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Metabolic excretion associated with nutrient-growth dysregulation promotes the rapid evolution of an overt metabolic defect.

ABSTRACT: In eukaryotes, conserved mechanisms ensure that cell growth is coordinated with nutrient availability. Overactive growth during nutrient limitation ("nutrient-growth dysregulation") can lead to rapid cell death. Here, we demonstrate that cells can adapt to nutrient-growth dysregulation by evolving major metabolic defects. Specifically, when yeast lysine-auxotrophic mutant lys- encountered lysine limitation, an evolutionarily novel stress, cells suffered nutrient-growth dysregulation. A subpopulation repeatedly evolved to lose the ability to synthesize organosulfurs (lys-orgS-). Organosulfurs, mainly reduced glutathione (GSH) and GSH conjugates, were released by lys- cells during lysine limitation when growth was dysregulated, but not during glucose limitation when growth was regulated. Limiting organosulfurs conferred a frequency-dependent fitness advantage to lys-orgS- by eliciting a proper slow growth program, including autophagy. Thus, nutrient-growth dysregulation is associated with rapid organosulfur release, which enables the selection of organosulfur auxotrophy to better tune cell growth to the metabolic environment. We speculate that evolutionarily novel stresses can trigger atypical release of certain metabolites, setting the stage for the evolution of new ecological interactions.

SUBMITTER: Green R

PROVIDER: S-EPMC7470746 | biostudies-literature | 2020 Aug

REPOSITORIES: biostudies-literature

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Metabolic excretion associated with nutrient-growth dysregulation promotes the rapid evolution of an overt metabolic defect.

Green Robin R Sonal Wang Lin L Hart Samuel F M SFM Lu Wenyun W Skelding David D Burton Justin C JC Mi Hanbing H Capel Aric A Chen Hung Alex HA Lin Aaron A Subramaniam Arvind R AR Rabinowitz Joshua D JD Shou Wenying W

PLoS biology 20200824 8

In eukaryotes, conserved mechanisms ensure that cell growth is coordinated with nutrient availability. Overactive growth during nutrient limitation ("nutrient-growth dysregulation") can lead to rapid cell death. Here, we demonstrate that cells can adapt to nutrient-growth dysregulation by evolving major metabolic defects. Specifically, when yeast lysine-auxotrophic mutant lys- encountered lysine limitation, an evolutionarily novel stress, cells suffered nutrient-growth dysregulation. A subpopula ...[more]

PMID: 32833957

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Project description:Rapid adaptation can aid invasive populations in their competitive success. Resource allocation trade-off hypotheses predict higher resource availability or the lack of natural enemies in introduced ranges allow for increased growth and reproduction, thus contributing to invasive success. Evidence for such hypotheses is however equivocal and tests among multiple ranges over productivity gradients are required to provide a better understanding of the general applicability of these theories.Using common gardens, we investigated the adaptive divergence of various constitutive and inducible defence-related traits between the native North American and introduced European and Australian ranges, while controlling for divergence due to latitudinal trait clines, individual resource budgets, and population differentiation, using >11,000 SNPs.Rapid, repeated clinal adaptation in defence-related traits was apparent despite distinct demographic histories. We also identified divergence among ranges in some defence-related traits, although differences in energy budgets among ranges may explain some, but not all, defence-related trait divergence. We do not identify a general reduction in defence in concert with an increase in growth among the multiple introduced ranges as predicted trade-off hypotheses. Synthesis: The rapid spread of invasive species is affected by a multitude of factors, likely including adaptation to climate and escape from natural enemies. Unravelling the mechanisms underlying invasives' success enhances understanding of eco-evolutionary theory and is essential to inform management strategies in the face of ongoing climate change. OPEN RESEARCH BADGES:This article has been awarded Open Materials, Open Data, Preregistered Research Designs Badges. All materials and data are publicly accessible via the Open Science Framework at https://doi.org/10.6084/m9.figshare.8028875.v1, https://github.com/lotteanna/defence_adaptation,https://doi.org/10.1101/435271.

Dataset Information

Metabolic excretion associated with nutrient-growth dysregulation promotes the rapid evolution of an overt metabolic defect.

Publications

Metabolic excretion associated with nutrient-growth dysregulation promotes the rapid evolution of an overt metabolic defect.

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