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

Ricardo A Ribeiro,Miguel V Vitorino,Mário S Rodrigues,Cláudia P Godinho,Fábio Fernandes,Isabel Sá-Correia,Nuno Bourbon-Melo,Tiago T Robalo

doi:10.1038/s41598-021-92069-3

Abstract

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.

Highlights

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
Genes involved in 1-3 β-glucan synthesis (FKS1, ROM2), 1-6 β-glucan synthesis (KRE6), 1-3 β-glucan elongation and branching (GAS1), chitin synthesis (CHS1, CHS5) and cell wall protein mannosylation (MNN2, MNN9, MNN11, KTR4) are reported determinants of tolerance to acetic acid[6]
This seems to point towards a role for the cell wall in acetic acid stress response and tolerance, the transcript levels from the acetic acid tolerance determinant genes CHS1, KTR4, MNN9 and FKS1 were reported to decrease in acetic acid stressed cells[7]

Summary

Introduction

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. 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. Among them is the alteration of the molecular composition and physical properties of plasma membrane and cell wall, leading to the decrease of cell envelope p ermeability[2,15,16,17] Such adaptation, at the level of the cell envelope, is essential to reduce the diffusion rate of this weak acid from the cell exterior to the intracellular medium. Results provide a global view on mechanisms underlying the time-course of yeast cell adaptation to acetic acid stress at the cell wall level

Objectives

Methods

Results

Conclusion