Program in Bioinformatics and Integrative Biology
Amino Acids, Peptides, and Proteins | Biochemical Phenomena, Metabolism, and Nutrition | Cellular and Molecular Physiology | Evolution | Molecular Biology | Nucleic Acids, Nucleotides, and Nucleosides | Structural Biology
Prokaryotes evolved to thrive in an extremely diverse set of habitats, and their proteomes bear signatures of environmental conditions. Although correlations between amino acid usage and environmental temperature are well-documented, understanding of the mechanisms of thermal adaptation remains incomplete. Here, we couple the energetic costs of protein folding and protein homeostasis to build a microscopic model explaining both the overall amino acid composition and its temperature trends. Low biosynthesis costs lead to low diversity of physical interactions between amino acid residues, which in turn makes proteins less stable and drives up chaperone activity to maintain appropriate levels of folded, functional proteins. Assuming that the cost of chaperone activity is proportional to the fraction of unfolded client proteins, we simulated thermal adaptation of model proteins subject to minimization of the total cost of amino acid synthesis and chaperone activity. For the first time, we predicted both the proteome-average amino acid abundances and their temperature trends simultaneously, and found strong correlations between model predictions and 402 genomes of bacteria and archaea. The energetic constraint on protein evolution is more apparent in highly expressed proteins, selected by codon adaptation index. We found that in bacteria, highly expressed proteins are similar in composition to thermophilic ones, whereas in archaea no correlation between predicted expression level and thermostability was observed. At the same time, thermal adaptations of highly expressed proteins in bacteria and archaea are nearly identical, suggesting that universal energetic constraints prevail over the phylogenetic differences between these domains of life.
chaperones, evolution, homeostasis, protein folding, thermophiles
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Copyright The Author 2017. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact email@example.com.
DOI of Published Version
Mol Biol Evol. 2018 Jan 1;35(1):211-224. doi: 10.1093/molbev/msx282. Link to article on publisher's site
Molecular biology and evolution
Venev SV, Zeldovich KB. (2018). Thermophilic Adaptation in Prokaryotes Is Constrained by Metabolic Costs of Proteostasis. Open Access Publications by UMass Chan Authors. https://doi.org/10.1093/molbev/msx282. Retrieved from https://escholarship.umassmed.edu/oapubs/3382
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This work is licensed under a Creative Commons Attribution-Noncommercial 4.0 License
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