Abstract
To date, the proposed mechanisms of nitrogenase-driven photosynthetic H2 production by the diazotrophic unicellular cyanobacterium Cyanothece sp. ATCC 51142 have assumed that reductant and ATP requirements are derived solely from glycogen oxidation and cyclic-electron flow around photosystem I. Through genome-scale transcript and protein profiling, this study presents and tests a new hypothesis on the metabolic relationship between oxygenic photosynthesis and nitrogenase-mediated H2 production in Cyanothece 51142. Our results show that net-positive rates of oxygenic photosynthesis and increased expression of photosystem II reaction centers correspond and are synchronized with nitrogenase expression and H2 production. These findings provide a new and more complete view on the metabolic processes contributing to the energy budget of photosynthetic H2 production and highlight the role of concurrent photocatalytic H2O oxidation as a participating process.
Highlights
Photobiological H2 production is still a nascent technology with long-term potential for sustainable energy production with a low environmental impact
The maximum specific rate of H2 production by Cyanothece 51142 was reached after 14.5 hours of N-depletion and measured to be 3.12 mmol-H2 hr−1 g−1CDW (279 μ mol-H2 mg-Chl a−1 hr−1) which, to our knowledge, is the highest reported rate of H2 production per unit biomass under photoautotrophic conditions[7]
These results frame the concept of active reductant and ATP generation originating from a combination of energy metabolism processes including linear electron flow through PS II
Summary
Photobiological H2 production is still a nascent technology with long-term potential for sustainable energy production with a low environmental impact. To date, the kinetic rates and sustainability of hydrogenase-mediated H2 production are low in comparison to those reported for some diazotrophic organisms that produce H2 in oxic-environments as a byproduct of nitrogenase catalyzed N2 fixation[4,5,6]. We present evidence to support a new model whereby energy derived directly from oxygenic photosynthesis (i.e., linear electron flow through PS II) is an important process in funding the energy budget required for nitrogenase activity under illuminated, nitrogen-deplete conditions. These conclusions are supported by a combined analysis of detailed process and integrated transcriptome and proteome profiles across a photosynthetically driven H2 production process
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