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Mutations in global regulators lead to metabolic selection during adaptation to complex environments.

Saxer G, Krepps MD, Merkley ED, Ansong C, Deatherage Kaiser BL, Valovska MT, Ristic N, Yeh PT, Prakash VP, Leiser OP, Nakhleh L, Gibbons HS, Kreuzer HW, Shamoo Y - PLoS Genet. (2014)

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of BioSciences, Rice University, Houston, Texas, United States of America.

ABSTRACT
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.

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The underlying genetic diversity of the adapted populations is readily observed as phenotypic diversity, when plated on tetrazolium arabinose plates.When arabinose is provided as the carbon source, the diversity of genotypes in the adapted populations is seen as a marked increase in phenotypic diversity. Colony size, morphology and the ability to use arabinose (as indicated by the darkness of the colony) varied widely in the adapted populations compared to the ancestor.
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pgen-1004872-g002: The underlying genetic diversity of the adapted populations is readily observed as phenotypic diversity, when plated on tetrazolium arabinose plates.When arabinose is provided as the carbon source, the diversity of genotypes in the adapted populations is seen as a marked increase in phenotypic diversity. Colony size, morphology and the ability to use arabinose (as indicated by the darkness of the colony) varied widely in the adapted populations compared to the ancestor.

Mentions: As a consequence of weak selection, considerable genetic variation evolved over the course of our experiment. This was evident both at the phenotypic as well as the genotypic level. We observed considerable phenotypic variation in colony size and in the ability to utilize arabinose (Fig. 2), in redox activity, in exopolysaccharide content and loss of motility (S2A-D Figure, respectively). Interestingly, evolved E. coli populations had at least one colony among the 8 colonies assessed per population that lost motility, but only one single C. freundii colony out of all the colonies assessed (two sets of 96 colonies in total) lost motility (S1 Text).


Mutations in global regulators lead to metabolic selection during adaptation to complex environments.

Saxer G, Krepps MD, Merkley ED, Ansong C, Deatherage Kaiser BL, Valovska MT, Ristic N, Yeh PT, Prakash VP, Leiser OP, Nakhleh L, Gibbons HS, Kreuzer HW, Shamoo Y - PLoS Genet. (2014)

The underlying genetic diversity of the adapted populations is readily observed as phenotypic diversity, when plated on tetrazolium arabinose plates.When arabinose is provided as the carbon source, the diversity of genotypes in the adapted populations is seen as a marked increase in phenotypic diversity. Colony size, morphology and the ability to use arabinose (as indicated by the darkness of the colony) varied widely in the adapted populations compared to the ancestor.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC4263409&req=5

pgen-1004872-g002: The underlying genetic diversity of the adapted populations is readily observed as phenotypic diversity, when plated on tetrazolium arabinose plates.When arabinose is provided as the carbon source, the diversity of genotypes in the adapted populations is seen as a marked increase in phenotypic diversity. Colony size, morphology and the ability to use arabinose (as indicated by the darkness of the colony) varied widely in the adapted populations compared to the ancestor.
Mentions: As a consequence of weak selection, considerable genetic variation evolved over the course of our experiment. This was evident both at the phenotypic as well as the genotypic level. We observed considerable phenotypic variation in colony size and in the ability to utilize arabinose (Fig. 2), in redox activity, in exopolysaccharide content and loss of motility (S2A-D Figure, respectively). Interestingly, evolved E. coli populations had at least one colony among the 8 colonies assessed per population that lost motility, but only one single C. freundii colony out of all the colonies assessed (two sets of 96 colonies in total) lost motility (S1 Text).

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of BioSciences, Rice University, Houston, Texas, United States of America.

ABSTRACT
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.

Show MeSH
Related in: MedlinePlus