Abstract
BackgroundPurple nonsulfur bacteria (PNSB) are facultative photosynthetic bacteria and exhibit an extremely versatile metabolism. A central focus of research on PNSB dealt with the elucidation of mechanisms by which they manage to balance cellular redox under diverse conditions, in particular under photoheterotrophic growth.ResultsGiven the complexity of the central metabolism of PNSB, metabolic modeling becomes crucial for an integrated analysis of the accumulated biological knowledge. We reconstructed a stoichiometric model capturing the central metabolism of three important representatives of PNSB (Rhodospirillum rubrum, Rhodobacter sphaeroides and Rhodopseudomonas palustris). Using flux variability analysis, the model reveals key metabolic constraints related to redox homeostasis in these bacteria. With the help of the model we can (i) give quantitative explanations for non-intuitive, partially species-specific phenomena of photoheterotrophic growth of PNSB, (ii) reproduce various quantitative experimental data, and (iii) formulate several new hypotheses. For example, model analysis of photoheterotrophic growth reveals that - despite a large number of utilizable catabolic pathways - substrate-specific biomass and CO2 yields are fixed constraints, irrespective of the assumption of optimal growth. Furthermore, our model explains quantitatively why a CO2 fixing pathway such as the Calvin cycle is required by PNSB for many substrates (even if CO2 is released). We also analyze the role of other pathways potentially involved in redox metabolism and how they affect quantitatively the required capacity of the Calvin cycle. Our model also enables us to discriminate between different acetate assimilation pathways that were proposed recently for R. sphaeroides and R. rubrum, both lacking the isocitrate lyase. Finally, we demonstrate the value of the metabolic model also for potential biotechnological applications: we examine the theoretical capabilities of PNSB for photoheterotrophic hydrogen production and identify suitable genetic interventions to increase the hydrogen yield.ConclusionsTaken together, the metabolic model (i) explains various redox-related phenomena of the versatile metabolism of PNSB, (ii) delivers new hypotheses on the operation and relevance of several metabolic pathways, and (iii) holds significant potential as a tool for rational metabolic engineering of PNSB in biotechnological applications.
Highlights
Purple nonsulfur bacteria (PNSB) are facultative photosynthetic bacteria and exhibit an extremely versatile metabolism
For several reasons we intentionally refrained from constructing a genome-scale model and aimed instead at building a detailed and manually curated model of the core metabolism of PNSB
The results clearly show that a non-zero flux through the Calvin cycle is required for all organic substrates considered; the total amount of the flux depends on the oxidation values of the substrates and on structural constraints imposed by the pathways initially metabolizing the substrate
Summary
Purple nonsulfur bacteria (PNSB) are facultative photosynthetic bacteria and exhibit an extremely versatile metabolism. Purple nonsulfur bacteria (PNSB; Rhodospirillaceae) are widely used as model organisms in microbiology and, to an increasing extent, for systems biology They were extensively studied with respect to the molecular structure of their photosynthetic apparatus [1] and draw donor such as hydrogen are supplied). The ability to utilize di-nitrogen (N2) as source of organic nitrogen (via a nitrogenase) further demonstrates the wide spectrum of metabolic abilities of these bacteria [12,13,14] Given this extraordinary metabolic versatility, the elucidation of key mechanisms enabling these organisms to switch between different lifestyles thereby maintaining redox balance has been an important focus of research [5,10,11,15,16,17,18]
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