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Christiaens J.F.,VIB Laboratory of Systems Biology | Christiaens J.F.,Catholic University of Leuven | Franco L.M.,Catholic University of Leuven | Franco L.M.,Center for the Biology of Disease | And 9 more authors.
Cell Reports | Year: 2014

Yeast cells produce various volatile metabolites that are key contributors to the pleasing fruity and flowery aroma of fermented beverages. Several of these fruity metabolites, including isoamyl acetate and ethyl acetate, are produced by a dedicated enzyme, the alcohol acetyl transferase Atf1. However, despite much research, the physiological role of acetate ester formation in yeast remains unknown. Using a combination of molecular biology, neurobiology, and behavioral tests, we demonstrate that deletion of ATF1 alters the olfactory response in the antennal lobe of fruit flies that feed on yeast cells. The flies are much less attracted to the mutant yeast cells, and this in turn results in reduced dispersal of the mutant yeast cells by the flies. Together, our results uncover the molecular details of an intriguing aroma-based communication and mutualism between microbes and their insect vectors. Similar mechanisms may exist in other microbes, including microbes on flowering plants and pathogens. © 2014 The Authors.


PubMed | VIB, Catholic University of Leuven, VIB Laboratory of Systems Biology, Stanford University and The Switch
Type: | Journal: Scientific reports | Year: 2016

Hexanucleotide repeat expansions in C9orf72 are the most common cause of amyotrophic lateral sclerosis (ALS) and frontotemporal degeneration (FTD) (c9ALS/FTD). Unconventional translation of these repeats produces dipeptide repeat proteins (DPRs) that may cause neurodegeneration. We performed a modifier screen in Drosophila and discovered a critical role for importins and exportins, Ran-GTP cycle regulators, nuclear pore components, and arginine methylases in mediating DPR toxicity. These findings provide evidence for an important role for nucleocytoplasmic transport in the pathogenic mechanism of c9ALS/FTD.


Cerulus B.,Catholic University of Leuven | Cerulus B.,VIB Laboratory of Systems Biology | New A.,Catholic University of Leuven | New A.,VIB Laboratory of Systems Biology | And 6 more authors.
Current Biology | Year: 2016

The fitness effect of biological noise remains unclear. For example, even within clonal microbial populations, individual cells grow at different speeds. Although it is known that the individuals' mean growth speed can affect population-level fitness, it is unclear how or whether growth speed heterogeneity itself is subject to natural selection. Here, we show that noisy single-cell division times can significantly affect population-level growth rate. Using time-lapse microscopy to measure the division times of thousands of individual S. cerevisiae cells across different genetic and environmental backgrounds, we find that the length of individual cells' division times can vary substantially between clonal individuals and that sublineages often show epigenetic inheritance of division times. By combining these experimental measurements with mathematical modeling, we find that, for a given mean division time, increasing heterogeneity and epigenetic inheritance of division times increases the population growth rate. Furthermore, we demonstrate that the heterogeneity and epigenetic inheritance of single-cell division times can be linked with variation in the expression of catabolic genes. Taken together, our results reveal how a change in noisy single-cell behaviors can directly influence fitness through dynamics that operate independently of effects caused by changes to the mean. These results not only allow a better understanding of microbial fitness but also help to more accurately predict fitness in other clonal populations, such as tumors. The fitness effect of growth noise is poorly understood. Cerulus et al. show that certain yeast populations can show high variability and epigenetic inheritance of division times. Mathematical modeling shows that, for a given mean, increasing these traits increases the population growth rate. These traits are linked to catabolic gene expression. © 2016 Elsevier Ltd.


New A.M.,VIB Laboratory of Systems Biology | New A.M.,Catholic University of Leuven | Cerulus B.,VIB Laboratory of Systems Biology | Cerulus B.,Catholic University of Leuven | And 11 more authors.
PLoS Biology | Year: 2014

Organisms respond to environmental changes by adapting the expression of key genes. However, such transcriptional reprogramming requires time and energy, and may also leave the organism ill-adapted when the original environment returns. Here, we study the dynamics of transcriptional reprogramming and fitness in the model eukaryote Saccharomyces cerevisiae in response to changing carbon environments. Population and single-cell analyses reveal that some wild yeast strains rapidly and uniformly adapt gene expression and growth to changing carbon sources, whereas other strains respond more slowly, resulting in long periods of slow growth (the so-called "lag phase") and large differences between individual cells within the population. We exploit this natural heterogeneity to evolve a set of mutants that demonstrate how the frequency and duration of changes in carbon source can favor different carbon catabolite repression strategies. At one end of this spectrum are "specialist" strategies that display high rates of growth in stable environments, with more stringent catabolite repression and slower transcriptional reprogramming. The other mutants display less stringent catabolite repression, resulting in leaky expression of genes that are not required for growth in glucose. This "generalist" strategy reduces fitness in glucose, but allows faster transcriptional reprogramming and shorter lag phases when the cells need to shift to alternative carbon sources. Whole-genome sequencing of these mutants reveals that mutations in key regulatory genes such as HXK2 and STD1 adjust the regulation and transcriptional noise of metabolic genes, with some mutations leading to alternative gene regulatory strategies that allow "stochastic sensing" of the environment. Together, our study unmasks how variable and stable environments favor distinct strategies of transcriptional reprogramming and growth. © 2014 New et al.


Aslankoohi E.,VIB Laboratory of Systems Biology | Aslankoohi E.,Catholic University of Leuven | Zhu B.,VIB Laboratory of Systems Biology | Zhu B.,Catholic University of Leuven | And 9 more authors.
Applied and Environmental Microbiology | Year: 2013

The behavior of yeast cells during industrial processes such as the production of beer, wine, and bioethanol has been extensively studied. In contrast, our knowledge about yeast physiology during solid-state processes, such as bread dough, cheese, or cocoa fermentation, remains limited. We investigated changes in the transcriptomes of three genetically distinct Saccharomyces cerevisiae strains during bread dough fermentation. Our results show that regardless of the genetic background, all three strains exhibit similar changes in expression patterns. At the onset of fermentation, expression of glucose-regulated genes changes dramatically, and the osmotic stress response is activated. The middle fermentation phase is characterized by the induction of genes involved in amino acid metabolism. Finally, at the latest time point, cells suffer from nutrient depletion and activate pathways associated with starvation and stress responses. Further analysis shows that genes regulated by the high-osmolarity glycerol (HOG) pathway, the major pathway involved in the response to osmotic stress and glycerol homeostasis, are among the most differentially expressed genes at the onset of fermentation. More importantly, deletion of HOG1 and other genes of this pathway significantly reduces the fermentation capacity. Together, our results demonstrate that cells embedded in a solid matrix such as bread dough suffer severe osmotic stress and that a proper induction of the HOG pathway is critical for optimal fermentation. © 2013, American Society for Microbiology.


Vervoort Y.,VIB Laboratory of Systems Biology | Vervoort Y.,Catholic University of Leuven | Herrera-Malaver B.,VIB Laboratory of Systems Biology | Herrera-Malaver B.,Catholic University of Leuven | And 13 more authors.
Journal of Applied Microbiology | Year: 2016

Aim: Plant materials used in the food industry contain up to five times more aromas bound to glucose (glucosides) than free, unbound aromas, making these bound aromas an unused flavouring potential. The aim of this study was to identify and purify a novel β-glucosidase from Brettanomyces yeasts that are capable of releasing bound aromas present in various food products. Methods and Results: We screened 428 different yeast strains for β-glucosidase activity and are the first to sequence the whole genome of two Brettanomyces yeasts (Brettanomyces anomalus and Brettanomyces bruxellensis) with exceptionally high β-glucosidase activity. Heterologous expression and purification of the identified B. anomalus β-glucosidase showed that it has an optimal activity at a higher pH (5·75) and lower temperature (37°C) than commercial β-glucosidases. Adding this B. anomalus β-glucosidase to cherry beers and forest fruit milks resulted in increased amounts of benzyl alcohol, eugenol, linalool and methyl salicylate compared to Aspergillus niger and Almond glucosidase. Conclusions: The newly identified B. anomalus β-glucosidase offers new possibilities for food bioflavouring. Significance and Impact of the Study: This study is the first to sequence the B. anomalus genome and to identify the β-glucosidase-encoding genes of two Brettanomyces species, and reports a new bioflavouring enzyme. © 2016 The Authors. Journal of Applied Microbiology published by John Wiley & Sons Ltd on behalf of Society for Applied Microbiology.


PubMed | VIB Laboratory of Systems Biology
Type: Journal Article | Journal: Applied and environmental microbiology | Year: 2013

The behavior of yeast cells during industrial processes such as the production of beer, wine, and bioethanol has been extensively studied. In contrast, our knowledge about yeast physiology during solid-state processes, such as bread dough, cheese, or cocoa fermentation, remains limited. We investigated changes in the transcriptomes of three genetically distinct Saccharomyces cerevisiae strains during bread dough fermentation. Our results show that regardless of the genetic background, all three strains exhibit similar changes in expression patterns. At the onset of fermentation, expression of glucose-regulated genes changes dramatically, and the osmotic stress response is activated. The middle fermentation phase is characterized by the induction of genes involved in amino acid metabolism. Finally, at the latest time point, cells suffer from nutrient depletion and activate pathways associated with starvation and stress responses. Further analysis shows that genes regulated by the high-osmolarity glycerol (HOG) pathway, the major pathway involved in the response to osmotic stress and glycerol homeostasis, are among the most differentially expressed genes at the onset of fermentation. More importantly, deletion of HOG1 and other genes of this pathway significantly reduces the fermentation capacity. Together, our results demonstrate that cells embedded in a solid matrix such as bread dough suffer severe osmotic stress and that a proper induction of the HOG pathway is critical for optimal fermentation.


PubMed | Leuven Food Science and Nutrition Research Center and VIB Laboratory of Systems Biology
Type: Journal Article | Journal: Journal of applied microbiology | Year: 2016

Plant materials used in the food industry contain up to five times more aromas bound to glucose (glucosides) than free, unbound aromas, making these bound aromas an unused flavouring potential. The aim of this study was to identify and purify a novel -glucosidase from Brettanomyces yeasts that are capable of releasing bound aromas present in various food products.We screened 428 different yeast strains for -glucosidase activity and are the first to sequence the whole genome of two Brettanomyces yeasts (Brettanomyces anomalus and Brettanomyces bruxellensis) with exceptionally high -glucosidase activity. Heterologous expression and purification of the identified B.anomalus -glucosidase showed that it has an optimal activity at a higher pH (575) and lower temperature (37C) than commercial -glucosidases. Adding this B.anomalus -glucosidase to cherry beers and forest fruit milks resulted in increased amounts of benzyl alcohol, eugenol, linalool and methyl salicylate compared to Aspergillus niger and Almond glucosidase.The newly identified B.anomalus -glucosidase offers new possibilities for food bioflavouring.This study is the first to sequence the B.anomalus genome and to identify the -glucosidase-encoding genes of two Brettanomyces species, and reports a new bioflavouring enzyme.

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