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The Phylogenomic Roots of Modern Biochemistry: Origins of Proteins, Cofactors and Protein Biosynthesis

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An Erratum to this article was published on 01 February 2012

Abstract

The complexity of modern biochemistry developed gradually on early Earth as new molecules and structures populated the emerging cellular systems. Here, we generate a historical account of the gradual discovery of primordial proteins, cofactors, and molecular functions using phylogenomic information in the sequence of 420 genomes. We focus on structural and functional annotations of the 54 most ancient protein domains. We show how primordial functions are linked to folded structures and how their interaction with cofactors expanded the functional repertoire. We also reveal protocell membranes played a crucial role in early protein evolution and show translation started with RNA and thioester cofactor-mediated aminoacylation. Our findings allow elaboration of an evolutionary model of early biochemistry that is firmly grounded in phylogenomic information and biochemical, biophysical, and structural knowledge. The model describes how primordial α-helical bundles stabilized membranes, how these were decorated by layered arrangements of β-sheets and α-helices, and how these arrangements became globular. Ancient forms of aminoacyl-tRNA synthetase (aaRS) catalytic domains and ancient non-ribosomal protein synthetase (NRPS) modules gave rise to primordial protein synthesis and the ability to generate a code for specificity in their active sites. These structures diversified producing cofactor-binding molecular switches and barrel structures. Accretion of domains and molecules gave rise to modern aaRSs, NRPS, and ribosomal ensembles, first organized around novel emerging cofactors (tRNA and carrier proteins) and then more complex cofactor structures (rRNA). The model explains how the generation of protein structures acted as scaffold for nucleic acids and resulted in crystallization of modern translation.

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Abbreviations

aaRS:

Aminoacyl-tRNA synthetase

CoA:

Coenzyme A

F:

Fold

FSF:

Fold superfamily

FF:

Fold family

nd:

Node distance

PCP:

Peptidyl carrier protein

r-protein:

Ribosomal protein

SCOP:

Structural classification of proteins

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Acknowledgments

Research was supported by the National Science Foundation (MCB-0749836), 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, Urbana, IL, 61801, USA

    Gustavo Caetano-Anollés & Derek Caetano-Anollés

  2. Korean Bioinformation Center (KOBIC), Korea Research Institute of Bioscience and Biotechnology (KRIBB), 111 Gwahangno, Yuseong-gu, Daejeon, 305-806, Korea

    Kyung Mo Kim

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

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An erratum to this article can be found at http://dx.doi.org/10.1007/s00239-012-9485-4.

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Caetano-Anollés, G., Kim, K.M. & Caetano-Anollés, D. The Phylogenomic Roots of Modern Biochemistry: Origins of Proteins, Cofactors and Protein Biosynthesis. J Mol Evol 74, 1–34 (2012). https://doi.org/10.1007/s00239-011-9480-1

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