Bacterial fitness landscapes stratify based on proteome allocation associated with discrete aero-types

PLoS Comput Biol. 2021 Jan 19;17(1):e1008596. doi: 10.1371/journal.pcbi.1008596. eCollection 2021 Jan.

Abstract

The fitness landscape is a concept commonly used to describe evolution towards optimal phenotypes. It can be reduced to mechanistic detail using genome-scale models (GEMs) from systems biology. We use recently developed GEMs of Metabolism and protein Expression (ME-models) to study the distribution of Escherichia coli phenotypes on the rate-yield plane. We found that the measured phenotypes distribute non-uniformly to form a highly stratified fitness landscape. Systems analysis of the ME-model simulations suggest that this stratification results from discrete ATP generation strategies. Accordingly, we define "aero-types", a phenotypic trait that characterizes how a balanced proteome can achieve a given growth rate by modulating 1) the relative utilization of oxidative phosphorylation, glycolysis, and fermentation pathways; and 2) the differential employment of electron-transport-chain enzymes. This global, quantitative, and mechanistic systems biology interpretation of fitness landscape formed upon proteome allocation offers a fundamental understanding of bacterial physiology and evolution dynamics.

Publication types

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

MeSH terms

  • Adenosine Triphosphate / metabolism
  • Escherichia coli Proteins / genetics
  • Escherichia coli Proteins / metabolism
  • Escherichia coli* / classification
  • Escherichia coli* / genetics
  • Escherichia coli* / metabolism
  • Evolution, Molecular
  • Gene Expression Regulation, Bacterial / genetics
  • Genetic Fitness / genetics*
  • Genome, Bacterial / genetics
  • Models, Genetic
  • Nitrates / metabolism
  • Phenotype
  • Proteome* / genetics
  • Proteome* / metabolism
  • Systems Biology

Substances

  • Escherichia coli Proteins
  • Nitrates
  • Proteome
  • Adenosine Triphosphate