Lipid digestion and autophagy are critical energy providers during acute glucose depletion in Saccharomyces cerevisiae

AbstractThe ability to tolerate and thrive in diverse environments is paramount to all living organisms, and many organisms spend a large part of their lifetime in starvation. Upon acute glucose starvation, yeast cells undergo drastic physiological and metabolic changes and reestablish a constant - though lower – level of energy production within minutes. The molecules that are rapidly metabolized to fuel energy production under these conditions are unknown. Here, we combine metabolomics and genetics, to characterize the cells’ response to acute glucose depletion and identify pathways that ensure survival during starvation. We show that the ability to respire is essential for maintaining the energy status and to ensure viability during starvation. Measuring the cells’ immediate metabolic response, we find that central metabolites drastically deplete and that the intracellular AMP to ATP ratio strongly increases within 20-30 seconds. Furthermore, we detect changes in both amino acid and lipid metabolite levels. Consistent with this, bulk autophagy, a process that frees amino acids, as well as lipid degradation via β-oxidation contribute in parallel to energy maintenance upon acute starvation. In addition, both these pathways ensure long-term survival during starvation. Thus, our results identify bulk autophagy and β-oxidation as important energy providers during acute glucose starvation.

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β-Oxidation and autophagy are critical energy providers during acute glucose depletion in Saccharomyces cerevisiae

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1913370117 ◽

2020 ◽

Vol 117 (22) ◽

pp. 12239-12248 ◽

Cited By ~ 1

Author(s):

Carmen A. Weber ◽

Karthik Sekar ◽

Jeffrey H. Tang ◽

Philipp Warmer ◽

Uwe Sauer ◽

...

Keyword(s):

Energy Production ◽

Metabolic Response ◽

Critical Energy ◽

Yeast Cells ◽

Glucose Starvation ◽

Energy Status ◽

Term Survival ◽

Glucose Depletion ◽

Living Organisms

The ability to tolerate and thrive in diverse environments is paramount to all living organisms, and many organisms spend a large part of their lifetime in starvation. Upon acute glucose starvation, yeast cells undergo drastic physiological and metabolic changes and reestablish a constant—although lower—level of energy production within minutes. The molecules that are rapidly metabolized to fuel energy production under these conditions are unknown. Here, we combine metabolomics and genetics to characterize the cells’ response to acute glucose depletion and identify pathways that ensure survival during starvation. We show that the ability to respire is essential for maintaining the energy status and to ensure viability during starvation. Measuring the cells’ immediate metabolic response, we find that central metabolites drastically deplete and that the intracellular AMP-to-ATP ratio strongly increases within 20 to 30 s. Furthermore, we detect changes in both amino acid and lipid metabolite levels. Consistent with this, both bulk autophagy, a process that frees amino acids, and lipid degradation via β-oxidation contribute in parallel to energy maintenance upon acute starvation. In addition, both these pathways ensure long-term survival during starvation. Thus, our results identify bulk autophagy and β-oxidation as important energy providers during acute glucose starvation.

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AMPK and vacuole-associated Atg14p orchestrate μ-lipophagy for energy production and long-term survival under glucose starvation

eLife ◽

10.7554/elife.21690 ◽

2017 ◽

Vol 6 ◽

Cited By ~ 64

Author(s):

Arnold Y Seo ◽

Pick-Wei Lau ◽

Daniel Feliciano ◽

Prabuddha Sengupta ◽

Mark A Le Gros ◽

...

Keyword(s):

Energy Source ◽

Energy Production ◽

Alternative Energy ◽

Yeast Cells ◽

Survival Strategies ◽

Glucose Starvation ◽

Term Survival ◽

Long Term Survival ◽

Glucose Depletion

Dietary restriction increases the longevity of many organisms, but the cell signaling and organellar mechanisms underlying this capability are unclear. We demonstrate that to permit long-term survival in response to sudden glucose depletion, yeast cells activate lipid-droplet (LD) consumption through micro-lipophagy (µ-lipophagy), in which fat is metabolized as an alternative energy source. AMP-activated protein kinase (AMPK) activation triggered this pathway, which required Atg14p. More gradual glucose starvation, amino acid deprivation or rapamycin did not trigger µ-lipophagy and failed to provide the needed substitute energy source for long-term survival. During acute glucose restriction, activated AMPK was stabilized from degradation and interacted with Atg14p. This prompted Atg14p redistribution from ER exit sites onto liquid-ordered vacuole membrane domains, initiating µ-lipophagy. Our findings that activated AMPK and Atg14p are required to orchestrate µ-lipophagy for energy production in starved cells is relevant for studies on aging and evolutionary survival strategies of different organisms.

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Decision letter: AMPK and vacuole-associated Atg14p orchestrate μ-lipophagy for energy production and long-term survival under glucose starvation

10.7554/elife.21690.028 ◽

2016 ◽

Keyword(s):

Energy Production ◽

Glucose Starvation ◽

Term Survival ◽

Long Term Survival

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Author response: AMPK and vacuole-associated Atg14p orchestrate μ-lipophagy for energy production and long-term survival under glucose starvation

10.7554/elife.21690.029 ◽

2017 ◽

Cited By ~ 2

Author(s):

Arnold Y Seo ◽

Pick-Wei Lau ◽

Daniel Feliciano ◽

Prabuddha Sengupta ◽

Mark A Le Gros ◽

...

Keyword(s):

Energy Production ◽

Author Response ◽

Glucose Starvation ◽

Term Survival ◽

Long Term Survival

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Superposition of Potential Chemical Polluants and Radioisotopes and Their Influence Upon the Environment and Living Organisms

Revista de Chimie ◽

10.37358/rc.17.9.5853 ◽

2017 ◽

Vol 68 (9) ◽

pp. 2189-2195

Author(s):

Valeriu V. Jinescu ◽

Simona Eugenia Manea ◽

George Jinescu ◽

Vali Ifigenia Nicolof

Keyword(s):

Solid Waste ◽

Critical Energy ◽

Radioactive Isotopes ◽

Nuclear Facility ◽

Chemical Pollutants ◽

Living Organisms

Following the activities developed in a nuclear facility result gaseous and liquid radioactive effluents and radioactive solid waste. All these waste contain radioactive isotopes which are potentially pollutants for the environment. In the same time chemicals are, also, pollutants. According to the legislation, discharging of chemicals and radioactive liquid and gaseous effluents into the environment, should meet the requirements of the unrestricted discharge. However, what happens when several pollutants superpose: only chemical pollutants, or only radioactive pollutants, or chemical and radioactive pollutants? Such problems have been solved in this paper on the basis of the principle of critical energy.

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Energy status of starving yeast cells immobilized by covalent linkage

Biotechnology Letters ◽

10.1007/bf01026845 ◽

1989 ◽

Vol 11 (12) ◽

pp. 881-884 ◽

Cited By ~ 2

Author(s):

Vladimir Jirků

Keyword(s):

Yeast Cells ◽

Energy Status ◽

Covalent Linkage

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Estimation of anaerobic energy production and efficiency in rats during exercise

Journal of Applied Physiology ◽

10.1152/jappl.1984.56.2.520 ◽

1984 ◽

Vol 56 (2) ◽

pp. 520-525 ◽

Cited By ~ 31

Author(s):

G. A. Brooks ◽

C. M. Donovan ◽

T. P. White

Keyword(s):

Total Energy ◽

Energy Production ◽

Metabolic Response ◽

Lactate Production ◽

Energy Transduction ◽

Energy Turnover ◽

External Work ◽

Gross Efficiency ◽

Lactate Turnover ◽

Anaerobic Energy

o assess the effects of gradient and running speed on efficiency of exercise, and to evaluate contributions of oxidative and anaerobic energy production (Ean) during locomotion, two sets of experiments were performed. The caloric expenditures of rats were determined from O2 consumption (VO2) while they ran at three speeds (13.4, 26.8, and 43.1 m/min) on five grades (1, 5, 10, 15, and 20%). In addition, lactate turnover (LaT) and oxidation (Laox) were determined on rats at rest or during running at 13.4 and 26.8 m/min on 1% grade, respectively. Lactate production not represented in the VO2 (i.e., Ean) was calculated from the LaT not accounted for by oxidation [(LaT an) = LaT-Laox)]. The Ean was calculated as: Ean = [LaT an(mumol/min)] [1.38 ATP/La] [11 mcal/mumol ATP]. Gross efficiency of exercise (the caloric equivalent of external work/caloric equivalent of VO2 X 100) ranged from 1.7 to 4.5%. Apparent efficiency (the inverse of the regression of caloric equivalent of VO2 on the caloric equivalent of work X 100) ranged from 20.5 to 26.4% and reflected the metabolic response of rats to applied external work. The contribution of Ean to total energy turnover ranged from 1.6% at rest to 0.8% during running at 13.4 m/min on a 1% grade. Despite active LaT during steady-state exercise, Ean contributes insignificantly to total energy transduction, because over 70% of the lactate produced is removed through oxidation. VO2 adequately represents metabolism under these conditions.

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Preference of Proteomonas Sulcata Anion Channelrhodopsin for Nitrate Revealed Using a pH Electrode Method

10.21203/rs.3.rs-153619/v1 ◽

2021 ◽

Author(s):

Chihiro Kikuchi ◽

Hina Kurane ◽

Takuma Watanabe ◽

Makoto Demura ◽

Takashi Kikukawa ◽

...

Keyword(s):

Transmembrane Helix ◽

Anion Transport ◽

Yeast Cells ◽

Ion Pump ◽

Transport Activity ◽

Electrode Method ◽

Anion Transport Activity ◽

Living Organisms ◽

Stable Forms ◽

Ph Electrode

Abstract Ion channel proteins are physiologically important molecules in living organisms. Their molecular functions have been investigated using electrophysiological methods, which enable quantitative, precise and advanced measurements and thus require complex instruments and experienced operators. For simpler and easier measurements, we measured the anion transport activity of light-gated anion channelrhodopsins (ACRs) using a pH electrode method, which has already been established for ion pump rhodopsins. Using that method, we successfully measured the anion transport activity and its dependence on the wavelength of light, i.e. its action spectra, and on the anion species, i.e. its selectivity or preference, of several ACRs expressed in yeast cells. In addition, we identified the strong anion transport activity and the preference for NO3- of an ACR from a marine cryptophyte algae Proteomonas sulcata, named PsuACR_353. Such a preference was discovered for the first time in microbial pump- or channel-type rhodopsins. Nitrate is one of the most stable forms of nitrogen and is used as a nitrogen source by most organisms including plants. Therefore, PsuACR_353 may play a role in NO3- transport and might take part in NO3--related cellular functions in nature. Measurements of a mutant protein revealed that a Thr residue in the 3rd transmembrane helix, which corresponds to Cys102 in GtACR1, contributed to the preference for NO3-. These findings will be helpful to understand the mechanisms of anion transport, selectivity and preference of PsuACR_353.

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Autotoxin-mediated voluntary triage in starved yeast community

10.1101/2020.10.17.344093 ◽

2020 ◽

Author(s):

Arisa H. Oda ◽

Miki Tamura ◽

Kunihiko Kaneko ◽

Kunihiro Ohta ◽

Tetsuhiro S. Hatakeyama

Keyword(s):

Environmental Changes ◽

Yeast Cells ◽

Glucose Starvation ◽

Uniform Stress ◽

Universal System ◽

Stressful Environment ◽

Yeast Community ◽

Unicellular Organisms ◽

Multicellular Organisms ◽

Cell Community

When organisms face crises, such as starvation, every individual should adapt to environmental changes (1, 2), or the community alters their behaviour (3–5). Because a stressful environment reduces the carrying capacity (6), the population size of unicellular organisms shrinks in such conditions (7, 8). However, the uniform stress response of the cell community may lead to overall extinction or severely damage their entire fitness. How microbial communities accommodate this dilemma remains poorly understood. Here, we demonstrate an elaborate strategy of the yeast community against glucose starvation, named the voluntary triage. During starvation, yeast cells release some autotoxins, such as leucic acid and L-2keto-3methylvalerate, which can even kill the cells producing them. Although it may look like mass suicide at first glance, cells use epigenetic “tags” to adapt to the autotoxin inheritably. If non-tagged latecomers, regardless of whether they are closely related, try to invade the habitat, autotoxins kill them and inhibit their growth, but the tagged cells can selectively survive. Phylogenetically distant fission and budding yeast (9) share this strategy using the same autotoxins, which implies that the universal system of voluntary triage may be relevant to the major evolutional transition from unicellular to multicellular organisms (10).

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