The Crabtree Effect Shapes the Saccharomyces cerevisiae Lag Phase during the Switch between Different Carbon Sources

Perez-Samper, Gemma; Cerulus, Bram; Jariani, Abbas; Vermeersch, Lieselotte; Simancas, Nuria Barrajón; Bisschops, Markus M.M.; Brink, Joost van den; Solis-Escalante, Daniel; Gallone, Brigida; Maeyer, Dries De; Bael, Elise van; Wenseleers, Tom; Michiels, Jan; Marchal, Kathleen; Daran‐Lapujade, Pascale; Verstrepen, Kevin J.

doi:10.1128/mbio.01331-18

Cited by 54 publications

(59 citation statements)

References 76 publications

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“…Our hypothesis that HDB is due to a gradual decrease in respiratory activity during glucose growth is consistent with a previous report demonstrating a gradual decrease of respiration over multiple generations in glucose ( Slavov et al, 2014 ) as well as with a recent study showing the importance of respiration for a switch from glucose to other carbon sources ( Perez-Samper et al, 2018 ). Our results from the mating and heterokaryon experiments are also consistent with this hypothesis.…”

Section: Discussionsupporting

confidence: 93%

“…Cells can face sudden and dramatic changes in their environment such as nutrient depletion, temperature shifts, and osmotic shock. In general, cells adapt to such changes by activating and repressing specific genes and processes required to function in the new environment ( Brewster et al, 1993 ; Gasch et al, 2000 ; Jacob and Monod, 1961 ; Mitchell et al, 2009a ; Perez-Samper et al, 2018 ). Such physiological re-programming can take a considerable amount of time and resources during which the cells do not function optimally, a phenomenon known as the lag phase.…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Transition between fermentation and respiration determines history-dependent behavior in fluctuating carbon sources

Cerulus

Jariani

Perez-Samper

et al. 2018

eLife

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Cells constantly adapt to environmental fluctuations. These physiological changes require time and therefore cause a lag phase during which the cells do not function optimally. Interestingly, past exposure to an environmental condition can shorten the time needed to adapt when the condition re-occurs, even in daughter cells that never directly encountered the initial condition. Here, we use the molecular toolbox of Saccharomyces cerevisiae to systematically unravel the molecular mechanism underlying such history-dependent behavior in transitions between glucose and maltose. In contrast to previous hypotheses, the behavior does not depend on persistence of proteins involved in metabolism of a specific sugar. Instead, presence of glucose induces a gradual decline in the cells’ ability to activate respiration, which is needed to metabolize alternative carbon sources. These results reveal how trans-generational transitions in central carbon metabolism generate history-dependent behavior in yeast, and provide a mechanistic framework for similar phenomena in other cell types.

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Section: Discussionsupporting

confidence: 93%

Section: Introductionmentioning

confidence: 99%

Transition between fermentation and respiration determines history-dependent behavior in fluctuating carbon sources

Cerulus

Jariani

Perez-Samper

et al. 2018

eLife

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“…Furthermore, lag takes many forms and is characterised by complexity in relation to heterogeneity within populations of individual microbes, and in the context of evolutionary biology. For instance, a cell's environmental and life history can determine rates (and other aspects) of adaption including length of lag 96 . Many studies also show phenotypic and behavioural heterogenity within populations of individual strains [97][98][99][100] .…”

Section: Discussionmentioning

confidence: 99%

Microbial lag phase can be indicative of, or independent from, cellular stress

Hamill

Stevenson

McMullan

et al. 2020

Sci Rep

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Measures of microbial growth, used as indicators of cellular stress, are sometimes quantified at a single time-point. in reality, these measurements are compound representations of length of lag, exponential growth-rate, and other factors. Here, we investigate whether length of lag phase can act as a proxy for stress, using a number of model systems (Aspergillus penicillioides; Bacillus subtilis; Escherichia coli; Eurotium amstelodami, E. echinulatum, E. halophilicum, and e. repens; Mrakia frigida; Saccharomyces cerevisiae; Xerochrysium xerophilum; Xeromyces bisporus) exposed to mechanistically distinct types of cellular stress including low water activity, other solute-induced stresses, and dehydrationrehydration cycles. Lag phase was neither proportional to germination rate for X. bisporus (FRR3443) in glycerol-supplemented media (r 2 = 0.012), nor to exponential growth-rates for other microbes. In some cases, growth-rates varied greatly with stressor concentration even when lag remained constant. By contrast, there were strong correlations for B. subtilis in media supplemented with polyethyleneglycol 6000 or 600 (r 2 = 0.925 and 0.961), and for other microbial species. We also analysed data from independent studies of food-spoilage fungi under glycerol stress (Aspergillus aculeatinus and A. sclerotiicarbonarius); mesophilic/psychrotolerant bacteria under diverse, solute-induced stresses (Brochothrix thermosphacta, Enterococcus faecalis, Pseudomonas fluorescens, Salmonella typhimurium, Staphylococcus aureus); and fungal enzymes under acid-stress (Terfezia claveryi lipoxygenase and Agaricus bisporus tyrosinase). these datasets also exhibited diversity, with some strong-and moderate correlations between length of lag and exponential growth-rates; and sometimes none. in conclusion, lag phase is not a reliable measure of stress because length of lag and growth-rate inhibition are sometimes highly correlated, and sometimes not at all. Chemical reactions and thermodynamic and biological processes often experience a lag period prior to reaching their maximum rate. This phenomenon that can be observed at various levels; thermodynamic processes (e.g. thermal lag), chemical reactions, biochemical activities 1 , cellular physiology 2 , microbial growth kinetics, and ecosystem functions 3. The term lag, used in English since the early 14 th century, has been applied to biological processes since at least the 1680s 4. In the context of microbial growth kinetics, lag, once known as 'latency' , was studied since the 1800s, including work of Louis Pasteur 5. Despite this long pedigree of research into this phenomenon, however, some aspects of the biology and application of the lag phase are not yet resolved. Accurate assessments of microbial growth must account for the various growth processes, including: mycelial extension, cell division within planktonic populations, increases in the mass of individual cells, accumulation of compatible solutes or other endogenous reserves, cell elongation or growth, sporulation, germination,...

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“…Using a standard zymolyase-based protocol, genomic DNA was extracted from the two initial and four final samples. UPTAGs and DNTAGs were then amplified in separate PCR reactions using the primers described in Perez-Samper et al. (2018) .…”

Section: Methodsmentioning

confidence: 99%

Gene Loss Predictably Drives Evolutionary Adaptation

Helsen

Voordeckers

Vanderwaeren

et al. 2020

Molecular Biology and Evolution

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Abstract Loss of gene function is common throughout evolution, even though it often leads to reduced fitness. In this study, we systematically evaluated how an organism adapts after deleting genes that are important for growth under oxidative stress. By evolving, sequencing, and phenotyping over 200 yeast lineages, we found that gene loss can enhance an organism’s capacity to evolve and adapt. Whereas gene loss often led to an immediate decrease in fitness, many mutants rapidly acquired suppressor mutations that restored fitness. Depending on the strain’s genotype, some ultimately even attained higher fitness levels than similarly adapted wild-type cells. Further, cells with deletions in different modules of the genetic network followed distinct and predictable mutational trajectories. Finally, losing highly connected genes increased evolvability by facilitating the emergence of a more diverse array of phenotypes after adaptation. Together, our findings show that loss of specific parts of a genetic network can facilitate adaptation by opening alternative evolutionary paths.

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The Crabtree Effect Shapes the Saccharomyces cerevisiae Lag Phase during the Switch between Different Carbon Sources

Cited by 54 publications

References 76 publications

Transition between fermentation and respiration determines history-dependent behavior in fluctuating carbon sources

Transition between fermentation and respiration determines history-dependent behavior in fluctuating carbon sources

Microbial lag phase can be indicative of, or independent from, cellular stress

Gene Loss Predictably Drives Evolutionary Adaptation

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