Abstract
Anabaena sp. PCC 7120 is a nitrogen-fixing filamentous cyanobacterium. Under nitrogen-limiting conditions, a fraction of the vegetative cells in each filament terminally differentiate to nongrowing heterocysts. Heterocysts are metabolically and structurally specialized to enable O2-sensitive nitrogen fixation. The functionality of the filament, as an association of vegetative cells and heterocysts, is postulated to depend on metabolic exchange of electrons, carbon, and fixed nitrogen. In this study, we compile and evaluate a comprehensive curated stoichiometric model of this two-cell system, with the objective function based on the growth of the filament under diazotrophic conditions. The predicted growth rate under nitrogen-replete and -deplete conditions, as well as the effect of external carbon and nitrogen sources, was thereafter verified. Furthermore, the model was utilized to comprehensively evaluate the optimality of putative metabolic exchange reactions between heterocysts and vegetative cells. The model suggested that optimal growth requires at least four exchange metabolites. Several combinations of exchange metabolites resulted in predicted growth rates that are higher than growth rates achieved by only considering exchange of metabolites previously suggested in the literature. The curated model of the metabolic network of Anabaena sp. PCC 7120 enhances our ability to understand the metabolic organization of multicellular cyanobacteria and provides a platform for further study and engineering of their metabolism.
Highlights
Cyanobacteria are highly diverse in terms of morphology: Some species are filamentous, others are unicellular or can form aggregates, several species are capable of nitrogen fixation in differentiated heterocysts, and some form motile hormogonia or spore-like akinetes (Flores and Herrero, 2010; Singh and Montgomery, 2011)
Approximately every tenth vegetative cell irreversibly transforms into a heterocyst to provide a low-oxygen environment for the nitrogenase enzyme to function (Golden and Yoon, 2003)
Balanced biochemical reactions were sorted into six intracellular compartments in order to simulate the growth of vegetative cells on a combined nitrogen source
Summary
The functionality of the filament, as an association of vegetative cells and heterocysts, is postulated to depend on metabolic exchange of electrons, carbon, and fixed nitrogen. Approximately every tenth vegetative cell irreversibly transforms into a heterocyst to provide a low-oxygen environment for the nitrogenase enzyme to function (Golden and Yoon, 2003). This enzyme is responsible for the conversion of atmospheric molecular nitrogen into ammonia in a highly energyexpensive reaction, consuming chemical energy stored in 16 molecules of ATP and eight electrons carried by ferredoxin molecules for every molecule of nitrogen assimilated. FdxH for nitrogenasec (Razquin et al, 1996) Contains cox and cox only (Valladares et al, 2003)
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