Low oxygen levels as a trigger for enhancement of respiratory metabolism in Saccharomyces cerevisiae

Rintala, Eija; Toivari, Mervi; Pitkänen, Juha-Pekka; Wiebe, Marilyn G.; Ruohonen, Laura; Penttilä, Merja

doi:10.1186/1471-2164-10-461

Cited by 61 publications

(85 citation statements)

References 86 publications

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“…After 24 h, there were 597 and 707 genes differentially expressed, compared to the initial steady state, that had not shown earlier changes in expression in the cultures initially oxygen-limited and fully aerobic, respectively. Gene expression in the final anaerobic steady state of cultures that had been either initially fully aerobic or oxygen-limited, differed for only 3 genes ( p-value <0.05) and was similar to that observed previously (Rintala et al, 2009).…”

Section: Resultssupporting

confidence: 86%

“…Interestingly, in the initially fully aerobic cultures the transcription of these genes recovered to a higher level than in the initial steady state. The same was observed in the comparison of different steady states with varying levels of oxygen provision: the lowest expression level of these genes was observed in the fully aerobic cultures, compared to the oxygen-limited and anaerobic cultures (Rintala et al, 2009). This may be an indication of still unknown functions of mitochondria under oxygen-limited and anaerobic conditions.…”

supporting

confidence: 64%

“…Samples were removed at intervals (0.2, 1, 3, 8, 24, and 79 (20.9% O 2 ) or 72 (1.0% O 2 ) h after the switch to 100% N 2 ) until a new steady state was achieved. These cultivations have been previously described in Wiebe et al (2008) and biomass and metabolite analyses of the cultures were described in Wiebe et al (2008), whereas the role of the glucose transporters during the transition was described in Rintala et al (2008) and the transcriptomes of the initial steady states were described in Rintala et al (2009).…”

Section: Strain and Culture Conditionsmentioning

confidence: 99%

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Transcriptional Responses ofSaccharomyces cerevisiaeto Shift from Respiratory and Respirofermentative to Fully Fermentative Metabolism

Rintala

Jouhten

Toivari

et al. 2011

OMICS: A Journal of Integrative Biology

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In industrial fermentations of Saccharomyces cerevisiae, transient changes in oxygen concentration commonly occur and it is important to understand the behavior of cells during these changes. Glucose-limited chemostat cultivations were used to study the time-dependent effect of sudden oxygen depletion on the transcriptome of S. cerevisiae cells initially in fully aerobic or oxygen-limited conditions. The overall responses to anaerobic conditions of cells initially in different conditions were very similar. Independent of initial culture conditions, transient downregulation of genes related to growth and cell proliferation, mitochondrial translation and protein import, and sulphate assimilation was seen. In addition, transient or permanent upregulation of genes related to protein degradation, and phosphate and amino acid uptake was observed in all cultures. However, only in the initially oxygen-limited cultures was a transient upregulation of genes related to fatty acid oxidation, peroxisomal biogenesis, oxidative phosphorylation, TCA cycle, response to oxidative stress, and pentose phosphate pathway observed. Furthermore, from the initially oxygen-limited conditions, a rapid response around the metabolites of upper glycolysis and the pentose phosphate pathway was seen, while from the initially fully aerobic conditions, a slower response around the pathways for utilization of respiratory carbon sources was observed.

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Section: Resultssupporting

confidence: 86%

supporting

confidence: 64%

Section: Strain and Culture Conditionsmentioning

confidence: 99%

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Transcriptional Responses ofSaccharomyces cerevisiaeto Shift from Respiratory and Respirofermentative to Fully Fermentative Metabolism

Rintala

Jouhten

Toivari

et al. 2011

OMICS: A Journal of Integrative Biology

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“…The genes for subunits of the other respiratory complexes, cytochrome bc 1 (CYC1 and -7, CYT1, QCR2, and QCR6 to -9) and cytochrome oxidase (COX4, COX5B, and COX6 and -7) also showed an increase in ⌬grx2 mutant. Up-regulation of storage carbohydrate genes and respiratory genes is reminiscent of adaptation to intermediate oxygen tension through heme-dependent signaling pathways and of changes that take place prior to diauxic shift (39,40). These results suggest that redox changes inflicted on the proteome by the absence of Grx2p might cause the activation of the same transcription factors as those that govern both processes.…”

Section: Resultsmentioning

confidence: 93%

“…Our findings show that in the absence of Grx2p, the cell responds by up-regulating respiratory genes, mimicking a situation of intermediate oxygen tension governed by Hap2/3/4/5p transcription factor (39). There is a strict correlation between oxygen tension and heme concentration (53), with heme serving as a secondary signal for oxygen.…”

Section: Discussionmentioning

confidence: 91%

Biosynthetic and Iron Metabolism Is Regulated by Thiol Proteome Changes Dependent on Glutaredoxin-2 and Mitochondrial Peroxiredoxin-1 in Saccharomyces cerevisiae

Padilla

Pedrajas

Bárcena

2011

Journal of Biological Chemistry

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Redoxins are involved in maintenance of thiol redox homeostasis, but their exact sites of action are only partly known. We have applied a combined redox proteomics and transcriptomics experimental strategy to discover specific functions of two interacting redoxins: dually localized glutaredoxin 2 (Grx2p) and mitochondrial peroxiredoxin 1 (Prx1p). We have identified 139 proteins showing differential postranslational thiol redox modifications when the cells do not express Grx2p, Prx1p, or both and have mapped the precise cysteines involved in each case. Some of these modifications constitute functional switches that affect metabolic and signaling pathways as the primary effect, leading to gene transcription remodeling as the secondary adaptive effect as demonstrated by a parallel high throughput gene expression analysis. The results suggest that in the absence of Grx2p, the metabolic flow toward nucleotide and aromatic amino acid biosynthesis is slowed down by redox modification of the key enzymes Rpe1p (D-ribulose-5-phosphate 3-epimerase), Tkl1p (transketolase) and Aro4p (3-deoxy-D-arabino-heptulosonate-7-phosphate synthase). The glycolytic mainstream is then diverted toward carbohydrate storage by induction of trehalose and glycogen biosynthesis genes. Porphyrin biosynthesis may also be compromised by inactivation of the redox-sensitive cytosolic enzymes Hem12p (uroporphyrinogen decarboxylase) and Sam1p (S-adenosyl methionine synthetase) and a battery of respiratory genes sensitive to low heme levels are induced. Genes of the Aft1p-dependent iron regulon were induced specifically in the absence of Prx1p despite optimal mitochondrial Fe-S biogenesis, suggesting dysfunction of the mitochondria to the cytosol signaling pathway. Strikingly, requirement of Grx2p for these events places dithiolic Grx2 in the framework of iron metabolism.

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Sterol synthesis and cell size distribution under oscillatory growth conditions in Saccharomyces cerevisiae scale‐down cultivations

Marbà-Ardébol

Bockisch

Neubauer

et al. 2017

Yeast

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Physiological responses of yeast to oscillatory environments as they appear in the liquid phase in large-scale bioreactors have been the subject of past studies. So far, however, the impact on the sterol content and intracellular regulation remains to be investigated. Since oxygen is a cofactor in several reaction steps within sterol metabolism, changes in oxygen availability, as occurs in production-scale aerated bioreactors, might have an influence on the regulation and incorporation of free sterols into the cell lipid layer. Therefore, sterol and fatty acid synthesis in two- and three-compartment scale-down Saccharomyces cerevisiae cultivation were studied and compared with typical values obtained in homogeneous lab-scale cultivations. While cells were exposed to oscillating substrate and oxygen availability in the scale-down cultivations, growth was reduced and accumulation of carboxylic acids was increased. Sterol synthesis was elevated to ergosterol at the same time. The higher fluxes led to increased concentrations of esterified sterols. The cells thus seem to utilize the increased availability of precursors to fill their sterol reservoirs; however, this seems to be limited in the three-compartment reactor cultivation due to a prolonged exposure to oxygen limitation. Besides, a larger heterogeneity within the single-cell size distribution was observed under oscillatory growth conditions with three-dimensional holographic microscopy. Hence the impact of gradients is also observable at the morphological level. The consideration of such a single-cell-based analysis provides useful information about the homogeneity of responses among the population.

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Low oxygen levels as a trigger for enhancement of respiratory metabolism in Saccharomyces cerevisiae

Cited by 61 publications

References 86 publications

Transcriptional Responses ofSaccharomyces cerevisiaeto Shift from Respiratory and Respirofermentative to Fully Fermentative Metabolism

Transcriptional Responses ofSaccharomyces cerevisiaeto Shift from Respiratory and Respirofermentative to Fully Fermentative Metabolism

Biosynthetic and Iron Metabolism Is Regulated by Thiol Proteome Changes Dependent on Glutaredoxin-2 and Mitochondrial Peroxiredoxin-1 in Saccharomyces cerevisiae

Sterol synthesis and cell size distribution under oscillatory growth conditions in Saccharomyces cerevisiae scale‐down cultivations

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