Crosstalk between Yeast Cell Plasma Membrane Ergosterol Content and Cell Wall Stiffness under Acetic Acid Stress Involving Pdr18
Acetic acid is a major inhibitory compound in several industrial bioprocesses, in particular in lignocellulosic yeast biorefineries. Cell envelope remodeling, involving cell wall and plasma membrane composition, structure and function, is among the mechanisms behind yeast adaptation and tolerance to...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2022-01-01
|
| Series: | Journal of Fungi |
| Subjects: | |
| Online Access: | https://www.mdpi.com/2309-608X/8/2/103 |
| _version_ | 1797478942542659584 |
|---|---|
| author | Ricardo A. Ribeiro Cláudia P. Godinho Miguel V. Vitorino Tiago T. Robalo Fábio Fernandes Mário S. Rodrigues Isabel Sá-Correia |
| author_facet | Ricardo A. Ribeiro Cláudia P. Godinho Miguel V. Vitorino Tiago T. Robalo Fábio Fernandes Mário S. Rodrigues Isabel Sá-Correia |
| author_sort | Ricardo A. Ribeiro |
| collection | DOAJ |
| description | Acetic acid is a major inhibitory compound in several industrial bioprocesses, in particular in lignocellulosic yeast biorefineries. Cell envelope remodeling, involving cell wall and plasma membrane composition, structure and function, is among the mechanisms behind yeast adaptation and tolerance to stress. Pdr18 is a plasma membrane ABC transporter of the pleiotropic drug resistance family and a reported determinant of acetic acid tolerance mediating ergosterol transport. This study provides evidence for the impact of Pdr18 expression in yeast cell wall during adaptation to acetic acid stress. The time-course of acetic-acid-induced transcriptional activation of cell wall biosynthetic genes (<i>FKS1</i>, <i>BGL2</i>, <i>CHS3</i>, <i>GAS1</i>) and of increased cell wall stiffness and cell wall polysaccharide content in cells with the <i>PDR18</i> deleted, compared to parental cells, is reported. Despite the robust and more intense adaptive response of the <i>pdr18</i>Δ population, the stress-induced increase of cell wall resistance to lyticase activity was below parental strain levels, and the duration of the period required for intracellular pH recovery from acidification and growth resumption was higher in the less tolerant <i>pdr18</i>Δ population. The ergosterol content, critical for plasma membrane stabilization, suffered a drastic reduction in the first hour of cultivation under acetic acid stress, especially in <i>pdr18</i>Δ cells. Results revealed a crosstalk between plasma membrane ergosterol content and cell wall biophysical properties, suggesting a coordinated response to counteract the deleterious effects of acetic acid. |
| first_indexed | 2024-03-09T21:38:47Z |
| format | Article |
| id | doaj.art-f8c14ffd785f49fb8cba370838b36cd7 |
| institution | Directory Open Access Journal |
| issn | 2309-608X |
| language | English |
| last_indexed | 2024-03-09T21:38:47Z |
| publishDate | 2022-01-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Journal of Fungi |
| spelling | doaj.art-f8c14ffd785f49fb8cba370838b36cd72023-11-23T20:36:55ZengMDPI AGJournal of Fungi2309-608X2022-01-018210310.3390/jof8020103Crosstalk between Yeast Cell Plasma Membrane Ergosterol Content and Cell Wall Stiffness under Acetic Acid Stress Involving Pdr18Ricardo A. Ribeiro0Cláudia P. Godinho1Miguel V. Vitorino2Tiago T. Robalo3Fábio Fernandes4Mário S. Rodrigues5Isabel Sá-Correia6iBB—Institute for Bioengineering and Biosciences, Instituto Superior Técnico, Universidade de Lisboa, Av. Rovisco Pais, 1049-001 Lisbon, PortugaliBB—Institute for Bioengineering and Biosciences, Instituto Superior Técnico, Universidade de Lisboa, Av. Rovisco Pais, 1049-001 Lisbon, PortugalBioISI—Biosystems and Integrative Sciences Institute, Faculdade de Ciências, Universidade de Lisboa, Campo Grande 16, 1749-016 Lisbon, PortugalBioISI—Biosystems and Integrative Sciences Institute, Faculdade de Ciências, Universidade de Lisboa, Campo Grande 16, 1749-016 Lisbon, PortugaliBB—Institute for Bioengineering and Biosciences, Instituto Superior Técnico, Universidade de Lisboa, Av. Rovisco Pais, 1049-001 Lisbon, PortugalBioISI—Biosystems and Integrative Sciences Institute, Faculdade de Ciências, Universidade de Lisboa, Campo Grande 16, 1749-016 Lisbon, PortugaliBB—Institute for Bioengineering and Biosciences, Instituto Superior Técnico, Universidade de Lisboa, Av. Rovisco Pais, 1049-001 Lisbon, PortugalAcetic acid is a major inhibitory compound in several industrial bioprocesses, in particular in lignocellulosic yeast biorefineries. Cell envelope remodeling, involving cell wall and plasma membrane composition, structure and function, is among the mechanisms behind yeast adaptation and tolerance to stress. Pdr18 is a plasma membrane ABC transporter of the pleiotropic drug resistance family and a reported determinant of acetic acid tolerance mediating ergosterol transport. This study provides evidence for the impact of Pdr18 expression in yeast cell wall during adaptation to acetic acid stress. The time-course of acetic-acid-induced transcriptional activation of cell wall biosynthetic genes (<i>FKS1</i>, <i>BGL2</i>, <i>CHS3</i>, <i>GAS1</i>) and of increased cell wall stiffness and cell wall polysaccharide content in cells with the <i>PDR18</i> deleted, compared to parental cells, is reported. Despite the robust and more intense adaptive response of the <i>pdr18</i>Δ population, the stress-induced increase of cell wall resistance to lyticase activity was below parental strain levels, and the duration of the period required for intracellular pH recovery from acidification and growth resumption was higher in the less tolerant <i>pdr18</i>Δ population. The ergosterol content, critical for plasma membrane stabilization, suffered a drastic reduction in the first hour of cultivation under acetic acid stress, especially in <i>pdr18</i>Δ cells. Results revealed a crosstalk between plasma membrane ergosterol content and cell wall biophysical properties, suggesting a coordinated response to counteract the deleterious effects of acetic acid.https://www.mdpi.com/2309-608X/8/2/103<i>Saccharomyces cerevisiae</i>adaptation and tolerance to acetic acidcell envelopeplasma membranecell wall stiffnesscell wall remodeling |
| spellingShingle | Ricardo A. Ribeiro Cláudia P. Godinho Miguel V. Vitorino Tiago T. Robalo Fábio Fernandes Mário S. Rodrigues Isabel Sá-Correia Crosstalk between Yeast Cell Plasma Membrane Ergosterol Content and Cell Wall Stiffness under Acetic Acid Stress Involving Pdr18 Journal of Fungi <i>Saccharomyces cerevisiae</i> adaptation and tolerance to acetic acid cell envelope plasma membrane cell wall stiffness cell wall remodeling |
| title | Crosstalk between Yeast Cell Plasma Membrane Ergosterol Content and Cell Wall Stiffness under Acetic Acid Stress Involving Pdr18 |
| title_full | Crosstalk between Yeast Cell Plasma Membrane Ergosterol Content and Cell Wall Stiffness under Acetic Acid Stress Involving Pdr18 |
| title_fullStr | Crosstalk between Yeast Cell Plasma Membrane Ergosterol Content and Cell Wall Stiffness under Acetic Acid Stress Involving Pdr18 |
| title_full_unstemmed | Crosstalk between Yeast Cell Plasma Membrane Ergosterol Content and Cell Wall Stiffness under Acetic Acid Stress Involving Pdr18 |
| title_short | Crosstalk between Yeast Cell Plasma Membrane Ergosterol Content and Cell Wall Stiffness under Acetic Acid Stress Involving Pdr18 |
| title_sort | crosstalk between yeast cell plasma membrane ergosterol content and cell wall stiffness under acetic acid stress involving pdr18 |
| topic | <i>Saccharomyces cerevisiae</i> adaptation and tolerance to acetic acid cell envelope plasma membrane cell wall stiffness cell wall remodeling |
| url | https://www.mdpi.com/2309-608X/8/2/103 |
| work_keys_str_mv | AT ricardoaribeiro crosstalkbetweenyeastcellplasmamembraneergosterolcontentandcellwallstiffnessunderaceticacidstressinvolvingpdr18 AT claudiapgodinho crosstalkbetweenyeastcellplasmamembraneergosterolcontentandcellwallstiffnessunderaceticacidstressinvolvingpdr18 AT miguelvvitorino crosstalkbetweenyeastcellplasmamembraneergosterolcontentandcellwallstiffnessunderaceticacidstressinvolvingpdr18 AT tiagotrobalo crosstalkbetweenyeastcellplasmamembraneergosterolcontentandcellwallstiffnessunderaceticacidstressinvolvingpdr18 AT fabiofernandes crosstalkbetweenyeastcellplasmamembraneergosterolcontentandcellwallstiffnessunderaceticacidstressinvolvingpdr18 AT mariosrodrigues crosstalkbetweenyeastcellplasmamembraneergosterolcontentandcellwallstiffnessunderaceticacidstressinvolvingpdr18 AT isabelsacorreia crosstalkbetweenyeastcellplasmamembraneergosterolcontentandcellwallstiffnessunderaceticacidstressinvolvingpdr18 |