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TitleFilamentID reveals the composition and function of metabolic enzyme polymers during gametogenesis.
Journal, issue, pagesCell, Vol. 187, Issue 13, Page 3303-3318.e18, Year 2024
Publish dateJun 20, 2024
AuthorsJannik Hugener / Jingwei Xu / Rahel Wettstein / Lydia Ioannidi / Daniel Velikov / Florian Wollweber / Adrian Henggeler / Joao Matos / Martin Pilhofer /
PubMed AbstractGamete 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 ...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 partially lysed cells or organelles. FilamentID identified the mitochondrial filaments as being composed of the conserved aldehyde dehydrogenase Ald4 and the nucleoplasmic/cytoplasmic filaments as consisting of acetyl-coenzyme A (CoA) synthetase Acs1. Structural characterization further revealed the mechanism underlying polymerization and enabled us to genetically 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.
External linksCell / PubMed:38906101
MethodsEM (helical sym.) / EM (single particle) / EM (subtomogram averaging) / EM (tomography)
Resolution3.5 - 44.0 Å
Structure data

19548

8rwj

EMDB-19548, PDB-8rwj:
cryoEM structure of Acs1 filament determined by FilamentID
Method: EM (helical sym.) / Resolution: 3.5 Å

19549

8rwk

EMDB-19549, PDB-8rwk:
cryoEM structure of the central Ald4 filament determined by FilamentID
Method: EM (single particle) / Resolution: 3.8 Å

EMDB-19550: cryoEM structure of purified Acs1 filament from meiotic yeast cells
Method: EM (single particle) / Resolution: 3.6 Å

EMDB-19551: cryo sub-tomogram average of Acs1 filament from spread meiotic yeast spheroplasts
Method: EM (subtomogram averaging) / Resolution: 18.3 Å

EMDB-19552: cryo sub-tomogram average of Ald4 filaments from purified meiotic yeast mitochondria
Method: EM (subtomogram averaging) / Resolution: 44.0 Å

EMDB-19553: cryo-tomogram of FIB-milled meiotic yeast cell containing filaments in mitochondria
Method: EM (tomography)

EMDB-19554: cryo-tomogram of FIB-milled meiotic yeast cell containing filaments in the nucleus
Method: EM (tomography)

EMDB-19555: cryo-tomogram of FIB-milled meiotic yeast cell containing filaments in the cytoplasm
Method: EM (tomography)

EMDB-19556: cryo-tomogram of purified meiotic yeast mitochondrion containing Ald4 filaments
Method: EM (tomography)

EMDB-19557: cryo-tomogram of spread meiotic yeast spheroplast containing Acs1 filaments
Method: EM (tomography)

EMDB-19558: cryo-tomogram of spread starved yeast spheroplast containing filaments
Method: EM (tomography)

Chemicals

ChemComp-6R9:
[[(2~{R},3~{S},4~{R},5~{R})-5-(6-aminopurin-9-yl)-3,4-bis(oxidanyl)oxolan-2-yl]methoxy-oxidanyl-phosphoryl] ethanoate

ChemComp-NAP:
NADP NICOTINAMIDE-ADENINE-DINUCLEOTIDE PHOSPHATE

Source
  • Saccharomyces cerevisiae (brewer's yeast)
  • saccharomyces cerevisiae sk1 (yeast)
KeywordsCYTOSOLIC PROTEIN / metabolic enzyme / filament / cryoEM

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