期刊论文详细信息
Biotechnology for Biofuels
Comparative energetics and kinetics of autotrophic lipid and starch metabolism in chlorophytic microalgae: implications for biomass and biofuel production
Sowmya Subramanian1  Amanda N Barry2  Shayani Pieris3  Richard T Sayre2 
[1] New Mexico Consortium, 100 Entrada Rd., Los Alamos, NM 87544, USA
[2] Bioscience Division, Los Alamos National Lab, M888, Los Alamos, NM 87545, USA
[3] Natural Sciences Division, Missouri Baptist University, One College Park Drive, St. Louis, MO 63141, USA
关键词: Cultivation;    Metabolism;    Biomass;    Photosynthesis;    Energetics;    Oil;    Starch;    Storage carbohydrate;    Plant;    Algae;    Biofuel;   
Others  :  797798
DOI  :  10.1186/1754-6834-6-150
 received in 2013-04-26, accepted in 2013-09-12,  发布年份 2013
PDF
【 摘 要 】

Due to the growing need to provide alternatives to fossil fuels as efficiently, economically, and sustainably as possible there has been growing interest in improved biofuel production systems. Biofuels produced from microalgae are a particularly attractive option since microalgae have production potentials that exceed the best terrestrial crops by 2 to 10-fold. In addition, autotrophically grown microalgae can capture CO2 from point sources reducing direct atmospheric greenhouse gas emissions. The enhanced biomass production potential of algae is attributed in part to the fact that every cell is photosynthetic. Regardless, overall biological energy capture, conversion, and storage in microalgae are inefficient with less than 8% conversion of solar into chemical energy achieved. In this review, we examine the thermodynamic and kinetic constraints associated with the autotrophic conversion of inorganic carbon into storage carbohydrate and oil, the dominant energy storage products in Chlorophytic microalgae. We discuss how thermodynamic restrictions including the loss of fixed carbon during acetyl CoA synthesis reduce the efficiency of carbon accumulation in lipids. In addition, kinetic limitations, such as the coupling of proton to electron transfer during plastoquinone reduction and oxidation and the slow rates of CO2 fixation by Rubisco reduce photosynthetic efficiency. In some cases, these kinetic limitations have been overcome by massive increases in the numbers of effective catalytic sites, e.g. the high Rubisco levels (mM) in chloroplasts. But in other cases, including the slow rate of plastoquinol oxidation, there has been no compensatory increase in the abundance of catalytically limiting protein complexes. Significantly, we show that the energetic requirements for producing oil and starch relative to the recoverable energy stored in these molecules are very similar on a per carbon basis. Presently, the overall rates of starch and lipid synthesis in microalgae are very poorly characterized. Increased understanding of the kinetic constraints of lipid and starch synthesis, accumulation and turnover would facilitate the design of improved biomass production systems.

【 授权许可】

   
2013 Subramanian et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20140706081438348.pdf 1088KB PDF download
Figure 4. 52KB Image download
Figure 3. 167KB Image download
Figure 2. 69KB Image download
Figure 1. 90KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

【 参考文献 】
  • [1]Khan SA, Rashmi J, Hussain MZ, Prasad S, Banerjee UC: Prospects of biodiesel production from microalgae in India. Renew Sustain Energy Rev 2009, 13(9):2361-2372.
  • [2]Sayre R: Microalgae: the potential for carbon capture. Bioscience 2010, 60(9):722-727.
  • [3]National Research Council: Sustainable Development of Algal Biofuels in the United States. Washington, DC: The National Academies Press; 2012.
  • [4]Bondioli P, Della Bella L, Rivolta G, Chini Zittelli G, Bassi N, Rodolfi L, Casini D, Prussi M, Chiaramonti D, Tredici MR: Oil production by the marine microalgae Nannochloropsis sp. F&M-M24 and Tetraselmis suecica F&M-M33. Bioresource technol 2012, 114:567-572.
  • [5]Mata TM, Martins AA, Caetano NS: Microalgae for biodiesel production and other applications: a review. Renew Sustain Energy Rev 2010, 14(1):217-232.
  • [6]Rodolfi L, Chini Zittelli G, Bassi N, Padovani G, Biondi N, Bonini G, Tredici MR: Microalgae for oil: strain selection, induction of lipid synthesis and outdoor mass cultivation in a low-cost photobioreactor. Biotechnol Bioeng 2009, 102(1):100-112.
  • [7]Xu H, Miao X, Wu Q: High quality biodiesel production from a microalga chlorella protothecoides by heterotrophic growth in fermenters. J Biotechnol 2006, 126(4):499-507.
  • [8]Chisti Y: Biodiesel from microalgae beats bioethanol. Trends Biotechnol 2008, 26(3):126-131.
  • [9]Wigmosta MS, Coleman AM, Skaggs RJ, Huesemann MH, Lane LJ: National microalgae biofuel production potential and resource demand. Water Resour Res 2011, 47(3):W00H04.
  • [10]Christenson L, Sims R: Production and harvesting of microalgae for wastewater treatment, biofuels, and bioproducts. Biotechnol Adv 2011, 29(6):686-702.
  • [11]Broekhuizen N, Park JBK, McBride GB, Craggs RJ: Modification, calibration and verification of the IWA river water quality model to simulate a pilot-scale high rate algal pond. Water Res 2012, 46(9):2911-2926.
  • [12]Richardson JW, Johnson MD, Outlaw JL: Economic comparison of open pond raceways to photo bio-reactors for profitable production of algae for transportation fuels in the Southwest. Algal Res 2012, 1(1):93-100.
  • [13]Liu J, Huang J, Sun Z, Zhong Y, Jiang Y, Chen F: Differential lipid and fatty acid profiles of photoautotrophic and heterotrophic chlorella zofingiensis: assessment of algal oils for biodiesel production. Bioresource Technol 2011, 102(1):106-110.
  • [14]Chen YH, Walker TH: Biomass and lipid production of heterotrophic microalgae chlorella protothecoides by using biodiesel-derived crude glycerol. Biotechnol Lett 2011, 33(10):1973-1983.
  • [15]Heredia-Arroyo T, Wei W, Hu B: Oil accumulation via heterotrophic/mixotrophic chlorella protothecoides. Appl Biochem Biotechnol 2010, 162(7):1978-1995.
  • [16]O’Grady J, Morgan J: Heterotrophic growth and lipid production of chlorella protothecoides on glycerol. Bioproc Biosyst Eng 2011, 34(1):121-125.
  • [17]Kosa M, Ragauskas AJ: Lipids from heterotrophic microbes: advances in metabolism research. Trends Biotechnol 2011, 29(2):53-61.
  • [18]Chen CY, Yeh KL, Aisyah R, Lee DJ, Chang JS: Cultivation, photobioreactor design and harvesting of microalgae for biodiesel production: a critical review. Bioresource Technol 2011, 102(1):71-81.
  • [19]Batan L, Quinn J, Willson B, Bradley T: Net energy and greenhouse gas emission evaluation of biodiesel derived from microalgae. Environ Sci Technol 2010, 44(20):7975-7980.
  • [20]Campbell PK, Beer T, Batten D: Life cycle assessment of biodiesel production from microalgae in ponds. Bioresource Technol 2011, 102(1):50-56.
  • [21]Illman AM, Scragg AH, Shales SW: Increase in chlorella strains calorific values when grown in low nitrogen medium. Enzyme Microbial Technol 2000, 27(8):631-635.
  • [22]Williams PJB, Laurens LML: Microalgae as biodiesel & biomass feedstocks: review & analysis of the biochemistry, energetics & economics. Energy Environ Sci 2010, 3(5):554-590.
  • [23]Sharma KK, Schuhmann H, Schenk PM: High lipid induction in microalgae for biodiesel production. Energies 2012, 5(5):1532-1553.
  • [24]Metting FB Jr: Biodiversity and application of microalgae. J Ind Microbiol 1996, 17(5–6):477-489.
  • [25]Spolaore P, Joannis-Cassan C, Duran E, Isambert A: Commercial applications of microalgae. J Biosci Bioeng 2006, 101(2):87-96.
  • [26]Cardol P, Forti G, Finazzi G: Regulation of electron transport in microalgae. Biochim Biophys Acta - Bioenergetics 2011, 1807(8):912-918.
  • [27]Radakovits R, Jinkerson RE, Darzins A, Posewitz MC: Genetic engineering of algae for enhanced biofuel production. Eukaryot Cell 2010, 9(4):486-501.
  • [28]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 2012, 23(3):290-297.
  • [29]Gokhale Z, Sayre RT: Photosystem II, A Structural Perspective. In The Chlamydomonas Sourcebook. Second edition. Edited by Stern DB. San Diego: Academic Press; 2009.
  • [30]Croce R, Muller MG, Bassi R, Holzwarth AR: Carotenoid-to-chlorophyll energy transfer in recombinant major light-harvesting complex (LHCII) of higher plants. I. Femtosecond transient absorption measurements. Biophys J 2001, 80(2):901-915.
  • [31]Ishizaki A, Fleming GR: Quantum coherence in photosynthetic light harvesting. Ann Rev Cond Matter Phys 2012, 3(1):333-361.
  • [32]Merkli M, Berman G, Sayre R: Electron transfer reactions: generalized spin-boson approach. J Math Chem 2013, 51:890-913.
  • [33]Perrine Z, Negi S, Sayre RT: Optimization of photosynthetic light energy utilization by microalgae. Algal Res 2012, 1:134-142.
  • [34]Lewis KLM, Ogilvie JP: Probing photosynthetic energy and charge transfer with Two-dimensional electronic spectroscopy. J Phys Chem Lett 2012, 3(4):503-510.
  • [35]Pawlowicz NP, Groot ML, van Stokkum IH, Breton J, van Grondelle R: Charge separation and energy transfer in the photosystem II core complex studied by femtosecond midinfrared spectroscopy. Biophys J 2007, 93(8):2732-2742.
  • [36]Stiehl HH, Witt HT: Quantitative treatment of the function of plastoquinone in phostosynthesis. Z Naturforsch B 1969, 24(12):1588-1598.
  • [37]Kirchhoff H, Mukherjee U, Galla HJ: Molecular architecture of the thylakoid membrane: lipid diffusion space for plastoquinone. Biochem 2002, 41(15):4872-4882.
  • [38]Harris GC, Königer M: The 'high’ concentrations of enzymes within the chloroplast. Photosynth Res 1997, 54(1):5-23.
  • [39]Govindjee G, Kern JF, Messinger J, Whitmarsh J: Photosystem II. Hoboken, NJ: John Wiley & Sons, Ltd; 2001.
  • [40]Johnson X, Alric J: Interaction between starch breakdown, acetate assimilation, and photosynthetic cyclic electron flow in chlamydomonas reinhardtii. JBiol Chem 2012, 287(31):26445-26452.
  • [41]Junesch U, Gräber P: The rate of ATP synthesis as a function of ΔpH in normal and dithiothreitol-modified chloroplasts. BBA - Bioenerg 1985, 809(3):429-434.
  • [42]Etzold C, Deckers-Hebestreit G, Altendorf K: Turnover number of Escherichia coli F0F1 ATP synthase for ATP synthesis in membrane vesicles. Eur J Biochem / FEBS 1997, 243(1–2):336-343.
  • [43]Kramer DM, Avenson TJ, Edwards GE: Dynamic flexibility in the light reactions of photosynthesis governed by both electron and proton transfer reactions. Trends Plant Sci 2004, 9(7):349-357.
  • [44]Yamori W, Takahashi S, Makino A, Price GD, Badger MR, von Caemmerer S: The roles of ATP synthase and the cytochrome b6/f complexes in limiting chloroplast electron transport and determining photosynthetic capacity. Plant Physiol 2011, 155(2):956-962.
  • [45]Baker NR, Harbinson J, Kramer DM: Determining the limitations and regulation of photosynthetic energy transduction in leaves. Plant Cell Eviron 2007, 30(9):1107-1125.
  • [46]Kanazawa A, Kramer DM: In vivo modulation of nonphotochemical exciton quenching (NPQ) by regulation of the chloroplast ATP synthase. Proc Natl Acad Sci U S A 2002, 99(20):12789-12794.
  • [47]Owens TG, Webb SP, Mets L, Alberte RS, Fleming GR: Antenna size dependence of fluorescence decay in the core antenna of photosystem I: estimates of charge separation and energy transfer rates. Proc Natl Acad Sci USA 1987, 84(6):1532-1536.
  • [48]Ley AC, Mauzerall DC: Absolute absorption cross-sections for photosystem II and the minimum quantum requirement for photosynthesis in chlorella vulgaris. BBA - Bioenerg 1982, 680(1):95-106.
  • [49]Muller P, Li XP, Niyogi KK: Non-photochemical quenching. A response to excess light energy. Plant Physiol 2001, 125(4):1558-1566.
  • [50]Melis A: Solar energy conversion efficiencies in photosynthesis: minimizing the chlorophyll antenna to maximize efficiency. Plant Sci 2009, 177(4):272-280.
  • [51]Björkman O, Demmig B: Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 1987, 170(4):489-504.
  • [52]Long SP, Postl WF, Bolhár-Nordenkampf HR: Quantum yields for uptake of carbon dioxide in C3 vascular plants of contrasting habitats and taxonomic groupings. Planta 1993, 189(2):226-234.
  • [53]Mussgnug JH, Thomas-Hall S, Rupprecht J, Foo A, Klassen V, McDowall A, Schenk PM, Kruse O, Hankamer B: Engineering photosynthetic light capture: impacts on improved solar energy to biomass conversion. Plant Biotechnol J 2007, 5(6):802-814.
  • [54]Polle J, Kanakagiri S-D, Melis A: tla1, a DNA insertional transformant of the green alga Chlamydomonas reinhardtii with a truncated light-harvesting chlorophyll antenna size. Planta 2003, 217(1):49-59.
  • [55]Spreitzer RJ, Salvucci ME: RUBISCO: structure, regulatory interactions, and possibilities for a better enzyme. Ann Rev Plant Biol 2002, 53(1):449-475.
  • [56]Wingler A, Lea PJ, Quick WP, Leegood RC: Photorespiration: metabolic pathways and their role in stress protection. Philos Trans R Soc Lond B Biol Sci 2000, 355(1402):1517-1529.
  • [57]Moroney JV, Ynalvez RA: Proposed carbon dioxide concentrating mechanism in chlamydomonas reinhardtii. Eukaryot Cell 2007, 6(8):1251-1259.
  • [58]Spalding MH: Microalgal carbon-dioxide-concentrating mechanisms: Chlamydomonas inorganic carbon transporters. J Exp Bot 2008, 59(7):1463-1473.
  • [59]Duanmu D, Miller AR, Horken KM, Weeks DP, Spalding MH: Knockdown of limiting-CO2–induced gene HLA3 decreases HCO3- transport and photosynthetic Ci affinity in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 2009, 106(14):5990-5995.
  • [60]Cardol P, Alric J, Girard-Bascou J, Franck F, Wollman F-A, Finazzi G: Impaired respiration discloses the physiological significance of state transitions in Chlamydomonas. Proc Natl Acad Sci USA 2009, 106(37):15979-15984.
  • [61]Miyagawa Y, Tamoi M, Shigeoka S: Overexpression of a cyanobacterial fructose-1,6-/sedoheptulose-1,7-bisphosphatase in tobacco enhances photosynthesis and growth. Nature Biotechnol 2001, 19(10):965-969.
  • [62]Schwender J, Ohlrogge J, Shachar-Hill Y: Understanding flux in plant metabolic networks. Curr Opin Plant Biol 2004, 7(3):309-317.
  • [63]Szecowka M, Heise R, Tohge T, Nunes-Nesi A, Vosloh D, Huege J, Feil R, Lunn J, Nikoloski Z, Stitt M, et al.: Metabolic fluxes in an illuminated Arabidopsis rosette. Plant Cell 2013, 25(2):694-714.
  • [64]Zhu XG, Long SP, Ort DR: Improving photosynthetic efficiency for greater yield. Ann Rev Plant Biol 2010, 61:235-261.
  • [65]Hohmann-Marriott MF, Blankenship RE: Evolution of photosynthesis. Ann Rev Plant Biol 2011, 62:515-548.
  • [66]Larkum AWD: Light Harvesting Systems in Algae. In Photosynthesis in Algae. Edited by Larkum AWD, Douglas SE, Raven JA. Netherlands: Kluwer Academic Publishers; 2003:277-282.
  • [67]Zouni A, Witt HT, Kern J, Fromme P, Krauss N, Saenger W, Orth P: Crystal structure of photosystem II from Synechococcus elongatus at 3.8 A resolution. Nature 2001, 409(6821):739-743.
  • [68]Kamiya N, Shen JR: Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-A resolution. Proc Natl Acad Sci USA 2003, 100(1):98-103.
  • [69]Liu Z, Yan H, Wang K, Kuang T, Zhang J, Gui L, An X, Chang W: Crystal structure of spinach major light-harvesting complex at 2.72 A resolution. Nature 2004, 428(6980):287-292.
  • [70]Ben-Shem A, Frolow F, Nelson N: Crystal structure of plant photosystem I. Nature 2003, 426(6967):630-635.
  • [71]Green BR, Durnford DG: The chlorophyll-carotenoid proteins of oxygenic photosynthesis. Ann Rev Plant Physiol Plant Mol Biol 1996, 47:685-714.
  • [72]Niyogi KK: photoprotection revisited: genetic and molecular approaches. Ann Rev Plant Physiol Plant Mol Biol 1999, 50:333-359.
  • [73]Aro EM, Virgin I, Andersson B: Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1993, 1143(2):113-134.
  • [74]Baker N: Photoinhibition of Photosynthesis. In Light as an Energy Source and Information Carrier in Plant Physiology, Volume 287. Edited by Jennings R, Zucchelli G, Ghetti F, Colombetti G. New York, NY: Springer US; 1996:89-97.
  • [75]Crimi M, Dorra D, Bosinger CS, Giuffra E, Holzwarth AR, Bassi R: Time-resolved fluorescence analysis of the recombinant photosystem II antenna complex CP29. Effects of zeaxanthin, pH and phosphorylation. Eur J Biochem / FEBS 2001, 268(2):260-267.
  • [76]Holt NE, Zigmantas D, Valkunas L, Li XP, Niyogi KK, Fleming GR: Carotenoid cation formation and the regulation of photosynthetic light harvesting. Science 2005, 307(5708):433-436.
  • [77]Avenson TJ, Ahn TK, Zigmantas D, Niyogi KK, Li Z, Ballottari M, Bassi R, Fleming GR: Zeaxanthin radical cation formation in minor light-harvesting complexes of higher plant antenna. J Biol Chem 2008, 283(6):3550-3558.
  • [78]Wiederrecht GP, Seibert M, Govindjee , Wasielewski MR: Femtosecond photodichroism studies of isolated photosystem II reaction centers. Proc Natl Acad Sci USA 1994, 91(19):8999-9003.
  • [79]Hillier W, Babcock GT: Photosynthetic reaction centers. Plant Physiol 2001, 125(1):33-37.
  • [80]Golbeck JH: Photosystem I: The Light-Driven Plastocyanin: Ferredoxin Oxidoreductase. Dordrecht: Springer; 2006.
  • [81]Emerson R: The quantum yield of photosynthesis. Annu Rev Plant Physiol 1958, 9(1):1-24.
  • [82]Govindjee : On the requirement of minimum number of four versus eight quanta of light for the evolution of one molecule of oxygen in photosynthesis: a historical note. Photosynth Res 1999, 59(2–3):249-254.
  • [83]Skillman JB: Quantum yield variation across the three pathways of photosynthesis: not yet out of the dark. J Exp Bot 2008, 59(7):1647-1661.
  • [84]Hogewoning SW, Wientjes E, Douwstra P, Trouwborst G, van Ieperen W, Croce R, Harbinson J: Photosynthetic quantum yield dynamics: from photosystems to leaves. Plant Cell 2012, 24(5):1921-1935.
  • [85]Singsaas EL, Ort DR, DeLucia EH: Variation in measured values of photosynthetic quantum yield in ecophysiological studies. Oecologia 2001, 128:15-23.
  • [86]Van Walraven HS, Strotmann H, Schwarz O, Rumberg B: The H+/ATP coupling ratio of the ATP synthase from thiol-modulated chloroplasts and two cyanobacterial strains is four. FEBS Lett 1996, 379(3):309-313.
  • [87]Turina P, Samoray D, Graber P: H+/ATP ratio of proton transport-coupled ATP synthesis and hydrolysis catalysed by CF0F1-liposomes. EMBO J 2003, 22(3):418-426.
  • [88]Steigmiller S, Turina P, Graber P: The thermodynamic H+/ATP ratios of the H+-ATPsynthases from chloroplasts and Escherichia coli. Proc Natl Acad Sci U S A 2008, 105(10):3745-3750.
  • [89]Seelert H, Poetsch A, Dencher NA, Engel A, Stahlberg H, Muller DJ: Structural biology. Proton-powered turbine of a plant motor. Nature 2000, 405(6785):418-419.
  • [90]Vollmar M, Schlieper D, Winn M, Buchner C, Groth G: Structure of the c14 rotor ring of the proton translocating chloroplast ATP synthase. J Biol Chem 2009, 284(27):18228-18235.
  • [91]Sacksteder CA, Kanazawa A, Jacoby ME, Kramer DM: The proton to electron stoichiometry of steady-state photosynthesis in living plants: a proton-pumping Q cycle is continuously engaged. Proc Natl Acad Sci USA 2000, 97(26):14283-14288.
  • [92]Jia H, Oguchi R, Hope AB, Barber J, Chow WS: Differential effects of severe water stress on linear and cyclic electron fluxes through photosystem I in spinach leaf discs in CO(2)-enriched air. Planta 2008, 228(5):803-812.
  • [93]Baker NR, Ort DR: Light and crop photosynthetic performance. In Crop Photosyntheis: Spatial and Temporal Determinants. Edited by Baker NR, Thomas H. Amsterdam: Elsevier Science Publishers; 1992:289-312.
  • [94]Spalding MH: Photosynthesis and photorespiration in freshwater green algae. Aquat Bot 1989, 34(1–3):181-209.
  • [95]Birmingham BC, Coleman JR, Colman B: Measurement of photorespiration in algae. Plant Physiol 1982, 69(1):259-262.
  • [96]Becker EW: Micro-algae as a source of protein. Biotechnol Adv 2007, 25(2):207-210.
  • [97]Xiong W, Liu L, Wu C, Yang C, Wu Q: 13C-tracer and gas chromatography-mass spectrometry analyses reveal metabolic flux distribution in the oleaginous microalga Chlorella protothecoides. Plant Physiol 2010, 154(2):1001-1011.
  • [98]Hu H, Gao K: Response of growth and fatty acid compositions of Nannochloropsis sp. to environmental factors under elevated CO2 concentration. Biotechnology Lett 2006, 28(13):987-992.
  • [99]Buchannan B, Gruissem W, Jones RL: Biochemistry and Molecular Biology of Plants. Rockville, MD: American Society of Plant Biologists; 2000.
  • [100]Wunsche JN, Greer DH, Laing WA, Palmer JW: Physiological and biochemical leaf and tree responses to crop load in apple. Tree Physiol 2005, 25(10):1253-1263.
  • [101]Ihemere U, Arias-Garzon D, Lawrence S, Sayre R: Genetic modification of cassava for enhanced starch production. Plant Biotechnol J 2006, 4(4):453-465.
  • [102]Andre C, Haslam RP, Shanklin J: Feedback regulation of plastidic acetyl-CoA carboxylase by 18:1-acyl carrier protein in Brassica napus. Proc Natl Acad Sci USA 2012, 109(25):10107-10112.
  文献评价指标  
  下载次数:43次 浏览次数:40次