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The natural history of molecular functions inferred from an extensive phylogenomic analysis of gene ontology data

Ibrahim Koç, Gustavo Caetano-Anollés 


The origin and natural history of molecular functions hold the key to the emergence of cellular organization and modern biochemistry. Here we use a genomic census of Gene Ontology (GO) terms to reconstruct phylogenies at the three highest (1, 2 and 3) and the lowest (terminal) levels of the hierarchy of molecular functions, which reflect the broadest and the most specific GO definitions, respectively. These phylogenies define evolutionary timelines of functional innovation. We analyzed 249 free-living organisms comprising the three superkingdoms of life, Archaea, Bacteria, and Eukarya. Phylogenies indicate catalytic, binding and transport functions were the oldest, suggesting a ‘metabolism-first’ origin scenario for biochemistry. Metabolism made use of increasingly complicated organic chemistry. Primordial features of ancient molecular functions and functional recruitments were further distilled by studying the oldest child terms of the oldest level 1 GO definitions. Network analyses showed the existence of an hourglass pattern of enzyme recruitment in the molecular functions of the directed acyclic graph of molecular functions. Older high-level molecular functions were thoroughly recruited at younger lower levels, while very young high-level functions were used throughout the timeline. This pattern repeated in every one of the three mappings, which gave a criss-cross pattern. The timelines and their mappings were remarkable. They revealed the progressive evolutionary development of functional toolkits, starting with the early rise of metabolic activities, followed chronologically by the rise of macromolecular biosynthesis, the establishment of controlled interactions with the environment and self, adaptation to oxygen, and enzyme coordinated regulation, and ending with the rise of structural and cellular complexity. This historical account holds important clues for dissection of the emergence of biomcomplexity and life.

Citation: Koç I, Caetano-Anollés G (2017) The natural history of molecular functions inferred from an extensive phylogenomic analysis of gene ontology data. PLoS ONE 12(5): e0176129.

Editor: Natarajan Kannan, University of Georgia, UNITED STATES

Received: August 2, 2016; Accepted: April 5, 2017; Published: May 3, 2017

Copyright: © 2017 Koç, Caetano-Anollés. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All relevant data are within the paper and its Supporting Information files.

Funding: Computational biology in the Evolutionary Bioinformatics Laboratory (EBL) is supported by grants from the National Science Foundation (OISE-1132791) and the United States Department of Agriculture (ILLU-802-909 and ILLU-483-625) and by a Blue Waters computer grid allocation of the National Center for Supercomputer Applications (NCSA) to GCA. The visit of IK to EBL was supported by a grant from Scientific and Technological Research Council of Turkey (TUBITAK, No. no. 1059B141400573). All funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.