Abstract
Genome-scale metabolic models have proven useful for answering fundamental questions about metabolic capabilities of a variety of microorganisms, as well as informing their metabolic engineering. However, only a few models are available for oxygenic photosynthetic microorganisms, particularly in cyanobacteria in which photosynthetic and respiratory electron transport chains (ETC) share components. We addressed the complexity of cyanobacterial ETC by developing a genome-scale model for the diazotrophic cyanobacterium, Cyanothece sp. ATCC 51142. The resulting metabolic reconstruction, iCce806, consists of 806 genes associated with 667 metabolic reactions and includes a detailed representation of the ETC and a biomass equation based on experimental measurements. Both computational and experimental approaches were used to investigate light-driven metabolism in Cyanothece sp. ATCC 51142, with a particular focus on reductant production and partitioning within the ETC. The simulation results suggest that growth and metabolic flux distributions are substantially impacted by the relative amounts of light going into the individual photosystems. When growth is limited by the flux through photosystem I, terminal respiratory oxidases are predicted to be an important mechanism for removing excess reductant. Similarly, under photosystem II flux limitation, excess electron carriers must be removed via cyclic electron transport. Furthermore, in silico calculations were in good quantitative agreement with the measured growth rates whereas predictions of reaction usage were qualitatively consistent with protein and mRNA expression data, which we used to further improve the resolution of intracellular flux values.
Highlights
Cyanothece spp. are unicellular, diazotrophic cyanobacteria that temporally separate light-dependent oxygenic photosynthesis and glycogen accumulation from N2 fixation at night [1]
Cyanobacteria have been promoted as platforms for biofuel production due to their useful physiological properties such as photosynthesis, relatively rapid growth rates, ability to accumulate high amounts of intracellular compounds and tolerance to extreme environments
In silico predictions obtained from model analysis provided insights into the effects of light quantity and quality upon fluxes through electron transport pathways, alternative pathways for reductant consumption and carbon metabolism
Summary
Cyanothece spp. are unicellular, diazotrophic cyanobacteria that temporally separate light-dependent oxygenic photosynthesis and glycogen accumulation from N2 fixation at night [1]. When grown under nutrient excess, Cyanothece sp. Strain ATCC 51142 (thereafter Cyanothece 51142) cells can accumulate significant amounts of storage polymers including glycogen, polyphosphates, and cyanophycin [2]. The inter-thylakoid glycogen granules are significantly larger in size than those found in other cyanobacteria, which points at an unusual branching pattern and packaging of this compound. This presents an intriguing theoretical possibility to accumulate substantially higher amounts of polyglucose without any significant increase in the number of granules [3]. Cyanothece 51142 is of interest for bioenergy applications due to its ability to evolve large quantities of H2. H2 production in this organism can occur under light conditions in the presence of O2 and is mediated by nitrogenase [4,5]
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