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Mutations in Global Regulators Lead to Metabolic Selection during Adaptation to Complex Environments (Adaptation to Novel Environments Leads to Metabolic Selection)

Saxer, Gerda ; Krepps, Michael D ; Merkley, Eric D ; Ansong, Charles ; Deatherage Kaiser, Brooke L ; Valovska, Marie-Thérèse ; Ristic, Nikola ; Yeh, Ping T ; Prakash, Vittal P ; Leiser, Owen P ; Nakhleh, Luay ; Gibbons, Henry S ; Kreuzer, Helen W ; Shamoo, Yousif; Matic, Ivan (Editor)

2014, Vol.10(12), p.e1004872 [Tạp chí có phản biện]

ISSN: 1553-7390 ; E-ISSN: 1553-7404 ; DOI: 10.1371/journal.pgen.1004872

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  • Nhan đề:
    Mutations in Global Regulators Lead to Metabolic Selection during Adaptation to Complex Environments (Adaptation to Novel Environments Leads to Metabolic Selection)
  • Tác giả: Saxer, Gerda ; Krepps, Michael D ; Merkley, Eric D ; Ansong, Charles ; Deatherage Kaiser, Brooke L ; Valovska, Marie-Thérèse ; Ristic, Nikola ; Yeh, Ping T ; Prakash, Vittal P ; Leiser, Owen P ; Nakhleh, Luay ; Gibbons, Henry S ; Kreuzer, Helen W ; Shamoo, Yousif
  • Matic, Ivan (Editor)
  • Chủ đề: Research Article ; Biology And Life Sciences
  • Là 1 phần của: 2014, Vol.10(12), p.e1004872
  • Mô tả: 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. ; Changing environmental conditions are the norm in biology. However, understanding adaptation to complex environments presents many challenges. For example, adaptation to resource-rich environments can potentially have many successful evolutionary trajectories to increased fitness. Even in conditions of plenty, the utilization of numerous but novel resources can require multiple mutations before a benefit is accrued. We evolved two bacterial species isolated from the gut of healthy humans in two different, resource-rich media commonly used in the laboratory. We anticipated that under weak selection the population would evolve tremendous genetic diversity. Despite such a complex genetic background we were able to identify a strong degree of parallel evolution and using a combination of population proteomic and population genomic approaches we show that two global regulators, and are the principle targets of selection. Up-regulation of the different metabolic pathways that are controlled by these global regulators in combination with up-regulation of transporters that transport nutrients into the cell revealed increased use of the novel resources. Thus global regulators can provide a one-step model to shift metabolism efficiently and provide rapid a one-step reprogramming of the cell metabolic profile.
  • Ngôn ngữ: English
  • Số nhận dạng: ISSN: 1553-7390 ; E-ISSN: 1553-7404 ; DOI: 10.1371/journal.pgen.1004872

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