. Proc Natl Acad Sci U S A 111(44):15833–15838. doi:10.1073/pnas.1414567111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsai CH, Zienkiewicz K, Amstutz CL, Brink BG, Warakanont J, Roston R, Benning C (2015) Dynamics of protein and polar lipid recruitment during lipid droplet assembly in Chlamydomonas reinhardtii. Plant J 83(4):650–660. doi:10.1111/tpj.12917

    Article  CAS  PubMed  Google Scholar 

  • Valledor L, Furuhashi T, Recuenco-Munoz L, Wienkoop S, Weckwerth W (2014) System-level network analysis of nitrogen starvation and recovery in Chlamydomonas reinhardtii reveals potential new targets for increased lipid accumulation. Biotechnol Biofuels 7:171. doi:10.1186/s13068-014-0171-1

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Velmurugan N, Sung M, Yim SS, Park MS, Yang JW, Jeong KJ (2013) Evaluation of intracellular lipid bodies in Chlamydomonas reinhardtii strains by flow cytometry. Bioresour Technol 138:30–37. doi:10.1016/j.biortech.2013.03.078

    Article  CAS  PubMed  Google Scholar 

  • Wältermann M, Steinbüchel A (2006) Wax ester and triacylglycerol inclusions. In: Shively JM (ed) Inclusions in prokaryotes. Springer, Heidelberg, pp 137–166. doi:10.1007/7171_006/

    Chapter  Google Scholar 

  • Waltermann M, Stoveken T, Steinbuchel A (2007) Key enzymes for biosynthesis of neutral lipid storage compounds in prokaryotes: properties, function and occurrence of wax ester synthases/acyl-CoA: diacylglycerol acyltransferases. Biochimie 89(2):230–242. doi:10.1016/j.biochi.2006.07.013

    Article  PubMed  CAS  Google Scholar 

  • Wang ZT, Ullrich N, Joo S, Waffenschmidt S, Goodenough U (2009) Algal lipid bodies: stress induction, purification, and biochemical characterization in wild-type and starchless Chlamydomonas reinhardtii. Eukaryot Cell 8(12):1856–1868. doi:10.1128/EC.00272-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Warakanont J, Tsai CH, Michel EJ, Murphy GR 3rd, Hsueh PY, Roston RL, Sears BB, Benning C (2015) Chloroplast lipid transfer processes in Chlamydomonas reinhardtii involving a TRIGALACTOSYLDIACYLGLYCEROL 2 (TGD2) orthologue. Plant J 84(5):1005–1020. doi:10.1111/tpj.13060

    Article  CAS  PubMed  Google Scholar 

  • Welte MA (2007) Proteins under new management: lipid droplets deliver. Trends Cell Biol 17(8):363–369. doi:10.1016/j.tcb.2007.06.004

    Article  CAS  PubMed  Google Scholar 

  • Wijffels RH, Kruse O, Hellingwerf KJ (2013) Potential of industrial biotechnology with cyanobacteria and eukaryotic microalgae. Curr Opin Biotechnol 24(3):405–413. doi:10.1016/j.copbio.2013.04.004

    Article  CAS  PubMed  Google Scholar 

  • Wilfling F, Wang H, Haas JT, Krahmer N, Gould TJ, Uchida A, Cheng JX, Graham M, Christiano R, Frohlich F, Liu X, Buhman KK, Coleman RA, Bewersdorf J, Farese RV Jr, Walther TC (2013) Triacylglycerol synthesis enzymes mediate lipid droplet growth by relocalizing from the ER to lipid droplets. Dev Cell 24(4):384–399. doi:10.1016/j.devcel.2013.01.013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilfling F, Haas JT, Walther TC, Farese RV Jr (2014) Lipid droplet biogenesis. Curr Opin Cell Biol 29:39–45. doi:10.1016/j.ceb.2014.03.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Work VH, Radakovits R, Jinkerson RE, Meuser JE, Elliott LG, Vinyard DJ, Laurens LM, Dismukes GC, Posewitz MC (2010) Increased lipid accumulation in the Chlamydomonas reinhardtii sta7-10 starchless isoamylase mutant and increased carbohydrate synthesis in complemented strains. Eukaryot Cell 9(8):1251–1261. doi:10.1128/EC.00075-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wykoff DD, Davies JP, Melis A, Grossman AR (1998) The regulation of photosynthetic electron transport during nutrient deprivation in Chlamydomonas reinhardtii. Plant Physiol 117(1):129–139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie B, Stessman D, Hart JH, Dong H, Wang Y, Wright DA, Nikolau BJ, Spalding MH, Halverson LJ (2014) High-throughput fluorescence-activated cell sorting for lipid hyperaccumulating Chlamydomonas reinhardtii mutants. Plant Biotechnol J 12(7):872–882. doi:10.1111/pbi.12190

    Article  CAS  PubMed  Google Scholar 

  • Yan C, Fan J, Xu C (2013) Chapter 5- Analysis of oil droplets in microalgae, Methods in cell biology, vol 116, 1st edn. Elsevier, Oxford, UK. doi:10.1016/B978-0-12-408051-5.00005-X

    Google Scholar 

  • Yang W, Moroney JV, Moore TS (2004) Membrane lipid biosynthesis in Chlamydomonas reinhardtii: ethanolaminephosphotransferase is capable of synthesizing both phosphatidylcholine and phosphatidylethanolamine. Arch Biochem Biophys 430(2):198–209. doi:10.1016/j.abb.2004.07.016

    Article  CAS  PubMed  Google Scholar 

  • Yang W, Wittkopp TM, Li X, Warakanont J, Dubini A, Catalanotti C, Kim RG, Nowack EC, Mackinder LC, Aksoy M, Page MD, D'Adamo S, Saroussi S, Heinnickel M, Johnson X, Richaud P, Alric J, Boehm M, Jonikas MC, Benning C, Merchant SS, Posewitz MC, Grossman AR (2015) Critical role of Chlamydomonas reinhardtii ferredoxin-5 in maintaining membrane structure and dark metabolism. Proc Natl Acad Sci U S A 112(48):14978–14983. doi:10.1073/pnas.1515240112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoon K, Han D, Li Y, Sommerfeld M, Hu Q (2012) Phospholipid:diacylglycerol acyltransferase is a multifunctional enzyme involved in membrane lipid turnover and degradation while synthesizing triacylglycerol in the unicellular green microalga Chlamydomonas reinhardtii. Plant Cell 24(9):3708–3724. doi:10.1105/tpc.112.100701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zabawinski C, Van Den Koornhuyse N, D'Hulst C, Schlichting R, Giersch C, Delrue B, Lacroix JM, Preiss J, Ball S (2001) Starchless mutants of Chlamydomonas reinhardtii lack the small subunit of a heterotetrameric ADP-glucose pyrophosphorylase. J Bacteriol 183(3):1069–1077. doi:10.1128/JB.183.3.1069-1077.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang R, Patena W, Armbruster U, Gang SS, Blum SR, Jonikas MC (2014) High-throughput genotyping of green algal mutants reveals random distribution of mutagenic insertion sites and endonucleolytic cleavage of transforming DNA. Plant Cell 26(4):1398–1409. doi:10.1105/tpc.114.124099

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

I am grateful to Dr. Xiaobo Li for critical feedback and suggestions on the manuscript.

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  1. Institute of Low Temperature Science, Hokkaido University, Kita 19 Nishi 8, Kita-ku, Sapporo, 060-0819, Japan

    Mia Terashima

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  1. Institute of Plant Biology and Biotechnology, University of Münster, Münster, Germany

    Michael Hippler

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Terashima, M. (2017). Chlamydomonas: Triacylglycerol Accumulation. In: Hippler, M. (eds) Chlamydomonas: Biotechnology and Biomedicine. Microbiology Monographs, vol 31. Springer, Cham. https://doi.org/10.1007/978-3-319-66360-9_8

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