The Hrk1 kinase is a determinant of acetic acid tolerance in yeast by modulating H+ and K+ homeostasis

Acetic acid-induced stress is a common challenge in natural environments and industrial bioprocesses, significantly affecting the growth and metabolic per-formance of Saccharomyces cerevisiae. The adaptive response and tolerance to this stress involves the activation of a complex network of molecula...

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Main Authors: Miguel Antunes, Deepika Kale, Hana Sychrová, Isabel Sá-Correia
Format: Article
Language:English
Published: Shared Science Publishers OG 2023-11-01
Series:Microbial Cell
Subjects:
Online Access:http://microbialcell.com/researcharticles/2023a-antunes-microbial-cell/
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author Miguel Antunes
Deepika Kale
Hana Sychrová
Isabel Sá-Correia
author_facet Miguel Antunes
Deepika Kale
Hana Sychrová
Isabel Sá-Correia
author_sort Miguel Antunes
collection DOAJ
description Acetic acid-induced stress is a common challenge in natural environments and industrial bioprocesses, significantly affecting the growth and metabolic per-formance of Saccharomyces cerevisiae. The adaptive response and tolerance to this stress involves the activation of a complex network of molecular pathways. This study aims to delve deeper into these mechanisms in S. cerevisiae, particu-larly focusing on the role of the Hrk1 kinase. Hrk1 is a key determinant of acetic acid tolerance, belonging to the NPR/Hal family, whose members are implicat-ed in the modulation of the activity of plasma membrane transporters that orchestrate nutrient uptake and ion homeostasis. The influence of Hrk1 on S. cerevisiae adaptation to acetic acid-induced stress was explored by employing a physiological approach based on previous phosphoproteomics analyses. The results from this study reflect the multifunctional roles of Hrk1 in maintaining proton and potassium homeostasis during different phases of acetic acid-stressed cultivation. Hrk1 is shown to play a role in the activation of plasma membrane H+-ATPase, maintaining pH homeostasis, and in the modulation of plasma membrane potential under acetic acid stressed cultivation. Potassium (K+) supplementation of the growth medium, particularly when provided at limiting concentrations, led to a notable improvement in acetic acid stress tol-erance of the hrk1∆ strain. Moreover, abrogation of this kinase expression is shown to confer a physiological advantage to growth under K+ limitation also in the absence of acetic acid stress. The involvement of the alkali metal cation/H+ exchanger Nha1, another proposed molecular target of Hrk1, in improving yeast growth under K+ limitation or acetic acid stress, is proposed.
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spelling doaj.art-fa7a63a748df48df9850ee7d3ceac3d72025-03-12T13:46:43ZengShared Science Publishers OGMicrobial Cell2311-26382023-11-01101226127610.15698/mic2023.12.809The Hrk1 kinase is a determinant of acetic acid tolerance in yeast by modulating H+ and K+ homeostasisMiguel Antunes0Deepika Kale1Hana Sychrová2Isabel Sá-Correia3iBB—Institute for Bioengineering and Biosciences, Instituto Superior Técnico, Universidade de Lisboa, 1049-001 Lisbon, Portugal.Laboratory of Membrane Transport, Institute of Physiology, Czech Academy of Sciences, Videnska 1083, 142 00 Prague 4, Czech Republic.Laboratory of Membrane Transport, Institute of Physiology, Czech Academy of Sciences, Videnska 1083, 142 00 Prague 4, Czech Republic.iBB—Institute for Bioengineering and Biosciences, Instituto Superior Técnico, Universidade de Lisboa, 1049-001 Lisbon, Portugal.Acetic acid-induced stress is a common challenge in natural environments and industrial bioprocesses, significantly affecting the growth and metabolic per-formance of Saccharomyces cerevisiae. The adaptive response and tolerance to this stress involves the activation of a complex network of molecular pathways. This study aims to delve deeper into these mechanisms in S. cerevisiae, particu-larly focusing on the role of the Hrk1 kinase. Hrk1 is a key determinant of acetic acid tolerance, belonging to the NPR/Hal family, whose members are implicat-ed in the modulation of the activity of plasma membrane transporters that orchestrate nutrient uptake and ion homeostasis. The influence of Hrk1 on S. cerevisiae adaptation to acetic acid-induced stress was explored by employing a physiological approach based on previous phosphoproteomics analyses. The results from this study reflect the multifunctional roles of Hrk1 in maintaining proton and potassium homeostasis during different phases of acetic acid-stressed cultivation. Hrk1 is shown to play a role in the activation of plasma membrane H+-ATPase, maintaining pH homeostasis, and in the modulation of plasma membrane potential under acetic acid stressed cultivation. Potassium (K+) supplementation of the growth medium, particularly when provided at limiting concentrations, led to a notable improvement in acetic acid stress tol-erance of the hrk1∆ strain. Moreover, abrogation of this kinase expression is shown to confer a physiological advantage to growth under K+ limitation also in the absence of acetic acid stress. The involvement of the alkali metal cation/H+ exchanger Nha1, another proposed molecular target of Hrk1, in improving yeast growth under K+ limitation or acetic acid stress, is proposed.http://microbialcell.com/researcharticles/2023a-antunes-microbial-cell/acetic acid tolerancepma1 activityplasma membrane h+-atpasenha1saccharomyces cerevisiaeyeast kinasesnpr/hal family
spellingShingle Miguel Antunes
Deepika Kale
Hana Sychrová
Isabel Sá-Correia
The Hrk1 kinase is a determinant of acetic acid tolerance in yeast by modulating H+ and K+ homeostasis
Microbial Cell
acetic acid tolerance
pma1 activity
plasma membrane h+-atpase
nha1
saccharomyces cerevisiae
yeast kinases
npr/hal family
title The Hrk1 kinase is a determinant of acetic acid tolerance in yeast by modulating H+ and K+ homeostasis
title_full The Hrk1 kinase is a determinant of acetic acid tolerance in yeast by modulating H+ and K+ homeostasis
title_fullStr The Hrk1 kinase is a determinant of acetic acid tolerance in yeast by modulating H+ and K+ homeostasis
title_full_unstemmed The Hrk1 kinase is a determinant of acetic acid tolerance in yeast by modulating H+ and K+ homeostasis
title_short The Hrk1 kinase is a determinant of acetic acid tolerance in yeast by modulating H+ and K+ homeostasis
title_sort hrk1 kinase is a determinant of acetic acid tolerance in yeast by modulating h and k homeostasis
topic acetic acid tolerance
pma1 activity
plasma membrane h+-atpase
nha1
saccharomyces cerevisiae
yeast kinases
npr/hal family
url http://microbialcell.com/researcharticles/2023a-antunes-microbial-cell/
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