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A Tree of Cellular Life Inferred from a Genomic Census of Molecular Functions

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Abstract

Phylogenomics aims to describe evolutionary relatedness between organisms by analyzing genomic data. The common practice is to produce phylogenomic trees from molecular information in the sequence, order, and content of genes in genomes. These phylogenies describe the evolution of life and become valuable tools for taxonomy. The recent availability of structural and functional data for hundreds of genomes now offers the opportunity to study evolution using more deep, conserved, and reliable sets of molecular features. Here, we reconstruct trees of life from the functions of proteins. We start by inferring rooted phylogenomic trees and networks of organisms directly from Gene Ontology annotations. Phylogenies and networks yield novel insights into the emergence and evolution of cellular life. The ancestor of Archaea originated earlier than the ancestors of Bacteria and Eukarya and was thermophilic. In contrast, basal bacterial lineages were non-thermophilic. A close relationship between Plants and Metazoa was also identified that disagrees with the traditional Fungi-Metazoa grouping. While measures of evolutionary reticulation were minimum in Eukarya and maximum in Bacteria, the massive role of horizontal gene transfer in microbes did not materialize in phylogenomic networks. Phylogenies and networks also showed that the best reconstructions were recovered when problematic taxa (i.e., parasitic/symbiotic organisms) and horizontally transferred characters were excluded from analysis. Our results indicate that functionomic data represent a useful addition to the set of molecular characters used for tree reconstruction and that trees of cellular life carry in deep branches considerable predictive power to explain the evolution of living organisms.

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Acknowledgments

We are thankful to the members of GCA laboratory for fruitful discussions and anonymous reviewers who reviewed the paper and provided comments that significantly improved the manuscript. Research was supported by grants from the National Science Foundation (MCB-0749836 and OISE-1132791) and the United States Department of Agriculture (ILLU-802-909 and ILLU-483-625) to GCA and grants from KRIBB Research Initiative Program and the Next-Generation BioGreen 21 Program, Rural Development Administration (PJ0090192013) to KMK.

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  1. Kyuin Hwang

    Present address: Division of Polar Life Sciences, Korea Polar Research Institute, Incheon, 406-840, Republic of Korea

Authors and Affiliations

  1. Microbial Resource Center, Korea Research Institute of Bioscience and Biotechnology, Daejeon, 305-806, Korea

    Kyung Mo Kim & Kyuin Hwang

  2. Department of Bioinformatics, University of Science and Technology, Daejeon, 305-350, Korea

    Kyung Mo Kim & Kyuin Hwang

  3. Evolutionary Bioinformatics Laboratory, Department of Crop Sciences, University of Illinois, Urbana, IL, 61801, USA

    Arshan Nasir & Gustavo Caetano-Anollés

  4. Illinois Informatics Institute, University of Illinois, Urbana, IL, 61801, USA

    Arshan Nasir & Gustavo Caetano-Anollés

Authors
  1. Kyung Mo Kim
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  2. Arshan Nasir
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  3. Kyuin Hwang
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  4. Gustavo Caetano-Anollés
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Corresponding author

Correspondence to Gustavo Caetano-Anollés.

Additional information

Kyung Mo Kim and Arshan Nasir contributed equally to this work.

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Kim, K.M., Nasir, A., Hwang, K. et al. A Tree of Cellular Life Inferred from a Genomic Census of Molecular Functions. J Mol Evol 79, 240–262 (2014). https://doi.org/10.1007/s00239-014-9637-9

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  • DOI: https://doi.org/10.1007/s00239-014-9637-9

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