Data from: Mutations in global regulators lead to metabolic selection during adaptation to complex environments

  • Luay Nakhleh (Contributor)
  • Eric D. Merkley (Contributor)
  • Gerda Saxer (Contributor)
  • Ping T. Yeh (Contributor)
  • Brooke L. Deatherage Kaiser (Contributor)
  • Vittal P. Prakash (Contributor)
  • Henry S. Gibbons (Contributor)
  • Helen W. Kreuzer (Contributor)
  • Michael D. Krepps (Contributor)
  • Marie-Thérèse Valovska (Contributor)
  • Charles Ansong (Contributor)
  • O. P. Leiser (Contributor)
  • Yousif Shamoo (Contributor)
  • Nikola Ristic (Contributor)



Adaptation to ecologically complex environments can provide insights into the evolutionary dynamics and functional constraints encountered by organisms during natural selection. Adaptation to a new environment with abundant and varied resources can be difficult to achieve by small incremental changes if many mutations are required to achieve even modest gains in fitness. Since changing complex environments are quite common in nature, we investigated how such an epistatic bottleneck can be avoided to allow rapid adaptation. We show that adaptive mutations arise repeatedly in independently evolved populations in the context of greatly increased genetic and phenotypic diversity. We go on to show that weak selection requiring substantial metabolic reprogramming can be readily achieved by mutations in the global response regulator arcA and the stress response regulator rpoS. We identified 46 unique single-nucleotide variants of arcA and 18 mutations in rpoS, nine of which resulted in stop codons or large deletions, suggesting that subtle modulations of ArcA function and knockouts of rpoS are largely responsible for the metabolic shifts leading to adaptation. These mutations allow a higher order metabolic selection that eliminates epistatic bottlenecks, which could occur when many changes would be required. Proteomic and carbohydrate analysis of adapting E. coli populations revealed an up-regulation of enzymes associated with the TCA cycle and amino acid metabolism, and an increase in the secretion of putrescine. The overall effect of adaptation across populations is to redirect and efficiently utilize uptake and catabolism of abundant amino acids. Concomitantly, there is a pronounced spread of more ecologically limited strains that results from specialization through metabolic erosion. Remarkably, the global regulators arcA and rpoS can provide a “one-step” mechanism of adaptation to a novel environment, which highlights the importance of global resource management as a powerful strategy to adaptation.,Saxer_et_al_PlosGen_CarbohydrateDataData from carbohydrate analyses of cell extract and spend media from E. coli RU1 ancestor and E. coli RU1-BHI evolved populationsSaxer_et_al_PlosGen_pHpH of stationary phase cultures of the ancestor and evolved populations of E. coli RU1 and C. freundii RU2 in LB and BHI (in their selective media)Saxer_et_al_PlosGen_MigrationDataMigration data of single colonies isolated from the populations of E. coli and C. freundii evolved in LB and BHISaxer_et_al_PlosGen_GrowthOD600_BHIOD readings of E. coli and C. freundii populations evolved in BHI over the course of a growth cycle in BHISaxer_et_al_PlosGen_GrowthOD600_LBOD readings of LB-evolved populations of E. coli and C. freundii in LB with the respective ancestorsSaxer_et_al_PlosGen_PopulationKey_correctedThis files contains the name of all the populations and ancestors, their selection regime and the accession number for the genomic and proteomics data, if applicable.,
Date made availableDec 1 2014

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