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Nitrogen limitation reveals large reserves in metabolic and translational capacities of yeast

Cells maintain reserves in their metabolic and translational capacities as a strategy to quickly respond to changing environments. Here we quantify these reserves by stepwise reducing nitrogen availability in yeast steady-state chemostat cultures, imposing severe restrictions on total cellular prote...

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Autores principales: Yu, Rosemary, Campbell, Kate, Pereira, Rui, Björkeroth, Johan, Qi, Qi, Vorontsov, Egor, Sihlbom, Carina, Nielsen, Jens
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7171132/
https://www.ncbi.nlm.nih.gov/pubmed/32312967
http://dx.doi.org/10.1038/s41467-020-15749-0
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author Yu, Rosemary
Campbell, Kate
Pereira, Rui
Björkeroth, Johan
Qi, Qi
Vorontsov, Egor
Sihlbom, Carina
Nielsen, Jens
author_facet Yu, Rosemary
Campbell, Kate
Pereira, Rui
Björkeroth, Johan
Qi, Qi
Vorontsov, Egor
Sihlbom, Carina
Nielsen, Jens
author_sort Yu, Rosemary
collection PubMed
description Cells maintain reserves in their metabolic and translational capacities as a strategy to quickly respond to changing environments. Here we quantify these reserves by stepwise reducing nitrogen availability in yeast steady-state chemostat cultures, imposing severe restrictions on total cellular protein and transcript content. Combining multi-omics analysis with metabolic modeling, we find that seven metabolic superpathways maintain >50% metabolic capacity in reserve, with glucose metabolism maintaining >80% reserve capacity. Cells maintain >50% reserve in translational capacity for 2490 out of 3361 expressed genes (74%), with a disproportionately large reserve dedicated to translating metabolic proteins. Finally, ribosome reserves contain up to 30% sub-stoichiometric ribosomal proteins, with activation of reserve translational capacity associated with selective upregulation of 17 ribosomal proteins. Together, our dataset provides a quantitative link between yeast physiology and cellular economics, which could be leveraged in future cell engineering through targeted proteome streamlining.
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spelling pubmed-71711322020-04-23 Nitrogen limitation reveals large reserves in metabolic and translational capacities of yeast Yu, Rosemary Campbell, Kate Pereira, Rui Björkeroth, Johan Qi, Qi Vorontsov, Egor Sihlbom, Carina Nielsen, Jens Nat Commun Article Cells maintain reserves in their metabolic and translational capacities as a strategy to quickly respond to changing environments. Here we quantify these reserves by stepwise reducing nitrogen availability in yeast steady-state chemostat cultures, imposing severe restrictions on total cellular protein and transcript content. Combining multi-omics analysis with metabolic modeling, we find that seven metabolic superpathways maintain >50% metabolic capacity in reserve, with glucose metabolism maintaining >80% reserve capacity. Cells maintain >50% reserve in translational capacity for 2490 out of 3361 expressed genes (74%), with a disproportionately large reserve dedicated to translating metabolic proteins. Finally, ribosome reserves contain up to 30% sub-stoichiometric ribosomal proteins, with activation of reserve translational capacity associated with selective upregulation of 17 ribosomal proteins. Together, our dataset provides a quantitative link between yeast physiology and cellular economics, which could be leveraged in future cell engineering through targeted proteome streamlining. Nature Publishing Group UK 2020-04-20 /pmc/articles/PMC7171132/ /pubmed/32312967 http://dx.doi.org/10.1038/s41467-020-15749-0 Text en © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Yu, Rosemary
Campbell, Kate
Pereira, Rui
Björkeroth, Johan
Qi, Qi
Vorontsov, Egor
Sihlbom, Carina
Nielsen, Jens
Nitrogen limitation reveals large reserves in metabolic and translational capacities of yeast
title Nitrogen limitation reveals large reserves in metabolic and translational capacities of yeast
title_full Nitrogen limitation reveals large reserves in metabolic and translational capacities of yeast
title_fullStr Nitrogen limitation reveals large reserves in metabolic and translational capacities of yeast
title_full_unstemmed Nitrogen limitation reveals large reserves in metabolic and translational capacities of yeast
title_short Nitrogen limitation reveals large reserves in metabolic and translational capacities of yeast
title_sort nitrogen limitation reveals large reserves in metabolic and translational capacities of yeast
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7171132/
https://www.ncbi.nlm.nih.gov/pubmed/32312967
http://dx.doi.org/10.1038/s41467-020-15749-0
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