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H2-Driven CO2 Fixation by Extremely Thermoacidophilic Archaea

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H2-Driven CO2 Fixation by Extremely Thermoacidophilic Archaea H2-driven CO2 Fixation by Extremely Thermoacidophilic Archaea Michael W.W. Adams, University of Georgia Robert M. Kelly, North Carolina State University Primary CO2 Electron Biofuel Source Reduced LIGHT Product DARK H2O H2 CH/O ARPA-E Workshop on Direct Solar Fuels October 21, 2009 SOLAR BIOFUEL PRODUCTION Primary Electron Biofuel Source Reduced Product SOLAR BIOFUEL PRODUCTION Primary Electron Biofuel Source Reduced Product Secondary Biomass Electron Green Plants Reduced Conversion Source Product SUGARS H O 2 SUGARS PS CC Microbial VISIBLE LIGHT Conversion Oxidized Oxidized Primary Substrate Biofuel Electron Reduced CO (of choice*) Source Product 2 O2 NADPH CO PS = photosynthesis (I+II) 2 CF = CO2 fixation (Calvin cycle) *CxHy / CaHbOc SOLAR BIOFUEL PRODUCTION Primary Electron Biofuel Source Reduced Product Secondary Electron Algae Reduced Source Product H O 2 SUGARS PS CC VISIBLE LIGHT H Oxidized 2 Oxidized Primary Substrate Electron Reduced Biofuel CO Source Product 2 O2 NADPH CO PS = photosynthesis (I+II) 2 CF = CO2 fixation (Calvin cycle) SOLAR BIOFUEL PRODUCTION Primary Electron Biofuel Source Reduced Product Secondary Metabolic Electron Algae Reduced Engineering Biofuel Source Product (of choice) H O 2 SUGARS PS CC VISIBLE LIGHT Oxidized Oxidized Primary Substrate Electron Reduced CO Source Product 2 O2 NADPH CO Simplified (Biomimetic) PS = photosynthesis (I+II) 2 Scheme? CF = CO2 fixation (Calvin cycle) SOLAR BIOFUEL PRODUCTION Primary Electron Biofuel Source Reduced Product Electron PS CF Source Module Module H2O Biofuel (of choice) VISIBLE LIGHT Oxidized Oxidized Primary Substrate Electron Reduced CO Source Product 2 O2 H2 CO PS = photosynthesis (I+II) 2 CF = CO2 fixation (Calvin cycle) SOLAR BIOFUEL PRODUCTION Primary Electron Biofuel Source Reduced Product Electron PS CF Source Module Module H2O Biofuel (of choice) O2 VISIBLE LIGHT Oxidized Fuel use with Oxidized Primary CO Substrate oxidized source 2 Electron Reduced + CO (O ) regenerates Source Product 2 2 H O O substrates 2 2 H 2 (CO2, H2O) IDEAL SOLAR CO2 PS = photosynthesis (I+II) ENERGY CONVERSION CF = CO2 fixation (Calvin cycle) SYSTEM SOLAR BIOFUEL PRODUCTION Primary CO2 Electron Biofuel Source Reduced LIGHT Product DARK PSM CFM H2O H2 CH/O Electron PS CF Source Module Module H2O Biofuel (of choice) O2 VISIBLE LIGHT Oxidized Fuel use with Oxidized Primary CO Substrate oxidized source 2 Electron Reduced + CO (O ) regenerates Source Product 2 2 H O O substrates 2 2 H 2 (CO2, H2O) IDEAL SOLAR CO2 PS = photosynthesis (I+II) ENERGY CONVERSION CF = CO2 fixation (Calvin cycle) SYSTEM SOLAR BIOFUEL PRODUCTION Primary CO2 Electron Biofuel Source Reduced LIGHT Product DARK PSM CFM H2O H2 CH/O Electron PS CF Source Module Module H O Biofuel 2 H 2 (of choice) PS CO2 CHO/CH VISIBLE LIGHT H2 2H+ + 2e- H 2 Oxidized Oxidized Primary Substrate Electron Reduced Key Source CO2 Research Product Areas O2 H2 CO PS = photosynthesis (I+II) 2 CF = CO2 fixation SOLAR BIOFUEL PRODUCTION Primary CO2 Electron Biofuel Source Reduced LIGHT Product DARK PSM CFM H2O H2 CH/O Electron PS CF Source Module Module H2O Biofuel H2 CO CHO/CH (of choice) VISIBLE LIGHT PS 2 2H+ + 2e- H 2 Oxidized Oxidized Primary Substrate Electron Reduced Key Source CO2 Research Product Areas O2 H2 CO PS = photosynthesis (I+II) 2 CF = CO2 fixation SOLAR BIOFUEL PRODUCTION Primary CO2 Electron Biofuel Source Reduced LIGHT Product DARK PSM CFM H2O H2 CH/O Key Biological Reactions PSM: 1. Water photolysis (visible light): + - H2O O2 + 2H + 2e 2. Hydrogen production + - 2H + 2e H2 CFM: 1. Hydrogen activation + - H2 2H + 2e 2. CO2 to biofuel conversion (reduced carbon/CH/CHO) + - CO2 + 2H + 2e CxHy / CaHbOc Much higher energy yield using H2 as reductant for CO2 fixation to biofuel compared to sugar to biofuel Structure/Function Studies of NiFe-hydrogenase - Hydrogenase is not a ‘commodity enzyme’ - Very complex maturation process in vivo to assemble complex, O2-sensitive, NiFe-catalytic site (CO, CN ligands, etc.) - No genetically-tractable organism that produces hydrogenase available for detailed structure/function studies - Recent breakthrough – production of recombinant form of the NADPH- dependent Pyrococcus hydrogenase in E. coli Fundamental structure/function studies to design: - ‘Minimal’ hydrogenases (NiFe-site plus peptides) -H2 production and H2 activation catalysts - Decreased O2-sensitivity - Electron carrier specificity - Pathways of electron transfer Hydrogen Production from Polyglucose (13 enzymes, Pi, NADP – catalytic) PPP (Pentose Phosphate Pathway) #13: NADPH-dependent H2-evolving Pyrococcus Hydrogenase Zhang et al. PLoS One 5, e456, 2008 (C6H10O5)n + 7 H2O 12 H2 + 6 CO2 Calvin Cycle plants, cyanobacteria, purple and green bacteria Microbial CO2 Fixation Pathways Reverse Tricarboxylic Acid Cycle Reductive Acetyl-CoA Pathway Chlorobium limicola Desulfobacter hydrogenophilus Acetobacterium woodii Hydrogenobacter thermophilus Defulfobacterium autotrophicum Adapted from http://lecturer.ukdw.ac.id/dhira/Metabolism/CarbonAssim.html 3-Hydroxypropionate Cycle Microbial CO2 Chloroflexus aurantiacus Fixation Pathways Alber, B. et al. (2006) (Thermophiles) Dicarboxylate/4-Hydroxybutyrate Cycle 3-Hydroxypropionate/4-Hydroxybutyrate Cycle Ignicoccus hospitalis Metallosphaera sedula Ramos-Vera, W. H. et al. (2009) Berg, I. A. et al. (2007) TheThe ExtremelyExtremely ThermoacidophilicThermoacidophilic ArchaeonArchaeon MetallosphaeraMetallosphaera sedulasedula Genome: 2.2 Mb (46.2% G + C) 2304 ORFs Growth: Mixotrophic aerobe; metal mobilizer Topt = 73°C; pHopt = 2.0 M. sedula genes closest sequence matches S. solfataricus other S. tokodaii S. acidocaldarius Sso Other sulfolobus species Sac (islandicus, metallicus, shibatae) Acidianus species Ferroplasma species Sto Thermoplasma species Huber et al. 1989 Pyrobaculum species Other / No top hit Auernik, K. S., Y. Maezato, P. H. Blum, and R. M. Kelly. 2008. The genome sequence of the metal-mobilizing, extremely thermoacidophilic archaeon Metallosphaera sedula provides insights into bioleaching-associated metabolism. Appl. Environ. Microbiol. 74:682-92. ComparativeComparative genomics:genomics: ExtremeExtreme thermoacidophilesthermoacidophiles ComparativeComparative genomics:genomics: ExtremeExtreme thermoacidophilesthermoacidophiles GrowingGrowing E.E. colicoli Oxoid Metal mobilization by M. sedula Chalcopyrite, t = 0 days with M. sedula Chalcopyrite, t = 21 days with M. sedula CuFeS2 solids 10g/L pH 2 Cu2+ Iron oxidation Sulfur oxidation (Inorganic) Carbon fixation Heavy metal tolerance Adhesion to solids Auernik, KS, Y. Maezato, PH Blum, and RM Kelly. 2008. Appl. Environ. Microbiol. 74(3): 682-692 Auernik, KS, CR Cooper, and RM Kelly. 2008. Curr. Opin. Biotechnol. 19(5):445-453 Metal and RISC oxidation components on Fe2+, S° Auernik, KS and RM Kelly. 2008. Appl. Environ. Microbiol. 74(24): 7723-7732 Metal and RISC oxidation components on CuFeS2 Auernik, KS, and RM Kelly. Molecular hydrogen impacts chalcopyrite bioleaching efficiency for the extremely thermoacidophilic archaeon Metallosphaera sedula. (submitted) Versatile growth physiology of M. sedula Mixotrophy (< 4hrs) Heterotrophy (5 hrs) Autotrophy (12 hrs) Auernik, KS, and RM Kelly. Physiological versatility of the extremely thermoacidophilic archaeon Metallosphaera sedula supported by heterotrophy, autotrophy and mixotrophy transcriptomes (submitted) M. sedula Hydrogenases Auernik, KS, and RM Kelly. Physiological versatility of the extremely thermoacidophilic archaeon Metallosphaera sedula supported by heterotrophy, autotrophy and mixotrophy transcriptomes (submitted) M. sedula 3-HP/4-HB CO2 fixation pathway ATP NAD 2 NADPH ATP NADPH ATP ATP 2 NADPH Overall: 2CO2 + 4ATP + 5NADPH + CoA + NAD Acetyl CoA + 3ADP+AMP + 3Pi + PPi + 5NADP + NADH Auernik et al. (2008) Curr. Opin. Biotech. 19, 445-453 M. sedula 3-HP/4-HB CO2 fixation pathway 4-hydroxybutyryl-CoA dehydratase H1H2 A1A2 M1M2 Auernik, KS, CR Cooper, and RM Kelly. 2008. Curr. Opin. Biotechnol. 19(5):445-453 Berg, I et al. 2007. Science. 318:1782-1786 M. sedula 3-HP/4-HB CO2 fixation pathway Auernik, KS, and RM Kelly. Physiological versatility of the extremely thermoacidophilic archaeon Metallosphaera sedula supported by heterotrophy, autotrophy and mixotrophy transcriptomes (submitted) 3-HP/4-HB CO2 Fixation Pathway in Metallosphaera sedula SOLAR BIOFUEL PRODUCTION Primary CO2 Electron Biofuel Source Reduced LIGHT Product DARK PSM CFM H2O H2 CH/O Fundamental Studies Needed: 1. Photosystems I and II 2. Hydrogenases 3. CO2 fixation pathways Key issues: 1. Mechanisms of catalysis and design of biomimetic systems? 2. Electron transfer pathways between the three systems?.
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