Physiological Genomics of Multistress Resistance in the Yeast Cell Model and Factory: Focus on MDR/MXR Transporters

Godinho, Cláudia P.; Sá‐Correia, Isabel

doi:10.1007/978-3-030-13035-0_1

Cited by 5 publications

(7 citation statements)

References 198 publications

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“…This response counteracts the re-entry of the acid form after the active expulsion of acetate from the cell interior, presumably catalysed by efflux pumps (e.g. Tpo2, Tpo3, Aqr1, Pdr18) 18 and, in this way, limits the associated futile cycle 2 , 19 .…”

Section: Introductionmentioning

confidence: 99%

Yeast adaptive response to acetic acid stress involves structural alterations and increased stiffness of the cell wall

Ribeiro

Vitorino

Godinho

et al. 2021

Sci Rep

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This work describes a coordinate and comprehensive view on the time course of the alterations occurring at the level of the cell wall during adaptation of a yeast cell population to sudden exposure to a sub-lethal stress induced by acetic acid. Acetic acid is a major inhibitory compound in industrial bioprocesses and a widely used preservative in foods and beverages. Results indicate that yeast cell wall resistance to lyticase activity increases during acetic acid-induced growth latency, corresponding to yeast population adaptation to sudden exposure to this stress. This response correlates with: (i) increased cell stiffness, assessed by atomic force microscopy (AFM); (ii) increased content of cell wall β-glucans, assessed by fluorescence microscopy, and (iii) slight increase of the transcription level of the GAS1 gene encoding a β-1,3-glucanosyltransferase that leads to elongation of (1→3)-β-d-glucan chains. Collectively, results reinforce the notion that the adaptive yeast response to acetic acid stress involves a coordinate alteration of the cell wall at the biophysical and molecular levels. These alterations guarantee a robust adaptive response essential to limit the futile cycle associated to the re-entry of the toxic acid form after the active expulsion of acetate from the cell interior.

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Section: Introductionmentioning

confidence: 99%

Yeast adaptive response to acetic acid stress involves structural alterations and increased stiffness of the cell wall

Ribeiro

Vitorino

Godinho

et al. 2021

Sci Rep

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“…Among a multitude of mechanisms that S . cerevisiae has developed to cope with the challenging conditions present in its natural environment and in industrial bioprocesses is the ability to change plasma membrane lipid and protein composition and organization (Godinho and Sá‐Correia, 2019). Plasma membrane transporters belonging to the ABC superfamily may play a dual role in yeast tolerance to chemical stresses (drugs and other xenobiotic compounds); they are hypothesized to catalyse the active efflux of the corresponding toxic compounds but some of them were implicated in lipid transport and control of plasma membrane lipidic environment (Godinho and Sá‐Correia, 2019).…”

Section: Discussionmentioning

confidence: 99%

“…Among other mechanisms, the acquisition of resistance to multiple stresses is mediated by plasma membrane proteins of the ABC (ATP‐binding cassette) or the major facilitator superfamily (MFS) superfamilies proposed to catalyse the extrusion of the corresponding toxic compounds (Godinho and Sá‐Correia, 2019). The present study is focused on the Pdr18 transporter belonging to the ABC superfamily and previously confirmed to be involved in multidrug/multixenobiotic resistance (MDR/MXR) (Godinho and Sá‐Correia, 2019). In line with accumulating evidence supporting the notion that yeast ABC proteins perform biological activities other than their accepted role as drug exporters, among them the transport of lipids (dos Santos et al ., 2014; dos Santos and Sá‐Correia, 2015; Prasad et al ., 2016; Godinho and Sá‐Correia, 2019), Pdr18 was proposed to be responsible for the active transport of ergosterol at the plasma membrane level (Cabrito et al ., 2011; Godinho et al ., 2018a).…”

Section: Introductionmentioning

confidence: 99%

“…The present study is focused on the Pdr18 transporter belonging to the ABC superfamily and previously confirmed to be involved in multidrug/multixenobiotic resistance (MDR/MXR) (Godinho and Sá‐Correia, 2019). In line with accumulating evidence supporting the notion that yeast ABC proteins perform biological activities other than their accepted role as drug exporters, among them the transport of lipids (dos Santos et al ., 2014; dos Santos and Sá‐Correia, 2015; Prasad et al ., 2016; Godinho and Sá‐Correia, 2019), Pdr18 was proposed to be responsible for the active transport of ergosterol at the plasma membrane level (Cabrito et al ., 2011; Godinho et al ., 2018a). Ergosterol concentration in the plasma membrane is essential to counteract acetic acid and the herbicide 2,4‐dichlorophenoxyacetic acid (2,4‐D) stress‐induced permeabilization and reduce the passive diffusion rate of the undissociated toxic forms of these weak acids (Cabrito et al ., 2011; Godinho et al ., 2018a).…”

Section: Introductionmentioning

confidence: 99%

“…Among other mechanisms, the acquisition of resistance to multiple stresses is mediated by plasma membrane proteins of the ABC (ATP-binding cassette) or the major facilitator superfamily (MFS) superfamilies proposed to catalyse the extrusion of the corresponding toxic compounds (Godinho and Sá-Correia, 2019). The present study is focused on the Pdr18 transporter belonging to the ABC superfamily and previously confirmed to be involved in multidrug/multixenobiotic resistance (MDR/MXR) (Godinho and Sá-Correia, 2019).…”

Section: Introductionmentioning

confidence: 99%

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The ABC transporter Pdr18 is required for yeast thermotolerance due to its role in ergosterol transport and plasma membrane properties

Godinho

Costa

Sá‐Correia

2020

Environmental Microbiology

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Among the mechanisms by which yeast overcomes multiple stresses is the expression of genes encoding ATP-binding cassette (ABC) transporters required for resistance to a wide range of toxic compounds. These substrates may include weak acids, alcohols, agricultural pesticides, polyamines, metal cations, as in the case of Pdr18. This pleotropic drug resistance transporter was previously proposed to transport ergosterol at the plasma membrane (PM) level contributing to the maintenance of PM lipid organization and reduced diffusional permeation induced by lipophilic compounds. The present work reports a novel phenotype associated with the putative drug/xenobiotic-efflux-pump transporter Pdr18: the resistance to heat shock and to long-term growth at supra-optimal temperatures. Cultivation at 40 C was demonstrated to lead to higher PM permeabilization of a pdr18Δ cell population with the PDR18 gene deleted compared with the parental strain population, as indicated by flow cytometry analysis of propidium iodide stained cells. Cells of pdr18Δ grown at 40 C also exhibited increased transcription levels from genes of the ergosterol biosynthetic pathway, compared with parental cells. However, this adaptive response at 40 C was not enough to maintain PM physiological ergosterol levels in the population lacking the Pdr18 transporter and free ergosterol precursors accumulate in the deletion mutant cells.

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

Antunes,

Kale,

Sychrová

et al. 2023

Microb Cell

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Acetic acid-induced stress is a common challenge in natural environments and industrial bioprocesses, significantly affecting the growth and metabolic performance 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, particularly 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 implicated 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 tolerance 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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Physiological Genomics of Multistress Resistance in the Yeast Cell Model and Factory: Focus on MDR/MXR Transporters

Cited by 5 publications

References 198 publications

Yeast adaptive response to acetic acid stress involves structural alterations and increased stiffness of the cell wall

Yeast adaptive response to acetic acid stress involves structural alterations and increased stiffness of the cell wall

The ABC transporter Pdr18 is required for yeast thermotolerance due to its role in ergosterol transport and plasma membrane properties

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

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