Natural Variation in Preparation for Nutrient Depletion Reveals a Cost–Benefit Tradeoff

Wang, Jue; Atolia, Esha; Hua, Bo; Savir, Yonatan; Escalante-Chong, Renan; Springer, Michael

doi:10.1371/journal.pbio.1002041

Cited by 131 publications

(174 citation statements)

References 54 publications

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“…there is a trade-off between the speed of switching and the efficiency of switching. This recapitulates the relationship found empirically by Wang et al (2015). It really means that cells that for a cell to be able to switch fast, it needs to start to switch well before glucose is depleted from the environment.…”

Section: Introductionsupporting

confidence: 82%

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Limited by sensing - A minimal stochastic model of the lag-phase during diauxic growth

Chu

2017

Journal of Theoretical Biology

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Many microbes when grown on a mixture of two carbon sources utilise first and exclusively the preferred sugar, before switching to the less preferred carbon source. This results in two distinct exponential growth phases, often interrupted by a lag-phase of reduced growth termed the lag-phase. While the lag-phase appears to be an evolved feature, it is not clear what drives its evolution, as it comes with a substantial up-front fitness penalty due to lost growth. In this article a minimal mathematical model based on a master-equation approach is proposed. This model can explain many empirically observed phenomena. It suggests that the lag-phase can be understood as a manifestation of the trade-off between switching speed and switching efficiency. Moreover, the model predicts heterogeneity of the population during the lag-phase. Finally, it is shown that the switch from one carbon source to another one is a sensing problem and the lag-phase is a manifestation of known fundamental limitations of biological sensors.

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Section: Introductionsupporting

confidence: 82%

“…Interestingly, our minimal model reproduces the empirical relationship found by Wang et al (2015) between early switching and short lag-phase. Note that the Wang study focussed not on bacteria but on yeast which are regulated differently.…”

Section: Trade-off Between the Efficiency And The Speedsupporting

confidence: 71%

Limited by sensing - A minimal stochastic model of the lag-phase during diauxic growth

Chu

2017

Journal of Theoretical Biology

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“…1E) have a shorter diauxic lag than a strain that responds at a higher galactose to glucose ratio (YJM978; Fig. 1E) (38).…”

Section: Discussionmentioning

confidence: 90%

Galactose metabolic genes in yeast respond to a ratio of galactose and glucose

Escalante-Chong

Savir

Carroll

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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125

145

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Natural environments are filled with multiple, often competing, signals. In contrast, biological systems are often studied in "wellcontrolled" environments where only a single input is varied, potentially missing important interactions between signals. Catabolite repression of galactose by glucose is one of the best-studied eukaryotic signal integration systems. In this system, it is believed that galactose metabolic (GAL) genes are induced only when glucose levels drop below a threshold. In contrast, we show that GAL gene induction occurs at a constant external galactose:glucose ratio across a wide range of sugar concentrations. We systematically perturbed the components of the canonical galactose/glucose signaling pathways and found that these components do not account for ratio sensing. Instead we provide evidence that ratio sensing occurs upstream of the canonical signaling pathway and results from the competitive binding of the two sugars to hexose transporters. We show that a mutant that behaves as the classical model expects (i.e., cannot use galactose above a glucose threshold) has a fitness disadvantage compared with wild type. A number of common biological signaling motifs can give rise to ratio sensing, typically through negative interactions between opposing signaling molecules. We therefore suspect that this previously unidentified nutrient sensing paradigm may be common and overlooked in biology.nutrient signaling | signal integration | gene regulation | ratio sensing | yeast

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“…Many of the mutants displayed a reduced catabolite repression of maltose genes, which most likely explains the reduced recovery time after the abrupt shift to maltose [39]. In natural isolates of S. cerevisiae, a better recovery after a shift from glucose to galactose is influenced by the early induction of galactose utilization (GAL) genes, which prepares the transition to galactose metabolism in some strains [41]. In the reverse situation, when glucose is added to the system containing galactose, post-transcriptional regulation is involved through the degradation of galactose network transcripts [43].…”

Section: (B) Memorymentioning

confidence: 99%

Molecular and cellular bases of adaptation to a changing environment in microorganisms

Bleuven

Landry

2016

Proc. R. Soc. B.

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Environmental heterogeneity constitutes an evolutionary challenge for organisms. While evolutionary dynamics under variable conditions has been explored for decades, we still know relatively little about the cellular and molecular mechanisms involved. It is of paramount importance to examine these molecular bases because they may play an important role in shaping the course of evolution. In this review, we examine the diversity of adaptive mechanisms in the face of environmental changes. We exploit the recent literature on microbial systems because those have benefited the most from the recent emergence of genetic engineering and experimental evolution followed by genome sequencing. We identify four emerging trends: (i) an adaptive molecular change in a pathway often results in fitness trade-off in alternative environments but the effects are dependent on a mutation's genetic background; (ii) adaptive changes often modify transcriptional and signalling pathways; (iii) several adaptive changes may occur within the same molecular pathway but be associated with pleiotropy of different signs across environments; (iv) because of their large associated costs, macromolecular changes such as gene amplification and aneuploidy may be a rapid mechanism of adaptation in the short-term only. The course of adaptation in a variable environment, therefore, depends on the complexity of the environment but also on the molecular relationships among the genes involved and between the genes and the phenotypes under selection.

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Natural Variation in Preparation for Nutrient Depletion Reveals a Cost–Benefit Tradeoff

Abstract: Yeast can anticipate the depletion of a preferred nutrient by preemptively activating genes for alternative nutrients; the degree of this preparation varies across natural strains and is subject to a fitness tradeoff.

Cited by 131 publications

References 54 publications

Limited by sensing - A minimal stochastic model of the lag-phase during diauxic growth

Limited by sensing - A minimal stochastic model of the lag-phase during diauxic growth

Galactose metabolic genes in yeast respond to a ratio of galactose and glucose

Molecular and cellular bases of adaptation to a changing environment in microorganisms

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