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Journal Article

The layered costs and benefits of translational redundancy

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Ngan,  Wing Yui
Research Group Microbial Evolutionary Dynamics (Gallie), Department Evolutionary Theory (Traulsen), Max Planck Institute for Evolutionary Biology, Max Planck Society;
IMPRS for Evolutionary Biology, Max Planck Institute for Evolutionary Biology, Max Planck Society;

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Gallie,  Jenna       
Research Group Microbial Evolutionary Dynamics (Gallie), Department Evolutionary Theory (Traulsen), Max Planck Institute for Evolutionary Biology, Max Planck Society;

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elife-81005-v1.pdf
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elife-81005-mdarchecklist1-v1.docx
(Supplementary material), 102KB

elife-81005-supp3-v1.xlsx
(Supplementary material), 181KB

elife-81005-supp2-v1.xlsx
(Supplementary material), 151KB

elife-81005-supp1-v1.xlsx
(Supplementary material), 21KB

Citation

Raval, P. K., Ngan, W. Y., Gallie, J., & Agashe, D. (2023). The layered costs and benefits of translational redundancy. eLife, 12: e81005. doi:10.7554/eLife.81005.


Cite as: https://hdl.handle.net/21.11116/0000-000C-B453-B
Abstract
The rate and accuracy of translation hinges upon multiple components – including transfer RNA (tRNA) pools, tRNA modifying enzymes, and rRNA molecules – many of which are redundant in terms of gene copy number or function. It has been hypothesized that the redundancy evolves under selection, driven by its impacts on growth rate. However, we lack empirical measure-ments of the fitness costs and benefits of redundancy, and we have poor a understanding of how this redundancy is organized across components. We manipulated redundancy in multiple translation components of Escherichia coli by deleting 28 tRNA genes, 3 tRNA modifying systems, and 4 rRNA operons in various combinations. We find that redundancy in tRNA pools is beneficial when nutrients are plentiful and costly under nutrient limitation. This nutrient- dependent cost of redundant tRNA genes stems from upper limits to translation capacity and growth rate, and therefore varies as a function of the maximum growth rate attainable in a given nutrient niche. The loss of redundancy in rRNA genes and tRNA modifying enzymes had similar nutrient- dependent fitness consequences. Importantly, these effects are also contingent upon interactions across translation components, indicating a layered hierarchy from copy number of tRNA and rRNA genes to their expression and downstream processing. Overall, our results indicate both positive and negative selection on redundancy in translation components, depending on a species’ evolutionary history with feasts and famines.