Myriocin‐induced adaptive laboratory evolution of an industrial strain of Saccharomyces cerevisiae reveals its potential to remodel lipid composition and heat tolerance

Summary The modification of lipid composition allows cells to adjust membrane biophysical properties in response to changes in environmental temperature. Here, we use adaptive laboratory evolution (ALE) in the presence of myriocin, a sphingolipid (SLs) biosynthesis inhibitor, to remodel the lipid pr...

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Main Authors: Francisca Randez‐Gil, Jose A. Prieto, Alejandro Rodríguez‐Puchades, Josefina Casas, Vicente Sentandreu, Francisco Estruch
Format: Article
Language:English
Published: Wiley 2020-07-01
Series:Microbial Biotechnology
Online Access:https://doi.org/10.1111/1751-7915.13555
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author Francisca Randez‐Gil
Jose A. Prieto
Alejandro Rodríguez‐Puchades
Josefina Casas
Vicente Sentandreu
Francisco Estruch
author_facet Francisca Randez‐Gil
Jose A. Prieto
Alejandro Rodríguez‐Puchades
Josefina Casas
Vicente Sentandreu
Francisco Estruch
author_sort Francisca Randez‐Gil
collection DOAJ
description Summary The modification of lipid composition allows cells to adjust membrane biophysical properties in response to changes in environmental temperature. Here, we use adaptive laboratory evolution (ALE) in the presence of myriocin, a sphingolipid (SLs) biosynthesis inhibitor, to remodel the lipid profile of an industrial yeast strain (LH) of Saccharomyces cerevisiae. The approach enabled to obtain a heterogeneous population (LHev) of myriocin‐tolerant evolved clones characterized by its growth capacity at high temperature. Myriocin exposure also caused tolerance to soraphen A, an inhibitor of the acetyl‐CoA carboxylase Acc1, the rate‐limiting enzyme in fatty acid de novo production, supporting a change in lipid metabolism during ALE. In line with this, characterization of two randomly selected clones, LH03 and LH09, showed the presence of lipids with increased saturation degree and reduced acyl length. In addition, the clone LH03, which displays the greater improvement in fitness at 40°C, exhibited higher SL content as compared with the parental strain. Analysis of the LH03 and LH09 genomes revealed a loss of chromosomes affecting genes that have a role in fatty acid synthesis and elongation. The link between ploidy level and growth at high temperature was further supported by the analysis of a fully isogenic set of yeast strains with ploidy between 1N and 4N which showed that the loss of genome content provides heat tolerance. Consistent with this, a thermotolerant evolved population (LH40°) generated from the parental LH strain by heat‐driven ALE exhibited a reduction in the chromosome copy number. Thus, our results identify myriocin‐driven evolution as a powerful approach to investigate the mechanisms of acquired thermotolerance and to generate improved strains.
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spelling doaj.art-b9ae57654e0c4093b419b21b9ebfa8152022-12-21T21:24:47ZengWileyMicrobial Biotechnology1751-79152020-07-011341066108110.1111/1751-7915.13555Myriocin‐induced adaptive laboratory evolution of an industrial strain of Saccharomyces cerevisiae reveals its potential to remodel lipid composition and heat toleranceFrancisca Randez‐Gil0Jose A. Prieto1Alejandro Rodríguez‐Puchades2Josefina Casas3Vicente Sentandreu4Francisco Estruch5Department of Biotechnology Instituto de Agroquímica y Tecnología de los Alimentos Consejo Superior de Investigaciones Científicas Avda. Agustín Escardino 7 Paterna Valencia 46980 SpainDepartment of Biotechnology Instituto de Agroquímica y Tecnología de los Alimentos Consejo Superior de Investigaciones Científicas Avda. Agustín Escardino 7 Paterna Valencia 46980 SpainDepartment of Biotechnology Instituto de Agroquímica y Tecnología de los Alimentos Consejo Superior de Investigaciones Científicas Avda. Agustín Escardino 7 Paterna Valencia 46980 SpainResearch Unit on BioActive Molecules (RUBAM) Instituto de Química Avanzada de Cataluña Consejo Superior de Investigaciones Científicas Jordi Girona 18‐26. Barcelona 08034 SpainGenomics Section Central Service for Experimental Research (SCSIE) Universitat de València Dr. Moliner 50 Burjassot 46100 SpainDepartament of Biochemistry and Molecular Biology Universitat de València Dr. Moliner 50 Burjassot 46100 SpainSummary The modification of lipid composition allows cells to adjust membrane biophysical properties in response to changes in environmental temperature. Here, we use adaptive laboratory evolution (ALE) in the presence of myriocin, a sphingolipid (SLs) biosynthesis inhibitor, to remodel the lipid profile of an industrial yeast strain (LH) of Saccharomyces cerevisiae. The approach enabled to obtain a heterogeneous population (LHev) of myriocin‐tolerant evolved clones characterized by its growth capacity at high temperature. Myriocin exposure also caused tolerance to soraphen A, an inhibitor of the acetyl‐CoA carboxylase Acc1, the rate‐limiting enzyme in fatty acid de novo production, supporting a change in lipid metabolism during ALE. In line with this, characterization of two randomly selected clones, LH03 and LH09, showed the presence of lipids with increased saturation degree and reduced acyl length. In addition, the clone LH03, which displays the greater improvement in fitness at 40°C, exhibited higher SL content as compared with the parental strain. Analysis of the LH03 and LH09 genomes revealed a loss of chromosomes affecting genes that have a role in fatty acid synthesis and elongation. The link between ploidy level and growth at high temperature was further supported by the analysis of a fully isogenic set of yeast strains with ploidy between 1N and 4N which showed that the loss of genome content provides heat tolerance. Consistent with this, a thermotolerant evolved population (LH40°) generated from the parental LH strain by heat‐driven ALE exhibited a reduction in the chromosome copy number. Thus, our results identify myriocin‐driven evolution as a powerful approach to investigate the mechanisms of acquired thermotolerance and to generate improved strains.https://doi.org/10.1111/1751-7915.13555
spellingShingle Francisca Randez‐Gil
Jose A. Prieto
Alejandro Rodríguez‐Puchades
Josefina Casas
Vicente Sentandreu
Francisco Estruch
Myriocin‐induced adaptive laboratory evolution of an industrial strain of Saccharomyces cerevisiae reveals its potential to remodel lipid composition and heat tolerance
Microbial Biotechnology
title Myriocin‐induced adaptive laboratory evolution of an industrial strain of Saccharomyces cerevisiae reveals its potential to remodel lipid composition and heat tolerance
title_full Myriocin‐induced adaptive laboratory evolution of an industrial strain of Saccharomyces cerevisiae reveals its potential to remodel lipid composition and heat tolerance
title_fullStr Myriocin‐induced adaptive laboratory evolution of an industrial strain of Saccharomyces cerevisiae reveals its potential to remodel lipid composition and heat tolerance
title_full_unstemmed Myriocin‐induced adaptive laboratory evolution of an industrial strain of Saccharomyces cerevisiae reveals its potential to remodel lipid composition and heat tolerance
title_short Myriocin‐induced adaptive laboratory evolution of an industrial strain of Saccharomyces cerevisiae reveals its potential to remodel lipid composition and heat tolerance
title_sort myriocin induced adaptive laboratory evolution of an industrial strain of saccharomyces cerevisiae reveals its potential to remodel lipid composition and heat tolerance
url https://doi.org/10.1111/1751-7915.13555
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