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Title: Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production

Abstract

Here, lignocellulosic biomass is a common resource across the globe, and its fermentation offers a promising option for generating renewable liquid transportation fuels. The deconstruction of lignocellulosic biomass releases sugars that can be fermented by microbes, but these processes also produce fermentation inhibitors, such as aromatic acids and aldehydes. Several research projects have investigated lignocellulosic biomass fermentation by the baker’s yeast Saccharomyces cerevisiae. Most projects have taken synthetic biological approaches or have explored naturally occurring diversity in S. cerevisiae to enhance stress tolerance, xylose consumption, or ethanol production. Despite these efforts, improved strains with new properties are needed. In other industrial processes, such as wine and beer fermentation, interspecies hybrids have combined important traits from multiple species, suggesting that interspecies hybridization may also offer potential for biofuel research.

Authors:
ORCiD logo [1];  [1];  [1];  [1];  [1];  [1];  [1];  [2];  [3];  [4];  [5];  [6];  [6];  [7];  [7];  [8];  [8];  [1]; ORCiD logo [1]
  1. Univ. of Wisconsin, Madison, WI (United States)
  2. Centro Regional Univ. Bariloche, Rio Negro (Argentina)
  3. Univ. of Wisconsin, Madison, WI (United States); Chinese Academy of Sciences, Beijing (China)
  4. Chinese Academy of Sciences, Beijing (China)
  5. Univ. de Montreal, Montreal, QC (Canada); Univ. Laval, Quebec City, QC (Canada)
  6. Univ. Laval, Quebec City, QC (Canada)
  7. Univ. Nova de Lisboa, Caparica (Portugal)
  8. Washington Univ., St. Louis, MO (United States)
Publication Date:
Research Org.:
Univ. of Wisconsin, Madison, WI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1361200
Grant/Contract Number:  
FC02-07ER64494
Resource Type:
Accepted Manuscript
Journal Name:
Biotechnology for Biofuels
Additional Journal Information:
Journal Volume: 10; Journal Issue: 1; Journal ID: ISSN 1754-6834
Publisher:
BioMed Central
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; 60 APPLIED LIFE SCIENCES; Saccharomyces; biodiversity; ammonia fiber expansion (AFEX); AFEX-pretreated corn stover hydrolysate (ACSH); hybridization; bioethanol; xylose; hydrolysate toxins

Citation Formats

Peris, David, Moriarty, Ryan V., Alexander, William G., Baker, EmilyClare, Sylvester, Kayla, Sardi, Maria, Langdon, Quinn K., Libkind, Diego, Wang, Qi -Ming, Bai, Feng -Yan, Leducq, Jean-Baptiste, Charron, Guillaume, Landry, Christian R., Sampaio, José Paulo, Gonçalves, Paula, Hyma, Katie E., Fay, Justin C., Sato, Trey K., and Hittinger, Chris Todd. Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production. United States: N. p., 2017. Web. doi:10.1186/s13068-017-0763-7.
Peris, David, Moriarty, Ryan V., Alexander, William G., Baker, EmilyClare, Sylvester, Kayla, Sardi, Maria, Langdon, Quinn K., Libkind, Diego, Wang, Qi -Ming, Bai, Feng -Yan, Leducq, Jean-Baptiste, Charron, Guillaume, Landry, Christian R., Sampaio, José Paulo, Gonçalves, Paula, Hyma, Katie E., Fay, Justin C., Sato, Trey K., & Hittinger, Chris Todd. Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production. United States. doi:10.1186/s13068-017-0763-7.
Peris, David, Moriarty, Ryan V., Alexander, William G., Baker, EmilyClare, Sylvester, Kayla, Sardi, Maria, Langdon, Quinn K., Libkind, Diego, Wang, Qi -Ming, Bai, Feng -Yan, Leducq, Jean-Baptiste, Charron, Guillaume, Landry, Christian R., Sampaio, José Paulo, Gonçalves, Paula, Hyma, Katie E., Fay, Justin C., Sato, Trey K., and Hittinger, Chris Todd. Mon . "Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production". United States. doi:10.1186/s13068-017-0763-7. https://www.osti.gov/servlets/purl/1361200.
@article{osti_1361200,
title = {Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production},
author = {Peris, David and Moriarty, Ryan V. and Alexander, William G. and Baker, EmilyClare and Sylvester, Kayla and Sardi, Maria and Langdon, Quinn K. and Libkind, Diego and Wang, Qi -Ming and Bai, Feng -Yan and Leducq, Jean-Baptiste and Charron, Guillaume and Landry, Christian R. and Sampaio, José Paulo and Gonçalves, Paula and Hyma, Katie E. and Fay, Justin C. and Sato, Trey K. and Hittinger, Chris Todd},
abstractNote = {Here, lignocellulosic biomass is a common resource across the globe, and its fermentation offers a promising option for generating renewable liquid transportation fuels. The deconstruction of lignocellulosic biomass releases sugars that can be fermented by microbes, but these processes also produce fermentation inhibitors, such as aromatic acids and aldehydes. Several research projects have investigated lignocellulosic biomass fermentation by the baker’s yeast Saccharomyces cerevisiae. Most projects have taken synthetic biological approaches or have explored naturally occurring diversity in S. cerevisiae to enhance stress tolerance, xylose consumption, or ethanol production. Despite these efforts, improved strains with new properties are needed. In other industrial processes, such as wine and beer fermentation, interspecies hybrids have combined important traits from multiple species, suggesting that interspecies hybridization may also offer potential for biofuel research.},
doi = {10.1186/s13068-017-0763-7},
journal = {Biotechnology for Biofuels},
number = 1,
volume = 10,
place = {United States},
year = {2017},
month = {3}
}

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Works referenced in this record:

Energetics of the effect of acetic acid on growth of Saccharomyces cerevisiae
journal, March 2000


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
  • DOI: 10.1007/s00253-004-1642-2

Evaluation of ammonia fibre expansion (AFEX) pretreatment for enzymatic hydrolysis of switchgrass harvested in different seasons and locations
journal, January 2010

  • Bals, Bryan; Rogers, Chad; Jin, Mingjie
  • Biotechnology for Biofuels, Vol. 3, Issue 1
  • DOI: 10.1186/1754-6834-3-1

Exploring the northern limit of the distribution of Saccharomyces cerevisiae and Saccharomyces paradoxus in North America
journal, October 2013

  • Charron, Guillaume; Leducq, Jean-Baptiste; Bertin, Chloé
  • FEMS Yeast Research, Vol. 14, Issue 2
  • DOI: 10.1111/1567-1364.12100

Trimmomatic: a flexible trimmer for Illumina sequence data
journal, April 2014


Analysis of the constitution of the beer yeast genome by PCR, sequencing and subtelomeric sequence hybridization.
journal, July 2001

  • Casaregola, S.; Kotyk, A.; Nguyen, H. V.
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 51, Issue 4
  • DOI: 10.1099/00207713-51-4-1607

Fuelling the future: microbial engineering for the production of sustainable biofuels
journal, March 2016

  • Liao, James C.; Mi, Luo; Pontrelli, Sammy
  • Nature Reviews Microbiology, Vol. 14, Issue 5
  • DOI: 10.1038/nrmicro.2016.32

Phenotypic characterisation of Saccharomyces spp. yeast for tolerance to stresses encountered during fermentation of lignocellulosic residues to produce bioethanol
journal, January 2014

  • Wimalasena, Tithira T.; Greetham, Darren; Marvin, Marcus E.
  • Microbial Cell Factories, Vol. 13, Issue 1
  • DOI: 10.1186/1475-2859-13-47

Remarkably ancient balanced polymorphisms in a multi-locus gene network
journal, February 2010

  • Hittinger, Chris Todd; Gonçalves, Paula; Sampaio, José Paulo
  • Nature, Vol. 464, Issue 7285
  • DOI: 10.1038/nature08791

Complex Ancestries of Lager-Brewing Hybrids Were Shaped by Standing Variation in the Wild Yeast Saccharomyces eubayanus
journal, July 2016


Population genomics of domestic and wild yeasts
journal, February 2009

  • Liti, Gianni; Carter, David M.; Moses, Alan M.
  • Nature, Vol. 458, Issue 7236
  • DOI: 10.1038/nature07743

Combining inhibitor tolerance and D-xylose fermentation in industrial Saccharomyces cerevisiae for efficient lignocellulose-based bioethanol production
journal, January 2013

  • Demeke, Mekonnen M.; Dumortier, Françoise; Li, Yingying
  • Biotechnology for Biofuels, Vol. 6, Issue 1
  • DOI: 10.1186/1754-6834-6-120

Comparative genomics of xylose-fermenting fungi for enhanced biofuel production
journal, July 2011

  • Wohlbach, D. J.; Kuo, A.; Sato, T. K.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 32, p. 13212-13217
  • DOI: 10.1073/pnas.1103039108

High quality de novo sequencing and assembly of the Saccharomyces arboricolus genome
journal, January 2013


SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing
journal, May 2012

  • Bankevich, Anton; Nurk, Sergey; Antipov, Dmitry
  • Journal of Computational Biology, Vol. 19, Issue 5
  • DOI: 10.1089/cmb.2012.0021

S. cerevisiae × S. eubayanus interspecific hybrid, the best of both worlds and beyond
journal, March 2015

  • Hebly, Marit; Brickwedde, Anja; Bolat, Irina
  • FEMS Yeast Research, Vol. 15, Issue 3
  • DOI: 10.1093/femsyr/fov005

Characterization of natural hybrids of Saccharomyces cerevisiae and Saccharomyces bayanus var. uvarum
journal, June 2007


The Awesome Power of Yeast Evolutionary Genetics: New Genome Sequences and Strain Resources for the Saccharomyces sensu stricto Genus
journal, June 2011

  • Scannell, Devin R.; Zill, Oliver A.; Rokas, Antonis
  • G3: Genes|Genomes|Genetics, Vol. 1, Issue 1
  • DOI: 10.1534/g3.111.000273

Effects of deletion of glycerol-3-phosphate dehydrogenase and glutamate dehydrogenase genes on glycerol and ethanol metabolism in recombinant Saccharomyces cerevisiae
journal, September 2011

  • Kim, Jin-Woo; Chin, Young-Wook; Park, Yong-Cheol
  • Bioprocess and Biosystems Engineering, Vol. 35, Issue 1-2
  • DOI: 10.1007/s00449-011-0590-3

Temperature and host preferences drive the diversification of Saccharomyces and other yeasts: a survey and the discovery of eight new yeast species
journal, March 2015

  • Sylvester, Kayla; Wang, Qi-Ming; James, Brielle
  • FEMS Yeast Research, Vol. 15, Issue 3
  • DOI: 10.1093/femsyr/fov002

The Genome Sequence of Saccharomyces eubayanus and the Domestication of Lager-Brewing Yeasts
journal, August 2015

  • Baker, EmilyClare; Wang, Bing; Bellora, Nicolas
  • Molecular Biology and Evolution, Vol. 32, Issue 11
  • DOI: 10.1093/molbev/msv168

Impact of Chromatin Structures on DNA Processing for Genomic Analyses
journal, August 2009


Rapid Evolution of Recombinant Saccharomyces cerevisiae for Xylose Fermentation through Formation of Extra-chromosomal Circular DNA
journal, March 2015


On the Complexity of the Saccharomyces bayanus Taxon: Hybridization and Potential Hybrid Speciation
journal, April 2014


Fermentative stress adaptation of hybrids within the Saccharomyces sensu stricto complex
journal, February 2008


A simple method of preparing plant samples for PCR
journal, January 1993

  • Wang, Hong; Qi, Meiqing; Cutler, Adrian J.
  • Nucleic Acids Research, Vol. 21, Issue 17
  • DOI: 10.1093/nar/21.17.4153

Genome Sequence and Analysis of a Stress-Tolerant, Wild-Derived Strain of Saccharomyces cerevisiae Used in Biofuels Research
journal, April 2016

  • McIlwain, Sean J.; Peris, David; Sardi, Maria
  • G3: Genes|Genomes|Genetics, Vol. 6, Issue 6
  • DOI: 10.1534/g3.116.029389

Death by a thousand cuts: the challenges and diverse landscape of lignocellulosic hydrolysate inhibitors
journal, March 2014


Harnessing Genetic Diversity in Saccharomyces cerevisiae for Fermentation of Xylose in Hydrolysates of Alkaline Hydrogen Peroxide-Pretreated Biomass
journal, November 2013

  • Sato, Trey K.; Liu, Tongjun; Parreiras, Lucas S.
  • Applied and Environmental Microbiology, Vol. 80, Issue 2
  • DOI: 10.1128/AEM.01885-13

Cellulosic ethanol production from AFEX-treated corn stover using Saccharomyces cerevisiae 424A(LNH-ST)
journal, January 2009

  • Lau, M. W.; Dale, B. E.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 5, p. 1368-1373
  • DOI: 10.1073/pnas.0812364106

Engineering yeasts for xylose metabolism
journal, June 2006


Population structure and reticulate evolution of Saccharomyces eubayanus and its lager-brewing hybrids
journal, April 2014

  • Peris, David; Sylvester, Kayla; Libkind, Diego
  • Molecular Ecology, Vol. 23, Issue 8
  • DOI: 10.1111/mec.12702

Evolutionary Role of Interspecies Hybridization and Genetic Exchanges in Yeasts
journal, November 2012

  • Morales, Lucia; Dujon, Bernard
  • Microbiology and Molecular Biology Reviews, Vol. 76, Issue 4
  • DOI: 10.1128/MMBR.00022-12

Identification of multiple interacting alleles conferring low glycerol and high ethanol yield in Saccharomyces cerevisiae ethanolic fermentation
journal, January 2013

  • Hubmann, Georg; Mathé, Lotte; Foulquié-Moreno, Maria R.
  • Biotechnology for Biofuels, Vol. 6, Issue 1
  • DOI: 10.1186/1754-6834-6-87

Engineering Cellular Metabolism
journal, March 2016


Local climatic adaptation in a widespread microorganism
journal, February 2014

  • Leducq, Jean-Baptiste; Charron, Guillaume; Samani, Pedram
  • Proceedings of the Royal Society B: Biological Sciences, Vol. 281, Issue 1777
  • DOI: 10.1098/rspb.2013.2472

Efficient engineering of marker-free synthetic allotetraploids of Saccharomyces
journal, April 2016

  • Alexander, William G.; Peris, David; Pfannenstiel, Brandon T.
  • Fungal Genetics and Biology, Vol. 89
  • DOI: 10.1016/j.fgb.2015.11.002

Crosses between Saccharomyces cerevisiae and Saccharomyces bayanus generate fertile hybrids
journal, January 2002


Temperature Adaptation Markedly Determines Evolution within the Genus Saccharomyces
journal, February 2011

  • Salvadó, Z.; Arroyo-López, F. N.; Guillamón, J. M.
  • Applied and Environmental Microbiology, Vol. 77, Issue 7
  • DOI: 10.1128/AEM.01861-10

Fermentation of lignocellulosic hydrolysates for ethanol production
journal, April 1996


Chimeric Genomes of Natural Hybrids of Saccharomyces cerevisiae and Saccharomyces kudriavzevii
journal, February 2009

  • Belloch, C.; Perez-Torrado, R.; Gonzalez, S. S.
  • Applied and Environmental Microbiology, Vol. 75, Issue 8
  • DOI: 10.1128/AEM.02282-08

Polyploidy can drive rapid adaptation in yeast
journal, March 2015

  • Selmecki, Anna M.; Maruvka, Yosef E.; Richmond, Phillip A.
  • Nature, Vol. 519, Issue 7543
  • DOI: 10.1038/nature14187

Mitochondrial introgression suggests extensive ancestral hybridization events among Saccharomyces species
journal, March 2017


Phenotypic selection of a wild Saccharomyces cerevisiae strain for simultaneous saccharification and co-fermentation of AFEX™ pretreated corn stover
journal, January 2013

  • Jin, Mingjie; Sarks, Cory; Gunawan, Christa
  • Biotechnology for Biofuels, Vol. 6, Issue 1
  • DOI: 10.1186/1754-6834-6-108

Bulk Segregant Analysis by High-Throughput Sequencing Reveals a Novel Xylose Utilization Gene from Saccharomyces cerevisiae
journal, May 2010


New Hybrids between Saccharomyces Sensu Stricto Yeast Species Found among Wine and Cider Production Strains
journal, October 1998


Reconstruction of the genome origins and evolution of the hybrid lager yeast Saccharomyces pastorianus
journal, August 2008


Sugar beet waste and its component ferulic acid inhibits external mycelium of arbuscular mycorrhizal fungus
journal, July 2011


Genome Sequence of the Lager Brewing Yeast, an Interspecies Hybrid
journal, January 2009


Comparative Genomics of Saccharomyces cerevisiae Natural Isolates for Bioenergy Production
journal, September 2014

  • Wohlbach, Dana J.; Rovinskiy, Nikolay; Lewis, Jeffrey A.
  • Genome Biology and Evolution, Vol. 6, Issue 9
  • DOI: 10.1093/gbe/evu199

Natural Populations of Saccharomyces kudriavzevii in Portugal Are Associated with Oak Bark and Are Sympatric with S. cerevisiae and S. paradoxus
journal, February 2008

  • Sampaio, J. P.; Goncalves, P.
  • Applied and Environmental Microbiology, Vol. 74, Issue 7
  • DOI: 10.1128/AEM.02396-07

A Yeast Hybrid Provides Insight into the Evolution of Gene Expression Regulation
journal, April 2009


Physiological and genomic characterisation of Saccharomyces cerevisiae hybrids with improved fermentation performance and mannoprotein release capacity
journal, July 2015


Modeling Microbial Growth Curves with GCAT
journal, February 2015


Multiplexed Engineering in Biology
journal, March 2016


Saccharomyces diversity and evolution: a budding model genus
journal, May 2013


A Gondwanan imprint on global diversity and domestication of wine and cider yeast Saccharomyces uvarum
journal, June 2014

  • Almeida, Pedro; Gonçalves, Carla; Teixeira, Sara
  • Nature Communications, Vol. 5, Issue 1
  • DOI: 10.1038/ncomms5044

Gradual genome stabilisation by progressive reduction of the genome in an interspecific hybrid with
journal, December 2005


Phenolic Amides Are Potent Inhibitors of De Novo Nucleotide Biosynthesis
journal, June 2015

  • Pisithkul, Tippapha; Jacobson, Tyler B.; O'Brien, Thomas J.
  • Applied and Environmental Microbiology, Vol. 81, Issue 17
  • DOI: 10.1128/AEM.01324-15

In Silico Whole Genome Sequencer and Analyzer (iWGS): a Computational Pipeline to Guide the Design and Analysis of de novo Genome Sequencing Studies
journal, September 2016

  • Zhou, Xiaofan; Peris, David; Kominek, Jacek
  • G3: Genes|Genomes|Genetics, Vol. 6, Issue 11
  • DOI: 10.1534/g3.116.034249

An overview of second generation biofuel technologies
journal, March 2010


Interspecies hybridization and recombination in Saccharomyces wine yeasts
journal, November 2008


Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast
journal, August 2011

  • Libkind, D.; Hittinger, C. T.; Valerio, E.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 35
  • DOI: 10.1073/pnas.1105430108

Evidence for multiple interspecific hybridization in Saccharomyces sensu stricto species
journal, January 2002


Complex Physiology and Compound Stress Responses during Fermentation of Alkali-Pretreated Corn Stover Hydrolysate by an Escherichia coli Ethanologen
journal, March 2012

  • Schwalbach, Michael S.; Keating, David H.; Tremaine, Mary
  • Applied and Environmental Microbiology, Vol. 78, Issue 9, p. 3442-3457
  • DOI: 10.1128/AEM.07329-11

Phylogeny of the genus Kluyveromyces inferred from the mitochondrial cytochrome-c oxidase II gene
journal, January 2000

  • Belloch, C.; Querol, A.; Garcia, M. D.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 50, Issue 1
  • DOI: 10.1099/00207713-50-1-405

Engineered Saccharomyces cerevisiae capable of simultaneous cellobiose and xylose fermentation
journal, December 2010

  • Ha, S. -J.; Galazka, J. M.; Rin Kim, S.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 2
  • DOI: 10.1073/pnas.1010456108

Molecular Characterization of New Natural Hybrids of Saccharomyces cerevisiae and S. kudriavzevii in Brewing
journal, February 2008

  • Gonzalez, S. S.; Barrio, E.; Querol, A.
  • Applied and Environmental Microbiology, Vol. 74, Issue 8
  • DOI: 10.1128/AEM.01867-07

Yeasts illustrate the molecular mechanisms of eukaryotic genome evolution
journal, July 2006


Speciation driven by hybridization and chromosomal plasticity in a wild yeast
journal, January 2016

  • Leducq, Jean-Baptiste; Nielly-Thibault, Lou; Charron, Guillaume
  • Nature Microbiology, Vol. 1, Issue 1
  • DOI: 10.1038/nmicrobiol.2015.3

High-Efficiency Genome Editing and Allele Replacement in Prototrophic and Wild Strains of Saccharomyces
journal, September 2014


Comparative functional genomics to reveal the molecular basis of phenotypic diversities and guide the genetic breeding of industrial yeast strains
journal, January 2013

  • Zheng, Dao-Qiong; Liu, Tian-Zhe; Chen, Jie
  • Applied Microbiology and Biotechnology, Vol. 97, Issue 5
  • DOI: 10.1007/s00253-013-4698-z

Reconstruction of the Evolutionary History of Saccharomyces cerevisiae x S. kudriavzevii Hybrids Based on Multilocus Sequence Analysis
journal, September 2012


Allopatric Divergence, Secondary Contact, and Genetic Isolation in Wild Yeast Populations
journal, March 2007


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