Dethlefsen, L. 2004. Translational power differs between bacteria pursuing different ecological strategies. Dissertation, Michigan State University, East Lansing, Michigan, USA.

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Translation, the polymerization of amino acids into protein, consumes more energy than any other process in the bacterial cell. The translational apparatus, including ribosomes, translation factors, tRNA molecules, tRNA synthetases, and other less abundant components, accounts for a substantial fraction of bacterial cell mass. Hence, selection for optimal performance of the translational apparatus is likely to be strong. Nonetheless, premature translational termination events, known as processivity errors, are not rare in laboratory-adapted Escherichia coli, the only organism for which data exist. Genetic, biochemical and physiological evidence, as well as models of translation, suggest the existence of an evolutionary tradeoff between translational power (the net rate of protein synthesis per mass invested in the translational apparatus) and translational yield (the net mass of protein synthesized per energy consumed). Microorganisms selected for fast maximal growth rates and a rapid response to resource abundance may favor high translational power to permit rapid protein synthesis and rapid growth, at the expense of more frequent processivity errors that waste energy by generating truncated polypeptides that are subsequently degraded. On the other hand, microorganisms adapted to exploit small fluctuations and limited availability of resources may favor high translational yield to minimize resource thresholds for growth and survival, at the expense of a reduced rate of protein synthesis for a given investment in the translational apparatus. This hypothesis is tested using a collection of recent soil isolates containing bacteria of contrasting ecological strategies in each of several diverse phylogenetic groups, as well as one well-characterized representative of each ecological strategy. The specific growth rate, cell density and cell volume were measured for each of these 10 bacterial strains in batch culture in two media; a novel protocol was developed for measurement of the DNA, RNA and protein content of small samples of bacterial biomass. As predicted, translational power is higher in bacteria capable of a rapid growth response to abundant resources. Codon usage analysis can provide a comparison of the relative strength of selection for translational power between strains, so the relationship between codon bias and ecological strategy was examined in a large number of bacteria with fully sequenced genomes, using the number of copies of the ribosomal RNA operon per genome as an index of ecological strategy. The observed pattern of stronger translational selection in organisms with more copies of the rRNA operon is consistent with expectations based on macromolecular measurements. This pattern is better explained by a cost associated with translational power rather than the absence of a benefit of translational power among strains adapted to small resource fluctuations. Because codon bias directly affects translational power, we investigated whether variation in codon bias among organisms could explain the observed variation in translational power. However, the degree to which codon bias accelerates translation in E. coli is too small to explain the observed variation in translational power between strains. Instead, differences in translational power among microbes must be explained by differences in the performance of the translational apparatus itself.

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