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Alternative Glycerol Balance Strategies among Saccharomyces Species in Response to Winemaking Stress.

Pérez-Torrado R, Oliveira BM, Zemančíková J, Sychrová H, Querol A - Front Microbiol (2016)

Bottom Line: The results show different pattern and level of expression among the different species, especially for STL1.These experiments also revealed a different functionality of the glycerol transporters among the different species studied.All these data point to different strategies to handle glycerol accumulation in response to winemaking stresses as hyperosmotic or cold-hyperosmotic stress in the different species, with variable emphasis in the production, influx, or efflux of glycerol.

View Article: PubMed Central - PubMed

Affiliation: Food Biotechnology Department, Systems Biology in Yeast of Biotechnological Interest, Instituto de Agroquímica y Tecnología de los Alimentos, IATA-CSIC Valencia, Spain.

ABSTRACT
Production and balance of glycerol is essential for the survival of yeast cells in certain stressful conditions as hyperosmotic or cold shock that occur during industrial processes as winemaking. These stress responses are well-known in S. cerevisiae, however, little is known in other phylogenetically close related Saccharomyces species associated with natural or fermentation environments such as S. uvarum, S. paradoxus or S. kudriavzevii. In this work we have investigated the expression of four genes (GPD1, GPD2, STL1, and FPS1) crucial in the glycerol pool balance in the four species with a biotechnological potential (S. cerevisiae; S. paradoxus; S. uvarum; and S. kudriavzevii), and the ability of strains to grow under osmotic and cold stresses. The results show different pattern and level of expression among the different species, especially for STL1. We also studied the function of Stl1 glycerol symporter in the survival to osmotic changes and cell growth capacity in winemaking environments. These experiments also revealed a different functionality of the glycerol transporters among the different species studied. All these data point to different strategies to handle glycerol accumulation in response to winemaking stresses as hyperosmotic or cold-hyperosmotic stress in the different species, with variable emphasis in the production, influx, or efflux of glycerol.

No MeSH data available.


Related in: MedlinePlus

Schematic representation of the weight of glycerol production, efflux, influx, or other actions regarding glycerol balance after hyperosmotic stress. This representation compares the dynamics of glycerol accumulation in response to hyperosmotic stress that has been quantitatively analyzed and modeled using physiologic, metabolic, enzymatic, and transcriptomic data of the key actors in S. cerevisiae (Petelenz-Kurdziel et al., 2013). Here we compared with the other species (S. paradoxus, S. uvarum, and S. kudriavzevii) using data provided in this work and others as Oliveira et al. (2014).
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Figure 6: Schematic representation of the weight of glycerol production, efflux, influx, or other actions regarding glycerol balance after hyperosmotic stress. This representation compares the dynamics of glycerol accumulation in response to hyperosmotic stress that has been quantitatively analyzed and modeled using physiologic, metabolic, enzymatic, and transcriptomic data of the key actors in S. cerevisiae (Petelenz-Kurdziel et al., 2013). Here we compared with the other species (S. paradoxus, S. uvarum, and S. kudriavzevii) using data provided in this work and others as Oliveira et al. (2014).

Mentions: In winemaking conditions, cells suffer hyperosmotic or cold hyperosmotic mild stresses that do not affect cell growth capacity in any Saccharomyces species (results not shown). This hyperosmotic stress produced by the elevated amount of sugars may determine different lag phase adaptations. In fact, significant differences can be observed in extra and intracellular glycerol levels and also in gene expression of key genes involved in glycerol homeostasis. These data also suggest that the Saccharomyces species are using different strategies to face alterations in the osmotic pressure and cold temperatures. In fact this argument is not that surprising since Saccharomyces species are genetically quite distant showing coding region identities such as the one showed when comparing human and mouse (85%; Lapidot et al., 2001). The dynamics of glycerol accumulation in hyperosmotic stress has been quantitatively analyzed and modeled using physiologic, metabolic, enzymatic, and transcriptomic data in S. cerevisiae (Petelenz-Kurdziel et al., 2013). The strategy of this species consists in a transcriptional activation of GPD1 to increase glycerol accumulation inside the cell by redirecting glycolytic flux. On the other hand, the glycerol efflux stops by the closing of Fps1channel. These are the principal mechanisms to balance glycerol after a hyperosmotic shock. Glycerol influx and other elements contribute in a minor fraction (Figure 6). From the results of this work and others, we can hypothesize that non-cerevisiae Saccharomyces species have changed the weight of the different elements involved in glycerol balance. Based on STL1 gene activation and Stl1 functionality assays we speculate that S. uvarum and S. kudriavzevii rely more in the glycerol import to compensate the osmotic pressure when extracellular glycerol is accumulated (Figure 6). This strategy is not exclusive of these species, In fact, it has been shown that the most osmotolerant yeasts species present a very efficient glycerol-import capacity (Lages et al., 1999).


Alternative Glycerol Balance Strategies among Saccharomyces Species in Response to Winemaking Stress.

Pérez-Torrado R, Oliveira BM, Zemančíková J, Sychrová H, Querol A - Front Microbiol (2016)

Schematic representation of the weight of glycerol production, efflux, influx, or other actions regarding glycerol balance after hyperosmotic stress. This representation compares the dynamics of glycerol accumulation in response to hyperosmotic stress that has been quantitatively analyzed and modeled using physiologic, metabolic, enzymatic, and transcriptomic data of the key actors in S. cerevisiae (Petelenz-Kurdziel et al., 2013). Here we compared with the other species (S. paradoxus, S. uvarum, and S. kudriavzevii) using data provided in this work and others as Oliveira et al. (2014).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4814467&req=5

Figure 6: Schematic representation of the weight of glycerol production, efflux, influx, or other actions regarding glycerol balance after hyperosmotic stress. This representation compares the dynamics of glycerol accumulation in response to hyperosmotic stress that has been quantitatively analyzed and modeled using physiologic, metabolic, enzymatic, and transcriptomic data of the key actors in S. cerevisiae (Petelenz-Kurdziel et al., 2013). Here we compared with the other species (S. paradoxus, S. uvarum, and S. kudriavzevii) using data provided in this work and others as Oliveira et al. (2014).
Mentions: In winemaking conditions, cells suffer hyperosmotic or cold hyperosmotic mild stresses that do not affect cell growth capacity in any Saccharomyces species (results not shown). This hyperosmotic stress produced by the elevated amount of sugars may determine different lag phase adaptations. In fact, significant differences can be observed in extra and intracellular glycerol levels and also in gene expression of key genes involved in glycerol homeostasis. These data also suggest that the Saccharomyces species are using different strategies to face alterations in the osmotic pressure and cold temperatures. In fact this argument is not that surprising since Saccharomyces species are genetically quite distant showing coding region identities such as the one showed when comparing human and mouse (85%; Lapidot et al., 2001). The dynamics of glycerol accumulation in hyperosmotic stress has been quantitatively analyzed and modeled using physiologic, metabolic, enzymatic, and transcriptomic data in S. cerevisiae (Petelenz-Kurdziel et al., 2013). The strategy of this species consists in a transcriptional activation of GPD1 to increase glycerol accumulation inside the cell by redirecting glycolytic flux. On the other hand, the glycerol efflux stops by the closing of Fps1channel. These are the principal mechanisms to balance glycerol after a hyperosmotic shock. Glycerol influx and other elements contribute in a minor fraction (Figure 6). From the results of this work and others, we can hypothesize that non-cerevisiae Saccharomyces species have changed the weight of the different elements involved in glycerol balance. Based on STL1 gene activation and Stl1 functionality assays we speculate that S. uvarum and S. kudriavzevii rely more in the glycerol import to compensate the osmotic pressure when extracellular glycerol is accumulated (Figure 6). This strategy is not exclusive of these species, In fact, it has been shown that the most osmotolerant yeasts species present a very efficient glycerol-import capacity (Lages et al., 1999).

Bottom Line: The results show different pattern and level of expression among the different species, especially for STL1.These experiments also revealed a different functionality of the glycerol transporters among the different species studied.All these data point to different strategies to handle glycerol accumulation in response to winemaking stresses as hyperosmotic or cold-hyperosmotic stress in the different species, with variable emphasis in the production, influx, or efflux of glycerol.

View Article: PubMed Central - PubMed

Affiliation: Food Biotechnology Department, Systems Biology in Yeast of Biotechnological Interest, Instituto de Agroquímica y Tecnología de los Alimentos, IATA-CSIC Valencia, Spain.

ABSTRACT
Production and balance of glycerol is essential for the survival of yeast cells in certain stressful conditions as hyperosmotic or cold shock that occur during industrial processes as winemaking. These stress responses are well-known in S. cerevisiae, however, little is known in other phylogenetically close related Saccharomyces species associated with natural or fermentation environments such as S. uvarum, S. paradoxus or S. kudriavzevii. In this work we have investigated the expression of four genes (GPD1, GPD2, STL1, and FPS1) crucial in the glycerol pool balance in the four species with a biotechnological potential (S. cerevisiae; S. paradoxus; S. uvarum; and S. kudriavzevii), and the ability of strains to grow under osmotic and cold stresses. The results show different pattern and level of expression among the different species, especially for STL1. We also studied the function of Stl1 glycerol symporter in the survival to osmotic changes and cell growth capacity in winemaking environments. These experiments also revealed a different functionality of the glycerol transporters among the different species studied. All these data point to different strategies to handle glycerol accumulation in response to winemaking stresses as hyperosmotic or cold-hyperosmotic stress in the different species, with variable emphasis in the production, influx, or efflux of glycerol.

No MeSH data available.


Related in: MedlinePlus