Growth temperature exerts differential physiological and transcriptional responses in laboratory and wine strains of Saccharomyces cerevisiae

Francisco J. Pizarra, Michael Christopher Jewett, Jens Nielsen, Eduardo Agosin

    Research output: Contribution to journalJournal articleResearchpeer-review

    Abstract

    Laboratory strains of Saccharomyces cerevisiae have been widely used as a model for studying eukaryotic cells and mapping the molecular mechanisms of many different human diseases. Industrial wine yeasts, on the other hand, have been selected on the basis of their adaptation to stringent environmental conditions and the organoleptic properties that they confer to wine. Here, we used a two-factor design to study the responses of a standard laboratory strain, CEN.PK113-7D, and an industrial wine yeast strain, EC1118, to growth temperatures of 15 degrees C and 30 degrees C in nitrogen-limited, anaerobic, steady-state chemostat cultures. Physiological characterization revealed that the growth temperature strongly impacted the biomass yield of both strains. Moreover, we found that the wine yeast was better adapted to mobilizing resources for biomass production and that the laboratory yeast exhibited higher fermentation rates. To elucidate mechanistic differences controlling the growth temperature response and underlying adaptive mechanisms between the strains, DNA microarrays and targeted metabolome analysis were used. We identified 1,007 temperature-dependent genes and 473 strain-dependent genes. The transcriptional response was used to identify highly correlated gene expression subnetworks within yeast metabolism. We showed that temperature differences most strongly affect nitrogen metabolism and the heat shock response. A lack of stress response element-mediated gene induction, coupled with reduced trehalose levels, indicated that there was a decreased general stress response at 15 degrees C compared to that at 30 degrees C. Differential responses among strains were centered on sugar uptake, nitrogen metabolism, and expression of genes related to organoleptic properties. Our study provides global insight into how growth temperature affects differential physiological and transcriptional responses in laboratory and wine strains of S. cerevisiae.
    Original languageEnglish
    JournalApplied and Environmental Microbiology
    Volume74
    Issue number20
    Pages (from-to)6358-6368
    ISSN0099-2240
    DOIs
    Publication statusPublished - 2008

    Cite this

    @article{fe7aa4147df0423ab13c7855584bdf6c,
    title = "Growth temperature exerts differential physiological and transcriptional responses in laboratory and wine strains of Saccharomyces cerevisiae",
    abstract = "Laboratory strains of Saccharomyces cerevisiae have been widely used as a model for studying eukaryotic cells and mapping the molecular mechanisms of many different human diseases. Industrial wine yeasts, on the other hand, have been selected on the basis of their adaptation to stringent environmental conditions and the organoleptic properties that they confer to wine. Here, we used a two-factor design to study the responses of a standard laboratory strain, CEN.PK113-7D, and an industrial wine yeast strain, EC1118, to growth temperatures of 15 degrees C and 30 degrees C in nitrogen-limited, anaerobic, steady-state chemostat cultures. Physiological characterization revealed that the growth temperature strongly impacted the biomass yield of both strains. Moreover, we found that the wine yeast was better adapted to mobilizing resources for biomass production and that the laboratory yeast exhibited higher fermentation rates. To elucidate mechanistic differences controlling the growth temperature response and underlying adaptive mechanisms between the strains, DNA microarrays and targeted metabolome analysis were used. We identified 1,007 temperature-dependent genes and 473 strain-dependent genes. The transcriptional response was used to identify highly correlated gene expression subnetworks within yeast metabolism. We showed that temperature differences most strongly affect nitrogen metabolism and the heat shock response. A lack of stress response element-mediated gene induction, coupled with reduced trehalose levels, indicated that there was a decreased general stress response at 15 degrees C compared to that at 30 degrees C. Differential responses among strains were centered on sugar uptake, nitrogen metabolism, and expression of genes related to organoleptic properties. Our study provides global insight into how growth temperature affects differential physiological and transcriptional responses in laboratory and wine strains of S. cerevisiae.",
    author = "Pizarra, {Francisco J.} and Jewett, {Michael Christopher} and Jens Nielsen and Eduardo Agosin",
    year = "2008",
    doi = "10.1128/AEM.00602-08",
    language = "English",
    volume = "74",
    pages = "6358--6368",
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    Growth temperature exerts differential physiological and transcriptional responses in laboratory and wine strains of Saccharomyces cerevisiae. / Pizarra, Francisco J.; Jewett, Michael Christopher; Nielsen, Jens; Agosin, Eduardo.

    In: Applied and Environmental Microbiology, Vol. 74, No. 20, 2008, p. 6358-6368.

    Research output: Contribution to journalJournal articleResearchpeer-review

    TY - JOUR

    T1 - Growth temperature exerts differential physiological and transcriptional responses in laboratory and wine strains of Saccharomyces cerevisiae

    AU - Pizarra, Francisco J.

    AU - Jewett, Michael Christopher

    AU - Nielsen, Jens

    AU - Agosin, Eduardo

    PY - 2008

    Y1 - 2008

    N2 - Laboratory strains of Saccharomyces cerevisiae have been widely used as a model for studying eukaryotic cells and mapping the molecular mechanisms of many different human diseases. Industrial wine yeasts, on the other hand, have been selected on the basis of their adaptation to stringent environmental conditions and the organoleptic properties that they confer to wine. Here, we used a two-factor design to study the responses of a standard laboratory strain, CEN.PK113-7D, and an industrial wine yeast strain, EC1118, to growth temperatures of 15 degrees C and 30 degrees C in nitrogen-limited, anaerobic, steady-state chemostat cultures. Physiological characterization revealed that the growth temperature strongly impacted the biomass yield of both strains. Moreover, we found that the wine yeast was better adapted to mobilizing resources for biomass production and that the laboratory yeast exhibited higher fermentation rates. To elucidate mechanistic differences controlling the growth temperature response and underlying adaptive mechanisms between the strains, DNA microarrays and targeted metabolome analysis were used. We identified 1,007 temperature-dependent genes and 473 strain-dependent genes. The transcriptional response was used to identify highly correlated gene expression subnetworks within yeast metabolism. We showed that temperature differences most strongly affect nitrogen metabolism and the heat shock response. A lack of stress response element-mediated gene induction, coupled with reduced trehalose levels, indicated that there was a decreased general stress response at 15 degrees C compared to that at 30 degrees C. Differential responses among strains were centered on sugar uptake, nitrogen metabolism, and expression of genes related to organoleptic properties. Our study provides global insight into how growth temperature affects differential physiological and transcriptional responses in laboratory and wine strains of S. cerevisiae.

    AB - Laboratory strains of Saccharomyces cerevisiae have been widely used as a model for studying eukaryotic cells and mapping the molecular mechanisms of many different human diseases. Industrial wine yeasts, on the other hand, have been selected on the basis of their adaptation to stringent environmental conditions and the organoleptic properties that they confer to wine. Here, we used a two-factor design to study the responses of a standard laboratory strain, CEN.PK113-7D, and an industrial wine yeast strain, EC1118, to growth temperatures of 15 degrees C and 30 degrees C in nitrogen-limited, anaerobic, steady-state chemostat cultures. Physiological characterization revealed that the growth temperature strongly impacted the biomass yield of both strains. Moreover, we found that the wine yeast was better adapted to mobilizing resources for biomass production and that the laboratory yeast exhibited higher fermentation rates. To elucidate mechanistic differences controlling the growth temperature response and underlying adaptive mechanisms between the strains, DNA microarrays and targeted metabolome analysis were used. We identified 1,007 temperature-dependent genes and 473 strain-dependent genes. The transcriptional response was used to identify highly correlated gene expression subnetworks within yeast metabolism. We showed that temperature differences most strongly affect nitrogen metabolism and the heat shock response. A lack of stress response element-mediated gene induction, coupled with reduced trehalose levels, indicated that there was a decreased general stress response at 15 degrees C compared to that at 30 degrees C. Differential responses among strains were centered on sugar uptake, nitrogen metabolism, and expression of genes related to organoleptic properties. Our study provides global insight into how growth temperature affects differential physiological and transcriptional responses in laboratory and wine strains of S. cerevisiae.

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    JF - Applied and Environmental Microbiology

    SN - 0099-2240

    IS - 20

    ER -