Alcohols enhance the rate of acetic acid diffusion in S. cerevisiae : biophysical mechanisms and implications for acetic acid tolerance

Authors:

Lina Lindahl1, Samuel Genheden2, Fábio Faria-Oliveira1, Stefan Allard3, Leif A. Eriksson2, Lisbeth Olsson1, Maurizio Bettiga1,4

doi: 10.15698/mic2018.01.609
Volume 5, pp. 42 to 55, published 01/12/2017.

PDF Download PubMed Link Supplemental Information
Affiliations:

1 Department of Biology and Biological Engineering, Division of Industrial Biotechnology, Chalmers University of Technology, Gothenburg, Sweden.

2 Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden.

3 Department of Chemistry and Chemical Engineering, Division of Energy and Materials, Nuclear Chemistry, Chalmers University of Technology, Gothenburg, Sweden.

4 EviKrets Biobased Processes Consultants, Gothenburg, Sweden.

Keywords: 

ethanol, n-butanol, lignocellulose, inhibitors, molecular dynamics simulations, membrane permeation, carbon-14 uptake

Corresponding Author(s):

Maurizio Bettiga, Department of Biology and Biological Engineering, Division of Industrial Biotechnology, Chalmers University of Technology, Kemivägen 10, SE 412 96 Gothenburg, Sweden, Tel: +46 (0)31 772 3852; maurizio.bettiga@chalmers.se

Conflict of interest statement:

The authors declare that they have no competing interests.

Please cite this article as:

Lina Lindahl, Samuel Genheden, Fábio Faria-Oliveira, Stefan Allard, Leif A Eriksson, Lisbeth Olsson, Maurizio Bettiga (2017). Alcohols enhance the rate of acetic acid diffusion in S. cerevisiae: Biophysical mechanisms and implications for acetic acid tolerance. Microbial Cell 5(1): 42-55. doi: 10.15698/mic2018.01.609

© 2017 Lindahl et al. This is an open-access article released under the terms of the Creative Commons Attribution (CC BY) license, which allows the unrestricted use, distribution, and reproduction in any medium, provided the original author and source are acknowledged.

Abstract:

Microbial cell factories with the ability to maintain high productivity in the presence of weak organic acids, such as acetic acid, are required in many industrial processes. For example, fermentation media derived from lignocellulosic biomass are rich in acetic acid and other weak acids. The rate of diffusional entry of acetic acid is one parameter determining the ability of microorganisms to tolerance the acid. The present study demonstrates that the rate of acetic acid diffusion in S. cerevisiae is strongly affected by the alcohols ethanol and n-butanol. Ethanol of 40 g/L and n-butanol of 8 g/L both caused a 65% increase in the rate of acetic acid diffusion, and higher alcohol concentrations caused even greater increases. Molecular dynamics simulations of membrane dynamics in the presence of alcohols demonstrated that the partitioning of alcohols to the head group region of the lipid bilayer causes a considerable increase in the membrane area, together with reduced membrane thickness and lipid order. These changes in physiochemical membrane properties lead to an increased number of water molecules in the membrane interior, providing biophysical mechanisms for the alcohol-induced increase in acetic acid diffusion rate. n-butanol affected S. cerevisiae and the cell membrane properties at lower concentrations than ethanol, due to greater and deeper partitioning in the membrane. This study demonstrates that the rate of acetic acid diffusion can be strongly affected by compounds that partition into the cell membrane, and highlights the need for considering interaction effects between compounds in the design of microbial processes.