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Costs of accuracy determined by a maximal growth rate constraint

Published online by Cambridge University Press:  17 March 2009

Måns Ehrenberg
Affiliation:
Department of Molecular Biology, The Biomedical Center, Box 590, 751 24 Uppsala, Sweden
C. G. Kurland
Affiliation:
Department of Molecular Biology, The Biomedical Center, Box 590, 751 24 Uppsala, Sweden

Extract

The present study is best understood as an extension and critique of two schools of thought. The first is that of Malloe and his students, among whom we number ourselves. It is to Maaloe that we are indebted for the idea that logarithmically growing bacteria assemble and use tibosomes in amounts that are optimally adjusted to yield the maximal growth rates supported by different media. Her, we begin our analysis by applying this optimization priciple to all the components of a logarithmically growing system. Our objective is to use the growth optimization constraint as a tool to explore the physiological limits on the accuracy of gene expression. This brings us to our second source of inspiration, which is Orgel's (1963) conception of a problem that Ninio (1982) has referred to as the ‘great error loop’.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1984

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References

Andersson, D. & Kurland, C. G. (1983) RAM ribosomes are defective proofreaders. Molec. & Gen. Genet. 191, 378381.CrossRefGoogle ScholarPubMed
Andersson, S., Buckingham, R. & Kurland, C. G. (1984) Does codon-composition influence ribosome function? EMBO J. 1, 9194.CrossRefGoogle Scholar
Andersson, D., Bohman, K., Isaksson, L. & Kurland, C. G. (1982) Translation rates and misreading characteristics of rpsD mutants in Escherichia coli. Molec. & Gen. Genet. 187, 467472.CrossRefGoogle ScholarPubMed
Blomberg, C., Ehrenberg, M. & Kurland, C. G. (1980) Free energy dissipation constraints on the accuracy of enzymatic selections. Q. Rev. Biophys. 13, 231254.CrossRefGoogle ScholarPubMed
Bouadloun, F., Donner, D. & Kurland, C. G. (1983) Codon-specific missense errors in vivo. EMBO J. 2, 13511356.CrossRefGoogle ScholarPubMed
Chavancy, G. & Garel, J. (1981) Does quantitative tRNA adaptation to codon content in mRNA optimize the ribosomal translation efficiency? Proposal for a translation system model. Biochimie 63, 187195.CrossRefGoogle ScholarPubMed
Churchward, G., Estiva, E. & Bremer, H. (1981) Growth rsate-dependent control of chromosome replication initiation in Escherichia Coli. J. Bacter. 145, 12321238.CrossRefGoogle ScholarPubMed
Churchward, G., Bremer, H. & Young, R. (1982) Macros-molecular composition of bacteria. J. theor. Biol. 94, 651670.CrossRefGoogle ScholarPubMed
Ehrenberg, M. & Blomberg, C. (1980) Thermodynamic constraints on kinetic proofreading in biosynthetic pathways. Biophys. J. 31, 333358.CrossRefGoogle ScholarPubMed
Fersht, A. (1977) Enzyme Structure and Mechanism. San Francisco: W. H. Freeman.Google Scholar
Fiers, W., Contreras, R., De Wachter, R., Haegeman, G., Merregaert, J., Min Jou, W. & Vandenberghe, A. (1971) Recent progress in the sequence determination of bacteriophage MS2 RNA. Biochimie 53, 495506.CrossRefGoogle ScholarPubMed
Galas, J. & Branscomb, W. (1976) Ribosome slowed by mutation to streptomycin resistance. Nature, Lond. 262, 617619.CrossRefGoogle ScholarPubMed
Gallant, J. & Prothero, J. (1980) Testing models of error propagation. J. theor. Biol. 83, 561578.CrossRefGoogle ScholarPubMed
Garel, J. (1974) Functional adaptation of tRNA population. J. theor. Biol. 43, 211225.CrossRefGoogle ScholarPubMed
Goel, N. & Ycas, M. (1975) The error catastrophe hypothesis with reference to aging and the evolution of the protein synthesizing machinery. J. theor. Biol. 55, 245282.CrossRefGoogle ScholarPubMed
Gorini, L. (1971) Ribosomal discrimination of tRNAs. Nature (New Biol.) 234, 261264.Google ScholarPubMed
Grantham, R. & Gautier, C. (1980) Genetic distances from mRNA sequences. Naturwissenschaften 67, 9394.CrossRefGoogle ScholarPubMed
Grantham, R., Gautier, C., Gouy, M., Jacobzone, M. & Mercier, R. (1981) Codon catalog usage is a genome strategy modulated for gene expressivity. Nucl. Acids Res. 9, r43–r74.CrossRefGoogle ScholarPubMed
Grosjean, H. & Fiers, W. (1982) Preferential codon usage in prokaryotic genes: the optimal codon-anticodon interaction energy and the selective codon usage in efficiently expressed genes. Gene 18, 199209.CrossRefGoogle ScholarPubMed
Hoffman, G. W. (1974) On the origin of the genetic code and the stability of the translation apparatus. J. molec. Biol. 86, 349362.CrossRefGoogle Scholar
Hopfield, J. J. (1974) Kinetic proofreading: a new mechanism for reducing errors in biosynthetic processes requiring high specificity. Proc. natn. Acad. Sci. U.S.A. 71, 41354139.CrossRefGoogle ScholarPubMed
Ikemura, T. (1981) Correlation between the abundance of Escherichia Coli transfer RNAs and the occurrence of the respective codons in its protein genes. J. molec. Biol. 146, 121.CrossRefGoogle ScholarPubMed
Jelenc, P. & Kurland, C. G. (1984) Multiple effects of kanamycin on translational accuracy. Molec. & Gen. Genet. 194, 195199.CrossRefGoogle ScholarPubMed
Kirkwood, T. & Holiday, R. (1975) The stability of the translation apparatus. J. molec. Biol. 97, 257265.CrossRefGoogle ScholarPubMed
Kirkwood, T. (1977) Evolution of ageing. Nature, Lond. 270, 301303.CrossRefGoogle ScholarPubMed
Kjeldgaard, N. O. & Kurland, C. G. (1963) The distribution of soluble and ribosomal RNA as a function of growth rate. J. molec. Biol. 6, 341348.CrossRefGoogle Scholar
Kurland, C. G. (1978) The role of guanine nucleotides in protein biosynthesis. Biophys. J. 22, 373388.CrossRefGoogle ScholarPubMed
Kurland, C. G. & Ehrenberg, M. (1983) Optimization of translational accuracy. Progr. Mol. Biol. and Nucl. Acids Res. (in the Press).Google Scholar
Kurland, C. G., Andersson, D., Andersson, S., Bohman, K., Bouad-Loun, F., Ehrenberg, M., Jelenc, P. & Ruusala, T. (1983) Translational accuracy and bacterial growth. In Gene Expression. Alfred Benzon Symposium 19. Copenhagen: Munksgaard.Google Scholar
Maaløe, O. (1979). Regulation of the protein-synthesizing machinery ribosomes, tRNA, factors and so on. In Biological Regulation and Development (ed. Goldberger, R. F.), pp. 487542. New York: Plenum.CrossRefGoogle Scholar
Neidhardt, F., Block, P., Pedersen, S. & Reeh, S. (1977) Chemical measurement of steady-state levels of ten aminoacyl-transfer ribonu-cleic acid synthetases in Escherichia coli. J. Bact. 129, 378387.CrossRefGoogle ScholarPubMed
Ninio, J. (1974) A semi-quantitative treatment of missense and nonsense suppression in the strA and RAM ribosomal mutants of Escherichia Coli. Evaluation of some molecular parameters of translation in vivo. J. molec. Biol. 84, 297313.CrossRefGoogle ScholarPubMed
Ninio, J. (1975) Kinetic amplification of enzyme discrimination. Biochimise 57, 587595.CrossRefGoogle ScholarPubMed
Ninio, J. (1982) Molecular Evolution. London: Pitman.Google Scholar
Orgel, L. E. (1963) The maintenance of the accuracy of protein synthesis and its relevance to ageing. Proc. natn. Acad. Sci. U.S.A. 49, 517521.CrossRefGoogle ScholarPubMed
Orgel, L. E. (1970) The maintenance of the accuracy of protein synthesis and its relevance to ageing: A correction. Proc. natn. Acad. Sci. U.S.A. 67, 14761480.CrossRefGoogle ScholarPubMed
Piepersberg, W., Noseda, V. & Böck, A. (1979). Bacterial ribosomes with two ambiguity mutations: Effects on translational fidelity on the response to aminoglycosides and on the rate of protein synthesis.CrossRefGoogle Scholar
Ruusala, T., Ehrenberg, M. & Kurland, C. G. (1982) Is there proofreading during polypeptide synthesis? EMBO J. 1, 741745.CrossRefGoogle ScholarPubMed
Thompson, R. & Karim, A. (1982) The accuracy of protein biosynthesis is limited by its speed: High fidelity selection by ribosomes of aminoacyl-tRNA ternary complexes containing GTP γS]. Proc. natn. Acad. Sci. U.S.A. 79, 49224926.CrossRefGoogle Scholar
Wain-Hobson, S., Nusssinov, R., Brown, R. & Sussman, J. (1981) Preferential codon usage in genes. Gene. 13, 355364.CrossRefGoogle ScholarPubMed
Von Heijne, G. (1979). The concentration dependence of the error frequencies and some related quantities in protein synthesis. J. theor. Biol. 78, 113120.CrossRefGoogle ScholarPubMed
Zengel, J., Young, R., Dennis, P. & Nomura, M. (1977) Role of ribosomal protein S12 in peptide chain elongation: Analysis of pleiotropic, streptomycin-resistant mutants of Escherichia coli. J. Bact. 129, 13201329.CrossRefGoogle ScholarPubMed