Optimization of photosynthetic light energy utilization by microalgae

Over 50% of the energy losses associated with the conversion of solar energy into chemical energy during photosynthesis are attributed to kinetic constraints between the fast rate of photon capture by the light harvesting apparatus and the slower downstream rate of photosynthetic electron transfer. At full sunlight intensities, energy flux from the light harvesting antennae to the reaction centers may be 100-folds greater than the overall linear electron flow resulting in the dissipation of up to 75% of the captured energy as heat or fluorescence. One possible means to couple energy capture and photosynthetic electron transfer more efficiently is to reduce the optical cross-section of the light harvesting antennae. We show that by partially reducing chlorophyll b levels in the green alga, Chlamydomonas reinhardtii, we can tune the peripheral light harvesting antennae size for increased photosynthetic efficiency resulting in more than a two-fold increase in photosynthetic rate at high light intensities and a 30% increase in growth rate at saturating light intensities. Unlike chlorophyll b-less mutants which lack the peripheral light harvesting antennae; transgenics with intermediate sized peripheral antennae have the advantage that they can carry out state transitions facilitating enhanced cyclic ATP synthesis and have robust zeaxanthin–violaxanthin cycles providing protection from high light levels. It is hypothesized that the large antennae size of wild-type algae and land plants offers a competitive advantage in mixed cultures due to the ability of photosynthetic organisms with large light harvesting antennae to shade competing species and to harvest light at low flux densities.

[1]  D. Kaftan,et al.  Flash fluorescence induction: a novel method to study regulation of Photosystem II , 1999 .

[2]  Luca Dall’Osto,et al.  Enhanced photoprotection by protein-bound vs free xanthophyll pools: a comparative analysis of chlorophyll b and xanthophyll biosynthesis mutants. , 2010, Molecular plant.

[3]  R. Ueda,et al.  Improvement of photosynthesis in dense microalgal suspension by reduction of light harvesting pigments , 1997, Journal of Applied Phycology.

[4]  C. Posten,et al.  Second Generation Biofuels: High-Efficiency Microalgae for Biodiesel Production , 2008, BioEnergy Research.

[5]  Lutz Wobbe,et al.  Improvement of light to biomass conversion by de-regulation of light-harvesting protein translation in Chlamydomonas reinhardtii. , 2009, Journal of biotechnology.

[6]  Luca Dall’Osto,et al.  Zeaxanthin Has Enhanced Antioxidant Capacity with Respect to All Other Xanthophylls in Arabidopsis Leaves and Functions Independent of Binding to PSII Antennae1[C][W] , 2007, Plant Physiology.

[7]  Kazuichi Yoshida,et al.  Chlorophyll a oxygenase (CAO) is involved in chlorophyll b formation from chlorophyll a. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[8]  K. Niyogi,et al.  Analysis of LhcSR3, a Protein Essential for Feedback De-Excitation in the Green Alga Chlamydomonas reinhardtii , 2011, PLoS biology.

[9]  B. Pogson,et al.  Genetic manipulation of carotenoid biosynthesis and photoprotection. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[10]  J. Rochaix,et al.  Role of Chloroplast Protein Kinase Stt7 in LHCII Phosphorylation and State Transition in Chlamydomonas , 2003, Science.

[11]  Elizabeth H. Harris,et al.  The Chlamydomonas Sourcebook: A Comprehensive Guide to Biology and Laboratory Use , 1989 .

[12]  T. Masuda,et al.  Truncated chlorophyll antenna size of the photosystems—a practical method to improve microalgal productivity and hydrogen production in mass culture , 2002 .

[13]  Paul G. Falkowski,et al.  Photoinhibition of Photosynthesis in Nature , 1994 .

[14]  M. Badger,et al.  The Prospect of Using Cyanobacterial Bicarbonate Transporters to Improve Leaf Photosynthesis in C3 Crop Plants[W] , 2010, Plant Physiology.

[15]  Teresa M. Mata,et al.  Microalgae for biodiesel production and other applications: A review , 2010 .

[16]  K. Kindle High-frequency nuclear transformation of Chlamydomonas reinhardtii. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[17]  G. Giuliano,et al.  Lutein is needed for efficient chlorophyll triplet quenching in the major LHCII antenna complex of higher plants and effective photoprotection in vivo under strong light , 2006, BMC Plant Biology.

[18]  Juergen E. W. Polle,et al.  tla1, a DNA insertional transformant of the green alga Chlamydomonas reinhardtii with a truncated light-harvesting chlorophyll antenna size , 2003, Planta.

[19]  G. Finazzi,et al.  Impaired respiration discloses the physiological significance of state transitions in Chlamydomonas , 2009, Proceedings of the National Academy of Sciences.

[20]  K. Niyogi,et al.  Non-photochemical quenching. A response to excess light energy. , 2001, Plant physiology.

[21]  F. Wollman,et al.  Changes in light energy distribution upon state transitions: an in vivo photoacoustic study of the wild type and photosynthesis mutants from Chlamydomonas reinhardtii , 1996 .

[22]  K. Niyogi,et al.  Arabidopsis Mutants Define a Central Role for the Xanthophyll Cycle in the Regulation of Photosynthetic Energy Conversion , 1998, Plant Cell.

[23]  F. Wollman State transitions reveal the dynamics and flexibility of the photosynthetic apparatus , 2001, The EMBO journal.

[24]  Y. Chisti Biodiesel from microalgae. , 2007, Biotechnology advances.

[25]  J. Benemann,et al.  Photosynthetic apparatus organization and function in the wild type and a chlorophyll b-less mutant of Chlamydomonas reinhardtii. Dependence on carbon source , 2000, Planta.

[26]  K. Niyogi,et al.  Sensing and responding to excess light. , 2009, Annual review of plant biology.

[27]  Richard T. Sayre,et al.  Microalgae: The Potential for Carbon Capture , 2010 .

[28]  J. Alric Cyclic electron flow around photosystem I in unicellular green algae , 2010, Photosynthesis Research.

[29]  A. Melis,et al.  Solar energy conversion efficiencies in photosynthesis: Minimizing the chlorophyll antennae to maximize efficiency , 2009 .

[30]  D. Ort,et al.  Optimizing Antenna Size to Maximize Photosynthetic Efficiency[W] , 2010, Plant Physiology.

[31]  R. Sayre,et al.  Photosystem II, a Structural Perspective , 2009 .

[32]  R. Bassi,et al.  Functional architecture of the major light-harvesting complex from higher plants. , 2001, Journal of molecular biology.

[33]  D. Arnon COPPER ENZYMES IN ISOLATED CHLOROPLASTS. POLYPHENOLOXIDASE IN BETA VULGARIS. , 1949, Plant physiology.

[34]  R. Tanaka,et al.  The N-Terminal Domain of Chlorophyllide a Oxygenase Confers Protein Instability in Response to Chlorophyll b Accumulation in Arabidopsis , 2005, The Plant Cell Online.

[35]  Xinguang Zhu,et al.  PSII Photochemistry and Xanthophyll Cycle in Two Superhigh-yield Rice Hybrids, Liangyoupeijiu and Hua-an 3 During Photoinhibition and Subsequent Restoration , 2002 .

[36]  James Barber,et al.  Comparing Photosynthetic and Photovoltaic Efficiencies and Recognizing the Potential for Improvement , 2011, Science.

[37]  N. Chua,et al.  Lithium dodecyl sulfate/polyacrylamide gel electrophoresis of thylakoid membranes at 4 degrees C: Characterizations of two additional chlorophyll a-protein complexes. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[38]  D. Durnford,et al.  Structural and functional diversification of the light-harvesting complexes in photosynthetic eukaryotes , 2010, Photosynthesis Research.

[39]  R. Goss,et al.  Regulation and function of xanthophyll cycle-dependent photoprotection in algae , 2010, Photosynthesis Research.

[40]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[41]  A. Melis,et al.  Optical properties of microalgae for enhanced biofuels production , 2008 .

[42]  L. Tian,et al.  Xanthophyll biosynthetic mutants of Arabidopsis thaliana: altered nonphotochemical quenching of chlorophyll fluorescence is due to changes in Photosystem II antenna size and stability. , 2002, Biochimica et biophysica acta.

[43]  P. Hegemann,et al.  A Streptomyces rimosus aphVIII gene coding for a new type phosphotransferase provides stable antibiotic resistance to Chlamydomonas reinhardtii. , 2001, Gene.

[44]  A. McDowall,et al.  Engineering photosynthetic light capture: impacts on improved solar energy to biomass conversion. , 2007, Plant biotechnology journal.

[45]  A. Melis Spectroscopic methods in photosynthesis: photosystem stoichiometry and chlorophyll antenna size , 1989 .