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Past, Present and Future of Microalgae Cultivation Developments Read chapter Read first chapter

2015 | OriginalPaper | Chapter

11. Genetic Engineering for Microalgae Strain Improvement in Relation to Biocrude Production Systems

Authors : Evan Stephens, Juliane Wolf, Melanie Oey, Eugene Zhang, Ben Hankamer, Ian L. Ross

Published in: Biomass and Biofuels from Microalgae

Publisher: Springer International Publishing

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Abstract

An advanced understanding of the genetics of microalgae and the availability of molecular biology tools are both critical to the development of advanced strains, which offer efficiency advantages for primary production, and more specifically in the context of production for biocrude and renewable energy. Consequently, we outline the current state of the art in microalgal molecular biology including the available genome sequences, molecular techniques and toolkits, amenable strains for transformation of nuclear and plastid genomes, and the control of transgenes at both transcriptional and translational levels. We also examine some strategies for improvement of expression and regulation. We suggest the primary strategies in strain improvement that are most relevant to biocrude applications; briefly illustrate the process of photosynthesis to enable identification of targets for improvement of net photosynthetic conversion efficiency in mass cultivation; and further discuss how improvement of metabolic systems may also be achieved and benefit production models. Finally, we acknowledge the aspects of prudent risk assessment and consequent regulation that are developing and how our knowledge of natural algae in existing ecosystems, and GM work in conventional agriculture both contribute lessons to these discussions. We conclude that if properly managed, these developments provide significant potential for increasing global capacity for renewable fuel production from microalgae and that these developments could also have benefits for other applications.

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previous chapter Toward Applications of Genomics and Metabolic Modeling to Improve Algal Biomass Productivity
next chapter Harvesting of Microalgae by Means of Flocculation
Literature
Administration USFaD (2010b) GRAS Notice Inventory Micro-algal oil Ulkenia sp. SAM2179
Aldrich J, Cherney B, Merlin E, Williams C, Mets L (1985) Recombination within the inverted repeat sequences of the chlamydomonas reinhardtii chloroplast genome produces 2 orientation isomers. Curr Genet 9(3):233–238
Allen MD, del Campo JA, Kropat J, Merchant SS (2007) FEA1, FEA2, and FRE1, encoding two homologous secreted proteins and a candidate ferrireductase, are expressed coordinately with FOX1 and FTR1 in iron-deficient Chlamydomonas reinhardtii. Eukaryot Cell 6(10):1841–1852
Amundsen SK, Taylor AF, Reddy M, Smith GR (2007) Intersubunit signaling in RecBCD enzyme, a complex protein machine regulated by Chi Hot Spots. Genes Dev 21(24):3296–3307
Anderson DM (2009) Approaches to monitoring, control and management of harmful algal blooms (HABs). Ocean Coast Manag 52:342–347
Anderson DM, Glibert PM, Burkholder JM (2002) Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences. Estuaries 25:704–726
Anthonisen IL, Kasai S, Kato K, Salvador ML, Klein U (2002) Structural and functional characterization of a transcription-enhancing sequence element in the rbcL gene of the chlamydomonas chloroplast genome. Curr Genet 41(5):349–356
Apt KE, KrothPancic PG, Grossman AR (1996) Stable nuclear transformation of the diatom phaeodactylum tricornutum. Mol Gen Genet 252(5):572–579
Armbrust EV et al (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306(5693):79–86
Bai L-L et al (2013) A new strategy to produce a defensin: stable production of mutated NP-1 in nitrate reductase-deficient Chlorella ellipsoidea. PLoS One 8(1):e54966
Bailey S (2013) Global regulators of photosynthetic acclimation to irradiance. In: Paper presented at the 7th Algae Biomass Summit, Orlando, Florida, 1 Oct 2013
Baird TD, DeLorenzo ME (2010) Descriptive and mechanistic toxicity of conazole fungicides using the model test alga Dunaliella tertiolecta (chlorophyceae). Environ Toxicol 25(3):213–220
Barnes D, Franklin S, Schultz J, Henry R, Brown E, Coragliotti A, Mayfield SP (2005) Contribution of 5′- and 3′-untranslated regions of plastid mRNAs to the expression of Chlamydomonas reinhardtii chloroplast genes. Mol Genet Genomics 274(6):625–636
Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116(2):281–297
Bateman JM, Purton S (2000) Tools for chloroplast transformation in chlamydomonas: expression vectors and a new dominant selectable marker. Mol Gen Genet 263(3):404–410
Beckmann J, Lehr F, Finazzi G, Hankamer B, Posten C, Wobbe L, Kruse O (2009) Improvement of light to biomass conversion by de-regulation of light-harvesting protein translation in Chlamydomonas reinhardtii. J Biotech 142(1):70–77
Beisson F et al (2003) Arabidopsis genes involved in acyl lipid metabolism. A 2003 census of the candidates, a study of the distribution of expressed sequence tags in organs, and a web-based database. Plant Physiol 132(2):681–697
Ben-Amotz A, Avron M (1973) Role of glycerol in osmotic regulation of halophilic alga Dunaliella parva. Plant Physiol 51(5):875–878
Ben-Amotz A, Tornabene TG, Thomas WH (1985) Chemical profile of selected species of microalgae with emphasis on lipids. J Phycol 21(1):72–81
Berberoglu H, Pilon L, Melis A (2008) Radiation characteristics of Chlamydomonas reinhardtii CC125 and its truncated chlorophyll antenna transformants tla1, tlaX and tla1-CW + . Int J Hydrogen Energy 33(22):6467–6483
Berges JA, Charlebois DO, Mauzerall DC, Falkowski PG (1996) Differential effects of nitrogen limitation on photosynthetic efficiency of photosystems I and II in microalgae. Plant Physiol 110(2):689–696
Berthold P, Schmitt R, Mages W (2002) An engineered Streptomyces hygroscopicus aph 7” gene mediates dominant resistance against hygromycin B in Chlamydomonas reinhardtii. Protist 153(4):401–412
Bhattacharya D et al (2013) Genome of the red alga Porphyridium purpureum. Nat Commun 4:1941
Blanc G et al (2010) The Chlorella variabilis NC64A genome reveals adaptation to photosymbiosis, coevolution with viruses, and cryptic sex. Plant Cell 22(9):2943–2955
Blanc G et al (2012) The genome of the polar eukaryotic microalga Coccomyxa subellipsoidea reveals traits of cold adaptation. Genome Biol 13(5):R39
Blankenship RE, Chen M (2013) Spectral expansion and antenna reduction can enhance photosynthesis for energy production. Curr Opin Chem Biol 17(3):457–461
Bock R (2001) Transgenic plastids in basic research and plant biotechnology. J Mol Biol 312(3):425–438MathSciNet
Bogen C et al (2013) Reconstruction of the lipid metabolism for the microalga Monoraphidium neglectum from its genome sequence reveals characteristics suitable for biofuel production. BMC Genom 14:18
Borowitzka LJ, Brown AD (1974) Salt relations of marine and halophilic species of unicellular green-alga, Dunaliella—role of glycerol as a compatible solute. Arch Microbiol 96(1):37–52
Bowler C et al (2008) The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456(7219):239–244
Boyle NR et al (2012) Three acyltransferases and nitrogen-responsive regulator are implicated in nitrogen starvation-induced triacylglycerol accumulation in chlamydomonas. J Biol Chem 287(19):15811–15825
Boynton JE et al (1988) Chloroplast transformation in Chlamydomonas with high velocity microprojectiles. Science 240(4858):1534–1538
Brown MR, Jeffrey SW, Volkman JK, Dunstan GA (1997) Nutritional properties of microalgae for mariculture. Aquaculture 151(1–4):315–331
Casas-Mollano JA, Rohr J, Kim EJ, Balassa E, van Dijk K, Cerutti H (2008) Diversification of the core RNA interference machinery in Chlamydomonas reinhardtii and the role of DCL1 in transposon silencing. Genetics 179(1):69–81
Cerutti H, Casas-Mollano JA (2006) On the origin and functions of RNA-mediated silencing: from protists to man. Curr Genet 50(2):81–99
Cerutti H, Osman M, Grandoni P, Jagendorf AT (1992) A homolog of Escherichia coli RecA protein in plastids of higher-plants. Proc Natl Acad Sci USA 89(17):8068–8072
Cerutti H, Johnson AM, Boynton JE, Gillham NW (1995) Inhibition of chloroplast DNA recombination and repair by dominant-negative mutants of Escherichia coli RecA. Mol Cell Biol 15(6):3003–3011
Cerutti H, Johnson AM, Gillham NW, Boynton JE (1997a) Epigenetic silencing of a foreign gene in nuclear transformants of Chlamydomonas. Plant Cell 9(6):925–945
Cerutti H, Johnson AM, Gillham NW, Boynton JE (1997b) A eubacterial gene conferring spectinomycin resistance on Chlamydomonas reinhardtii: integration into the nuclear genome and gene expression. Genetics 145(1):97–110
Cerutti H, Ma X, Msanne J, Repas T (2011) RNA-mediated silencing in algae: biological roles and tools for analysis of gene function. Eukaryot Cell 10(9):1164–1172
Cha T-S, Chen C-F, Yee W, Aziz A, Loh S-H (2011) Cinnamic acid, coumarin and vanillin: alternative phenolic compounds for efficient agrobacterium-mediated transformation of the unicellular green alga. Nannochloropsis sp. J Microbiol Methods 84(3):430–434
Chen M, Blankenship RE (2011) Expanding the solar spectrum used by photosynthesis. Trends Plant Sci 16(8):427–431
Chen JE, Smith AG (2012) A look at diacylglycerol acyltransferases (DGATs) in algae. J Biotechnol 162(1):28–39
Chen HL, Li SS, Huang R, Tsai H-J (2008) Conditional production of a functional fish growth hormone in the transgenic line of Nannochloropsis oculata (Eustigmatophyceae). J Phycol 44(3):768–776
Chen M, Schliep M, Willows RD, Cai ZL, Neilan BA, Scheer H (2010) A Red-Shifted Chlorophyll. Science 329(5997):1318–1319
Chen M, Tang H, Ma H, Holland TC, Ng KYS, Salley SO (2011) Effect of nutrients on growth and lipid accumulation in the green algae Dunaliella tertiolecta. Bioresour Technol 102(2):1649–1655
Cheney DP, Metz B, Stiller J (2001) Agrobacterium-mediated genetic transformation in the macroscopic red alga Porphyra yezoensis. J Phycol 37:11
Cho SW, Kim S, Kim JM, Kim J-S (2013) Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nat Biotech 31(3):230–232
Cock JM et al (2010) The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature 465(7298):617–621
Collen J et al (2013) Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida. Proc Natl Acad Sci USA 110(13):5247–5252
Craigie JS, McLachlan J (1964) Glycerol as a photo-synthetic product in Dunaliella tertiolecta Butcher. Canadian J Bot 42(6):777–778
Croft MT, Moulin M, Webb ME, Smith AG (2007) Thiamine biosynthesis in algae is regulated by riboswitches. Proc Natl Acad Sci USA 104(52):20770–20775
Cui Y, Qin S, Jiang P (2014) Chloroplast transformation of platymonas (Tetraselmis) subcordiformis with the bar gene as selectable marker. PLoS One 9(6):e98607
Curtis BA et al (2012) Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs. Nature 492(7427):59–65
Dal’Molin CGD, Quek LE, Palfreyman RW, Nielsen LK (2011) AlgaGEM—a genome-scale metabolic reconstruction of algae based on the Chlamydomonas reinhardtii genome. BMC Genom 12:10
Davies JP, Yildiz FH, Grossman A (1996) Sac1, a putative regulator that is critical for survival of Chlamydomonas reinhardtii during sulfur deprivation. EMBO J 15(9):2150–2159
Dawson HN, Burlingame R, Cannons AC (1997) Stable transformation of Chlorella: Rescue of nitrate reductase-deficient mutants with the nitrate reductase gene. Curr Microbiol 35(6):356–362
Day A, Goldschmidt-Clermont M (2011) The chloroplast transformation toolbox: selectable markers and marker removal. Plant Biotechnol J 9(5):540–553
de Cambiaire JC, Otis C, Turmel M, Lemieux C (2007) The chloroplast genome sequence of the green alga Leptosira terrestris: multiple losses of the inverted repeat and extensive genome rearrangements within the Trebouxiophyceae. BMC Genom 8:213
De Riso V, Raniello R, Maumus F, Rogato A, Bowler C, Falciatore A (2009) Gene silencing in the marine diatom Phaeodactylum tricornutum. Nucleic Acids Res 37(14):e96
Debuchy R, Purton S, Rochaix JD (1989) The argininosuccinate lyase gene of Chlamydomonas reinhartii—an important tool for nuclear transformation and for correlating the genetic and molecular maps of the Arg7 locus. EMBO J 8(10):2803–2809
Dent RM, Haglund CM, Chin BL, Kobayashi MC, Niyogi KK (2005) Functional genomics of eukaryotic photosynthesis using insertional mutagenesis of Chlamydomonas reinhardtii. Plant Physiol 137(2):545–556
Derelle E et al (2006) Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc Natl Acad Sci USA 103(31):11647–11652
Diener DR, Curry AM, Johnson KA, Williams BD, Lefebvre PA, Kindle KL, Rosenbaum JL (1990) Rescue of a paralyzed-flagella mutant of Chlamydomonas by transformation. Proc Natl Acad Sci USA 87(15):5739–5743
Dittami SM, Michel G, Collen J, Boyen C, Tonon T (2010) Chlorophyll-binding proteins revisited—a multigenic family of light-harvesting and stress proteins from a brown algal perspective. BMC Evolut Biol 10:365
Doetsch NA, Favreau MR, Kuscuoglu N, Thompson MD, Hallick RB (2001) Chloroplast transformation in Euglena gracilis: splicing of a group III twintron transcribed from a transgenic psbK operon. Curr Genet 39(1):49–60
Douglas S et al (2001) The highly reduced genome of an enslaved algal nucleus. Nature 410(6832):1091–1096
Downes CM, Archambault S, Erickson C (2013) Formulation and estimation of a production function model of biofuels from microalgae. In: Paper presented at the 7th algae biomass summit, Orlando, Florida, 1 Oct 2013
Dreesen IA, Charpin-El Hamri G, Fussenegger M (2010) Heat-stable oral alga-based vaccine protects mice from staphylococcus aureus infection. J Biotechnol 145(3):273–280
Drop B, Webber-Birungi M, Fusetti F, Kouril R, Redding KE, Boekema EJ, Croce R (2011) Photosystem I of Chlamydomonas reinhardtii contains nine light-harvesting complexes (Lhca) located on one side of the core. J Biol Chem 286(52):44878–44887
Ducat DC, Avelar-Rivas JA, Way JC, Silver PA (2012) Rerouting carbon flux to enhance photosynthetic productivity. Appl Environ Microbiol 78(8):2660–2668
Dunahay TG (1993) Transformation of Chlamydomonas reinhardtii with silicon carbide whiskers. Biotechniques 15(3):452–455, 457–458, 460
Dunahay TG, Jarvis EE, Roessler PG (1995) Genetic transformation of the diatoms Cyclotella cryptica and Navicula saprophila. J Phycol 31(6):1004–1012
Dunahay TG, Jarvis EE, Dais SS, Roessler PG (1996) Manipulation of microalgal lipid production using genetic engineering. Appl Biochem Biotechnol 57–8:223–231
Eberhard S, Drapier D, Wollman FA (2002) Searching limiting steps in the expression of chloroplast-encoded proteins: relations between gene copy number, transcription, transcript abundance and translation rate in the chloroplast of Chlamydomonas reinhardtii. Plant J 31(2):149–160
Erickson JM, Rahire M, Bennoun P, Delepelaire P, Diner B, Rochaix JD (1984) Herbicide resistance in Chlamydomonas reinhardtii results from a mutation in the chloroplast gene for the 32-kilodalton protein of photosystem II. Proc Natl Acad Sci USA 81(12):3617–3621
Evans JR (2013) Improving photosynthesis. Plant Physiol 162(4):1780–1793
Falciatore A, Casotti R, Leblanc C, Abrescia C, Bowler C (1999) Transformation of nonselectable reporter genes in marine diatoms. Mar Biotechnol (NY) 1(3):239–251
Fang W et al (2012) Transcriptome-wide changes in Chlamydomonas reinhardtii gene expression regulated by carbon dioxide and the CO2-concentrating mechanism regulator CIA5/CCM1. Plant Cell 24(5):1876–1893
Fei X, Eriksson M, Yang J, Deng X (2009) An Fe deficiency responsive element with a core sequence of TGGCA regulates the expression of FEA1 in Chlamydomonas reinhardtii. J Biochem 146(2):157–166
Feng S, Xue L, Liu H, Lu P (2009) Improvement of efficiency of genetic transformation for Dunaliella salina by glass beads method. Mol Biol Rep 36(6):1433–1439
Feng Z et al (2013) Efficient genome editing in plants using a CRISPR/Cas system. Cell Res 23(10):1229–1232
Fernandez E, Schnell R, Ranum LPW, Hussey SC, Silflow CD, Lefebvre PA (1989) Isolation and characterization of the nitrate reductase structural gene of Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 86(17):6449–6453
Ferris PJ (1995) Localization of the NIC-7, AC-29 and THI-10 genes within the mating-type locus of Chlamydomonas reinhardtii. Genetics 141(2):543–549MathSciNet
Fischer H, Robl I, Sumper M, Kroger N (1999) Targeting and covalent modification of cell wall and membrane proteins heterologously expressed in the diatom Cylindrotheca fusiformis (Bacillariophyceae). J Phycol 35(1):113–120
Forrest ARR et al (2014) A promoter-level mammalian expression atlas. Nature 507(7493):462–470
Franklin SE, Mayfield SP (2005) Recent developments in the production of human therapeutic proteins in eukaryotic algae. Expert Opin Biol Ther 5(2):225–235
Franklin S, Ngo B, Efuet E, Mayfield SP (2002a) Development of a GFP reporter gene for Chlamydomonas reinhardtii chloroplast. Plant J 30(6):733–744
Franklin S, Ngo B, Efuet E, Mayfield SP (2002b) Development of a GFP reporter gene for Chlamydomonas reinhardtii chloroplast. Plant Journal 30(6):733–744
Fuhrmann M, Oertel W, Hegemann P (1999) A synthetic gene coding for the green fluorescent protein (GFP) is a versatile reporter in Chlamydomonas reinhardtii. Plant J 19(3):353–361
Fuhrmann M, Stahlberg A, Govorunova E, Rank S, Hegemann P (2001) The abundant retinal protein of the Chlamydomonas eye is not the photoreceptor for phototaxis and photophobic responses. J Cell Sci 114(Pt 21):3857–3863
Fuhrmann M, Hausherr A, Ferbitz L, Schodl T, Heitzer M, Hegemann P (2004) Monitoring dynamic expression of nuclear genes in Chlamydomonas reinhardtii by using a synthetic luciferase reporter gene. Plant Mol Biol 55(6):869–881
Fujiwara T, Ohnuma M, Yoshida M, Kuroiwa T, Hirano T (2013) Gene targeting in the red alga cyanidioschyzon merolae: single- and multi-copy insertion using authentic and chimeric selection markers. PLoS One 8(9):e73608
Fukuzawa H, Miura K, Ishizaki K, Kucho KI, Saito T, Kohinata T, Ohyama K (2001) Ccm1, a regulatory gene controlling the induction of a carbon-concentrating mechanism in Chlamydomonas reinhardtii by sensing CO2 availability. Proc Natl Acad Sci USA 98(9):5347–5352
Gao H, Wright DA, Li T, Wang Y, Horken K, Weeks DP, Yang B (2014) TALE activation of endogenous genes in Chlamydomonas reinhardtii. Algal Res 1(5):52–60
Geng DG, Han Y, Wang YQ, Wang P, Zhang LM, Li WB, Sun YR (2004) Construction of a system for the stable expression of foreign genes in Dunaliella salina. Acta Botanica Sinica 46(3):342–346
Gimpel JA, Mayfield SP (2013) Analysis of heterologous regulatory and coding regions in algal chloroplasts. Appl Microbiol Biotechnol 97(10):4499–4510
Gobler CJ et al (2011) Niche of harmful alga Aureococcus anophagefferens revealed through ecogenomics. Proc Natl Acad Sci USA 108(11):4352–4357
Goldschmidt-Clermont M (1991) Transgenic expression of aminoglycoside adenine transferase in the chloroplast: a selectable marker of site-directed transformation of Chlamydomonas. Nucleic Acids Res 19(15):4083–4089
Goulding SE, Olmstead RG, Morden CW, Wolfe KH (1996) Ebb and flow of the chloroplast inverted repeat. Mol Gen Genet 252(1–2):195–206
Gray BN, Ahner BA, Hanson MR (2009) High-level bacterial cellulase accumulation in chloroplast-transformed tobacco mediated by downstream box fusions. Biotechnol Bioeng 102(4):1045–1054
Gray BN, Yang H, Ahner BA, Hanson MR (2011) An efficient downstream box fusion allows high-level accumulation of active bacterial beta-glucosidase in tobacco chloroplasts. Plant Mol Biol 76(3–5):345–355
Gregory JA, Topol AB, Doerner DZ, Mayfield S (2013) Alga-produced cholera toxin-Pfs25 fusion proteins as oral vaccines. Appl Environ Microbiol 79(13):3917–3925
Gressel J, van der Vlugt CJB, Bergmans HEN (2013) Environmental risks of large scale cultivation of microalgae: mitigation of spills. Algal Res-Biomass Biofuels Bioproducts 2(3):286–298
Grossman AR (2000) Chlamydomonas reinhardtii and photosynthesis: genetics to genomics. Curr Opin Plant Biol 3(2):132–137MathSciNet
Grossman AR (2007) In the grip of algal genomics. Adv Exp Med Biol 616:54–76
Guckert JB, Cooksey KE (1990) Triglyceride accumulation and fatty-acid profile changes in Chlorella (Chlorophyta) during high pH-induced cell-cycle inhibition. J Phycol 26(1):72–79
Gumpel NJ, Rochaix JD, Purton S (1994) Studies on homologous recombination in the green-alga Chlamydomonas reinhardtii. Curr Genet 26(5–6):438–442
Guschina IA, Harwood JL (2006) Lipids and lipid metabolism in eukaryotic algae. Prog Lipid Res 45(2):160–186
Guschina IA, Harwood JL (2013) Algal lipids and their metabolism. In: Borowitzka MA, Moheimani NR (eds) Algae for biofuels and energy. Developments in applied phycology, vol 5. Springer, London
Gutierrez CL, Gimpel J, Escobar C, Marshall SH, Henriquez V (2012) Chloroplast genetic tool for the green microalgae Haematococcus pluvialis (Chlorophyceae, Volvocales). J Phycol 48(4):976–983
Hager M, Bock R (2000) Enslaved bacteria as new hope for plant biotechnologists. Appl Microbiol Biotechnol 54(3):302–310
Hallmann A, Rappel A (1999) Genetic engineering of the multicellular green alga Volvox: a modified and multiplied bacterial antibiotic resistance gene as a dominant selectable marker. Plant J 17(1):99–109
Hallmann A, Sumper M (1994) Reporter genes and highly regulated promoters as tools for transformation experiments in Volvox carteri. Proc Natl Acad Sci USA 91(24):11562–11566
Hallmann A, Sumper M (1996) The Chlorella Hexose H+ symporter is a useful selectable marker and biochemical reagent when expressed in Volvox. Proc Natl Acad Sci USA 93(2):669–673
Harris EH, Burkhart BD, Gillham NW, Boynton JE (1989) Antibiotic resistance mutations in the chloroplast 16S and 23S rRNA genes of Chlamydomonas reinhardtii: correlation of genetic and physical maps of the chloroplast genome. Genetics 123(2):281–292
Harris EH, Stern DB, Witman GB (2009) The Chlamydomonas sourcebook, 2nd edn. Academic Press, Oxford
Hasnain SE, Manavathu EK, Leung WC (1985) DNA-mediated transformation of Chlamydomonas reinhardii cells: use of aminoglycoside 3′-phosphotransferase as a selectable marker. Mol Cell Biol 5(12):3647–3650
Hauser CR, Gillham NW, Boynton JE (1996) Translational regulation of chloroplast genes—proteins binding to the 5′-untranslated regions of chloroplast mRNAs in Chlamydomonas reinhardtii. J Biol Chem 271(3):1486–1497
Hawkins RL, Nakamura M (1999) Expression of human growth hormone by the eukaryotic alga, Chlorella. Curr Microbiol 38(6):335–341
Heitzer M, Zschoernig B (2007) Construction of modular tandem expression vectors for the green alga Chlamydomonas reinhardtii using the Cre/lox-System. Biotechniques 43(3):324, 326, 328 passim
Heitzer M, Eckert A, Fuhrmann M, Griesbeck C (2007) Influence of codon bias on the expression of foreign genes in microalgae. Transgenic Microalgae Green Cell Factories 616:46–53
Heng RL, Lee E, Pilon L (2014) Radiation characteristics and optical properties of filamentous cyanobacterium Anabaena cylindrica. J Opt Soc Am Opt Image Sci Vis 31(4):836–845
Henley WJ, Litaker RW, Noyoyeska L, Duke CS, Quemada HD, Sayre RT (2013) Initial risk assessment of genetically modified (GM) microalgae for commodity-scale biofuel cultivation. Algal Res-Biomass Biofuels Bioprod 2(1):66–77
Herrin DL, Nickelsen J (2004) Chloroplast RNA processing and stability. Photosynth Res 82(3):301–314
Hill J, Nelson E, Tilman D, Polasky S, Tiffany D (2006) Environmental, economic, and energetic costs and benefits of biodiesel and ethanol biofuels. Proc Natl Acad Sci USA 103(30):11206–11210
Hiramatsu T, Nakamura S, Misumi O, Kuroiwa T, Nakamura S (2006) Morphological changes in mitochondrial and chloroplast nucleoids and mitochondria during the Chlamydomonas reinhardtii (Chlorophyceae) cell cycle. J Phycol 42(5):1048–1058
Holloway SP, Herrin DL (1998) Processing of a composite large subunit rRNA: studies with Chlamydomonas mutants deficient in maturation of the 23S-like rRNA. Plant Cell 10(7):1193–1206
Hsu PD, Lander ES, Zhang F (2014) Development and applications of CRISPR-Cas9 for genome engineering. Cell 157(6):1262–1278
Huesemann MH, Hausmann TS, Bartha R, Aksoy M, Weissman JC, Benemann JR (2009) Biomass productivities in wild type and pigment mutant of Cyclotella sp. (Diatom). Appl Biochem Biotechnol 157(3):507–526
Inouye T, Odahara M, Fujita T, Hasebe M, Sekine Y (2008) Expression and complementation analyses of a chloroplast-localized homolog of bacterial RecA in the moss physcomitrella patens. Biosci Biotechnol Biochem 72(5):1340–1347
Iwai M, Takizawa K, Tokutsu R, Okamuro A, Takahashi Y, Minagawa J (2010) Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis. Nature 464(7292):1210–1213
Jakobiak T, Mages W, Scharf B, Babinger P, Stark K, Schmitt R (2004) The bacterial paromomycin resistance gene, aphH, as a dominant selectable marker in Volvox carteri. Protist 155(4):381–393
Jarvis EE, Brown LM (1991) Transient expression of firefly luciferase in protoplasts of the green-alga Chlorella ellipsoidea. Curr Genet 19(4):317–321
Jia Y, Li S, Allen G, Feng S, Xue L (2012) A novel glyceraldehyde-3-phosphate dehydrogenase (GAPDH) promoter for expressing transgenes in the halotolerant alga Dunaliella salina. Curr Microbiol 64(5):506–513
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
Jones PR (2014) Genetic instability in cyanobacteria—an elephant in the room? Front Bioeng Biotechnoly 2
Kandilian R, Lee E, Pilon L (2013) Radiation and optical properties of Nannochloropsis oculata grown under different irradiances and spectra. Bioresour Technol 137:63–73
Kargul J, Turkina MV, Nield J, Benson S, Vener AV, Barber J (2005) Light-harvesting complex II protein CP29 binds to photosystem I of Chlamydomonas reinhardtii under State 2 conditions. FEBS J 272(18):4797–4806
Kasai S, Yoshimura S, Ishikura K, Takaoka Y, Kobayashi K, Kato K, Shinmyo A (2003) Effect of coding regions on chloroplast gene expression in Chlamydomonas reinhardtii. J Biosci Bioeng 95(3):276–282
Kathiresan S, Chandrashekar A, Ravishankar GA, Sarada R (2009) Agrobacterium-mediated transformation in the green alga Haematococcus pluvialis (Chlorophyceae, Volvocales). J Phycol 45(3):642–649
Katz YS, Danon A (2002) The 3′-untranslated region of chloroplast psbA mRNA stabilizes binding of regulatory proteins to the leader of the message. J Biol Chem 277(21):18665–18669
Khozin-Goldberg I, Cohen Z (2011) Unraveling algal lipid metabolism: recent advances in gene identification. Biochimie 93(1):91–100
Kilian O, Benemann CS, Niyogi KK, Vick B (2011) High-efficiency homologous recombination in the oil-producing alga Nannochloropsis sp. Proc Natl Acad Sci USA 108(52):21265–21269
Kim DH, Kim YT, Cho JJ, Bae JH, Hur SB, Hwang I, Choi TJ (2002) Stable integration and functional expression of flounder growth hormone gene in transformed microalga, Chlorella ellipsoidea. Marine Biotechnol 4(1):63–73MATH
Kindle KL (1990) High-frequency nuclear transformation of Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 87(3):1228–1232
Kindle KL, Schnell RA, Fernandez E, Lefebvre PA (1989) Stable nuclear transformation of Chlamydomonas using the Chlamydomonas gene for nitrate reductase. J Cell Biol 109(6):2589–2601
Kroth PG et al (2008) A model for carbohydrate metabolism in the diatom Phaeodactylum tricornutum deduced from comparative whole genome analysis. PLoS ONE 3(1):14
Kumar SV, Misquitta RW, Reddy VS, Rao BJ, Rajam MV (2004) Genetic transformation of the green alga—Chlamydomonas reinhardtii by Agrobacterium tumefaciens. Plant Sci 166(3):731–738
Kuroda H, Maliga P (2001a) Complementarity of the 16S rRNA penultimate stem with sequences downstream of the AUG destabilizes the plastid mRNAs. Nucleic Acids Res 29(4):970–975
Kuroda H, Maliga P (2001b) Sequences downstream of the translation initiation codon are important determinants of translation efficiency in chloroplasts. Plant Physiol 125(1):430–436
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
Lambertz C, Hemschemeier A, Happe T (2010) Anaerobic expression of the ferredoxin-encoding FDX5 gene of Chlamydomonas reinhardtii is regulated by the Crr1 transcription factor. Eukaryot Cell 9(11):1747–1754
Lapidot M, Raveh D, Sivan A, Arad S, Shapira M (2002) Stable chloroplast transformation of the unicellular red alga Porphyridium species. Plant Physiol 129(1):7–12
Lauersen KJ, Berger H, Mussgnug JH, Kruse O (2013) Efficient recombinant protein production and secretion from nuclear transgenes in Chlamydomonas reinhardtii. J Biotechnol 167(2):101–110
Lee H, Bingham SE, Webber AN (1996) Function of 3′ non-coding sequences and stop codon usage in expression of the chloroplast psaB gene in Chlamydomonas reinhardtii. Plant Mol Biol 31(2):337–354
Lee E, Heng RL, Pilon L (2013) Spectral optical properties of selected photosynthetic microalgae producing biofuels. J Quant Spectrosc Radiat Transfer 114:122–135
Lerche K, Hallmann A (2009) Stable nuclear transformation of Gonium pectorale. BMC Biotechnology 9:64
Lerche K, Hallmann A (2013) Stable nuclear transformation of Eudorina elegans. BMC Biotechnol 13:11
Li S-S, Tsai H-J (2009) Transgenic microalgae as a non-antibiotic bactericide producer to defend against bacterial pathogen infection in the fish digestive tract. Fish Shellfish Immunol 26(2):316–325MathSciNet
Li J, Xue L, Yan H, Wang L, Liu L, Lu Y, Xie H (2007) The nitrate reductase gene-switch: a system for regulated expression in transformed cells of Dunaliella salina. Gene 403(1–2):132–142
Li YT, Han DX, Hu GR, Sommerfeld M, Hu QA (2010) Inhibition of starch synthesis results in overproduction of lipids in Chlamydomonas reinhardtii. Biotechnol Bioeng 107(2):258–268
Li F, Gao D, Hu H (2014) High-efficiency nuclear transformation of the oleaginous marine Nannochloropsis species using PCR product. Biosci Biotechnol Biochem 78(5):812–817
Lin Z, Kong H, Nei M, Ma H (2006) Origins and evolution of the recA/RAD51 gene family: evidence for ancient gene duplication and endosymbiotic gene transfer. Proc Natl Acad Sci USA 103(27):10328–10333
Lin MT, Occhialini A, Andralojc PJ, Parry MAJ, Hanson MR (2014) A faster rubisco with potential to increase photosynthesis in crops. Nature 513(7519):547–550
Liu BS, Benning C (2013) Lipid metabolism in microalgae distinguishes itself. Curr Opin Biotechnol 24(2):300–309
Liu CH, Chang CY, Liao Q, Zhu X, Chang JS (2013) Photoheterotrophic growth of Chlorella vulgaris ESP6 on organic acids from dark hydrogen fermentation effluents. Bioresour Technol 145:331–336
Lommer M et al (2012) Genome and low-iron response of an oceanic diatom adapted to chronic iron limitation. Genome Biol 13(7):R66
Lu YM, Li J, Xue LX, Yan HX, Yuan HJ, Wang C (2011) A duplicated carbonic anhydrase 1 (DCA1) promoter mediates the nitrate reductase gene switch of Dunaliella salina. J Appl Phycol 23(4):673–680
Malasarn D et al (2013) Zinc deficiency impacts CO2 assimilation and disrupts copper homeostasis in Chlamydomonas reinhardtii. J Biol Chem 288(15):10672–10683
Mali P et al (2013) RNA-guided human genome engineering via Cas9. Science 339(6121):823–826
Manning WM, Strain HH (1943) Chlorophyll d, a green pigment of red algae. J Biol Chem 151(1):1–19
Manuell AL et al (2007) Robust expression of a bioactive mammalian protein in Chlamydomonas Chloroplast. Plant Biotechnol J 5(3):402–412
Marin-Navarro J, Manuell AL, Wu J, S PM (2007) Chloroplast translation regulation. Photosynth Res 94(2–3):359-374
Maruyama M, Horakova I, Honda H, Xing XH, Shiragami N, Unno H (1994) Introduction of foreign DNA into Chlorella saccharophila by electroporation. Biotechnol Tech 8(11):821–826
Matsuoka M, Takahama K, Ogawa T (2001) Gene replacement in cyanobacteria mediated by a dominant streptomycin-sensitive rps12 gene that allows selection of mutants free from drug resistance markers. Microbiology-Sgm 147:2077–2087
Matsuzaki M et al (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428(6983):653–657
Maul JE, Jason WL, Cui L, dePamphilis CW, Miller W, Harris EH, Stern DB (2002) The Chlamydomonas reinhardtii plastid chromosome: islands of genes in a sea of repeats. Plant Cell 14(11):2659–2679
Mayfield SP, Franklin SE (2005) Expression of human antibodies in eukaryotic micro-algae. Vaccine 23(15):1828–1832
Mayfield SP, Kindle KL (1990) Stable nuclear transformation of Chlamydomonas reinhardtii by using a C. reinhardtii gene as the selectable marker. Proc Natl Acad Sci USA 87(6):2087–2091
Mayfield SP, Schultz J (2004) Development of a luciferase reporter gene, luxCt, for Chlamydomonas reinhardtii chloroplast. Plant J 37(3):449–458
Mayfield SP, Franklin SE, Lerner RA (2003) Expression and assembly of a fully active antibody in algae. Proc Natl Acad Sci USA 100(2):438–442
Melis A (2009) Solar energy conversion efficiencies in photosynthesis: minimizing the chlorophyll antennae to maximize efficiency. Plant Sci 177(4):272–280
Melis A (2013) Carbon partitioning in photosynthesis. Curr Opin Chem Biol 17(3):453–456
Merchant SS et al (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318(5848):245–250
Merchant SS, Kropat J, Liu BS, 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
Minko I, Holloway SP, Nikaido S, Carter M, Odom OW, Johnson CH, Herrin DL (1999) Renilla luciferase as a vital reporter for chloroplast gene expression in Chlamydomonas. Mol Gen Genet 262(3):421–425
Minoda A, Sakagami R, Yagisawa F, Kuroiwa T, Tanaka K (2004) Improvement of culture conditions and evidence for nuclear transformation by homologous recombination in a red alga, Cyanidioschyzon merolae 10D. Plant Cell Physiol 45(6):667–671
Mitchell DR, Kang Y (1991) Identification of ODA6 as a chlamydomonas dynein mutant by rescue with the wild-type gene. J Cell Biol 113(4):835–842
Mitra M, Melis A (2008) Optical properties of microalgae for enhanced biofuels production. Opt Express 16(26):21807–21820
Miyagawa A, Okami T, Kira N, Yamaguchi H, Ohnishi K, Adachi M (2009) Research note: high efficiency transformation of the diatom Phaeodactylum tricornutum with a promoter from the diatom Cylindrotheca fusiformis. Phycol Res 57(2):142–146
Miyagawa-Yamaguchi A, Okami T, Kira N, Yamaguchi H, Ohnishi K, Adachi M (2011) Stable nuclear transformation of the diatom Chaetoceros sp. Phycol Res 59(2):113–119
Miyashita H, Ikemoto H, Kurano N, Adachi K, Chihara M, Miyachi S (1996) Chlorophyll d as a major pigment. Nature 383(6599):402
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
Molnar A, Schwach F, Studholme DJ, Thuenemann EC, Baulcombe DC (2007) miRNAs control gene expression in the single-cell alga Chlamydomonas reinhardtii. Nature 447(7148):1126–1129
Molnar A et al (2009) Highly specific gene silencing by artificial microRNAs in the unicellular alga Chlamydomonas reinhardtii. Plant Journal 58(1):165–174
Monde RA, Greene JC, Stern DB (2000) The sequence and secondary structure of the 3′-UTR affect 3′-end maturation, RNA accumulation, and translation in tobacco chloroplasts. Plant Mol Biol 44(4):529–542
Moore CE, Curtis B, Mills T, Tanifuji G, Archibald JM (2012) Nucleomorph genome sequence of the cryptophyte alga Chroomonas mesostigmatica CCMP1168 reveals lineage-specific gene loss and genome complexity. Genome Biol Evol 4(11):1162–1175
Moseley JL, Gonzalez-Ballester D, Pootakham W, Bailey S, Grossman AR (2009) Genetic interactions between regulators of Chlamydomonas phosphorus and sulfur deprivation responses. Genetics 181(3):889–905
Mussgnug JH et al (2005) NAB1 is an RNA binding protein involved in the light-regulated differential expression of the light-harvesting antenna of Chlamydomonas reinhardtii. Plant Cell 17(12):3409–3421
Mussgnug JH et al (2007) Engineering photosynthetic light capture: impacts on improved solar energy to biomass conversion. Plant Biotechnol J 5(6):802–814
Nakazato E, Fukuzawa H, Tabata S, Takahashi H, Tanaka K (2003) Identification and expression analysis of cDNA encoding a chloroplast recombination protein REC1, the chloroplast RecA homologue in Chlamydomonas reinhardtii. Biosci Biotechnol Biochem 67(12):2608–2613
Nelson JA, Lefebvre PA (1995) Targeted disruption of the NIT8 gene in Chlamydomonas reinhardtii. Mol Cell Biol 15(10):5762–5769
Nelson JA, Savereide PB, Lefebvre PA (1994) The CRY1 gene in Chlamydomonas reinhardtii: structure and use as a dominant selectable marker for nuclear transformation. Mol Cell Biol 14(6):4011–4019
Nickelsen J (2003) Chloroplast RNA-binding proteins. Curr Genet 43(6):392–399
Oey M, Lohse M, Kreikemeyer B, Bock R (2009) Exhaustion of the chloroplast protein synthesis capacity by massive expression of a highly stable protein antibiotic. Plant J 57(3):436–445
Oey M et al (2013) RNAi knock-down of LHCBM1, 2 and 3 increases photosynthetic H2 production efficiency of the green alga Chlamydomonas reinhardtii. PLoS ONE 8(4):e61375
Oey M, Ross IL, Hankamer B (2014) Gateway-assisted vector construction to facilitate expression of foreign proteins in the chloroplast of single celled algae. PLoS ONE 9(2):e86841
Ohnishi N, Mukherjee B, Tsujikawa T, Yanase M, Nakano H, Moroney JV, Fukuzawa H (2010) Expression of a low CO(2)-inducible protein, LCI1, increases inorganic carbon uptake in the green alga Chlamydomonas reinhardtii. Plant Cell 22(9):3105–3117
Ohnuma M, Yokoyama T, Inouye T, Sekine Y, Tanaka K (2008) Polyethylene glycol (PEG)-mediated transient gene expression in a red alga, Cyanidioschyzon merolae 10D. Plant Cell Physiol 49(1):117–120
Ohnuma M, Misumi O, Fujiwara T, Watanabe S, Tanaka K, Kuroiwa T (2009) Transient gene suppression in a red alga, Cyanidioschyzon merolae 10D. Protoplasma 236(1–4):107–112
O’Neill BM et al (2012) An exogenous chloroplast genome for complex sequence manipulation in algae. Nucleic Acids Res 40(6):2782–2792MathSciNet
Pahlow M, Oschlies A (2013) Optimal allocation backs Droop’s cell-quota model. Mar Ecol Prog Ser 473:1–5
Palenik B et al (2007) The tiny eukaryote Ostreococcus provides genomic insights into the paradox of plankton speciation. Proc Natl Acad Sci USA 104(18):7705–7710
Palmer JD (1983) Chloroplast DNA exists in 2 orientations. Nature 301(5895):92–93
Palmer JD, Thompson WF (1982) Chloroplast DNA rearrangements are more frequent when a large inverted repeat sequence is lost. Cell 29(2):537–550
Pape M, Lambertz C, Happe T, Hemschemeier A (2012) Differential expression of the Chlamydomonas [FeFe]-hydrogenase-encoding HYDA1 gene is regulated by the copper response regulator1. Plant Physiol 159(4):1700–1712
Park S, Lee Y, Lee JH, Jin E (2013) Expression of the high light-inducible Dunaliella LIP promoter in Chlamydomonas reinhardtii. Planta 238:1147–1156
Perez-Garcia O, Escalante FME, de-Bashan LE, Bashan Y (2011) Heterotrophic cultures of microalgae: metabolism and potential products. Water Res 45(1):11–36
Perrine Z, Negi S, Sayre RT (2012) Optimization of photosynthetic light energy utilization by microalgae. Algal Res 1(2):134–142
Perry AS, Wolfe KH (2002) Nucleotide substitution rates in legume chloroplast DNA depend on the presence of the inverted repeat. J Mol Evol 55(5):501–508
Petroutsos D, Terauchi AM, Busch A, Hirschmann I, Merchant SS, Finazzi G, Hippler M (2009) PGRL1 participates in iron-induced remodeling of the photosynthetic apparatus and in energy metabolism in Chlamydomonas reinhardtii. J Biol Chem 284(47):32770–32781
Plaza M, Herrero M, Cifuentes A, Ibanez E (2009) Innovative natural functional ingredients from microalgae. J Agric Food Chem 57(16):7159–7170
Poerschmann J, Spijkerman E, Langer U (2004) Fatty acid patterns in Chlamydomonas sp as a marker for nutritional regimes and temperature under extremely acidic conditions. Microb Ecol 48(1):78–89
Polle JEW, Benemann JR, Tanaka A, Melis A (2000) Photosynthetic apparatus organization and function in the wild type and a chlorophyll b-less mutant of Chlamydomonas reinhardtii. Dependence on Carbon Source. Planta 211(3):335–344
Polle JEW, Niyogi KK, Melis A (2001) Absence of lutein, violaxanthin and neoxanthin affects the functional chlorophyll antenna size of photosystem-ii but not that of photosystem-I in the green alga Chlamydomonas reinhardtii. Plant Cell Physiol 42(5):482–491
Polle JE, Kanakagiri SD, Melis A (2003) tla1, a DNA insertional transformant of the green alga Chlamydomonas reinhardtii with a truncated light-harvesting chlorophyll antenna size. Planta 217(1):49–59
Pombert JF, Otis C, Lemieux C, Turmel M (2005) The chloroplast genome sequence of the green alga Pseudendoclonium akinetum (Ulvophyceae) reveals unusual structural features and new insights into the branching order of chlorophyte lineages. Mol Biol Evol 22(9):1903–1918
Popescu CE, Lee RW (2007) Mitochondrial genome sequence evolution in Chlamydomonas. Genetics 175(2):819–826
Poulsen N, Kroger N (2005) A new molecular tool for transgenic diatoms—control of mRNA and protein biosynthesis by an inducible promoter-terminator cassette. FEBS J 272(13):3413–3423
Poulsen N, Chesley PM, Kroger N (2006) Molecular genetic manipulation of the diatom Thalassiosira pseudonana (Bacillariophyceae). J Phycol 42(5):1059–1065
Price DC et al (2012) Cyanophora paradoxa genome elucidates origin of photosynthesis in algae and plants. Science 335(6070):843–847
Prochnik SE et al (2010) Genomic analysis of organismal complexity in the multicellular green alga Volvox carteri. Science 329(5988):223–226
Proschold T, Harris EH, Coleman AW (2005) Portrait of a species: Chlamydomonas reinhardtii. Genetics 170(4):1601–1610
Purton S (2007) Tools and techniques for chloroplast transformation of Chlamydomonas. Adv Exp Med Biol 616:34–45
Purton S, Szaub JB, Wannathong T, Young R, Economou CK (2013) Genetic engineering of algal chloroplasts: progress and prospects. Russ J Plant Physiol 60(4):491–499
Radakovits R, Eduafo PM, Posewitz MC (2011) Genetic engineering of fatty acid chain length in Phaeodactylum tricornutum. Metab Eng 13(1):89–95
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 Nannochloropis gaditana. Nat Commun 3:686
Randolph-Anderson BL, Boynton JE, Gillham NW, Harris EH, Johnson AM, Dorthu MP, Matagne RF (1993) Further characterization of the respiratory deficient DUM-1 mutation of Chlamydomonas reinhardtii and its use as a recipient for mitochondrial transformation. Mol Gen Genet 236(2–3):235–244
Rasala BA et al (2010) Production of therapeutic proteins in algae, analysis of expression of seven human proteins in the chloroplast of Chlamydomonas reinhardtii. Plant Biotechnol J 8(6):719–733
Rasala BA, Muto M, Sullivan J, Mayfield SP (2011) Improved heterologous protein expression in the chloroplast of Chlamydomonas reinhardtii through promoter and 5′ untranslated region optimization. Plant Biotechnol J 9(6):674–683
Rasala BA, Lee PA, Shen Z, Briggs SP, Mendez M, Mayfield SP (2012) Robust Expression and Secretion of Xylanase1 in Chlamydomonas reinhardtii by fusion to a selection gene and processing with the FMDV 2A Peptide. PLoS One 7(8):e43349
Rasala BA, Gimpel JA, Tran M, Hannon MJ, Miyake-Stoner SJ, Specht EA, Mayfield SP (2013) Genetic engineering to improve algal biofuels production. In: Borowitzka MA, Moheimani NR (eds) Algae for biofuels and energy. Developments in applied phycology, vol 5. Springer, Berlin, pp 99–113
Ravi V, Khurana JP, Tyagi AK, Khurana P (2008) An update on chloroplast genomes. Plant Syst Evol 271(1–2):101–122
Raymond JA, Kim HJ (2012) Possible role of horizontal gene transfer in the colonization of sea ice by algae. PLoS ONE 7(5):e35968
Read BA et al (2013) Pan genome of the phytoplankton Emiliania underpins its global distribution. Nature 499(7457):209–213
Reiss B, Klemm M, Kosak H, Schell J (1996) RecA protein stimulates homologous recombination in plants. Proc Natl Acad Sci USA 93(7):3094–3098
Reiss B, Schubert I, Kopchen K, Wendeler E, Schell J, Puchta H (2000) RecA stimulates sister chromatid exchange and the fidelity of double-strand break repair, but not gene targeting, in plants transformed by Agrobacterium. Proc Natl Acad Sci USA 97(7):3358–3363
Remacle C, Cardol P, Coosemans N, Gaisne M, Bonnefoy N (2006) High-efficiency biolistic transformation of Chlamydomonas mitochondria can be used to insert mutations in complex I genes. Proc Natl Acad Sci USA 103(12):4771–4776
Remacle C, Larosa V, Salinas T, Hamel P, Subrahmanian N, Bonnefoy N, Kempken F (2012) Transformation and nucleic acid delivery to mitochondria. In: Bock R, Knoop V (eds) Genomics of chloroplasts and mitochondria, vol 35., Advances in photosynthesis and respirationSpringer, Netherlands, pp 443–458
Riano-Pachon DM, Correa LGG, Trejos-Espinosa R, Mueller-Roeber B (2008) Green transcription factors: a chlamydomonas overview. Genetics 179(1):31–39
Rismani-Yazdi H, Haznedaroglu BZ, Bibby K, Peccia J (2011) Transcriptome sequencing and annotation of the microalgae Dunaliella tertiolecta: pathway description and gene discovery for production of next-generation biofuels. BMC Genom 12:17
Rochaix JD, Vandillewijn J (1982) Transformation of the green alga Chlamydomonas reinhardii with yeast DNA. Nature 296(5852):70–72
Rodolfi L, Zittelli GC, Bassi N, Padovani G, Biondi N, Bonini G, Tredici MR (2009) Microalgae for oil: strain selection, induction of lipid synthesis and outdoor mass cultivation in a low-cost photobioreactor. Biotechnol Bioeng 102(1):100–112
Roessler PG (1988a) Changes in the activities of various lipid and carbohydrate biosynthetic-enzymes in the diatom Cyclotella cryptica in response to silicon deficiency. Arch Biochem Biophys 267(2):521–528
Roessler PG (1988b) Effects of silicon deficiency on lipid-composition and metabolism in the diatom Cyclotella cryptica. J Phycol 24(3):394–400
Roessler PG (1990) Environmental-control of glycerolipid metabolism in microalgae—commercial implications and future-research directions. J Phycol 26(3):393–399
Rohr J, Sarkar N, Balenger S, Jeong BR, Cerutti H (2004) Tandem inverted repeat system for selection of effective transgenic RNAi strains in Chlamydomonas. Plant J 40(4):611–621
Rott R, Liveanu V, Drager RG, Stern DB, Schuster G (1998) The sequence and structure of the 3′-untranslated regions of chloroplast transcripts are important determinants of mRNA accumulation and stability. Plant Mol Biol 36(2):307–314
Rowan BA, Oldenburg DJ, Bendich AJ (2010) RecA maintains the integrity of chloroplast DNA molecules in Arabidopsis. J Exp Bot 61(10):2575–2588
Ruhlman T, Verma D, Samson N, Daniell H (2010) The role of heterologous chloroplast sequence elements in transgene integration and expression. Plant Physiol 152(4):2088–2104
Sakaguchi T, Nakajima K, Matsuda Y (2011) Identification of the UMP synthase gene by establishment of uracil auxotrophic mutants and the phenotypic complementation system in the marine diatom phaeodactylum tricornutum. Plant Physiol 156(1):78–89
Sakamoto W, Kindle KL, Stern DB (1993) Invivo analysis of chlamydomonas chloroplast petd gene-expression using stable transformation of beta-glucuronidase translational fusions. Proc Natl Acad Sci USA 90(2):497–501
Salvador ML, Klein U, Bogorad L (1993) 5′ sequences are important positive and negative determinants of the longevity of chlamydomonas chloroplast gene transcripts. Proc Natl Acad Sci USA 90(4):1556–1560
Sander JD, Joung JK (2014) CRISPR-cas systems for editing, regulating and targeting genomes. Nat Biotech 32(4):347–355
Schiedlmeier B, Schmitt R, Muller W, Kirk MM, Gruber H, Mages W, Kirk DL (1994) Nuclear transformation of Volvox carteri. Proc Natl Acad Sci USA 91(11):5080–5084
Schmollinger S, Strenkert D, Schroda M (2010) An inducible artificial microRNA system for Chlamydomonas reinhardtii confirms a key role for heat shock factor 1 in regulating thermotolerance. Curr Genet 56(4):383–389
Schönfeld C, Wobbe L, Borgstädt R, Kienast A, Nixon PJ, Kruse O (2004) The nucleus-encoded protein MOC1 is essential for mitochondrial light acclimation in Chlamydomonas reinhardtii. J Biol Chem 279(48):50366–50374
Schonknecht G et al (2013) Gene transfer from bacteria and archaea facilitated evolution of an extremophilic eukaryote. Science 339(6124):1207–1210
Schroda M, Vallon O, Wollman FA, Beck CF (1999) A chloroplast-targeted heat shock protein 70 (HSP70) contributes to the photoprotection and repair of photosystem II during and after photoinhibition. Plant Cell 11(6):1165–1178
Schroda M, Blocker D, Beck CF (2000) The HSP70A promoter as a tool for the improved expression of transgenes in Chlamydomonas. Plant J 21(2):121–131
Schulze T, Prager K, Dathe H, Kelm J, Kiessling P, Mittag M (2010) How the green alga Chlamydomonas reinhardtii keeps time. Protoplasma 244(1–4):3–14
Seitz SB, Voytsekh O, Mohan KM, Mittag M (2010) The role of an E-box element: multiple frunctions and interacting partners. Plant Signal Behav 5(9):1077–1080
Shalev G, Sitrit Y, Avivi-Ragolski N, Lichtenstein C, Levy AA (1999) Stimulation of homologous recombination in plants by expression of the bacterial resolvase RuvC. Proc Natl Acad Sci USA 96(13):7398–7402
Shaw J, Lickey EB, Schilling EE, Small RL (2007) Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: The tortoise and the hare III. Am J Bot 94(3):275–288
Sheehan J, Dunahay T, Benemann J, Roessler P (1998) A look back at the U.S. department of energy’s aquatic species program-biodiesel from algae. National Renewable Energy Institute, NREL/TP-580-24190, Golden, CO
Shimogawara K, Fujiwara S, Grossman A, Usuda H (1998) High-efficiency transformation of Chlamydomonas reinhardtii by electroporation. Genetics 148(4):1821–1828
Siaut M et al (2011) Oil accumulation in the model green alga Chlamydomonas reinhardtii: characterization, variability between common laboratory strains and relationship with starch reserves. BMC Biotechnol 11:7
Sizova I, Fuhrmann M, Hegemann P (2001) A Streptomyces rimosus aphVIII gene coding for a new type phosphotransferase provides stable antibiotic resistance to Chlamydomonas reinhardtii. Gene 277(1–2):221–229
Sizova I, Greiner A, Awasthi M, Kateriya S, Hegemann P (2013) Nuclear gene targeting in Chlamydomonas using engineered zinc-finger nucleases. Plant J 73:873–882
Smart EJ, Selman BR (1993) Complementation of a chlamydomonas-reinhardtii mutant defective in the nuclear gene encoding the chloroplast coupling factor-I (CF1) gamma-subunit (ATPC). J Bioenerg Biomembr 25(3):275–284
Smith GR (2012) How RecBCD enzyme and Chi promote DNA break repair and recombination: a molecular biologist’s view. Microbiol Mol Biol Rev 76(2):217–228
Smith VH, Sturm BSM, deNoyelles FJ, Billings SA (2010) The ecology of algal biodiesel production. Trends Ecol Evol 25(5):301–309
Sodeinde OA, Kindle KL (1993) Homologous recombination in the nuclear genome of Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 90(19):9199–9203
Sommer F, Kropat J, Malasarn D, Grossoehme NE, Chen X, Giedroc DP, Merchant SS (2010) The CRR1 nutritional copper sensor in Chlamydomonas contains two distinct metal-responsive domains. Plant Cell 22(12):4098–4113
Specht E, Miyake-Stoner S, Mayfield S (2010) Micro-algae come of age as a platform for recombinant protein production. Biotechnol Lett 32(10):1373–1383
Speight JG (2006) The Chemistry and Technology of Petroleum. CRC Press
Spoehr HA, Milner HW (1949) The chemical composition of chlorella—effect of environmental conditions. Plant Physiol 24(1):120–149
Stein DB, Palmer JD, Thompson WF (1986) Structural evolution and flip-flop recombination of chloroplast DNA in the fern genus osmunda. Curr Genet 10(11):835–841
Steinbrenner J, Sandmann G (2006) Transformation of the green alga Haematococcus pluvialis with a phytoene desaturase for accelerated astaxanthin biosynthesis. Appl Environ Microbiol 72(12):7477–7484
Stephens E, Ross IL, Hankamer B (2013b) Expanding the microalgal industry—continuing controversy or compelling case? Curr Opin Chem Biol 17(3):444–452
Stern DB, Gruissem W (1987) Control of plastid gene-expression—3′ inverted repeats act as messenger-RNA processing and stabilizing elements, But do not terminate transcription. Cell 51(6):1145–1157
Stern DB, Radwanski ER, Kindle KL (1991) A 3′ stem/loop structure of the Chlamydomonas chloroplast atpB gene regulates mRNA accumulation in vivo. Plant Cell 3(3):285–297
Stevens DR, Rochaix JD, Purton S (1996) The bacterial phleomycin resistance gene ble as a dominant selectable marker in Chlamydomonas. Mol Gen Genet 251(1):23–30
Strenkert D, Schmollinger S, Sommer F, Schulz-Raffelt M, Schroda M (2011) Transcription factor-dependent chromatin remodeling at heat shock and copper-responsive promoters in Chlamydomonas reinhardtii. Plant Cell 23(6):2285–2301
Strenkert D, Schmollinger S, Schroda M (2013) Heat shock factor 1 counteracts epigenetic silencing of nuclear transgenes in Chlamydomonas reinhardtii. Nucleic Acids Res 41(10):5273–5289
Sun Y, Yang Z, Gao X, Li Q, Zhang Q, Xu Z (2005) Expression of foreign genes in Dunaliella by electroporation. Mol Biotechnol 30(3):185–192
Sun G, Zhang X, Sui Z, Mao Y (2008) Inhibition of pds gene expression via the RNA interference approach in Dunaliella salina (Chlorophyta). Mar Biotechnol (NY) 10(3):219–226
Sunda WG, Graneli E, Gobler CJ (2006) Positive feedback and the development and persistence of ecosystem disruptive algal blooms. J Phycol 42:963–974
Sung P, Klein H (2006) Mechanism of homologous recombination: mediators and helicases take on regulatory functions. Nat Rev Mol Cell Biol 7(10):739–750
Surzycki R, Cournac L, Peltier G, Rochaix JD (2007) Potential for hydrogen production with inducible chloroplast gene expression in Chlamydomonas. Proc Natl Acad Sci USA 104(44):17548–17553
Surzycki R et al (2009) Factors effecting expression of vaccines in microalgae. Biologicals 37(3):133–138
Hosseini Tafreshi A, Shariati M (2009) Dunaliella biotechnology: methods and applications. J Appl Microbiol 107(1):14–35
Tam LW, Lefebvre PA (1993) Cloning of flagellar genes in Chlamydomonas reinhardtii by DNA insertional mutagenesis. Genetics 135(2):375–384
Tan C, Qin S, Zhang Q, Jiang P, Zhao F (2005) Establishment of a micro-particle bombardment transformation system for Dunaliella salina. J Microbiol 43(4):361–365
Tanaka A, Ito H, Tanaka R, Tanaka NK, Yoshida K, Okada K (1998) Chlorophyll a oxygenase (CAO) is Involved in Chlorophyll b Formation from Chlorophyll a. Proc Natl Acad Sci USA 95(21):12719–12723
ten Lohuis MR, Miller DJ (1998) Genetic transformation of dinoflagellates (Amphidinium and Symbiodinium): expression of GUS in microalgae using heterologous promoter constructs. Plant J 13(3):427–435
Teng CY, Qin S, Liu JG, Yu DZ, Liang CW, Tseng CK (2002) Transient expression of lacZ in bombarded unicellular green alga Haematococcus pluvialis. J Appl Phycol 14(6):497–500
Tolleter D et al (2011) Control of hydrogen photoproduction by the proton gradient generated by cyclic electron flow in Chlamydomonas reinhardtii. Plant Cell 23(7):2619–2630
Tran M, Zhou B, Pettersson PL, Gonzalez MJ, Mayfield SP (2009) Synthesis and assembly of a full-length human monoclonal antibody in algal chloroplasts. Biotechnol Bioeng 104(4):663–673
Tran M, Van C, Barrera DJ, Pettersson PL, Peinado CD, Bui J, Mayfield SP (2013) Production of unique immunotoxin cancer therapeutics in algal chloroplasts. Proc Natl Acad Sci USA 110(1):E15–E22
Trebitsh T, Levitan A, Sofer A, Danon A (2000) Translation of chloroplast psbA mRNA is modulated in the light by counteracting oxidizing and reducing activities. Mol Cell Biol 20(4):1116–1123
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 Natl Acad Sci USA 110(49):19748–19753
Vahrenholz C, Riemen G, Pratje E, Dujon B, Michaelis G (1993) Mitochondrial-DNA of Chlamydomonas reinhardtii—the structure of the ends of the linear 15.8-KB genome suggests mechanisms for DNA-replication. Curr Genet 24(3):241–247
Van Dolah FM, Roelke D, Greene RM (2001) Health and ecological impacts of harmful algal blooms: risk assessment needs. Hum Ecol Risk Assess 7:1329–1345
Vieler A et al (2012) Genome, functional gene annotation, and nuclear transformation of the heterokont oleaginous alga Nannochloropsis oceanica CCMP1779. Plos Genet 8(11):e1003064
Vinyard DJ, Gimpel J, Ananyev GM, Mayfield SP, Dismukes GC (2014) Engineered photosystem II reaction centers optimize photochemistry versus photoprotection at different solar intensities. J Am Chem Soc 136(10):4048–4055
Walker TL, Purton S, Becker DK, Collet C (2005) Microalgae as bioreactors. Plant Cell Rep 24(11):629–641
Wang C, Wang Y, Su Q, Gao X (2007) Transient expression of the GUS gene in a unicellular marine green alga, Chlorella sp MACC/C95, via electroporation. Biotechnol Bioprocess Eng 12(2):180–183
Wijffels RH, Kruse O, Hellingwerf KJ (2013) Potential of industrial biotechnology with cyanobacteria and eukaryotic microalgae. Curr Opin Biotechnol 24(3):405–413
Wilson NF, Lefebvre PA (2004) Regulation of flagellar assembly by glycogen synthase kinase 3 in Chlamydomonas reinhardtii. Eukaryot Cell 3(5):1307–1319
Wobbe L, Schwarz C, Nickelsen J, Kruse O (2008) Translational control of photosynthetic gene expression in phototrophic eukaryotes. Physiol Plant 133(3):507–515
Wobbe L, Blifernez O, Schwarz C, Mussgnug JH, Nickelsen J, Kruse O (2009) Cysteine modification of a specific repressor protein controls the translational status of nucleus-encoded LHCII mRNAs in Chlamydomonas. Proc Natl Acad Sci USA 106(32):13290–13295
Worden AZ et al (2009) Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas. Science 324(5924):268–272
Work VH et al (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
Wykoff DD, Grossman AR, Weeks DP, Usuda H, Shimogawara K (1999) Psr1, a nuclear localized protein that regulates phosphorus metabolism in Chlamydomonas. Proc Natl Acad Sci USA 96(26):15336–15341
Yamasaki T, Kurokawa S, Watanabe KI, Ikuta K, Ohama T (2005) Shared molecular characteristics of successfully transformed mitochondrial genomes in Chlamydomonas reinhardtii. Plant Mol Biol 58(4):515–527
Yamasaki T, Voshall A, Kim EJ, Moriyama E, Cerutti H, Ohama T (2013) Complementarity to an miRNA seed region is sufficient to induce moderate repression of a target transcript in the unicellular green alga Chlamydomonas reinhardtii. Plant J 76(6):1045–1056
Yoon K, Han DX, Li YT, 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
Yoshioka S, Taniguchi F, Miura K, Inoue T, Yamano T, Fukuzawa H (2004) The novel Myb transcription factor LCR1 regulates the CO2-responsive gene Cah1, encoding a periplasmic carbonic anhydrase in Chlamydomonas reinhardtii. Plant Cell 16(6):1466–1477
Yu WL, Ansari W, Schoepp NG, Hannon MJ, Mayfield SP, Burkart MD (2011) Modifications of the metabolic pathways of lipid and triacylglycerol production in microalgae. Microb Cell Fact 10:11
Zabawinski C et al (2001) Starchless mutants of Chlamydomonas reinhardtii lack the small subunit of a heterotetrameric ADP-glucose pyrophosphorylase. J Bacteriol 183(3):1069–1077
Zaslavskaia LA, Lippmeier JC, Kroth PG, Grossman AR, Apt KE (2000) Transformation of the diatom Phaeodactylum tricornutum (Bacillariophyceae) with a variety of selectable marker and reporter genes. J Phycol 36(2):379–386
Zaslavskaia LA, Lippmeier JC, Shih C, Ehrhardt D, Grossman AR, Apt KE (2001) Trophic obligate conversion of an photoautotrophic organism through metabolic engineering. Science 292(5524):2073–2075
Zerges W (2000) Translation in chloroplasts. Biochimie 82(6–7):583–601
Zhang X et al (2012) De novo sequencing and analysis of the Ulva linza transcriptome to discover putative mechanisms associated with its successful colonization of coastal ecosystems. BMC Genom 13:565
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
Zhao T, Li G, Mi S, Li S, Hannon GJ, Wang XJ, Qi Y (2007) A complex system of small RNAs in the unicellular green alga Chlamydomonas reinhardtii. Genes Dev 21(10):1190–1203
Zhao T, Wang W, Bai X, Qi Y (2009) Gene silencing by artificial microRNAs in Chlamydomonas. Plant J 58(1):157–164
Zhu XG, Long SP, Ort DR (2010) Improving photosynthetic efficiency for greater yield. Annu Rev Plant Biol 61(61):235–261
Zorin B, Hegemann P, Sizova I (2005) Nuclear-gene targeting by using single-stranded DNA avoids illegitimate DNA integration in Chlamydomonas reinhardtii. Eukaryot Cell 4(7):1264–1272
Zorin B, Lu Y, Sizova I, Hegemann P (2009) Nuclear gene targeting in Chlamydomonas as exemplified by disruption of the PHOT gene. Gene 432(1–2):91–96
Zou Z, Eibl C, Koop HU (2003) The stem-loop region of the tobacco psbA 5′ UTR is an important determinant of mRNA stability and translation efficiency. Mol Genet Genomics 269(3):340–349
Metadata
Title
Genetic Engineering for Microalgae Strain Improvement in Relation to Biocrude Production Systems
Authors
Evan Stephens
Juliane Wolf
Melanie Oey
Eugene Zhang
Ben Hankamer
Ian L. Ross
Copyright Year
2015
Book
Biomass and Biofuels from Microalgae

Print ISBN: 978-3-319-16639-1

Electronic ISBN: 978-3-319-16640-7

Copyright Year: 2015

DOI
https://doi.org/10.1007/978-3-319-16640-7_11