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Microalgae as bioreactors

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Abstract

Microalgae already serve as a major natural source of valuable macromolecules including carotenoids, long-chain polyunsaturated fatty acids and phycocolloids. As photoautotrophs, their simple growth requirements make these primitive plants potentially attractive bioreactor systems for the production of high-value heterologous proteins. The difficulty of producing stable transformants has meant that the field of transgenic microalgae is still in its infancy. Nonetheless, several species can now be routinely transformed and algal biotechnology companies have begun to explore the possibilities of synthesizing recombinant therapeutic proteins in microalgae and the engineering of metabolic pathways to produce increased levels of desirable compounds. In this review, we compare the current commercially viable bioreactor systems, outline recent progress in microalgal biotechnology and transformation, and discuss the potential of microalgae as bioreactors for the production of heterologous proteins.

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References

  • Allnutt FCT, Kyle DJ, Grossman AR, Apt KE (2000) Methods and tools for transformation of eukaryotic algae. United States of America Patent Number 6027900

  • Apt KE, Behrens PW (1999) Commercial developments in microalgal biotechnology. J Phycol 35:215–226

    Article  Google Scholar 

  • Apt KE, Kroth-Pancic PG, Grossman AR (1996) Stable nuclear transformation of the diatom Phaeodactylum tricornutum. Mol Gen Genet 252:572–579

    Article  PubMed  CAS  Google Scholar 

  • Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam N, Zhou S, Allen AE, Apt KE, Bechner M, Brzezinski MA, Chaal BK, Chiovitti A, Davis AK, Demarest MS, Detter JC, Glavina T, Goodstein D, Hadi MZ, Hellsten U, Hilldebrand M, Jenkins BD, Jurka J, Kapitonov VV, Kröger N, Lau WWY, Lane TW, Larimer FW, Lippmeier JC, Lucas S, Medina M, Monstant A, Orbornik M, Parker MS, Palenik B, Pazour GJ, Richardson PM, Rynearson TA, Saito MA, Schwartz DC, Thamatakoln K, Valentin K, Vardi A, Wilkerson FP, Rokshar D (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306:79–86

    Article  PubMed  CAS  Google Scholar 

  • Bateman JM, Purton S (2000) Tools for chloroplast transformation in Chlamydomonas: expression vectors and a new dominant selectable marker. Mol Gen Genet 263:404–410

    Article  PubMed  CAS  Google Scholar 

  • Banicki JJ (2004) An alga a day keeps the doctor away. Engineered algae as a new means to vaccinate fish. Twine Line 26:1–2

    Google Scholar 

  • Benemann JR (2003) Biofixation of CO2 and greenhouse gas abatement with microalgae—technology roadmap. Final report to the US Department of Energy, National Energy Technology Laboratory

  • Benemann JR, Oswald WJ (1996) Systems and economic analysis of microalgae ponds for conversion of CO2 to biomass. Final report to the US Department of Energy, Pittsburgh Energy Technology Center

  • Benfey PN, Ren L, Chua NH (1990) Tissue-specific expression from CaMV 35S enhancer subdomains in early stages of plant development. EMBO J 9:1677–1684

    PubMed  CAS  Google Scholar 

  • Borisjuk NV, Borisjuk LG, Logendra S, Petersen F, Gleba Y, Raskin I (1999) Production of recombinant proteins in plant root exudates. Nat Biotechnol 17:466–469

    Article  PubMed  CAS  Google Scholar 

  • Borovsky D (2003) Trypsin-modulating oostatic factor: a potential new larvicide for mosquito control. J Exp Biol 206:3869–3875

    Article  PubMed  CAS  Google Scholar 

  • Borowitzka MA (1988) Vitamins and fine chemicals from micro-algae. In: Borowitzka LJ, Borowitzka MA (eds) Micro-algal biotechnology. Cambridge University Press, Cambridge, pp 153–196

    Google Scholar 

  • Borowitzka MA (1999) Commercial production of microalgae. In: Cohen Z (ed) Chemicals from microalgae. Taylor & Francis, London, pp 313–352

    Google Scholar 

  • Boynton JE, Gillham NW, Harris EH, Hosler JP, Johnson AM, Jones AR, Randolph-Anderson BL, Robertson D, Klein TM, Shark KB, Sanford JC (1988) Chloroplast transformation in Chlamydomonas with high velocity microprojectiles. Science 240:1534–1538

    PubMed  CAS  Google Scholar 

  • Brown LE, Sprecher SL, Keller LR (1991) Introduction of exogenous DNA into Chlamydomonas reinhardtii by electroporation. Mol Cell Biol 11:2328–2332

    PubMed  CAS  Google Scholar 

  • Brown MR (2002) Nutritional value of microalgae for aquaculture. In: Cruz-Suarez LE, Ricque-Marie D, Tapia-Salazar M, Gaxiola-Cortes MG, Simoes N (eds) Avances en nutricion acuicola VI. Memorias del VI SymposiumInternacional de Nutricion Acuicola. 3–6th September, Cancun, Mexico

    Google Scholar 

  • Cabanes-Macheteau M, Fitchette-Laine AC, Loutelie-Bourhis C, Lange C, Vine N, Ma J, Lerouge P, Faye L (1999) N-Glycosylation of a mouse IgG expressed in transgenic tobacco plants. Glycobiology 9:365–372

    Article  PubMed  CAS  Google Scholar 

  • Cannell RJP (1993) Algae as a source of biologically active products. Pest Sci 39:147–153

    CAS  Google Scholar 

  • Cerutti H, Johnson AM, Gillham NW, Boynton JE (1997) A eubacterial gene conferring spectinomycin resistance on Chlamydomonas reinhardtii: integration into the nuclear genome and gene expression. Genetics 145:97–110

    PubMed  CAS  Google Scholar 

  • Chen Y, Wang Y, Sun Y., Zhang L, Li W (2001) Highly efficient expression of rabbit neutrophil peptide-1 gene in Chlorella ellipsoidea cells. Curr Genet 39:365–370

    Article  PubMed  CAS  Google Scholar 

  • Chow KC, Tung WL (1999) Electrotransformation of Chlorella vulgaris. Plant Cell Rep 18:778–780

    Article  CAS  Google Scholar 

  • Chu L, Robinson DK (2001) Industrial choices for protein productions by large-scale cell culture. Curr Opin Biotechnol 12:180–187

    Article  PubMed  CAS  Google Scholar 

  • Codd GA (1995) Cyanobacterial toxins: occurrence, properties and biological significance. Wat Sci Technol 32:149–156

    Article  CAS  Google Scholar 

  • Cohen Z (1999) (ed.) Chemicals from microalgae. Taylor & Francis Ltd., London

    Google Scholar 

  • Cramer CL, Weissenborn DL, Oishi KK, Grabau EA, Bennett S, Ponce E, Grabowski GA, Radin DN (1996) Bioproduction of human enzymes in transgenic tobacco. Ann NY Acad Sci 792:62–71

    PubMed  CAS  Google Scholar 

  • Cramer CL, Boothe JG, Oishi KK (1999) Transgenic plants for therapeutic proteins: linking upstream and downstream strategies. Curr Top Microbiol Immunol 240:95–118

    PubMed  CAS  Google Scholar 

  • Curtain C (2000) The growth of Australia's algal beta-carotene industry. Australian Biotechnol 10:19–23

    Google Scholar 

  • Davies JP, Weeks DP, Grossman AR (1992) Expression of the arylsulfatase gene from the beta 2-tubulin promoter in Chlamydomonas reinhardtii. Nucleic Acids Res 20:2959–2965

    PubMed  CAS  Google Scholar 

  • Dawson HN, Burlingame R, Cannons AC (1997) Stable transformation of Chlorella: Rescue of nitrate reductase-deficient mutants with the nitrate reductase gene. Curr Microbio 35:356–362

    Article  CAS  Google Scholar 

  • Debuchy R, Purton S, Rochaix JD (1989) The argininosuccinate lyase gene of Chlamydomonas reinhardtii: an important tool for nuclear transformation and for correlating the genetic and molecular maps of the ARG7 locus. EMBO J 8:2803–2809

    PubMed  CAS  Google Scholar 

  • De Cosa B, Moar W, Lee SB, Miller M, Daniell H (2001) Over expression of the Bt cry2Aa2 operon in chloroplasts leads to formation of insecticidal crystals. Nat Biotechnol 19:71–74

    Article  PubMed  Google Scholar 

  • 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 39:49–60

    Article  PubMed  CAS  Google Scholar 

  • Dunahay TG (1993) Transformation of Chlamydomonas reinhardtii with silicon carbide whiskers. Biotechniques 15:452–460

    PubMed  CAS  Google Scholar 

  • Dunahay TG, Jarvis EE, Roessler PG (1995) Genetic transformation of the diatoms Cyclotella cryptica and Navicula saprophila. J Phycol 31:1004–1012

    Article  CAS  Google Scholar 

  • Echelard Y (1996) Recombinant protein production in transgenic animals. Curr Opin Biotechnol 7:536–540

    Article  PubMed  CAS  Google Scholar 

  • El-Sheekh MM (1999) Stable transformation of the intact cells of Chlorella kessleri with high velocity microprojectiles. Biologia Plantarum 42:209–216

    Article  CAS  Google Scholar 

  • Falciatore A, Bowler C (2002) Revealing the molecular secrets of marine diatoms. Annu Rev Plant Biol 53:109–130

    Article  PubMed  CAS  Google Scholar 

  • Fernandez E, Schnell R, Ranum LP, Hussey SC, Silflow CD, Lefebvre PA (1989) Isolation and characterization of the nitrate reductase structural gene of Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 86:6449–6453

    PubMed  CAS  Google Scholar 

  • Fischer R, Emans N (2000) Molecular farming of pharmaceutical proteins. Transgenic Res 9:279–299

    Article  PubMed  CAS  Google Scholar 

  • Fischer R, Liao YC, Hoffmann K, Schillberg S, Emans N (1999) Molecular farming of recombinant antibodies in plants. Biol Chem 380:825–839

    Article  PubMed  CAS  Google Scholar 

  • Franklin SE, Mayfield SP (2004) Prospects for molecular farming in the green alga Chlamydomonas. Curr Opin Plant Biol 7:159–165

    Article  PubMed  CAS  Google Scholar 

  • Franklin S, Ngo B, Efuet E, Mayfield SP (2002) Development of a GFP reporter gene for Chlamydomonas reinhardtii chloroplast. Plant J 30:733–744

    Article  PubMed  CAS  Google Scholar 

  • Fuhrmann M (2002) Expanding the molecular toolkit for Chlamydomonas reinhardtii—from history to new frontiers. Protist 153:357–364

    Article  PubMed  Google Scholar 

  • Fuhrmann M, Hausherr A, Ferbitz L, Schödl 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 55:869–881

    PubMed  CAS  Google Scholar 

  • 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 19:353–361

    Article  PubMed  CAS  Google Scholar 

  • Ganz PR (1996) Expression of human blood proteins in transgenic plants: the cytokine GM-CSF as a model protein. In: Owen MRL, Pen J (eds) Transgenic plants: a production system for industrial and pharmaceutical proteins. Wiley, London, pp 281–297

    Google Scholar 

  • Garcia-Casado G, Sanchez-Monge R, Chrispeels MJ, Armentia A, Salcedo G, Gomez L (1996) Role of complex asparagine-linked glycans in the allergenicity of plant glycoproteins. Glycobiology 6:471–477

    PubMed  CAS  Google Scholar 

  • Geng D, Wang Y, Wang P, Li W, Sun Y (2003) Stable expression of hepatitis B surface antigen in Dunaliella salina (Chlorophyta). J App Phycol 15:451–456

    Article  CAS  Google Scholar 

  • Giddings G, Allison G, Brooks D, Carter A (2000) Transgenic plants as factories for biopharmaceuticals. Nat Biotechnol 18:1151–1155

    Article  PubMed  CAS  Google Scholar 

  • 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 19:4083–4089

    PubMed  CAS  Google Scholar 

  • Gomord V, Denmat LA, Fitchette-Laine AC, Satiat-Jeunemaitre B, Hawes C, Faye L (1997) The C-terminal HDEL sequence is sufficient for retention of secretory proteins in the endoplasmic reticulum (ER) but promotes vacuolar targeting of proteins that escape the ER. Plant J 11:101–103

    Article  Google Scholar 

  • Grinnell BW, Walls JD, Gerlitz B (1991) Glycosylation of human protein C affects its secretion, processing, functional activities, and activation by thrombin. J Biol Chem 266:9778–9785

    PubMed  CAS  Google Scholar 

  • Grossman AR, Harris EE, Hauser C, Lefebvre PA, Martinez D, Rokhsar D, Shrager J, Silflow CD, Stern D, Vallon O, Zhang Z (2003) Chlamydomonas reinhardtii at the crossroads of genomics. Eukaryotic Cell 2:1137–1150

    Article  PubMed  CAS  Google Scholar 

  • Hawkins RL, Nakamura M (1999) Expression of human growth hormone by the eukaryotic alga, Chlorella. Curr Microbiol 38:335–341

    PubMed  CAS  Google Scholar 

  • He Q (2003) Microalgae as platforms for recombinant proteins. In: Richmond A (ed) Handbook of microalgal culture: biotechnology and applied phycology. Blackwell Publishing, Oxford, UK, pp 471–484

    Google Scholar 

  • Herbers K, Sonnewald U (1999) Production of new/modified proteins in transgenic plants. Curr Opin Biotechnol 10:163–168

    Article  PubMed  CAS  Google Scholar 

  • Hiatt AC, Cafferkey R, Bowdish K (1989) Production of antibodies in transgenic plants. Nature 342:76–78

    Article  PubMed  CAS  Google Scholar 

  • Ishikura K, Tataoka Y, Kata K, Sekine M, Yoshida K, Shinmyo A (1999) Expression of a foreign gene in Chlamydomonas reinhardtii chloroplast. J Biosci Bioeng 87:307–334

    Article  PubMed  CAS  Google Scholar 

  • Janne J, Alhonen L, Hyttinen JM, Peura T, Tolvanen M, Korhonen VP (1998) Transgenic bioreactors. Biotechnol Annu Rev 4:55–74

    PubMed  CAS  Google Scholar 

  • Jarvis EE, Brown LM (1991) Transient expression of firefly luciferase in protoplasts of the green alga Chlorella ellipsoidea. Curr Genet 19:317–321

    Article  CAS  Google Scholar 

  • Jefferis R, Lund J (1997) Glycosylation of antibody molecules: structural and functional significance. Chem Immun Antibody Eng 65:111–128

    CAS  Google Scholar 

  • Kang M, Han JG, Liu PF, Ye Y, Tien P (2000) The regulation activity of Chlorella virus gene 5′ upstream sequence in Escherichia coli and eucaryotic algae. Sheng Wu Gong Cheng Xue Bao 16:443–446

    PubMed  CAS  Google Scholar 

  • Kelley BD (2001) Biochemical engineering: bioprocessing of therapeutic proteins. Curr Opin Biotechnol 12:173–174

    Article  PubMed  CAS  Google Scholar 

  • Kim D-H, Kim YT, Cho JJ, Bae J-H, Hur S-B, Hwang I, Choi T-J (2002) Stable integration and functional expression of flounder growth hormone gene in transformed microalga, Chlorella ellipsoidea. Marine Biotechnol 4:63–73

    Article  CAS  Google Scholar 

  • Kindle KL, Schnell RA, Fernandez E, Lefebvre PA (1989) Stable nuclear transformation of Chlamydomonas using the Chlamydomonas gene for nitrate reductase. J Cell Biol 109:2589–2601

    Article  PubMed  CAS  Google Scholar 

  • Kindle KL (1990) High-frequency nuclear transformation of Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 87:1228–1232

    PubMed  CAS  Google Scholar 

  • Komine Y, Kikis E, Schuster G, Stern D (2002) Evidence for in vivo modulation of chloroplast RNA stability by 3′-UTR homopolymeric tails in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 99:4085–4090

    Article  PubMed  CAS  Google Scholar 

  • Kovar JL, Zhang J, Funke RP, Weeks DP (2002) Molecular analysis of the acetolactate synthase gene of Chlamydomonas reinhardtii and development of a genetically engineered gene as a dominant selectable marker for genetic transformation. Plant J 29:109–117

    Article  PubMed  CAS  Google Scholar 

  • Kumar SV, Misquitta RW, Reddy VS, Rao BJ, Rajam MV (2004) Genetic transformation of the green alga—Chlamydomonas reinhardtii by Agrobacterium tumefaciens. Plant Science 166:731–738

    Article  CAS  Google Scholar 

  • Lapidot M, Raveh D, Sivan A, Arad SM, Shapira M (2002) Stable chloroplast transformation of the unicellular red alga Porphyridium species. Plant Physiol 129:7–12

    Article  PubMed  CAS  Google Scholar 

  • Larrick JW, Thomas DW (2001) Producing proteins in transgenic plants and animals. Curr Opin Biotechnol 12:411–418

    Article  PubMed  CAS  Google Scholar 

  • Lee Y-K (2001) Microalgal mass culture systems and methods: Their limitation and potential. J Appl Phycol 13:307–315

    Article  Google Scholar 

  • Lin Cereghino GPL, Cregg JM (1999) Applications of yeast in biotechnology: protein production and genetic analysis. Curr Opin Biotechnol 10:422–427

    Article  PubMed  CAS  Google Scholar 

  • Lorenz RT, Cysewski GR (2000) Commercial potential for Haematococcus microalgae as a natural source of astaxanthin. Trends Biotechnol 18:160–167

    Article  PubMed  CAS  Google Scholar 

  • Lumbreras V, Purton S (1998) Recent advances in Chlamydomonas transgenics. Protist 149:23–27

    Article  Google Scholar 

  • Lumbreras V, Stevens DR, Purton S (1998) Efficient foreign gene expression in Chlamydomonas reinhardtii mediated by an endogenous intron. Plant J 14:441–147

    Article  CAS  Google Scholar 

  • Ma JKC, Hiatt A (1996) Expressing antibodies in plants for immunotherapy. In: Owen MRL, Pen P (eds) Transgenic plants: a production system for industrial and pharmaceutical proteins. Wiley, London, pp 229–243

    Google Scholar 

  • Ma JKC, Hikmat BY, Wycoff K, Vine ND, Chargelegue D, Yu L, Hein MB, Lehner T (1998) Characterisation of a recombinant plant monoclonal secretory antibody and preventive immunotherapy in humans. Nat Med 4:601–606

    Article  PubMed  CAS  Google Scholar 

  • Mason HS, Lam DM, Arntzen CJ (1992) Expression of hepatitis B surface antigen in transgenic plants. Proc Natl Acad Sci USA 89:11745–11749

    PubMed  CAS  Google Scholar 

  • Mason HS, Arntzen CJ (1995) Transgenic plants as vaccine production systems. Trends Biotechnol 13:388–392

    Article  PubMed  CAS  Google Scholar 

  • Masuda T, Tanaka A, Melis A (2003) Chlorophyll antenna size adjustments by irradiance in Dunaliella salina involve coordinate regulation of chlorophyll a oxygenase (CAO) and Lhcb gene expression. Plant Mol Biol 51:757–771

    Article  PubMed  CAS  Google Scholar 

  • Matsuzaki M, Misumi O, Shin-I T, Maruyama S, Takahara M, Miyagishima S, Mori T, Nishida K, Yagisawa F, Nishida K, Yoshida Y, Nishimura Y, Nakao S, Kobayashi T, Momoyama Y, Higashiyama T, Minoda A, Sano M, Nomoto H, Oishi K, Hayashi H, Ohta F, Nishizaka S, Haga S, Miura S, Morishita T, Kabeya Y, Terasawa K, Suzuki Y, Ishii Y, Asakawa S, Takano H, Ohta N, Kuroiwa H, Tanaka K, Shimizu N, Sugano S, Sato N, Nozaki H, Ogasawara N, Kohara Y, Kuroiwa T (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428:653–657

    Article  PubMed  CAS  Google Scholar 

  • Mayfield SP, Franklin SE, Lerner RA (2003) Expression and assembly of a fully active antibody in algae. Proc Natl Acad Sci USA 100:438–442

    Article  PubMed  CAS  Google Scholar 

  • Mayfield SP, Schultz J (2004) Development of a luciferase reporter gene, luxCt, for Chlamydomonas reinhardtii chloroplast. Plant J 37:449–458

    Article  PubMed  CAS  Google Scholar 

  • Melis A, Neidhardt J, Benemann JR (1999) Dunaliella salina (Chlorophyta) with small chlorophyll antenna sizes exhibit higher photosynthetic productivities and photon use efficiencies than normally pigmented cells. J Appl Phycol 10:515–525

    Article  Google Scholar 

  • Melis A, Zhang L, Forestier M, Ghiradi ML, Seibert M (2000) Sustained hydrogen gas production upon reversible inactivation of oxygen evolution in the green alga Chlamydomonas reinhardtii. Plant Physiol 122:127–135

    Article  PubMed  CAS  Google Scholar 

  • Miele L (1997) Plants as bioreactors for biopharmaceuticals: regulatory considerations. Trends Biotechnol 15:45–50

    Article  PubMed  CAS  Google Scholar 

  • 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 45:667–671

    Article  PubMed  CAS  Google Scholar 

  • Mitra A, Higgins DW (1994) The Chlorella virus adenine methyltransferase gene promoter is a strong promoter in plants. Plant Mol Biol 26:85–93

    Article  PubMed  CAS  Google Scholar 

  • Moore RE (1996) Cyclic peptides and depsipeptides from cyanobacteria: a review. J Ind Microbiol 16:134–143

    Article  PubMed  CAS  Google Scholar 

  • Mor TS, Sternfeld M, Soreq H, Arntzen CJ, Mason HS (2001) Expression of recombinant human acetylcholinesterase in transgenic tomato plants. Biotechnol Bioeng 75:259–266

    Article  PubMed  CAS  Google Scholar 

  • Nakajima Y, Ueda R (2000) The effect of reducing light-harvesting pigment on marine microalgal productivity. J Appl Phycol 12:285–290

    Article  CAS  Google Scholar 

  • 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 14:4011–4019

    PubMed  CAS  Google Scholar 

  • Ördög V, Stirk WA, Lenobel R, Bancírová M, Strnad M, van Staden J, Szigeti J, Németh L (2004) Screening microalgae for some potentially useful agricultural and pharmaceutical secondary metabolites. J Appl Phycol 16:309–314

    Article  Google Scholar 

  • Polle JEW, Benemann JR, Tanaka A, Melis A (2000) Photosynthetic apparatus organisation and function in the wild type and a chlorophyll b-less mutant of Chlamydomonas reinhardtii. Dependence on carbon source. Planta 211:335–344

    Article  PubMed  CAS  Google Scholar 

  • Ramirez N, Ayala M, Lorenzo D, Palenzuela D, Herrera L, Doreste V, Perez M, Gavilond JV, Oramas P (2002) Expression of a single-chain Fv antibody fragment specific for the hepatitis B surface antigen in transgenic tobacco plants. Transgenic Res 11:61–64

    Article  PubMed  CAS  Google Scholar 

  • 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 236:235–244

    Article  PubMed  CAS  Google Scholar 

  • Randolph-Anderson BL, Sato R, Johnson AM, Harris EH, Hauser CR, Oeda K, Ishige F, Nishio S, Gillham NW, Boynton JE (1998) Isolation and characterization of a mutant protoporphyrinogen oxidase gene from Chlamydomonas reinhardtii conferring resistance to porphyric herbicides. Plant Mol Biol 38:839–859

    Article  PubMed  CAS  Google Scholar 

  • Rayon C, Cabanes-Macheteau M, Loutelie-Bourhis C, Saliot-Maire I, Lemoine J, Reiter WD, Lerouge P, Faye L (1999) Characterisation of M-glycans from Arabidopsis thaliana. Application to a fucose-deficient mutant of Arabidopsis. Science 261:1032–1035

    Google Scholar 

  • Reed ML, Wilson SK, Sutton CA, Hanson MR (2001) High-level expression of a synthetic red-shifted GFP coding region incorporated into transgenic chloroplasts. Plant J 27:257–265

    Article  PubMed  CAS  Google Scholar 

  • Rhame LG, Tan MW, Le L, Wong SM, Tompkins RG, Calderwood SB, Ausubel FM (1997) Use of model plant hosts to identify Pseudomonas aeruginosa virulence factors. Proc Natl Acad Sci USA 94:13245–13250

    Article  PubMed  Google Scholar 

  • Ruiz-Binder NE, Geimer S, Melkonian M (2002) In vivo localisation of centrin in the green alga Chlamydomonas reinhardtii. Cell Motil Cytoskeleton 52:43–55

    Article  PubMed  CAS  Google Scholar 

  • 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 91:5080–5084

    PubMed  CAS  Google Scholar 

  • Schutt C, Furll B, Stelter F, Jack RS, Witt S (1997) CHO transfectants produce large amounts of recombinant protein in suspension culture. J Immunol Methods 204:99–102

    Article  PubMed  CAS  Google Scholar 

  • Schroda M, Blocker D, Beck CF (2000) The HSP70A promoter as a tool for the improved expression of transgenes in Chlamydomonas. Plant J 21:121–131

    Article  PubMed  CAS  Google Scholar 

  • Schwartz RE, Hirsch CF, Sesin DF, Flor JE, Chartrain M, Fromtling RE, Harris GH, Salvatore MJ, Liesch JM, Yudin K (1990) Pharmaceuticals from cultured algae. J Ind Microbiol 5:113–124

    Article  CAS  Google Scholar 

  • Scott MR, Will R, Ironside J, Nguyen HO, Tremblay P, DeArmond SJ, Prusiner SB (1999) Compelling transgenic evidence for transmission of bovine spongiform encephalopathy prions to humans. Proc Natl Acad Sci USA 96:15137–15142

    Article  PubMed  CAS  Google Scholar 

  • Shimizu Y (1996) Microalgal metabolites: a new perspective. Ann Rev Microbiol 50:431–465

    Article  CAS  Google Scholar 

  • Shimogawara K, Fujiwara S, Grossman A, Usuda H (1998) High-efficiency transformation of Chlamydomonas reinhardtii by electroporation. Genetics 148:1821–1828

    PubMed  CAS  Google Scholar 

  • Sijmons PC, Dekker BMM, Schrammeijer B, Verwoerd TC, van den Elzen PJM, Hoekema A (1990) Production of correctly processed human serum albumin in transgenic plants. Bio/Technology 8:217–221

    Article  PubMed  CAS  Google Scholar 

  • Siripornadulsil S, Traina S, Verma DPS, Sayre RT (2002) Molecular mechanisms of proline-mediated tolerance to toxic heavy metals in transgenic microalgae. Plant Cell 14:2837–2847

    Article  PubMed  CAS  Google Scholar 

  • 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 277:221–229

    Article  PubMed  CAS  Google Scholar 

  • Staub JM, Garcia B, Graves J, Hajdukiewicz PTJ, Hunter P, Nehra N, Paradakar V, Schlittler M, Carroll JA, Spatola L, Ward D, Ye G, Russell DA (2000) High-yield production of a human therapeutic protein in tobacco chloroplasts. Nat Biotechnol 18:333–338

    Article  PubMed  CAS  Google Scholar 

  • Stevens DR, Rochaix JD, Purton S (1996) The bacterial phleomycin resistance gene ble as a dominant selectable marker in Chlamydomonas. Mol Gen Genet 251:23–30

    Article  PubMed  CAS  Google Scholar 

  • Stevens DR, Purton S (1997) Genetic engineering of eukaryotic algae: progress and prospects. J Phycol 33:713–722

    Article  CAS  Google Scholar 

  • Streatfield SJ, Lane JR, Brooks CA, Barker DK, Poage ML, Mayor JM, Lamphear BJ, Drees CF, Jilka JM, Hood EE, Howard JA (2003) Corn as a production system for human and animal vaccines. Vaccine 21:812–815

    Article  PubMed  CAS  Google Scholar 

  • Sun M, Qian K, Su N, Chang H, Liu J, Chen G (2003) Foot-and-mouth disease virus VP1 protein fused with cholera toxin B subunit expressed in Chlamydomonas reinhardtii chloroplast. Biotechnol Lett 25:1087–1092

    Article  PubMed  CAS  Google Scholar 

  • Swartz JR (2001) Advances in Escherichia coli production of therapeutic proteins. Curr Opin Biotechnol 12:195–201

    Article  PubMed  CAS  Google Scholar 

  • ten Lohuis MR, Miller DJ (1998) Genetic transformation of dinoflagellates (Amphidinium and Symbiodinium): expression of GUS in microalgae using heterologous promoter constructs. Plant J 13:427–435

    Article  Google Scholar 

  • Teng C, Qin S, Liu J, Yu D, Liang C, Tseng C (2002) Transient expression of lacZ in bombarded unicellular green alga Haematococcus pluvialis. J Appl Phycol 14:495–500

    Article  Google Scholar 

  • Tregoning JS, Nixon P, Kuroda H, Svab Z, Clare S, Bowe F, Fairweather N, Ytterberg J, van Wijk KJ, Dougan G, Maliga P (2003) Expression of tetanus toxin Fragment C in tobacco chloroplasts. Nucleic Acids Res 31:1174–1179

    Article  PubMed  CAS  Google Scholar 

  • von Schaewen A, Sturm A, O'Neill J, Chrispeels MJ (1993) Isolation of a mutant Arabidopsis plant that lacks N-acetylglucosaminyltransferase I is unable to synthesise Golgi-modified complex N-linked glycans. Plant Physiol 102:1109–1118

    Article  PubMed  Google Scholar 

  • Wall RJ, Hawk HW, Nel N (1992) Making transgenic livestock: Genetic engineering on a large scale. J Cell Biochem 49:113–120

    Article  PubMed  CAS  Google Scholar 

  • Wee EQ, Sherrier DJ, Prime TA, Dupree P (1998) Targeting of active sialyltransferase to the plant Golgi apparatus. Plant Cell 10:1759–1768

    Article  PubMed  CAS  Google Scholar 

  • Wenderoth I, von Schaewen A (2000) Isolation and characterisation of plant N-acetylglucosaminyltransferase I (GnTI) cDNA sequences. Functional analyses in the Arabidopsis cgl mutant and in antisense plants. Plant Physiol 123:1097–1108

    Article  PubMed  CAS  Google Scholar 

  • 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 Pycol 36:379–386

    CAS  Google Scholar 

  • Zaslavskaia LA, Lippmeier JC, Shih C, Ehrhardt D, Grossman AR, Apt KE (2001) Trophic conversion of an obligate photoautotrophic organism through metabolic engineering. Science 292:2073–2075

    PubMed  CAS  Google Scholar 

  • Zhang L, Happe T, Melis A (2002) Biochemical and morphological characterisation of sulphur-deprived and H2-producing Chlamydomonas reinhardtii (green alga). Planta 214:552–561

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Cluster for Molecular Biotechnology, Science Research Centre and CRC for Diagnostics, Queensland University of Technology, GPO Box 2434, Brisbane, QLD, Australia, 4000

    Tara L. Walker, Douglas K. Becker & Chris Collet

  2. Department of Biology, University College London, Gower Street, London, WC1E 6BT, United Kingdom

    Saul Purton

Authors
  1. Tara L. Walker
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  2. Saul Purton
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  3. Douglas K. Becker
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  4. Chris Collet
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Correspondence to Chris Collet.

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Communicated by P.P. Kumar

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Walker, T.L., Purton, S., Becker, D.K. et al. Microalgae as bioreactors. Plant Cell Rep 24, 629–641 (2005). https://doi.org/10.1007/s00299-005-0004-6

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  • DOI: https://doi.org/10.1007/s00299-005-0004-6

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