Metabolic evolution of a deep-branching hyperthermophilic chemoautotrophic bacterium

PLoS One. 2014 Feb 5;9(2):e87950. doi: 10.1371/journal.pone.0087950. eCollection 2014.

Abstract

Aquifex aeolicus is a deep-branching hyperthermophilic chemoautotrophic bacterium restricted to hydrothermal vents and hot springs. These characteristics make it an excellent model system for studying the early evolution of metabolism. Here we present the whole-genome metabolic network of this organism and examine in detail the driving forces that have shaped it. We make extensive use of phylometabolic analysis, a method we recently introduced that generates trees of metabolic phenotypes by integrating phylogenetic and metabolic constraints. We reconstruct the evolution of a range of metabolic sub-systems, including the reductive citric acid (rTCA) cycle, as well as the biosynthesis and functional roles of several amino acids and cofactors. We show that A. aeolicus uses the reconstructed ancestral pathways within many of these sub-systems, and highlight how the evolutionary interconnections between sub-systems facilitated several key innovations. Our analyses further highlight three general classes of driving forces in metabolic evolution. One is the duplication and divergence of genes for enzymes as these progress from lower to higher substrate specificity, improving the kinetics of certain sub-systems. A second is the kinetic optimization of established pathways through fusion of enzymes, or their organization into larger complexes. The third is the minimization of the ATP unit cost to synthesize biomass, improving thermodynamic efficiency. Quantifying the distribution of these classes of innovations across metabolic sub-systems and across the tree of life will allow us to assess how a tradeoff between maximizing growth rate and growth efficiency has shaped the long-term metabolic evolution of the biosphere.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Amino Acids, Branched-Chain / biosynthesis
  • Bacteria / metabolism*
  • Biological Evolution*
  • Biosynthetic Pathways / genetics
  • Carbon Cycle
  • Chemoautotrophic Growth*
  • Citric Acid Cycle
  • Coenzymes / metabolism
  • Energy Metabolism
  • Metabolic Networks and Pathways*
  • Nucleotides / biosynthesis
  • Phylogeny
  • Pyrroles / metabolism
  • Thioctic Acid / biosynthesis
  • Thioctic Acid / chemistry

Substances

  • Amino Acids, Branched-Chain
  • Coenzymes
  • Nucleotides
  • Pyrroles
  • Thioctic Acid

Grant support

Parts of this work were performed under support from NSF FIBR grant nr. 0526747– The Emergence of Life: From Geochemistry to the Genetic Code. RB was further supported by an SFI Omidyar Fellowship at the Santa Fe Institute. ES thanks Insight Venture Partners for support. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.