Adaptation to low pH and lignocellulosic inhibitors resulting in ethanolic fermentation and growth of Saccharomyces cerevisiae
Abstract
Here, lignocellulosic bioethanol from renewable feedstocks using Saccharomyces cerevisiae is a promising alternative to fossil fuels owing to environmental challenges. S. cerevisiae is frequently challenged by bacterial contamination and a combination of lignocellulosic inhibitors formed during the pre-treatment, in terms of growth, ethanol yield and productivity. We investigated the phenotypic robustness of a brewing yeast strain TMB3500 and its ability to adapt to low pH thereby preventing bacterial contamination along with lignocellulosic inhibitors by short-term adaptation and adaptive lab evolution (ALE). The short-term adaptation strategy was used to investigate the inherent ability of strain TMB3500 to activate a robust phenotype involving pre-culturing yeast cells in defined medium with lignocellulosic inhibitors at pH 5.0 until late exponential phase prior to inoculating them in defined media with the same inhibitor cocktail at pH 3.7. Adapted cells were able to grow aerobically, ferment anaerobically (glucose exhaustion by 19 +/- 5 h to yield 0.45 +/- 0.01 g ethanol g glucose-1) and portray significant detoxification of inhibitors at pH 3.7, when compared to non-adapted cells. ALE was performed to investigate whether a stable strain could be developed to grow and ferment at low pH with lignocellulosic inhibitors in a continuous suspension culture. Though amore »
- Authors:
-
- Lund Univ., Lund (Sweden)
- National Renewable Energy Lab. (NREL), Golden, CO (United States)
- Publication Date:
- Research Org.:
- National Renewable Energy Laboratory (NREL), Golden, CO (United States)
- Sponsoring Org.:
- Swedish National Energy Agency; USDOE
- OSTI Identifier:
- 1325063
- Report Number(s):
- NREL/JA-5100-67105
Journal ID: ISSN 2191-0855
- Grant/Contract Number:
- AC36-08GO28308
- Resource Type:
- Accepted Manuscript
- Journal Name:
- AMB Express
- Additional Journal Information:
- Journal Volume: 6; Journal Issue: 1; Journal ID: ISSN 2191-0855
- Publisher:
- Springer
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 09 BIOMASS FUELS; Saccharomyces cerevisiae; low pH; lignocellulosic inhibitors; phenotypic robustness; adaptation; ethanol yield
Citation Formats
Narayanan, Venkatachalam, Sànchez i Nogué, Violeta, van Niel, Ed W. J., and Gorwa-Grauslund, Marie F. Adaptation to low pH and lignocellulosic inhibitors resulting in ethanolic fermentation and growth of Saccharomyces cerevisiae. United States: N. p., 2016.
Web. doi:10.1186/s13568-016-0234-8.
Narayanan, Venkatachalam, Sànchez i Nogué, Violeta, van Niel, Ed W. J., & Gorwa-Grauslund, Marie F. Adaptation to low pH and lignocellulosic inhibitors resulting in ethanolic fermentation and growth of Saccharomyces cerevisiae. United States. https://doi.org/10.1186/s13568-016-0234-8
Narayanan, Venkatachalam, Sànchez i Nogué, Violeta, van Niel, Ed W. J., and Gorwa-Grauslund, Marie F. Fri .
"Adaptation to low pH and lignocellulosic inhibitors resulting in ethanolic fermentation and growth of Saccharomyces cerevisiae". United States. https://doi.org/10.1186/s13568-016-0234-8. https://www.osti.gov/servlets/purl/1325063.
@article{osti_1325063,
title = {Adaptation to low pH and lignocellulosic inhibitors resulting in ethanolic fermentation and growth of Saccharomyces cerevisiae},
author = {Narayanan, Venkatachalam and Sànchez i Nogué, Violeta and van Niel, Ed W. J. and Gorwa-Grauslund, Marie F.},
abstractNote = {Here, lignocellulosic bioethanol from renewable feedstocks using Saccharomyces cerevisiae is a promising alternative to fossil fuels owing to environmental challenges. S. cerevisiae is frequently challenged by bacterial contamination and a combination of lignocellulosic inhibitors formed during the pre-treatment, in terms of growth, ethanol yield and productivity. We investigated the phenotypic robustness of a brewing yeast strain TMB3500 and its ability to adapt to low pH thereby preventing bacterial contamination along with lignocellulosic inhibitors by short-term adaptation and adaptive lab evolution (ALE). The short-term adaptation strategy was used to investigate the inherent ability of strain TMB3500 to activate a robust phenotype involving pre-culturing yeast cells in defined medium with lignocellulosic inhibitors at pH 5.0 until late exponential phase prior to inoculating them in defined media with the same inhibitor cocktail at pH 3.7. Adapted cells were able to grow aerobically, ferment anaerobically (glucose exhaustion by 19 +/- 5 h to yield 0.45 +/- 0.01 g ethanol g glucose-1) and portray significant detoxification of inhibitors at pH 3.7, when compared to non-adapted cells. ALE was performed to investigate whether a stable strain could be developed to grow and ferment at low pH with lignocellulosic inhibitors in a continuous suspension culture. Though a robust population was obtained after 3600 h with an ability to grow and ferment at pH 3.7 with inhibitors, inhibitor robustness was not stable as indicated by the characterisation of the evolved culture possibly due to phenotypic plasticity. With further research, this short-term adaptation and low pH strategy could be successfully applied in lignocellulosic ethanol plants to prevent bacterial contamination.},
doi = {10.1186/s13568-016-0234-8},
journal = {AMB Express},
number = 1,
volume = 6,
place = {United States},
year = {Fri Aug 26 00:00:00 EDT 2016},
month = {Fri Aug 26 00:00:00 EDT 2016}
}
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Figures / Tables:
Fig. 1: Effect of low pH with 6 g L−1 acetic acid and individual inhibitors (1.5 g L−1 furfural or 0.5 g L−1 HMF or 1 g L−1 vanillin) on short‑term adapted (black) and non‑adapted (white) cells. pH 3.7 with inhibitors includes the IC
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Batch and continuous culture-based selection strategies for acetic acid tolerance in xylose-fermenting Saccharomyces cerevisiae
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- Almeida, João R. M.; Runquist, David; Sànchez Nogué, Violeta
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Variability of the response ofSaccharomyces cerevisiae strains to lignocellulose hydrolysate
journal, January 2008
- Modig, Tobias; Almeida, João R. M.; Gorwa-Grauslund, Marie F.
- Biotechnology and Bioengineering, Vol. 100, Issue 3
Evolutionary engineering of Saccharomyces cerevisiae for enhanced tolerance to hydrolysates of lignocellulosic biomass : Adaptive Evolution for Hydrolysates Tolerance in Yeast
journal, July 2013
- Almario, María P.; Reyes, Luis H.; Kao, Katy C.
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Reduction of invasive bacteria in ethanol fermentations using bacteriophages: Reduction of Invasive Bacteria Using Phages
journal, June 2015
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- Biotechnology and Bioengineering, Vol. 112, Issue 8
Differentiation of Brewery Yeast Strains by dna Fingerprinting
journal, March 1995
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Increased tolerance and conversion of inhibitors in lignocellulosic hydrolysates by Saccharomyces cerevisiae
journal, January 2007
- Almeida, Joao; Modig, Tobias; Petersson, Anneli
- Journal of Chemical Technology & Biotechnology, Vol. 82, Issue 4, p. 340-349
Effect of benzoic acid on metabolic fluxes in yeasts: A continuous-culture study on the regulation of respiration and alcoholic fermentation
journal, July 1992
- Verduyn, Cornelis; Postma, Erik; Scheffers, W. Alexander
- Yeast, Vol. 8, Issue 7
Ethanol Fermentation of Various Pretreated and Hydrolyzed Substrates at Low Initial pHááááá
book, January 2007
- Kadar, Zsofia; Maltha, San Feng; Szengyel, Zsolt
- Applied Biochemistry and Biotecnology
Inhibition of ethanol-producing yeast and bacteria by degradation products produced during pre-treatment of biomass
journal, August 2004
- Klinke, H. B.; Thomsen, A. B.; Ahring, B. K.
- Applied Microbiology and Biotechnology, Vol. 66, Issue 1, p. 10-26
Molecular mechanisms of yeast tolerance and in situ detoxification of lignocellulose hydrolysates
journal, March 2011
- Liu, Z. Lewis
- Applied Microbiology and Biotechnology, Vol. 90, Issue 3
Short-term adaptation improves the fermentation performance of Saccharomyces cerevisiae in the presence of acetic acid at low pH
journal, July 2013
- Sànchez i. Nogué, Violeta; Narayanan, Venkatachalam; Gorwa-Grauslund, Marie F.
- Applied Microbiology and Biotechnology, Vol. 97, Issue 16
Bacterial contaminants of fuel ethanol production
journal, August 2004
- Skinner, Kelly A.; Leathers, Timothy D.
- Journal of Industrial Microbiology & Biotechnology, Vol. 31, Issue 9
Effect of pH and lactic or acetic acid on ethanol productivity by Saccharomyces cerevisiae in corn mash
journal, February 2006
- Graves, Tara; Narendranath, Neelakantam V.; Dawson, Karl
- Journal of Industrial Microbiology & Biotechnology, Vol. 33, Issue 6
Yeast population dynamics of industrial fuel-ethanol fermentation process assessed by PCR-fingerprinting
journal, July 2005
- Silva-Filho, Eurípedes Alves da; Santos, Scheila Karina Brito dos; Resende, Alecsandra do Monte
- Antonie van Leeuwenhoek, Vol. 88, Issue 1
Ethanol fermentation of various pretreated and hydrolyzed substrates at low initial pH
journal, April 2007
- Kádár, Zsófia; Maltha, San Feng; Szengyel, Zsolt
- Applied Biochemistry and Biotechnology, Vol. 137-140, Issue 1-12
Screening of Saccharomyces cerevisiae strains with respect to anaerobic growth in non-detoxified lignocellulose hydrolysate
journal, July 2009
- Almeida, João R. M.; Karhumaa, Kaisa; Bengtsson, Oskar
- Bioresource Technology, Vol. 100, Issue 14
Inhibitor analysis and adaptive evolution of Saccharomyces cerevisiae for simultaneous saccharification and ethanol fermentation from industrial waste corncob residues
journal, April 2014
- Gu, Hanqi; Zhang, Jian; Bao, Jie
- Bioresource Technology, Vol. 157
Editorial overview: Energy biotechnology
journal, June 2015
- Papoutsakis, Eleftherios Terry; Pronk, Jack T.
- Current Opinion in Biotechnology, Vol. 33
DNA typing methods for differentiation of yeasts related to dry-cured meat products
journal, March 2006
- Andrade, M.; Rodriguez, M.; Sanchez, B.
- International Journal of Food Microbiology, Vol. 107, Issue 1
Importance of glucose-6-phosphate dehydrogenase (G6PDH) for vanillin tolerance in Saccharomyces cerevisiae
journal, September 2014
- Nguyen, Trinh Thi My; Kitajima, Sakihito; Izawa, Shingo
- Journal of Bioscience and Bioengineering, Vol. 118, Issue 3
Biofilm production by Zymomonas mobilis enhances ethanol production and tolerance to toxic inhibitors from rice bran hydrolysate
journal, September 2014
- Todhanakasem, Tatsaporn; Sangsutthiseree, Atit; Areerat, Kamonchanok
- New Biotechnology, Vol. 31, Issue 5
Antimicrobial strategies for limiting bacterial contaminants in fuel bioethanol fermentations
journal, June 2011
- Muthaiyan, Arunachalam; Limayem, Alya; Ricke, Steven C.
- Progress in Energy and Combustion Science, Vol. 37, Issue 3
Stochastic switching as a survival strategy in fluctuating environments
journal, March 2008
- Acar, Murat; Mettetal, Jerome T.; van Oudenaarden, Alexander
- Nature Genetics, Vol. 40, Issue 4
Microbial cell individuality and the underlying sources of heterogeneity
journal, August 2006
- Avery, Simon V.
- Nature Reviews Microbiology, Vol. 4, Issue 8
Low external pH induces HOG1-dependent changes in the organization of the Saccharomyces cerevisiae cell wall
journal, January 2001
- Kapteyn, J. C.; ter Riet, B.; Vink, E.
- Molecular Microbiology, Vol. 39, Issue 2
Metabolomic Study of Interactive Effects of Phenol, Furfural, and Acetic Acid on Saccharomyces cerevisiae
journal, October 2011
- Ding, Ming-Zhu; Wang, Xin; Yang, Yang
- OMICS: A Journal of Integrative Biology, Vol. 15, Issue 10
DNA diversity among clinical isolates of Helicobacter pylori detected by PCR-based RAPD fingerprinting
journal, January 1992
- Akopyanz, Natalia; Bukanov, Nickolai O.; Westblom, T. Ulf
- Nucleic Acids Research, Vol. 20, Issue 19
Physiology of the fuel ethanol strain Saccharomyces cerevisiae PE-2 at low pH indicates a context-dependent performance relevant for industrial applications
journal, October 2014
- Della-Bianca, Bianca E.; de Hulster, Erik; Pronk, Jack T.
- FEMS Yeast Research, Vol. 14, Issue 8
Physiological and molecular analysis of the stress response of Saccharomyces cerevisiae imposed by strong inorganic acid with implication to industrial fermentations: Inorganic acid tolerance in yeast
journal, December 2009
- De Melo, H. F.; Bonini, B. M.; Thevelein, J.
- Journal of Applied Microbiology
Flocculation, adhesion and biofilm formation in yeasts
journal, April 2006
- Verstrepen, Kevin J.; Klis, Frans M.
- Molecular Microbiology, Vol. 60, Issue 1
Adaptation of Microorganisms to Cold Temperatures, Weak Acid Preservatives, Low pH, and Osmotic Stress: A Review
journal, January 2004
- Beales, N.
- Comprehensive Reviews in Food Science and Food Safety, Vol. 3, Issue 1
Yeast genes involved in response to lactic acid and acetic acid: acidic conditions caused by the organic acids in Saccharomyces cerevisiae cultures induce expression of intracellular metal metabolism genes regulated by Aft1p
journal, September 2006
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Works referencing / citing this record:
Overcoming lignocellulose‐derived microbial inhibitors: advancing the Saccharomyces cerevisiae resistance toolbox
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