There is considerable interest in making use of solar energy through photosynthesis to create alternative forms of fuel. Here, we show that photosystem I from a thermophilic bacterium and cytochrome-c(6) can, in combination with a platinum catalyst, generate a stable supply of hydrogen in vitro upon illumination. The self-organized platinization of the photosystem I nanoparticles allows electron transport from sodium ascorbate to photosystem I via cytochrome-c(6) and finally to the platinum catalyst, where hydrogen gas is formed. Our system produces hydrogen at temperatures up to 55 degrees C and is temporally stable for >85 days with no decrease in hydrogen yield when tested intermittently. The maximum yield is approximately 5.5 micromol H(2) h(-1) mg(-1) chlorophyll and is estimated to be approximately 25-fold greater than current biomass-to-fuel strategies. Future work will further improve this yield by increasing the kinetics of electron transfer, extending the spectral response and replacing the platinum catalyst with a renewable hydrogenase.

Microorganisms can be engineered to produce useful products, including chemicals and fuels from sugars derived from renewable feedstocks, such as plant biomass. An alternative method is to use low potential reducing power from nonbiomass sources, such as hydrogen gas or electricity, to reduce carbon dioxide directly into products. This approach circumvents the overall low efficiency of photosynthesis and the production of sugar intermediates. Although significant advances have been made in manipulating microorganisms to produce useful products from organic substrates, engineering them to use carbon dioxide and hydrogen gas has not been reported. Herein, we describe a unique temperature-dependent approach that confers on a microorganism (the archaeon Pyrococcus furiosus, which grows optimally on carbohydrates at 100°C) the capacity to use carbon dioxide, a reaction that it does not accomplish naturally. This was achieved by the heterologous expression of five genes of the carbon fixation cycle of the archaeon Metallosphaera sedula, which grows autotrophically at 73°C. The engineered P. furiosus strain is able to use hydrogen gas and incorporate carbon dioxide into 3-hydroxypropionic acid, one of the top 12 industrial chemical building blocks. The reaction can be accomplished by cell-free extracts and by whole cells of the recombinant P. furiosus strain. Moreover, it is carried out some 30°C below the optimal growth temperature of the organism in conditions that support only minimal growth but maintain sufficient metabolic activity to sustain the production of 3-hydroxypropionate. The approach described here can be expanded to produce important organic chemicals, all through biological activation of carbon dioxide.

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