Remodeling of yeast vacuole membrane lipidomes from the log (one phase) to stationary stage (two phases)

Reinhard, John F.; Leveille, Chantelle L.; Cornell, Caitlin E.; Klose, Christian; Ernst, Robert; Keller, Sarah L.

doi:10.1016/j.bpj.2023.01.009

Cited by 16 publications

(24 citation statements)

References 121 publications

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“… a. Lipidome species of: Syn3B and M. mycoides ; M. extorquens 4 ; S. cerevisiae vacuole 7 ; S. cerevisiae whole cell lipidome 5 ; plasma membrane GPMV, from RBL cells 34 . Scatter plots represent averages across several growth conditions available, with variability shown as error bars.…”

Section: Resultsmentioning

confidence: 99%

“…1) M. extorquens filtered lipidome was taken from 4 ; the following conditions were considered for further analysis (in biological triplicates): a) Growth stages: early-, mid-, late-exponential and stationary (harvested at 30°C) b) Growth temperatures: 4°C, 13°C, 20°C (harvested at early-exponential growth stage) 2) S. cerevisiae whole cell lipidomes were taken from 5 . The following conditions were considered: a) Growth stages: early (OD 1)-, mid (OD 3.5)-, late-exponential (OD 6) and stationary phase b) Growth temperatures: 15°C, 24°C, 30°C, 37°C 3) S. cerevisiae vacuole lipidomes from 7…”

Section: Lipidomic Data Filteringmentioning

confidence: 99%

“…S. cerevisiae vacuole lipidomes from 7 . Conditions considered: Exponential growth stage (4 replicates) Stationary growth stage (4 replicates) …”

Section: Bacterial Strainsmentioning

confidence: 99%

See 2 more Smart Citations

From hot to cold: dissecting lipidome adaptation inMycoplasma mycoidesand the Minimal Cell JCVI-Syn3B

Safronova,

Junghans,

Saenz

2023

Preprint

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Cell membranes insulate and mediate interactions between life and its environment, with lipids determining their properties and functions. However, the intricacies of how cells adjust their lipidome compositions to tune membrane properties remain relatively undefined. The complexity of most model organisms has made it challenging to characterize lipidomic adaptation. An ideal model system would be a relatively simple organism with a single membrane that can adapt to environmental changes, particularly temperature, which is known to affect membrane properties. To this end, we used quantitative shotgun lipidomics to analyze temperature adaptation inMycoplasma mycoidesand its minimal synthetic counterpart, JCVI-Syn3B. Comparing with lipidomes from eukaryotes and bacteria, we observed a universal logarithmic distribution of lipid abundances. Additionally, the extent of lipid remodeling needed for temperature adaptation appears relatively constrained, irrespective of lipidomic or organismal complexity. Through lipid features analysis, we demonstrate head group-specific acyl chain remodeling as characteristic of temperature-induced lipidome adaptation and its deficiency in Syn3B is associated with impaired homeoviscous adaptation. Temporal analysis uncovers a two-stage cold adaptation process: swift cholesterol and cardiolipin shifts followed by gradual acyl chain modifications. This work provides an in-depth analysis of lipidome adaptation in minimal cells, laying a foundation to probe the fundamental design principles of living membranes.

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Section: Resultsmentioning

confidence: 99%

Section: Lipidomic Data Filteringmentioning

confidence: 99%

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From hot to cold: dissecting lipidome adaptation inMycoplasma mycoidesand the Minimal Cell JCVI-Syn3B

Safronova,

Junghans,

Saenz

2023

Preprint

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“…Additional applications might lie in engineering minimal cell systems to function with only two classes of lipids (35); if one of those classes were a sterol-lipid, it would be interesting to test if the cell membrane phase separated. Micron-scale, reversible, liquid-liquid phase separation has previously been observed in more complex membranes of living cells (1,36), where it has biological importance. For example, in yeast, phase separation of vacuole membranes promotes docking of lipid droplets during periods of nutrient restriction (37)(38)(39).…”

Section: Discussionmentioning

confidence: 96%

Sterol-lipids enable large-scale, liquid-liquid phase separation in bilayer membranes of only 2 components

Wilson,

Nguyen,

Gervay-Hague

et al. 2024

Preprint

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Despite longstanding excitement and progress toward understanding liquid-liquid phase separation in natural and artificial membranes, fundamental questions have persisted about which molecules are required for this phenomenon. Except in extraordinary circumstances, the smallest number of components that has produced large-scale, liquid-liquid phase separation in bilayers has stubbornly remained at three: a sterol, a phospholipid with ordered chains, and a phospholipid with disordered chains. This requirement of three components is puzzling for two reasons: (1) the Gibbs Phase Rule states that only two components are necessary, and (2) only two components are required for liquid-liquid phase separation in lipid monolayers, which resemble half of a bilayer. Inspired by reports that sterols interact closely with lipids with ordered chains, we tested whether phase separation would occur in bilayers in which a sterol and lipid were replaced by a single, joined sterol-lipid. By evaluating a panel of sterol-lipids, we discovered a minimal bilayer of only two components (PChemsPC and diPhyPC) that demixes into micron-scale, liquid phases. In this system, the sterol-lipid behaves as a 3:1 ratio of cholesterol to phospholipid. Our system gives the computation and theory community a two-component membrane that maps directly onto simplified theories and that can be used to validate simulation force fields. It suggests a new role for sterol-lipids in nature, and it gives experimental communities a membrane in which tie-lines (and, therefore, the lipid composition of each phase) are easily determined and will be consistent across multiple laboratories.Significance StatementA wide diversity of bilayer membranes, from those with hundreds of lipids (e.g., vacuoles of living yeast cells) to those with very few (e.g., artificial vesicles) phase separate into micron-scale liquid domains. The number of components required for liquid-liquid phase separation has been perplexing: only two should be necessary, but more are required except in extraordinary circumstances. What minimal set of molecular characteristics leads to liquid-liquid phase separation in bilayer membranes? This question inspired us to search for single, joined “sterol-lipid” molecules to replace both a sterol and a phospholipid in membranes undergoing liquid-liquid phase separation. By producing phase-separating membranes with only two components, we mitigate experimental challenges in determining tie-lines and in maintaining constant chemical potentials of lipids.

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“…This is complicated even further by the fact that the chemico-physical properties have only been determined (experimentally) for a relatively small amount of lipid species (Renne and de Kroon 2018; Koynova and Caffrey 1994). Recent studies have extrapolated data from trends observed in experimental studies (Reinhard et al 2023) or utilised atomistic molecular dynamics simulations (Smith et al 2021) to bypass this problem, but the lack of experimental studies addressing the chemico-physical properties of different lipids remains. By combining synthetic organic chemistry for the synthesis of specific lipid species and biophysical studies to determine lipid physico-chemical properties, future studies should greatly expand our knowledge of lipid properties.…”

Section: Discussionmentioning

confidence: 99%

Temperature adaptation of yeast phospholipid molecular species at the acyl chain positional level

Kelso,

Maccarone,

de Kroon

et al. 2024

Preprint

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The budding yeast Saccharomyces cerevisiae is a poikilothermic organism and adapts its lipid composition to the environmental temperature to maintain membrane physical properties. Studies addressing temperature-dependent adaptation of the lipidome in yeast have described changes in the phospholipid composition at the level of sum composition (e.g. PC 32:1) and molecular composition (e.g. PC 16:0_16:1). However, to date, there is no information at the level of positional isomers (e.g. PC 16:0/16:1 versus PC 16:1/16:0). In this study, combined Collision- and Ozone-Induced Dissociation (CID/OzID) mass spectrometry was deployed to investigate homeoviscous adaptation of PC, PE, and PS sn-molecular species composition. We determined the main species to be 16:1/16:1, 16:0/16:1, 16:1/18:1, 16:0/18:1, and 18:0/16:1. In general, at higher culture temperature, the sn-1 position is increased in saturated acyl chains, whereas the sn-2 position mainly is increased in acyl chain length. PC mainly increases in 16:0/16:1 and 16:0/18:1, at the expense of 16:1/16:1, whereas PS and PE increase in 16:1/18:1, at the expense of 16:1/16:1 and 16:0/16:1. Our data suggest distinct adaptation mechanisms of the sn-1 and sn-2 acyl chains, and different manners of sn-molecular species adaptation between PC and PE/PS.

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Remodeling of yeast vacuole membrane lipidomes from the log (one phase) to stationary stage (two phases)

Cited by 16 publications

References 121 publications

From hot to cold: dissecting lipidome adaptation inMycoplasma mycoidesand the Minimal Cell JCVI-Syn3B

From hot to cold: dissecting lipidome adaptation inMycoplasma mycoidesand the Minimal Cell JCVI-Syn3B

Sterol-lipids enable large-scale, liquid-liquid phase separation in bilayer membranes of only 2 components

Temperature adaptation of yeast phospholipid molecular species at the acyl chain positional level

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