413
Views
5
CrossRef citations to date
0
Altmetric
Review

Engineering pathways to biofuels in photoautotrophic microorganisms

Pages 67-78 | Published online: 09 Apr 2014

References

  • Falkowski P. Ocean science: the power of plankton. Nature483,S17–S20 (2012).
  • Bloom DE. 7 billion and counting. Science333,562–569 (2011).
  • Blankenship RE, Tiede DM, Barber J et al. Comparing photosynthetic and photovoltaic efficiencies and recognizing the potential for improvement. Science332,805–809 (2011).
  • Dismukes GC, Carrieri D, Bennette N, Ananyev GM, Posewitz MC. Aquatic phototrophs: efficient alternatives to land-based crops for biofuels. Curr. Opin. Biotechnol.19,235–240 (2008).
  • Hu Q, Sommerfeld M, Jarvis E et al. Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J.54,621–639 (2008).
  • Work VH, D’Adamo S, Radakovits R, Jinkerson RE, Posewitz MC. Improving photosynthesis and metabolic networks for the competitive production of phototroph-derived biofuels. Curr. Opin. Biotechnol.23,290–297 (2012).
  • Merchant SS, Kropat J, Liu B, Shaw J, Warakanont J. TAG, you’re it! Chlamydomonas as a reference organism for understanding algal triacylglycerol accumulation. Curr. Opin. Biotechnol.23,352–363 (2012).
  • Radakovits R, Jinkerson RE, Darzins A, Posewitz MC. Genetic engineering of algae for enhanced biofuel production. Eukaryot. Cell9,486–501 (2010).
  • Mitra M, Melis A. Optical properties of microalgae for enhanced biofuels production. Opt. Express16,21807–21820 (2008).
  • Huang HH, Camsund D, Lindblad P, Heidorn T. Design and characterization of molecular tools for a synthetic biology approach towards developing cyanobacterial biotechnology. Nucleic Acids Res.38,2577–2593 (2010).
  • Lindblad P, Lindberg P, Oliveira P, Stensjo K, Heidorn T. Design, engineering, and construction of photosynthetic microbial cell factories for renewable solar fuel production. Ambio41(Suppl. 2),163–168 (2012).
  • Rosgaard L, de Porcellinis AJ, Jacobsen JH, Frigaard NU, Sakuragi Y. Bioengineering of carbon fixation, biofuels, and biochemicals in cyanobacteria and plants. J. Biotechnol.162,134–147 (2012).
  • Voelker TA, Davies HM. Alteration of the specificity and regulation of fatty acid synthesis of Escherichia coli by expression of a plant medium-chain acyl-acyl carrier protein thioesterase. J. Bacteriol.176,7320–7327 (1994).
  • Voelker TA, Worrell AC, Anderson L et al. Fatty acid biosynthesis redirected to medium chains in transgenic oilseed plants. Science257,72–74 (1992).
  • Yuan L, Voelker TA, Hawkins DJ. Modification of the substrate specificity of an acyl-acyl carrier protein thioesterase by protein engineering. Proc. Natl Acad. Sci. USA92,10639–10643 (1995).
  • Dehesh K, Jones A, Knutzon DS, Voelker TA. Production of high levels of 8:0 and 10:0 fatty acids in transgenic canola by overexpression of Ch FatB2, a thioesterase cDNA from Cuphea hookeriana. Plant J.9,167–172 (1996).
  • Jiang P, Cronan JE Jr. Inhibition of fatty acid synthesis in Escherichia coli in the absence of phospholipid synthesis and release of inhibition by thioesterase action. J. Bacteriol.176,2814–2821 (1994).
  • Cho H, Cronan JE Jr. Defective export of a periplasmic enzyme disrupts regulation of fatty acid synthesis. J. Biol. Chem.270,4216–4219 (1995).
  • Ruffing AM, Jones HD. Physiological effects of free fatty acid production in genetically engineered Synechococcus elongatus PCC 7942. Biotechnol. Bioeng.109,2190–2199 (2012).
  • Desbois AP, Smith VJ. Antibacterial free fatty acids: activities, mechanisms of action and biotechnological potential. Appl. Microbiol. Biotechnol.85,1629–1642 (2010).
  • Liu X, Sheng J, Curtiss R 3rd. Fatty acid production in genetically modified cyanobacteria. Proc. Natl Acad. Sci. USA108,6899–6904 (2011).
  • Liu T, Vora H, Khosla C. Quantitative analysis and engineering of fatty acid biosynthesis in E. coli. Metab. Eng.12,378–386 (2010).
  • Lu X, Vora H, Khosla C. Overproduction of free fatty acids in E. coli: implications for biodiesel production. Metab. Eng.10,333–339 (2008).
  • Kaczmarzyk D, Fulda M. Fatty acid activation in cyanobacteria mediated by acyl-acyl carrier protein synthetase enables fatty acid recycling. Plant Physiol.152,1598–1610 (2010).
  • Kaiser BK, Carleton M, Hickman JW et al. Fatty aldehydes in cyanobacteria are a metabolically flexible precursor for a diversity of biofuel products. PLoS ONE8,e58307 (2013).
  • Radakovits R, Eduafo PM, Posewitz MC. Genetic engineering of fatty acid chain length in Phaeodactylum tricornutum. Metab. Eng.13,89–95 (2011).
  • Schirmer A, Rude MA, Li X, Popova E, del Cardayre SB. Microbial biosynthesis of alkanes. Science329,559–562 (2010).
  • Warui DM, Li N, Norgaard H, Krebs C, Bollinger JM Jr, Booker SJ. Detection of formate, rather than carbon monoxide, as the stoichiometric coproduct in conversion of fatty aldehydes to alkanes by a cyanobacterial aldehyde decarbonylase. J. Am. Chem. Soc.133,3316–3319 (2011).
  • Paul B, Das D, Ellington B, Marsh EN. Probing the mechanism of cyanobacterial aldehyde decarbonylase using a cyclopropyl aldehyde. J. Am. Chem. Soc.135,5234–5237 (2013).
  • Qiu Y, Tittiger C, Wicker-Thomas C et al. An insect-specific P450 oxidative decarbonylase for cuticular hydrocarbon biosynthesis. Proc. Natl Acad. Sci. USA109,14858–14863 (2012).
  • Bourdenx B, Bernard A, Domergue F et al. Overexpression of Arabidopsis ECERIFERUM1 promotes wax very-long-chain alkane biosynthesis and influences plant response to biotic and abiotic stresses. Plant Physiol.156,29–45 (2011).
  • Dennis MW, Kolattukudy PE. Alkane biosynthesis by decarbonylation of aldehyde catalyzed by a microsomal preparation from Botryococcus braunii. Arch. Biochem. Biophys.287,268–275 (1991).
  • Wang W, Liu X, Lu X. Engineering cyanobacteria to improve photosynthetic production of alka(e)nes. Biotechnol. Biofuels6,69 (2013).
  • Mendez-Perez D, Begemann MB, Pfleger BF. Modular synthase-encoding gene involved in alpha-olefin biosynthesis in Synechococcus sp. strain PCC 7002. Appl. Environ. Microbiol.77,4264–4267 (2011).
  • Reiser S, Somerville C. Isolation of mutants of Acinetobacter calcoaceticus deficient in wax ester synthesis and complementation of one mutation with a gene encoding a fatty acyl coenzyme A reductase. J. Bacteriol.179,2969–2975 (1997).
  • Wahlen BD, Oswald WS, Seefeldt LC, Barney BM. Purification, characterization, and potential bacterial wax production role of an NADPH-dependent fatty aldehyde reductase from Marinobacter aquaeolei VT8. Appl. Environ. Microbiol.75,2758–2764 (2009).
  • Hofvander P, Doan TT, Hamberg M. A prokaryotic acyl-CoA reductase performing reduction of fatty acyl-CoA to fatty alcohol. FEBS Lett.585,3538–3543 (2011).
  • Rowland O, Zheng H, Hepworth SR, Lam P, Jetter R, Kunst L. CER4 encodes an alcohol-forming fatty acyl-coenzyme A reductase involved in cuticular wax production in Arabidopsis. Plant Physiol.142,866–877 (2006).
  • Willis RM, Wahlen BD, Seefeldt LC, Barney BM. Characterization of a fatty acyl-CoA reductase from Marinobacter aquaeolei VT8: a bacterial enzyme catalyzing the reduction of fatty acyl-CoA to fatty alcohol. Biochemistry50,10550–10558 (2011).
  • Tan X, Yao L, Gao Q, Wang W, Qi F, Lu X. Photosynthesis driven conversion of carbon dioxide to fatty alcohols and hydrocarbons in cyanobacteria. Metab. Eng.13,169–176 (2011).
  • Gao Q, Wang W, Zhao H, Lu X. Effects of fatty acid activation on photosynthetic production of fatty acid-based biofuels in Synechocystis sp. PCC6803. Biotechnol. Biofuels5,17 (2012).
  • Kalscheuer R, Stolting T, Steinbuchel A. Microdiesel: Escherichia coli engineered for fuel production. Microbiology152,2529–2536 (2006).
  • Steen EJ, Kang Y, Bokinsky G et al. Microbial production of fatty-acid-derived fuels and chemicals from plant biomass. Nature463,559–562 (2010).
  • Akhtar MK, Turner NJ, Jones PR. Carboxylic acid reductase is a versatile enzyme for the conversion of fatty acids into fuels and chemical commodities. Proc. Natl Acad. Sci. USA110,87–92 (2013).
  • Venkitasubramanian P, Daniels L, Rosazza JP. Reduction of carboxylic acids by Nocardia aldehyde oxidoreductase requires a phosphopantetheinylated enzyme. J. Biol. Chem.282,478–485 (2007).
  • Behal RH, Buxton DB, Robertson JG, Olson MS. Regulation of the pyruvate dehydrogenase multienzyme complex. Annu. Rev. Nutr.13,497–520 (1993).
  • Brownsey RW, Boone AN, Elliott JE, Kulpa JE, Lee WM. Regulation of acetyl-CoA carboxylase. Biochem. Soc. Trans.34,223–227 (2006).
  • Ke J, Behal RH, Back SL, Nikolau BJ, Wurtele ES, Oliver DJ. The role of pyruvate dehydrogenase and acetyl-coenzyme A synthetase in fatty acid synthesis in developing Arabidopsis seeds. Plant Physiol.123,497–508 (2000).
  • Soo PC, Horng YT, Lai MJ et al. Pirin regulates pyruvate catabolism by interacting with the pyruvate dehydrogenase E1 subunit and modulating pyruvate dehydrogenase activity. J. Bacteriol.189,109–118 (2007).
  • Lim L, Linka M, Mullin KA, Weber APM, McFadden GI. The carbon and energy sources of the non-photosynthetic plastid in the malaria parasite. FEBS Lett.584,549–554 (2010).
  • Ohlrogge J, Pollard M, Bao X et al. Fatty acid synthesis: from CO2 to functional genomics. Biochem. Soc. Trans.28,567–574 (2000).
  • Oliver DJ, Nikolau BJ, Wurtele ES. Acetyl-CoA – Life at the metabolic nexus. Plant Sci.176,597–601 (2009).
  • Pleite R, Pike MJ, Garces R, Martinez-Force E, Rawsthorne S. The sources of carbon and reducing power for fatty acid synthesis in the heterotrophic plastids of developing sunflower (Helianthus annuus L.) embryos. J. Exp.Bot.56,1297–1303 (2005).
  • Rawsthorne S, Kang F, Eastmond PJ. Carbon flux to fatty acids in plastids. In: Regulation of Primary Metabolic Pathways in Plants. Springer, The Netherlands, 137–157 (1999).
  • Roesler K, Shintani D, Savage L, Boddupalli S, Ohlrogge J. Targeting of the Arabidopsis homomeric acetyl-coenzyme A carboxylase to plastids of rapeseeds. Plant Physiol.113,75–81 (1997).
  • Tovar-Mendez A, Miernyk JA, Randall DD. Regulation of pyruvate dehydrogenase complex activity in plant cells. Eur. J. Biochem.270,1043–1049 (2003).
  • Yasuno R, Wada H. The biosynthetic pathway for lipoic acid is present in plastids and mitochondria in Arabidopsis thaliana. FEBS Lett.517,110–114 (2002).
  • Huerlimann H, Heimann K. Comprehensive guide to acetyl-carboxylases in algae. Crit. Rev. Biotechnol.33,49–65 (2012).
  • Keeling CI, Bohlmann J. Plant terpenoids. In: Natural Products in Chemical Biology. Civjan N (Ed.). John Wiley and Sons, NY, USA, 121–142 (2002).
  • Chen F, Tholl D, Bohlmann J, Pichersky E. The family of terpene synthases in plants: a mid-size family of genes for specialized metabolism that is highly diversified throughout the kingdom. Plant J.66,212–229 (2011).
  • Bohlmann J, Phillips M, Ramachandiran V, Katoh S, Croteau R. cDNA cloning, characterization, and functional expression of four new monoterpene synthase members of the Tpsd gene family from grand fir (Abies grandis). Arch. Biochem. Biophys.368,232–243 (1999).
  • Demissie ZA, Sarker LS, Mahmoud SS. Cloning and functional characterization of beta-phellandrene synthase from Lavandula angustifolia. Planta233,685–696 (2011).
  • Schilmiller AL, Schauvinhold I, Larson M et al. Monoterpenes in the glandular trichomes of tomato are synthesized from a neryl diphosphate precursor rather than geranyl diphosphate. Proc. Natl Acad. Sci. USA106,10865–10870 (2009).
  • Peralta-Yahya PP, Ouellet M, Chan R, Mukhopadhyay A, Keasling JD, Lee TS. Identification and microbial production of a terpene-based advanced biofuel. Nat. Commun.2,483 (2011).
  • Bohlmann J, Keeling CI. Terpenoid biomaterials. Plant J.54,656–669 (2008).
  • Angermayr SA, Hellingwerf KJ, Lindblad P, de Mattos MJ. Energy biotechnology with cyanobacteria. Curr. Opin. Biotechnol.20,257–263 (2009).
  • Melis A. Solar energy conversion efficiencies in photosynthesis: minimizing the chlorophyll antennae to maximize efficiency. Plant Sci.177,272–280 (2009).
  • Melis A. Photosynthesis-to-fuels: from sunlight to hydrogen, isoprene, and botryococcene production. Energy Environ. Sci.5,5531–5539 (2012).
  • Lindberg P, Park S, Melis A. Engineering a platform for photosynthetic isoprene production in cyanobacteria, using Synechocystis as the model organism. Metab. Eng.12,70–79 (2010).
  • Bentley FK, Melis A. Diffusion-based process for carbon dioxide uptake and isoprene emission in gaseous/aqueous two-phase photobioreactors by photosynthetic microorganisms. Biotechnol. Bioeng.109,100–109 (2012).
  • Reinsvold RE, Jinkerson RE, Radakovits R, Posewitz MC, Basu C. The production of the sesquiterpene β-caryophyllene in a transgenic strain of the cyanobacterium Synechocystis. J. Plant Physiol.168,848–852 (2011).
  • Bentley FK, Garcia-Cerdan JG, Chen H-C, Melis A. Paradigm of monoterpenes (b-phellandrene) hydrocarbons production via photosynthesis in cyanobacteria. Bioeng. Res.6,917 (2013).
  • Lange BM, Rujan T, Martin W, Croteau R. Isoprenoid biosynthesis: the evolution of two ancient and distinct pathways across genomes. Proc. Natl Acad. Sci. USA97,13172–13177 (2000).
  • Lee PC, Schmidt-Dannert C. Metabolic engineering towards biotechnological production of carotenoids in microorganisms. Appl. Microbiol. Biotechnol.60,1–11 (2002).
  • Lichtenthaler HK. Non-mevalonate isoprenoid biosynthesis: enzymes, genes and inhibitors. Biochem. Soc. Trans.28,785–789 (2000).
  • Rohmer M. The discovery of a mevalonate-independent pathway for isoprenoid biosynthesis in bacteria, algae and higher plants. Nat. Prod. Rep.16,565–574 (1999).
  • Rohmer M, Seemann M, Horbach S, Bringer-Meyer S, Sahm H. Glyceraldehyde 3-phosphate and pyruvate as precursors of isoprenic units in an alternative non-mevalonate pathway for terpenoid biosynthesis. J. Am. Chem. Soc.118,2564–2566 (1996).
  • Farmer WR, Liao JC. Precursor balancing for metabolic engineering of lycopene production in Escherichia coli. Biotechnol. Prog.17,57–61 (2001).
  • Kim SW, Keasling JD. Metabolic engineering of the nonmevalonate isopentenyl diphosphate synthesis pathway in Escherichia coli enhances lycopene production. Biotechnol. Bioeng.72,408–415 (2001).
  • Leonard E, Ajikumar PK, Thayer K et al. Combining metabolic and protein engineering of a terpenoid biosynthetic pathway for overproduction and selectivity control. Proc. Natl Acad. Sci. USA107,13654–13659 (2010).
  • Zurbriggen A, Kirst H, Melis A. Isoprene production via the mevalonic acid pathway in Escherichia coli (bacteria). Bioenergy Res.5,814–828 (2012).
  • Miziorko HM. Enzymes of the mevalonate pathway of isoprenoid biosynthesis. Arch. Biochem. Biophys.505,131–143 (2011).
  • Martin VJ, Pitera DJ, Withers ST, Newman JD, Keasling JD. Engineering a mevalonate pathway in Escherichia coli for production of terpenoids. Nat. Biotechnol.21,796–802 (2003).
  • Vadali RV, Fu Y, Bennett GN, San KY. Enhanced lycopene productivity by manipulation of carbon flow to isopentenyl diphosphate in Escherichia coli. Biotechnol. Prog.21,1558–1561 (2005).
  • Yoon SH, Lee SH, Das A et al. Combinatorial expression of bacterial whole mevalonate pathway for the production of beta-carotene in E. coli. J. Biotechnol.140,218–226 (2009).
  • Lombard J, Moreira D. Origins and early evolution of the mevalonate pathway of isoprenoid biosynthesis in the three domains of life. Mol. Biol. Evol.28,87–99 (2011).
  • Choi SP, Nguyen MT, Sim SJ. Enzymatic pretreatment of Chlamydomonas reinhardtii biomass for ethanol production. Bioresour. Technol.101,5330–5336 (2010).
  • Nguyen MT, Choi SP, Lee J, Lee JH, Sim SJ. Hydrothermal acid pretreatment of Chlamydomonas reinhardtii biomass for ethanol production. J. Microbiol. Biotechnol.19,161–166 (2009).
  • Catalanotti C, Yang W, Posewitz MC, Grossman AR. Fermentation metabolism and its evolution in algae. Front. Plant Sci.4,150 (2013).
  • Dubini A, Mus F, Seibert M, Grossman AR, Posewitz MC. Flexibility in anaerobic metabolism as revealed in a mutant of Chlamydomonas reinhardtii lacking hydrogenase activity. J. Biol. Chem.284,7201–7213 (2009).
  • Deng MD, Coleman JR. Ethanol synthesis by genetic engineering in cyanobacteria. Appl. Environ. Microbiol.65,523–528 (1999).
  • Luo D, Hu Z, Choi DG, Thomas VM, Realff MJ, Chance RR. Life cycle energy and greenhouse gas emissions for an ethanol production process based on blue-green algae. Environ. Sci. Technol.44,8670–8677 (2010).
  • Cai X, Bennett GN. Improving the Clostridium acetobutylicum butanol fermentation by engineering the strain for co-production of riboflavin. J. Ind. Microbiol. Biotechnol.38,1013–1025 (2011).
  • Connor MR, Liao JC. Microbial production of advanced transportation fuels in non-natural hosts. Curr. Opin. Biotechnol.20,307–315 (2009).
  • Huo YX, Cho KM, Rivera JG et al. Conversion of proteins into biofuels by engineering nitrogen flux. Nat. Biotechnol.29,346–351 (2011).
  • Atsumi S, Liao JC. Metabolic engineering for advanced biofuels production from Escherichia coli. Curr. Opin. Biotechnol.19,414–419 (2008).
  • Atsumi S, Hanai T, Liao JC. Non-fermentative pathways for synthesis of branched-chain higher alcohols as biofuels. Nature451,86–89 (2008).
  • Atsumi S, Higashide W, Liao JC. Direct photosynthetic recycling of carbon dioxide to isobutyraldehyde. Nat. Biotechnol.27,1177–1180 (2009).
  • Takahama K, Matsuoka M, Nagahama K, Ogawa T. Construction and analysis of a recombinant cyanobacterium expressing a chromosomally inserted gene for an ethylene-forming enzyme at the psbAI locus. J. Biosci. Bioeng.95,302–305 (2003).
  • Ungerer J, Tao L, Davis M, Ghirardi M, Maness PC, Yu JP. Sustained photosynthetic conversion of CO2 to ethylene in recombinant cyanobacterium Synechocystis 6803. Energy Environ. Sci.5,8998–9006 (2012).
  • Wang ZT, Ullrich N, Joo S, Waffenschmidt S, Goodenough U. Algal lipid bodies: stress induction, purification, and biochemical characterization in wild-type and starchless Chlamydomonas reinhardtii. Eukaryot. Cell8,1856–1868 (2009).
  • Work VH, Radakovits R, Jinkerson RE et al. Increased lipid accumulation in the Chlamydomonas reinhardtii sta7–10 starchless isoamylase mutant and increased carbohydrate synthesis in complemented strains. Eukaryot. Cell9,1251–1261 (2010).
  • Li Y, Han D, Hu G et al. Chlamydomonas starchless mutant defective in ADP-glucose pyrophosphorylase hyper-accumulates triacylglycerol. Metab. Eng.12,387–391 (2010).
  • Carrieri D, Paddock T, Maness PC, Seibert M, Yu J. Photo-catalytic conversion of carbon dioxide to organic acids by a recombinant cyanobacterium incapable of glycogen storage. Energy Environ. Sci.5,9457–9461 (2012).
  • Gründel M, Scheunemann R, Lockau W, Zilliges Y. Impaired glycogen synthesis causes metabolic overflow reactions and affects stress responses in the cyanobacterium Synechocystis sp. PCC 6803. Microbiology158,3032–3043 (2012).
  • Wang ZT, Ullrich N, Joo S, Waffenschmidt S, Goodenough U. Algal lipid bodies: stress induction, purification, and biochemical characterization in wild-type and starch-less Chlamydomonas reinhardtii. Eukaryot. Cell8,1856–1868 (2009).
  • Li Y, Han D, Hu G, Sommerfeld M, Hu Q. Inhibition of starch synthesis results in overproduction of lipids in Chlamydomonas reinhardtii. Biotechnol. Bioeng.107,258–268 (2010).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.