Cargando…

Furfural induces reactive oxygen species accumulation and cellular damage in Saccharomyces cerevisiae

BACKGROUND: Biofuels offer a viable alternative to petroleum-based fuel. However, current methods are not sufficient and the technology required in order to use lignocellulosic biomass as a fermentation substrate faces several challenges. One challenge is the need for a robust fermentative microorga...

Descripción completa

Detalles Bibliográficos
Autores principales: Allen, Sandra A, Clark, William, McCaffery, J Michael, Cai, Zhen, Lanctot, Alison, Slininger, Patricia J, Liu, Z Lewis, Gorsich, Steven W
Formato: Texto
Lenguaje:English
Publicado: BioMed Central 2010
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2820483/
https://www.ncbi.nlm.nih.gov/pubmed/20150993
http://dx.doi.org/10.1186/1754-6834-3-2
_version_ 1782177379471327232
author Allen, Sandra A
Clark, William
McCaffery, J Michael
Cai, Zhen
Lanctot, Alison
Slininger, Patricia J
Liu, Z Lewis
Gorsich, Steven W
author_facet Allen, Sandra A
Clark, William
McCaffery, J Michael
Cai, Zhen
Lanctot, Alison
Slininger, Patricia J
Liu, Z Lewis
Gorsich, Steven W
author_sort Allen, Sandra A
collection PubMed
description BACKGROUND: Biofuels offer a viable alternative to petroleum-based fuel. However, current methods are not sufficient and the technology required in order to use lignocellulosic biomass as a fermentation substrate faces several challenges. One challenge is the need for a robust fermentative microorganism that can tolerate the inhibitors present during lignocellulosic fermentation. These inhibitors include the furan aldehyde, furfural, which is released as a byproduct of pentose dehydration during the weak acid pretreatment of lignocellulose. In order to survive in the presence of furfural, yeast cells need not only to reduce furfural to the less toxic furan methanol, but also to protect themselves and repair any damage caused by the furfural. Since furfural tolerance in yeast requires a functional pentose phosphate pathway (PPP), and the PPP is associated with reactive oxygen species (ROS) tolerance, we decided to investigate whether or not furfural induces ROS and its related cellular damage in yeast. RESULTS: We demonstrated that furfural induces the accumulation of ROS in Saccharomyces cerevisiae. In addition, furfural was shown to cause cellular damage that is consistent with ROS accumulation in cells which includes damage to mitochondria and vacuole membranes, the actin cytoskeleton and nuclear chromatin. The furfural-induced damage is less severe when yeast are grown in a furfural concentration (25 mM) that allows for eventual growth after an extended lag compared to a concentration of furfural (50 mM) that prevents growth. CONCLUSION: These data suggest that when yeast cells encounter the inhibitor furfural, they not only need to reduce furfural into furan methanol but also to protect themselves from the cellular effects of furfural and repair any damage caused. The reduced cellular damage seen at 25 mM furfural compared to 50 mM furfural may be linked to the observation that at 25 mM furfural yeast were able to exit the furfural-induced lag phase and resume growth. Understanding the cellular effects of furfural will help direct future strain development to engineer strains capable of tolerating or remediating ROS and the effects of ROS.
format Text
id pubmed-2820483
institution National Center for Biotechnology Information
language English
publishDate 2010
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-28204832010-02-12 Furfural induces reactive oxygen species accumulation and cellular damage in Saccharomyces cerevisiae Allen, Sandra A Clark, William McCaffery, J Michael Cai, Zhen Lanctot, Alison Slininger, Patricia J Liu, Z Lewis Gorsich, Steven W Biotechnol Biofuels Research BACKGROUND: Biofuels offer a viable alternative to petroleum-based fuel. However, current methods are not sufficient and the technology required in order to use lignocellulosic biomass as a fermentation substrate faces several challenges. One challenge is the need for a robust fermentative microorganism that can tolerate the inhibitors present during lignocellulosic fermentation. These inhibitors include the furan aldehyde, furfural, which is released as a byproduct of pentose dehydration during the weak acid pretreatment of lignocellulose. In order to survive in the presence of furfural, yeast cells need not only to reduce furfural to the less toxic furan methanol, but also to protect themselves and repair any damage caused by the furfural. Since furfural tolerance in yeast requires a functional pentose phosphate pathway (PPP), and the PPP is associated with reactive oxygen species (ROS) tolerance, we decided to investigate whether or not furfural induces ROS and its related cellular damage in yeast. RESULTS: We demonstrated that furfural induces the accumulation of ROS in Saccharomyces cerevisiae. In addition, furfural was shown to cause cellular damage that is consistent with ROS accumulation in cells which includes damage to mitochondria and vacuole membranes, the actin cytoskeleton and nuclear chromatin. The furfural-induced damage is less severe when yeast are grown in a furfural concentration (25 mM) that allows for eventual growth after an extended lag compared to a concentration of furfural (50 mM) that prevents growth. CONCLUSION: These data suggest that when yeast cells encounter the inhibitor furfural, they not only need to reduce furfural into furan methanol but also to protect themselves from the cellular effects of furfural and repair any damage caused. The reduced cellular damage seen at 25 mM furfural compared to 50 mM furfural may be linked to the observation that at 25 mM furfural yeast were able to exit the furfural-induced lag phase and resume growth. Understanding the cellular effects of furfural will help direct future strain development to engineer strains capable of tolerating or remediating ROS and the effects of ROS. BioMed Central 2010-01-15 /pmc/articles/PMC2820483/ /pubmed/20150993 http://dx.doi.org/10.1186/1754-6834-3-2 Text en Copyright ©2010 Allen et al; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research
Allen, Sandra A
Clark, William
McCaffery, J Michael
Cai, Zhen
Lanctot, Alison
Slininger, Patricia J
Liu, Z Lewis
Gorsich, Steven W
Furfural induces reactive oxygen species accumulation and cellular damage in Saccharomyces cerevisiae
title Furfural induces reactive oxygen species accumulation and cellular damage in Saccharomyces cerevisiae
title_full Furfural induces reactive oxygen species accumulation and cellular damage in Saccharomyces cerevisiae
title_fullStr Furfural induces reactive oxygen species accumulation and cellular damage in Saccharomyces cerevisiae
title_full_unstemmed Furfural induces reactive oxygen species accumulation and cellular damage in Saccharomyces cerevisiae
title_short Furfural induces reactive oxygen species accumulation and cellular damage in Saccharomyces cerevisiae
title_sort furfural induces reactive oxygen species accumulation and cellular damage in saccharomyces cerevisiae
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2820483/
https://www.ncbi.nlm.nih.gov/pubmed/20150993
http://dx.doi.org/10.1186/1754-6834-3-2
work_keys_str_mv AT allensandraa furfuralinducesreactiveoxygenspeciesaccumulationandcellulardamageinsaccharomycescerevisiae
AT clarkwilliam furfuralinducesreactiveoxygenspeciesaccumulationandcellulardamageinsaccharomycescerevisiae
AT mccafferyjmichael furfuralinducesreactiveoxygenspeciesaccumulationandcellulardamageinsaccharomycescerevisiae
AT caizhen furfuralinducesreactiveoxygenspeciesaccumulationandcellulardamageinsaccharomycescerevisiae
AT lanctotalison furfuralinducesreactiveoxygenspeciesaccumulationandcellulardamageinsaccharomycescerevisiae
AT sliningerpatriciaj furfuralinducesreactiveoxygenspeciesaccumulationandcellulardamageinsaccharomycescerevisiae
AT liuzlewis furfuralinducesreactiveoxygenspeciesaccumulationandcellulardamageinsaccharomycescerevisiae
AT gorsichstevenw furfuralinducesreactiveoxygenspeciesaccumulationandcellulardamageinsaccharomycescerevisiae