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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Main Authors: Luis Fernando Montaño-Gutierrez, Kevin Correia, Peter S Swain
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2022-04-01
Series:PLoS Computational Biology
Online Access:https://doi.org/10.1371/journal.pcbi.1010060
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author Luis Fernando Montaño-Gutierrez
Kevin Correia
Peter S Swain
author_facet Luis Fernando Montaño-Gutierrez
Kevin Correia
Peter S Swain
author_sort Luis Fernando Montaño-Gutierrez
collection DOAJ
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 doaj.art-83c3c08a5b3d4e83ba6a2dac15ff086c2022-12-22T01:53:32ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582022-04-01184e101006010.1371/journal.pcbi.1010060Multiple nutrient transporters enable cells to mitigate a rate-affinity tradeoff.Luis Fernando Montaño-GutierrezKevin CorreiaPeter S SwainEukaryotic 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.https://doi.org/10.1371/journal.pcbi.1010060
spellingShingle Luis Fernando Montaño-Gutierrez
Kevin Correia
Peter S Swain
Multiple nutrient transporters enable cells to mitigate a rate-affinity tradeoff.
PLoS Computational Biology
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
url https://doi.org/10.1371/journal.pcbi.1010060
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