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Proteome Evolution and the Metabolic Origins of Translation and Cellular Life

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Abstract

The origin of life has puzzled molecular scientists for over half a century. Yet fundamental questions remain unanswered, including which came first, the metabolic machinery or the encoding nucleic acids. In this study we take a protein-centric view and explore the ancestral origins of proteins. Protein domain structures in proteomes are highly conserved and embody molecular functions and interactions that are needed for cellular and organismal processes. Here we use domain structure to study the evolution of molecular function in the protein world. Timelines describing the age and function of protein domains at fold, fold superfamily, and fold family levels of structural complexity were derived from a structural phylogenomic census in hundreds of fully sequenced genomes. These timelines unfold congruent hourglass patterns in rates of appearance of domain structures and functions, functional diversity, and hierarchical complexity, and revealed a gradual build up of protein repertoires associated with metabolism, translation and DNA, in that order. The most ancient domain architectures were hydrolase enzymes and the first translation domains had catalytic functions for the aminoacylation and the molecular switch-driven transport of RNA. Remarkably, the most ancient domains had metabolic roles, did not interact with RNA, and preceded the gradual build-up of translation. In fact, the first translation domains had also a metabolic origin and were only later followed by specialized translation machinery. Our results explain how the generation of structure in the protein world and the concurrent crystallization of translation and diversified cellular life created further opportunities for proteomic diversification.

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Abbreviations

aRS:

Aminoacyl-tRNA synthetase

F:

Fold

FSF:

Fold superfamily

FF:

Fold family

Nd:

Node distance

r-Protein:

Ribosomal protein

SCOP:

Structural classification of proteins

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Acknowledgments

A substantial portion of this work is part of DCA’s undergraduate thesis. We thank Ajith Harish and Feng-Jie Sun for providing data on RNA-protein interactions, Minglei Wang for phylogenomic reconstruction, and Rakhee Kalelkar for help with construction of Z-diagrams. Research was supported by the National Science Foundation (MCB-0749836), the Illinois C-FAR program, CREES-USDA, and the International Atomic Energy Agency in Vienna. Any opinions, findings, and conclusions and recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the funding agencies.

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  1. Evolutionary Bioinformatics Laboratory, Department of Crop Sciences, University of Illinois, 332 NSRC, 1101 W Peabody Drive, Urbana, IL, 61801, USA

    Derek Caetano-Anollés, Kyung Mo Kim & Gustavo Caetano-Anollés

  2. School of Molecular and Cellular Biology, University of Illinois, Urbana, IL, 61801, USA

    Derek Caetano-Anollés

  3. Department of Cell and Developmental Biology, University of Illinois, Urbana, IL, 61801, USA

    Jay E. Mittenthal

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  1. Derek Caetano-Anollés
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Correspondence to Gustavo Caetano-Anollés.

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Caetano-Anollés, D., Kim, K.M., Mittenthal, J.E. et al. Proteome Evolution and the Metabolic Origins of Translation and Cellular Life. J Mol Evol 72, 14–33 (2011). https://doi.org/10.1007/s00239-010-9400-9

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