Emergence of robust growth laws from optimal regulation of ribosome synthesis
- PMID: 25149558
- PMCID: PMC4299513
- DOI: 10.15252/msb.20145379
Emergence of robust growth laws from optimal regulation of ribosome synthesis
Abstract
Bacteria must constantly adapt their growth to changes in nutrient availability; yet despite large-scale changes in protein expression associated with sensing, adaptation, and processing different environmental nutrients, simple growth laws connect the ribosome abundance and the growth rate. Here, we investigate the origin of these growth laws by analyzing the features of ribosomal regulation that coordinate proteome-wide expression changes with cell growth in a variety of nutrient conditions in the model organism Escherichia coli. We identify supply-driven feedforward activation of ribosomal protein synthesis as the key regulatory motif maximizing amino acid flux, and autonomously guiding a cell to achieve optimal growth in different environments. The growth laws emerge naturally from the robust regulatory strategy underlying growth rate control, irrespective of the details of the molecular implementation. The study highlights the interplay between phenomenological modeling and molecular mechanisms in uncovering fundamental operating constraints, with implications for endogenous and synthetic design of microorganisms.
Keywords: growth control; metabolic control; phenomenological model; resource allocation; synthetic biology.
© 2014 The Authors. Published under the terms of the CC BY 4.0 license.
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References
-
- Armstrong JB, Fairfield JA. A new method for the isolation of methionyl transfer RNA synthetase mutants from Escherichia coli. Can J Microbiol. 1975;21:754–758. - PubMed
-
- Ataide SF, Ibba M. Discrimination of cognate and noncognate substrates at the active site of class II lysyl-tRNA synthetase. Biochemistry. 2004;43:11836–11841. - PubMed
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