Role of Central Metabolism in the Osmoadaptation of the Halophilic Bacterium Chromohalobacter salexigens

Bacterial osmoadaptation involves the cytoplasmic accumulation of compatible solutes to counteract extracellular osmolarity. The halophilic and highly halotolerant bacterium Chromohalobacter salexigens is able to grow up to 3 m NaCl in a minimal medium due to the de novo synthesis of ectoines. This...

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Published in:The Journal of biological chemistry 2013-06, Vol.288 (24), p.17769-17781
Main Authors: Pastor, José M., Bernal, Vicente, Salvador, Manuel, Argandoña, Montserrat, Vargas, Carmen, Csonka, Laszlo, Sevilla, Ángel, Iborra, José L., Nieto, Joaquín J., Cánovas, Manuel
Format: Article
Language:English
Subjects:
Amino Acids - metabolism
Amino Acids, Diamino - biosynthesis
Bacterial Proteins - genetics
Biomass
Carbohydrate Metabolism
Carboxylic Acids - metabolism
Chromohalobacter - genetics
Chromohalobacter - growth & development
Chromohalobacter - metabolism
Citric Acid Cycle
Computational Biology
Ectoines
Entner-Doudoroff
Glucose - metabolism
Halophilic Bacteria
Metabolic Networks and Pathways
Metabolic Tracers
Metabolism
Microbiology
Nuclear Magnetic Resonance
Overflow Metabolism
Pyruvate Carboxylase
Salinity
Salt Adaptation
Salt Tolerance
Sodium Chloride - metabolism
Staining and Labeling
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Summary:Bacterial osmoadaptation involves the cytoplasmic accumulation of compatible solutes to counteract extracellular osmolarity. The halophilic and highly halotolerant bacterium Chromohalobacter salexigens is able to grow up to 3 m NaCl in a minimal medium due to the de novo synthesis of ectoines. This is an osmoregulated pathway that burdens central metabolic routes by quantitatively drawing off TCA cycle intermediaries. Consequently, metabolism in C. salexigens has adapted to support this biosynthetic route. Metabolism of C. salexigens is more efficient at high salinity than at low salinity, as reflected by lower glucose consumption, lower metabolite overflow, and higher biomass yield. At low salinity, by-products (mainly gluconate, pyruvate, and acetate) accumulate extracellularly. Using [1-13C]-, [2-13C]-, [6-13C]-, and [U-13C6]glucose as carbon sources, we were able to determine the main central metabolic pathways involved in ectoines biosynthesis from glucose. C. salexigens uses the Entner-Doudoroff pathway rather than the standard glycolytic pathway for glucose catabolism, and anaplerotic activity is high to replenish the TCA cycle with the intermediaries withdrawn for ectoines biosynthesis. Metabolic flux ratios at low and high salinity were similar, revealing a certain metabolic rigidity, probably due to its specialization to support high biosynthetic fluxes and partially explaining why metabolic yields are so highly affected by salinity. This work represents an important contribution to the elucidation of specific metabolic adaptations in compatible solute-accumulating halophilic bacteria. Background:Chromohalobacter salexigens synthesizes and accumulates ectoines. Results: High ratio of the anaplerotic and catabolic fluxes involved in ectoines synthesis supports high biosynthetic fluxes at high salinity and leads to metabolite overflow at low salinity. Conclusion: Evolution optimized the metabolism of C. salexigens to support high production of ectoines. Significance: Metabolic adaptations in a compatible solute-accumulating halophile are described for the first time.
ISSN:0021-9258
1083-351X
DOI:10.1074/jbc.M113.470567