Cargando…

Absolute yeast mitochondrial proteome quantification reveals trade-off between biosynthesis and energy generation during diauxic shift

Saccharomyces cerevisiae constitutes a popular eukaryal model for research on mitochondrial physiology. Being Crabtree-positive, this yeast has evolved the ability to ferment glucose to ethanol and respire ethanol once glucose is consumed. Its transition phase from fermentative to respiratory metabo...

Descripción completa

Detalles Bibliográficos
Autores principales: Di Bartolomeo, Francesca, Malina, Carl, Campbell, Kate, Mormino, Maurizio, Fuchs, Johannes, Vorontsov, Egor, Gustafsson, Claes M., Nielsen, Jens
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7132131/
https://www.ncbi.nlm.nih.gov/pubmed/32184324
http://dx.doi.org/10.1073/pnas.1918216117
_version_ 1783517385256337408
author Di Bartolomeo, Francesca
Malina, Carl
Campbell, Kate
Mormino, Maurizio
Fuchs, Johannes
Vorontsov, Egor
Gustafsson, Claes M.
Nielsen, Jens
author_facet Di Bartolomeo, Francesca
Malina, Carl
Campbell, Kate
Mormino, Maurizio
Fuchs, Johannes
Vorontsov, Egor
Gustafsson, Claes M.
Nielsen, Jens
author_sort Di Bartolomeo, Francesca
collection PubMed
description Saccharomyces cerevisiae constitutes a popular eukaryal model for research on mitochondrial physiology. Being Crabtree-positive, this yeast has evolved the ability to ferment glucose to ethanol and respire ethanol once glucose is consumed. Its transition phase from fermentative to respiratory metabolism, known as the diauxic shift, is reflected by dramatic rearrangements of mitochondrial function and structure. To date, the metabolic adaptations that occur during the diauxic shift have not been fully characterized at the organelle level. In this study, the absolute proteome of mitochondria was quantified alongside precise parametrization of biophysical properties associated with the mitochondrial network using state-of-the-art optical-imaging techniques. This allowed the determination of absolute protein abundances at a subcellular level. By tracking the transformation of mitochondrial mass and volume, alongside changes in the absolute mitochondrial proteome allocation, we could quantify how mitochondria balance their dual role as a biosynthetic hub as well as a center for cellular respiration. Furthermore, our findings suggest that in the transition from a fermentative to a respiratory metabolism, the diauxic shift represents the stage where major structural and functional reorganizations in mitochondrial metabolism occur. This metabolic transition, initiated at the mitochondria level, is then extended to the rest of the yeast cell.
format Online
Article
Text
id pubmed-7132131
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher National Academy of Sciences
record_format MEDLINE/PubMed
spelling pubmed-71321312020-04-09 Absolute yeast mitochondrial proteome quantification reveals trade-off between biosynthesis and energy generation during diauxic shift Di Bartolomeo, Francesca Malina, Carl Campbell, Kate Mormino, Maurizio Fuchs, Johannes Vorontsov, Egor Gustafsson, Claes M. Nielsen, Jens Proc Natl Acad Sci U S A Biological Sciences Saccharomyces cerevisiae constitutes a popular eukaryal model for research on mitochondrial physiology. Being Crabtree-positive, this yeast has evolved the ability to ferment glucose to ethanol and respire ethanol once glucose is consumed. Its transition phase from fermentative to respiratory metabolism, known as the diauxic shift, is reflected by dramatic rearrangements of mitochondrial function and structure. To date, the metabolic adaptations that occur during the diauxic shift have not been fully characterized at the organelle level. In this study, the absolute proteome of mitochondria was quantified alongside precise parametrization of biophysical properties associated with the mitochondrial network using state-of-the-art optical-imaging techniques. This allowed the determination of absolute protein abundances at a subcellular level. By tracking the transformation of mitochondrial mass and volume, alongside changes in the absolute mitochondrial proteome allocation, we could quantify how mitochondria balance their dual role as a biosynthetic hub as well as a center for cellular respiration. Furthermore, our findings suggest that in the transition from a fermentative to a respiratory metabolism, the diauxic shift represents the stage where major structural and functional reorganizations in mitochondrial metabolism occur. This metabolic transition, initiated at the mitochondria level, is then extended to the rest of the yeast cell. National Academy of Sciences 2020-03-31 2020-03-17 /pmc/articles/PMC7132131/ /pubmed/32184324 http://dx.doi.org/10.1073/pnas.1918216117 Text en Copyright © 2020 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Di Bartolomeo, Francesca
Malina, Carl
Campbell, Kate
Mormino, Maurizio
Fuchs, Johannes
Vorontsov, Egor
Gustafsson, Claes M.
Nielsen, Jens
Absolute yeast mitochondrial proteome quantification reveals trade-off between biosynthesis and energy generation during diauxic shift
title Absolute yeast mitochondrial proteome quantification reveals trade-off between biosynthesis and energy generation during diauxic shift
title_full Absolute yeast mitochondrial proteome quantification reveals trade-off between biosynthesis and energy generation during diauxic shift
title_fullStr Absolute yeast mitochondrial proteome quantification reveals trade-off between biosynthesis and energy generation during diauxic shift
title_full_unstemmed Absolute yeast mitochondrial proteome quantification reveals trade-off between biosynthesis and energy generation during diauxic shift
title_short Absolute yeast mitochondrial proteome quantification reveals trade-off between biosynthesis and energy generation during diauxic shift
title_sort absolute yeast mitochondrial proteome quantification reveals trade-off between biosynthesis and energy generation during diauxic shift
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7132131/
https://www.ncbi.nlm.nih.gov/pubmed/32184324
http://dx.doi.org/10.1073/pnas.1918216117
work_keys_str_mv AT dibartolomeofrancesca absoluteyeastmitochondrialproteomequantificationrevealstradeoffbetweenbiosynthesisandenergygenerationduringdiauxicshift
AT malinacarl absoluteyeastmitochondrialproteomequantificationrevealstradeoffbetweenbiosynthesisandenergygenerationduringdiauxicshift
AT campbellkate absoluteyeastmitochondrialproteomequantificationrevealstradeoffbetweenbiosynthesisandenergygenerationduringdiauxicshift
AT morminomaurizio absoluteyeastmitochondrialproteomequantificationrevealstradeoffbetweenbiosynthesisandenergygenerationduringdiauxicshift
AT fuchsjohannes absoluteyeastmitochondrialproteomequantificationrevealstradeoffbetweenbiosynthesisandenergygenerationduringdiauxicshift
AT vorontsovegor absoluteyeastmitochondrialproteomequantificationrevealstradeoffbetweenbiosynthesisandenergygenerationduringdiauxicshift
AT gustafssonclaesm absoluteyeastmitochondrialproteomequantificationrevealstradeoffbetweenbiosynthesisandenergygenerationduringdiauxicshift
AT nielsenjens absoluteyeastmitochondrialproteomequantificationrevealstradeoffbetweenbiosynthesisandenergygenerationduringdiauxicshift