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Multiple nutrient transporters enable cells to mitigate a rate-affinity tradeoff

Eukaryotic genomes often encode multiple transporters for the same nutrient. For example, budding yeast has 17 hexose transporters (HXTs), all of which potentially transport glucose. Using mathematical modelling, we show that transporters that use either facilitated diffusion or symport can have a r...

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Autores principales: Montaño-Gutierrez, Luis Fernando, Correia, Kevin, Swain, Peter S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9071158/
https://www.ncbi.nlm.nih.gov/pubmed/35468136
http://dx.doi.org/10.1371/journal.pcbi.1010060
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author Montaño-Gutierrez, Luis Fernando
Correia, Kevin
Swain, Peter S.
author_facet Montaño-Gutierrez, Luis Fernando
Correia, Kevin
Swain, Peter S.
author_sort Montaño-Gutierrez, Luis Fernando
collection PubMed
description Eukaryotic genomes often encode multiple transporters for the same nutrient. For example, budding yeast has 17 hexose transporters (HXTs), all of which potentially transport glucose. Using mathematical modelling, we show that transporters that use either facilitated diffusion or symport can have a rate-affinity tradeoff, where an increase in the maximal rate of transport decreases the transporter’s apparent affinity. These changes affect the import flux non-monotonically, and for a given concentration of extracellular nutrient there is one transporter, characterised by its affinity, that has a higher import flux than any other. Through encoding multiple transporters, cells can therefore mitigate the tradeoff by expressing those transporters with higher affinities in lower concentrations of nutrients. We verify our predictions using fluorescent tagging of seven HXT genes in budding yeast and follow their expression over time in batch culture. Using the known affinities of the corresponding transporters, we show that their regulation in glucose is broadly consistent with a rate-affinity tradeoff: as glucose falls, the levels of the different transporters peak in an order that mostly follows their affinity for glucose. More generally, evolution is constrained by tradeoffs. Our findings indicate that one such tradeoff often occurs in the cellular transport of nutrients.
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spelling pubmed-90711582022-05-06 Multiple nutrient transporters enable cells to mitigate a rate-affinity tradeoff Montaño-Gutierrez, Luis Fernando Correia, Kevin Swain, Peter S. PLoS Comput Biol Research Article Eukaryotic genomes often encode multiple transporters for the same nutrient. For example, budding yeast has 17 hexose transporters (HXTs), all of which potentially transport glucose. Using mathematical modelling, we show that transporters that use either facilitated diffusion or symport can have a rate-affinity tradeoff, where an increase in the maximal rate of transport decreases the transporter’s apparent affinity. These changes affect the import flux non-monotonically, and for a given concentration of extracellular nutrient there is one transporter, characterised by its affinity, that has a higher import flux than any other. Through encoding multiple transporters, cells can therefore mitigate the tradeoff by expressing those transporters with higher affinities in lower concentrations of nutrients. We verify our predictions using fluorescent tagging of seven HXT genes in budding yeast and follow their expression over time in batch culture. Using the known affinities of the corresponding transporters, we show that their regulation in glucose is broadly consistent with a rate-affinity tradeoff: as glucose falls, the levels of the different transporters peak in an order that mostly follows their affinity for glucose. More generally, evolution is constrained by tradeoffs. Our findings indicate that one such tradeoff often occurs in the cellular transport of nutrients. Public Library of Science 2022-04-25 /pmc/articles/PMC9071158/ /pubmed/35468136 http://dx.doi.org/10.1371/journal.pcbi.1010060 Text en © 2022 Montaño-Gutierrez et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Montaño-Gutierrez, Luis Fernando
Correia, Kevin
Swain, Peter S.
Multiple nutrient transporters enable cells to mitigate a rate-affinity tradeoff
title Multiple nutrient transporters enable cells to mitigate a rate-affinity tradeoff
title_full Multiple nutrient transporters enable cells to mitigate a rate-affinity tradeoff
title_fullStr Multiple nutrient transporters enable cells to mitigate a rate-affinity tradeoff
title_full_unstemmed Multiple nutrient transporters enable cells to mitigate a rate-affinity tradeoff
title_short Multiple nutrient transporters enable cells to mitigate a rate-affinity tradeoff
title_sort multiple nutrient transporters enable cells to mitigate a rate-affinity tradeoff
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9071158/
https://www.ncbi.nlm.nih.gov/pubmed/35468136
http://dx.doi.org/10.1371/journal.pcbi.1010060
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