Abstract
Metabolic acclimation to photosynthesis-associated stresses was examined in the thermophilic cyanobacterium Thermosynechococcus elongatus BP-1 using integrated computational and photobioreactor analyses. A genome-enabled metabolic model, complete with measured biomass composition, was analyzed using ecological resource allocation theory to predict and interpret metabolic acclimation to irradiance, O2, and nutrient stresses. Reduced growth efficiency, shifts in photosystem utilization, changes in photorespiration strategies, and differing byproduct secretion patterns were predicted to occur along culturing stress gradients. These predictions were compared with photobioreactor physiological data and previously published transcriptomic data and found to be highly consistent with observations, providing a systems-based rationale for the culture phenotypes. The analysis also indicated that cyanobacterial stress acclimation strategies created niches for heterotrophic organisms and that heterotrophic activity could enhance cyanobacterial stress tolerance by removing inhibitory metabolic byproducts. This study provides mechanistic insight into stress acclimation strategies in photoautotrophs and establishes a framework for predicting, designing, and engineering both axenic and photoautotrophic-heterotrophic systems as a function of controllable parameters.
Highlights
Environmental stresses dictate competitive ecological strategies impacting nutrient and energy flows from the scale of individual cells to ecosystems [1,2]
Genetic potential was mapped to enzymes and metabolic reactions which encompassed photosynthesis, central metabolism, and biosynthetic reactions leading to biomass production according to a defined macromolecular composition reaction
Subsequent elementary flux mode analysis (EFMA) resulted in a description of the phenotypic space spanning the range of possible nutrient uptake and product secretion rates, which could be analyzed for ecologically relevant stress acclimation strategies
Summary
Environmental stresses dictate competitive ecological strategies impacting nutrient and energy flows from the scale of individual cells to ecosystems [1,2]. Cyanobacteria are significant drivers of global nutrient and energy flows, accounting for ~10% of global primary productivity [3] and forming essential links in carbon and nitrogen biogeochemical cycles [4]. Cyanobacteria are deeply rooted in the tree of life and have adapted competitively to common stressors associated with photosynthesis and are model organisms for examining metabolic acclimation to these stresses. Photoinhibition is a broad term encompassing different types of photosynthesis-associated stresses including photo-damage by excitation, damage by reactive oxygen species (ROS), and high localized O2 concentrations [7].
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