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

Cerulus, Bram; Jariani, Abbas; Perez-Samper, Gemma; Vermeersch, Lieselotte; Pietsch, Julian; Crane, Matthew M.; New, Aaron M.; Gallone, Brigida; Roncoroni, Miguel; Dzialo, Maria C.; Govers, Sander K.; Hendrickx, Jhana O.; Galle, Eva; Coomans, Maarten; Berden, Pieter; Verbandt, Sara; Swain, Peter S.; Verstrepen, Kevin J.

doi:10.7554/elife.39234

Cited by 48 publications

(77 citation statements)

References 74 publications

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“…For instance, a study of S. cerevisiae cells from a glucose-containing (sole carbon source) medium were placed into a maltose-containing medium revealed profound differences in lag phase times. Indeed, up to 90% of cells never left the lag phase during the experimental period 101 , which may indicate genetic and/or epigenetic variation within the population; either of which can provide the basis for evolutionary changes 99 . Further examples can be found in the recent review by Bertrand 86 .…”

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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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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“…Recent studies have shown that genetically identical cells can vary in the time they need to adapt to the same nutrient switch (lag time), and often a fraction of cells cannot adapt at all [2][3][4][5][6][7][8][9]. This heterogeneity in response is primarily due to phenotypic differences among cells at the time of the switch, for instance in their protein levels or metabolic fluxes [2][3][4][5][6][7][8][9][10]. For example, the ability of Escherichia coli cells to switch from growth on glucose to growth on lactose depends on how many proteins of the lactose pathway the cells have at the time of the switch [9].…”

Section: Introductionmentioning

confidence: 99%

Metabolic activity affects response of single cells to a nutrient switch in structured populations

Ackermann

Vliet

2019

Preprint

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Microbes live in ever-changing environments where they need to adapt their metabolism to different nutrient conditions. Many studies have characterized the response of genetically identical cells to nutrient switches in homogenous cultures, however in nature microbes often live in spatially structured groups such as biofilms where cells can create metabolic gradients by consuming and releasing nutrients. Consequently, cells experience different local microenvironments and vary in their phenotype. How does this phenotypic variation affect the ability of cells to cope with nutrient switches? Here we address this question by growing dense populations of Escherichia coli in microfluidic chambers and studying a switch from glucose to acetate at the single cell level. Before the switch, cells vary in their metabolic activity: some grow on glucose while others cross-feed on acetate. After the switch, only few cells can resume growth after a period of lag. The probability to resume growth depends on a cells' phenotype prior to the switch: it is highest for cells crossfeeding on acetate, while it depends in a non-monotonic way on growth rate for cells growing on glucose. Our results suggest that the strong phenotypic variation in spatially structured populations might enhance their ability to cope with fluctuating environments.

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“…It is likely that this lag phase is a result of maintenance and propagation in media containing glucose as the only carbon source. The lag phase duration during a glucoseto-maltose shift in S. cerevisiae appears to be dependent mainly on the repressive effects of glucose on the respiratory metabolism [45]. With S. paradoxus, glucose repression seems to play a strong and a crucial role in the ability of the strains to use maltose.…”

Section: Discussionmentioning

confidence: 99%

Brewing potential of the wild yeast species Saccharomyces paradoxus

Nikulin

Vidgren

Krogerus

et al. 2020

Eur Food Res Technol

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Saccharomyces paradoxus is commonly isolated from environmental samples in Northern Europe and North America, but is rarely found associated with fermentation. However, as novelty has become a selling point in beer markets, interest toward non-conventional and local yeasts is increasing. Here, we report the first comprehensive investigation of the brewing potential of the species. Eight wild strains of S. paradoxus were isolated from oak trees growing naturally in Finland, screened in a series of fermentation trials and the most promising strain was selected for lager beer brewing at pilot scale (40 l). Yeasts were evaluated according to their ability to utilize wort sugars, their production of flavour-active aroma volatiles, diacetyl and organic acids, and sensorial quality of beers produced. All strains could assimilate maltose but this occurred after a considerable lag phase. Once adapted, most wild strains reached attenuation rates close to 70%. Adaptation to maltose could be maintained by re-pitching and with appropriate handling of the adapted yeast. Fermentation at 15 °C with the best performing strain was completed in 17 days. Maltose was consumed as efficiently as with a reference lager yeast, but no maltotriose use was observed. Bottled beers were evaluated by a trained sensory panel, and were generally rated as good as, or better than, reference beers. S. paradoxus beers were considered full-bodied and had a relatively clean flavour profile despite the presence of the clove-like 4-vinyl guaiacol. In conclusion, S. paradoxus exhibits a number of traits relevant to brewing, and with appropriate handling could be applied industrially.

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

Cited by 48 publications

References 74 publications

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

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

Metabolic activity affects response of single cells to a nutrient switch in structured populations

Brewing potential of the wild yeast species Saccharomyces paradoxus

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