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PreprintCited by 26Advanced Electron Microscopy Techniques and ApplicationsEnzyme Structure and FunctionReproductive Biology and Fertility

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FilamentID reveals the composition and function of metabolic enzyme polymers during gametogenesis

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Hugener, Jannik, Xu, Jingwei, Wettstein, Rahel, Ioannidi, Lydia, Velikov, Daniel, Wollweber, Florian, Henggeler, Adrian, Matos, Joao, Pilhofer, Martin·2024·Cell
DOI 10.1101/2024.03.26.586525

Preprint — published as 10.1016/j.cell.2024.04.026 · Paper page

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Abstract

SUMMARY: Gamete formation and subsequent offspring development often involve extended phases of suspended cellular development or even dormancy. How cells adapt to recover and resume growth remains poorly understood. Here, we visualized budding yeast cells undergoing meiosis by cryo-electron tomography (cryoET) and discovered elaborate filamentous assemblies decorating the nucleus, cytoplasm, and mitochondria. To determine filament composition, we developed a “Filament IDentification” (FilamentID) workflow that combines multiscale cryoET/cryo-electron microscopy (cryoEM) analyses of gently lysed cells. FilamentID identified the mitochondrial filaments as the conserved aldehyde dehydrogenase Ald4 ALDH2 and the nucleoplasmic/cytoplasmic filaments being composed of acetyl-CoA synthetase Acs1 ACSS2 . The near-native high-resolution structures revealed the mechanism underlying polymerization and enabled us to perturb filament formation. Acs1 polymerization facilitates the recovery of chronologically aged spores, and more generally, the cell cycle re-entry of starved cells. FilamentID is broadly applicable to characterize filaments of unknown identity in diverse cellular contexts. HIGHLIGHTS: FilamentID: a multiscale imaging workflow to characterize cellular filaments of unknown composition The conserved aldehyde dehydrogenase Ald4 ALDH2 polymerizes into filament arrays within meiotic mitochondria The conserved acetyl-CoA synthetase Acs1 ACSS2 forms filament arrays in the nucleus and the cytoplasm Metabolites mediate Acs1 polymerization to store Acs1 in an inactive state in gametes and starved cells Acs1 filament formation is required for efficient return to growth from starvation stress

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Metadata

Authors
Hugener, J., Xu, J., Wettstein, R., Ioannidi, L., Velikov, D., Wollweber, F., Henggeler, A., Matos, J., & Pilhofer, M.
Affiliations
  • University of Vienna (AT)
  • ETH Zurich (CH)
Corresponding author
  • Matos, Joao
  • Pilhofer, Martin
ORCID
Venue
Cell
Publisher
openRxiv
Published
2024-03-28
Volume
187
Issue
13
Pages
3303-3318.e18
ISSN
0092-8674 (ISSN-L)
DOI
10.1101/2024.03.26.586525
OpenAlex
W4399854874
Cited by
26
References
1
Citations by year
2026: 10 · 2025: 10 · 2024: 6
FWCI
4.73
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Cell (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • PubMed (publishedVersion)
  • Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
  • Repository for Publications and Research Data (ETH Zurich) (submittedVersion, cc-by)
  • ETH Zürich Research Collection
Funders
  • Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (176108)
  • Austrian Science Fund (SFB F - 8807-B)
  • Eidgenössische Technische Hochschule Zürich (31 17-2)
  • Universität Wien
  • NOMIS Stiftung (101000232)
  • European Research Council
  • H2020 European Research Council (101000232, 101002629)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Structural Biology › Advanced Electron Microscopy Techniques and Applications
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Structural Biology › Enzyme Structure and Function
  • Health Sciences › Medicine › Reproductive Medicine › Reproductive Biology and Fertility
Keywords
meiosis, gametogenesis, Saccharomyces cerevisiae, aldehyde dehydrogenase, acetyl-CoA synthetase, ACS1, polymerization mechanism, cell cycle re-entry, starved cells, cryo-electron tomography, cryo-electron microscopy
MeSH terms
Aldehyde Dehydrogenase, Cell Nucleus, Coenzyme A Ligases, Cytoplasm, Gametogenesis, Meiosis, Mitochondria, Models, Molecular, Saccharomyces cerevisiae, Spores, Fungal, Cryoelectron Microscopy, Protein Structure, Quaternary, Saccharomyces cerevisiae Proteins, Electron Microscope Tomography

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