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Autophagy facilitates adaptation of budding yeast to respiratory growth by recycling serine for one-carbon metabolism.

ABSTRACT: The mechanism and function of autophagy as a highly-conserved bulk degradation pathway are well studied, but the physiological role of autophagy remains poorly understood. We show that autophagy is involved in the adaptation of Saccharomyces cerevisiae to respiratory growth through its recycling of serine. On respiratory media, growth onset, mitochondrial initiator tRNA modification and mitochondrial protein expression are delayed in autophagy defective cells, suggesting that mitochondrial one-carbon metabolism is perturbed in these cells. The supplementation of serine, which is a key one-carbon metabolite, is able to restore mitochondrial protein expression and alleviate delayed respiratory growth. These results indicate that autophagy-derived serine feeds into mitochondrial one-carbon metabolism, supporting the initiation of mitochondrial protein synthesis and allowing rapid adaptation to respiratory growth.

SUBMITTER: May AI

PROVIDER: S-EPMC7542147 | biostudies-literature | 2020 Oct

REPOSITORIES: biostudies-literature

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Autophagy facilitates adaptation of budding yeast to respiratory growth by recycling serine for one-carbon metabolism.

May Alexander I AI Prescott Mark M Ohsumi Yoshinori Y

Nature communications 20201007 1

The mechanism and function of autophagy as a highly-conserved bulk degradation pathway are well studied, but the physiological role of autophagy remains poorly understood. We show that autophagy is involved in the adaptation of Saccharomyces cerevisiae to respiratory growth through its recycling of serine. On respiratory media, growth onset, mitochondrial initiator tRNA modification and mitochondrial protein expression are delayed in autophagy defective cells, suggesting that mitochondrial one-c ...[more]

PMID: 33028817

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Publisher Correction: Autophagy facilitates adaptation of budding yeast to respiratory growth by recycling serine for one-carbon metabolism.

Project description: Not available

| S-EPMC7782837 | biostudies-literature

Heat-induced longevity in budding yeast requires respiratory metabolism and glutathione recycling.

Project description:Heat-induced hormesis is a well-known conserved phenomenon in aging, traditionally attributed to the benefits conferred by increased amounts of heat shock (HS) proteins. Here we find that the key event for the HS-induced lifespan extension in budding yeast is the switch from glycolysis to respiratory metabolism. The resulting increase in reactive oxygen species activates the antioxidant response, supported by the redirection of glucose from glycolysis to the pentose phosphate pathway, increasing the production of NADPH. This sequence of events culminates in replicative lifespan (RLS) extension, implying decreased mortality per generation that persists even after the HS has finished. We found that switching to respiratory metabolism, and particularly the consequent increase in glutathione levels, were essential for the observed RLS extension. These results draw the focus away solely from the HS response and demonstrate that the antioxidant response has a key role in heat-induced hormesis. Our findings underscore the importance of the changes in cellular metabolic activity for heat-induced longevity in budding yeast.

| S-EPMC6188503 | biostudies-literature

Cold adaptation in budding yeast.

Project description:We have determined the transcriptional response of the budding yeast Saccharomyces cerevisiae to cold. Yeast cells were exposed to 10 degrees C for different lengths of time, and DNA microarrays were used to characterize the changes in transcript abundance. Two distinct groups of transcriptionally modulated genes were identified and defined as the early cold response and the late cold response. A detailed comparison of the cold response with various environmental stress responses revealed a substantial overlap between environmental stress response genes and late cold response genes. In addition, the accumulation of the carbohydrate reserves trehalose and glycogen is induced during late cold response. These observations suggest that the environmental stress response (ESR) occurs during the late cold response. The transcriptional activators Msn2p and Msn4p are involved in the induction of genes common to many stress responses, and we show that they mediate the stress response pattern observed during the late cold response. In contrast, classical markers of the ESR were absent during the early cold response, and the transcriptional response of the early cold response genes was Msn2p/Msn4p independent. This implies that the cold-specific early response is mediated by a different and as yet uncharacterized regulatory mechanism.

| S-EPMC532028 | biostudies-literature

Selective autophagy in budding yeast.

Project description:Autophagy is a bulk degradation system, widely conserved in eukaryotes. Upon starvation, autophagosomes enclose a portion of the cytoplasm and ultimately fuse with the vacuole. The contents of autophagosomes are degraded in the vacuole, and recycled to maintain the intracellular amino-acid pool required for protein synthesis and survival under starvation conditions. Previously, autophagy was thought to be an essentially nonselective pathway, but recent evidence suggests that autophagosomes carry selected cargoes. These studies have identified two categories of selective autophagy - one highly selective and dependent on autophagy-related 11 (Atg11); another, less selective, that is, independent of Atg11. The former, selective category comprises the Cvt pathway, mitophagy, pexophagy and piecemeal microautophagy of the nucleus; acetaldehyde dehydrogenase 6 degradation and ribophagy belong to the latter, less selective category. In this review, I focus on the mechanisms and the physiological roles of these selective types of autophagy.

| S-EPMC3524628 | biostudies-other

Parallel Actin-Independent Recycling Pathways Polarize Cdc42 in Budding Yeast.

Project description:The highly conserved Rho-family GTPase Cdc42 is an essential regulator of polarity in many different cell types. During polarity establishment, Cdc42 becomes concentrated at a cortical site, where it interacts with downstream effectors to orient the cytoskeleton along the front-back axis. To concentrate Cdc42, loss of Cdc42 by diffusion must be balanced by recycling to the front. In Saccharomyces cerevisiae, the guanine nucleotide dissociation inhibitor (GDI) Rdi1 recycles Cdc42 through the cytoplasm. Loss of Rdi1 slowed but did not eliminate Cdc42 accumulation at the front, suggesting the existence of other recycling pathways. One proposed pathway involves actin-directed trafficking of vesicles carrying Cdc42 to the front. However, we found no role for F-actin in Cdc42 concentration, even in rdi1Δ cells. Instead, Cdc42 was still able to exchange between the membrane and cytoplasm in rdi1Δ cells, albeit at a reduced rate. Membrane-cytoplasm exchange of GDP-Cdc42 was faster than that of GTP-Cdc42, and computational modeling indicated that such exchange would suffice to promote polarization. We also uncovered a novel role for the Cdc42-directed GTPase-activating protein (GAP) Bem2 in Cdc42 polarization. Bem2 was known to act in series with Rdi1 to promote recycling of Cdc42, but we found that rdi1Δ bem2Δ mutants were synthetically lethal, suggesting that they also act in parallel. We suggest that GAP activity cooperates with the GDI to counteract the dissipative effect of a previously unappreciated pathway whereby GTP-Cdc42 escapes from the polarity site through the cytoplasm.

| S-EPMC5956535 | biostudies-literature

Endogenous transcription at the centromere facilitates centromere activity in budding yeast.

Project description:The centromere (CEN) DNA-kinetochore complex is the specialized chromatin structure that mediates chromosome attachment to the spindle and is required for high-fidelity chromosome segregation. Although kinetochore function is conserved from budding yeast to humans, it was thought that transcription had no role in centromere function in budding yeast, in contrast to other eukaryotes including fission yeast.We report here that transcription at the centromere facilitates centromere activity in the budding yeast Saccharomyces cerevisiae. We identified transcripts at CEN DNA and found that Cbf1, which is a transcription factor that binds to CEN DNA, is required for transcription at CEN DNA. Chromosome instability of cbf1? cells is suppressed by transcription driven from an artificial promoter. Furthermore, we have identified Ste12, which is a transcription factor, and Dig1, a Ste12 inhibitor, as a novel CEN-associated protein complex by an in vitro kinetochore assembly system. Dig1 represses Ste12-dependent transcription at the centromere.Our studies reveal that transcription at the centromere plays an important role in centromere function in budding yeast.

| S-EPMC3218120 | biostudies-literature

Serine one-carbon catabolism with formate overflow.

Project description:Serine catabolism to glycine and a one-carbon unit has been linked to the anabolic requirements of proliferating mammalian cells. However, genome-scale modeling predicts a catabolic role with one-carbon release as formate. We experimentally prove that in cultured cancer cells and nontransformed fibroblasts, most of the serine-derived one-carbon units are released from cells as formate, and that formate release is dependent on mitochondrial reverse 10-CHO-THF synthetase activity. We also show that in cancer cells, formate release is coupled to mitochondrial complex I activity, whereas in nontransformed fibroblasts, it is partially insensitive to inhibition of complex I activity. We demonstrate that in mice, about 50% of plasma formate is derived from serine and that serine starvation or complex I inhibition reduces formate synthesis in vivo. These observations transform our understanding of one-carbon metabolism and have implications for the treatment of diabetes and cancer with complex I inhibitors.

| S-EPMC5091358 | biostudies-literature

Targeting of early endosomes by autophagy facilitates EGFR recycling and signalling.

Project description:Despite recently uncovered connections between autophagy and the endocytic pathway, the role of autophagy in regulating endosomal function remains incompletely understood. Here, we find that the ablation of autophagy-essential players disrupts EGF-induced endocytic trafficking of EGFR. Cells lacking ATG7 or ATG16L1 exhibit increased levels of phosphatidylinositol-3-phosphate (PI(3)P), a key determinant of early endosome maturation. Increased PI(3)P levels are associated with an accumulation of EEA1-positive endosomes where EGFR trafficking is stalled. Aberrant early endosomes are recognised by the autophagy machinery in a TBK1- and Gal8-dependent manner and are delivered to LAMP2-positive lysosomes. Preventing this homeostatic regulation of early endosomes by autophagy reduces EGFR recycling to the plasma membrane and compromises downstream signalling and cell survival. Our findings uncover a novel role for the autophagy machinery in maintaining early endosome function and growth factor sensing.

| S-EPMC6776898 | biostudies-literature

Carbon starvation induces autophagy and recycling of nutrients in the ectomycorrhizal fungus Paxillus involutus

Project description:Ectomycorrhizal fungi are dependent on host trees for carbon supply. In return ectomycorrhizal fungi supply trees with water and nutrients. It is known that when ectomycorrhizal fungi have exploited a nutrient rich patch in soil, the carbon allocation to mycelia in that patch is reduced, with the consequence of mycelia dying, but less is known of the dynamics of this senescence. We cultivated the ectomycorrhizal fungus Paxillus involutus in an axenic system. We collected growth and transcriptome data at different stages of carbon starvation during fungal growth. Carbon starvation induced a decrease in fungal biomass, which coincided with the release of NH4+ and the expression of genes connected with autophagy as well as protease and chitinase activity. Monoaromatic compounds, chitin and protease activity was detected in the liquid growth media during carbon starvation. The exudation of NH4+ and increase of monoaromatic compound during C starvation suggests senescence and autolysis of P. involutus. Together with the upregulation of genes involved in autophagy, chitinase and endopeptidase activity this points towards a controlled senescence including recycling of compounds originating from the fungi. Reduced C allocation to ectomycorrhizal mycelia in recently depleted nutrient patches in forest soils must be of ubiquitous nature. Understanding the mechanisms during exploitation of nutrients by ectomycorrhizal fungi is of great importance for understanding carbon and nutrient dynamics in forest soils. This is to our knowledge the first study describing the carbon starvation response in an ectomycorrhizal fungus. A one-chip study (data from 12 subarrays collected from a 12-plex Nimblegen microarray (ID 527890) using total RNA recovered from three separate glass-bead cultures of Paxillus involutus (ATCC200175) grown on Minimum Melin Norkrans medium (MMN) amended with ammonium (C/N ratio 3) and harvested at different times of carbon starvation.)

2014-04-01 | E-GEOD-54940 | biostudies-arrayexpress

Mnd1/Hop2 facilitates Dmc1-dependent interhomolog crossover formation in meiosis of budding yeast.

Project description:During meiosis, each chromosome must pair with its homolog and undergo meiotic crossover recombination in order to segregate properly at the first meiotic division. Recombination in meiosis in Saccharomyces cerevisiae relies on two Escherichia coli recA homologs, Rad51 and Dmc1, as well as the more recently discovered heterodimer Mnd1/Hop2. Meiotic recombination in S. cerevisiae mnd1 and hop2 single mutants is initiated via double-strand breaks (DSBs) but does not progress beyond this stage; heteroduplex DNA, joint molecules, and crossovers are not detected. Whereas hop2 and mnd1 single mutants are profoundly recombination defective, we show that mnd1 rad51, hop2 rad51, and mnd1 rad17 double mutants are able to carry out crossover recombination. Interestingly, noncrossover recombination is absent, indicating a role for Mnd1/Hop2 in the designation of DSBs for noncrossover recombination. We demonstrate that in the rad51 mnd1 double mutant, recombination is more likely to occur between repetitive sequences on nonhomologous chromosomes. Our results support a model in which Mnd1/Hop2 is required for DNA-DNA interactions that help ensure Dmc1-mediated stable strand invasion between homologous chromosomes, thereby preserving genomic integrity.

| S-EPMC1446936 | biostudies-literature

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