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

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

doi:10.1186/s13068-017-0763-7

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

Journal Article · Mon Mar 27 00:00:00 EDT 2017 · Biotechnology for Biofuels

DOI:https://doi.org/10.1186/s13068-017-0763-7· OSTI ID:1361200

^[1]; Moriarty, Ryan V. ^[1]; Alexander, William G. ^[1]; Baker, EmilyClare ^[1]; Sylvester, Kayla ^[1]; Sardi, Maria ^[1]; Langdon, Quinn K. ^[1]; Libkind, Diego ^[2]; Wang, Qi -Ming ^[3]; Bai, Feng -Yan ^[4]; Leducq, Jean-Baptiste ^[5]; Charron, Guillaume ^[6]; Landry, Christian R. ^[6]; Sampaio, José Paulo ^[7]; Gonçalves, Paula ^[7]; Hyma, Katie E. ^[8]; Fay, Justin C. ^[8]; Sato, Trey K. ^[1];

^[1]

Univ. of Wisconsin, Madison, WI (United States)
Centro Regional Univ. Bariloche, Rio Negro (Argentina)
Univ. of Wisconsin, Madison, WI (United States); Chinese Academy of Sciences, Beijing (China)
Chinese Academy of Sciences, Beijing (China)
Univ. de Montreal, Montreal, QC (Canada); Univ. Laval, Quebec City, QC (Canada)
Univ. Laval, Quebec City, QC (Canada)
Univ. Nova de Lisboa, Caparica (Portugal)
Washington Univ., St. Louis, MO (United States)

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.

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Research Organization:: Univ. of Wisconsin, Madison, WI (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: FC02-07ER64494

OSTI ID:: 1361200

Journal Information:: Biotechnology for Biofuels, Vol. 10, Issue 1; ISSN 1754-6834

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 50 works

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Complex Physiology and Compound Stress Responses during Fermentation of Alkali-Pretreated Corn Stover Hydrolysate by an Escherichia coli Ethanologen Schwalbach, Michael S.; Keating, David H.; Tremaine, Mary Applied and Environmental Microbiology, Vol. 78, Issue 9, p. 3442-3457 https://doi.org/10.1128/aem.07329-11	journal	March 2012
Evolutionary Role of Interspecies Hybridization and Genetic Exchanges in Yeasts Morales, Lucia; Dujon, Bernard Microbiology and Molecular Biology Reviews, Vol. 76, Issue 4 https://doi.org/10.1128/mmbr.00022-12	journal	November 2012

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In vivo recombination of Saccharomyces eubayanus maltose-transporter genes yields a chimeric transporter that enables maltotriose fermentation Brouwers, Nick; Gorter de Vries, Arthur R.; van den Broek, Marcel PLOS Genetics, Vol. 15, Issue 4 https://doi.org/10.1371/journal.pgen.1007853	journal	April 2019
Microbial Experimental Evolution – a proving ground for evolutionary theory and a tool for discovery McDonald, Michael J. EMBO reports, Vol. 20, Issue 8 https://doi.org/10.15252/embr.201846992	journal	July 2019
Bioethanol fermentation from kitchen waste using Saccharomyces cerevisiae Rahman, Shafkat Shamim; Hossain, Md. Mahboob; Choudhury, Naiyyum F1000Research, Vol. 7 https://doi.org/10.12688/f1000research.14594.1	journal	January 2018
sppIDer: A Species Identification Tool to Investigate Hybrid Genomes with High-Throughput Sequencing Langdon, Quinn K.; Peris, David; Kyle, Brian Molecular Biology and Evolution https://doi.org/10.1093/molbev/msy166	journal	September 2018
Adaptive evolution of Aspergillus oryzae 3.042 strain and process optimization to reduce the formation of tyrosine crystals in broad bean paste: XXXX Niu, Chengtuo; Min, Shihao; Jia, Yun Journal of Food Biochemistry, Vol. 43, Issue 2 https://doi.org/10.1111/jfbc.12716	journal	November 2018
New yeasts—new brews: modern approaches to brewing yeast design and development Gibson, B.; Geertman, J. -M. A.; Hittinger, C. T. FEMS Yeast Research, Vol. 17, Issue 4 https://doi.org/10.1093/femsyr/fox038	journal	June 2017
Fermentation innovation through complex hybridization of wild and domesticated yeasts Langdon, Quinn K.; Peris, David; Baker, EmilyClare P. Nature Ecology & Evolution, Vol. 3, Issue 11 https://doi.org/10.1038/s41559-019-0998-8	journal	October 2019
Lager-brewing yeasts in the era of modern genetics Gorter de Vries, Arthur R.; Pronk, Jack T.; Daran, Jean-Marc G. FEMS Yeast Research, Vol. 19, Issue 7 https://doi.org/10.1093/femsyr/foz063	journal	September 2019
The renaissance of yeasts as microbial factories in the modern age of biomanufacturing Payen, Celia; Thompson, Dawn Yeast, Vol. 36, Issue 12 https://doi.org/10.1002/yea.3439	journal	September 2019
Bioethanol production using vegetable peels medium and the effective role of cellulolytic bacterial (Bacillus subtilis) pre-treatment Promon, Salman Khan; Kamal, Wasif; Rahman, Shafkat Shamim F1000Research, Vol. 7 https://doi.org/10.12688/f1000research.13952.2	journal	January 2018
A Trichosporonales genome tree based on 27 haploid and three evolutionarily conserved ‘natural’ hybrid genomes: Trichosporonales genome tree Takashima, Masako; Sriswasdi, Sira; Manabe, Ri-Ichiroh Yeast, Vol. 35, Issue 1 https://doi.org/10.1002/yea.3284	journal	December 2017
Ethanol production using vegetable peels medium and the effective role of cellulolytic bacterial (Bacillus subtilis) pre-treatment Promon, Salman Khan; Kamal, Wasif; Rahman, Shafkat Shamim F1000Research, Vol. 7 https://doi.org/10.12688/f1000research.13952.1	journal	January 2018
On the origins and industrial applications of Saccharomyces cerevisiae × Saccharomyces kudriavzevii hybrids : Origins and applications of S. cerevisiae x S. kudriavzevii hybrids Peris, David; Pérez-Torrado, Roberto; Hittinger, Chris Todd Yeast, Vol. 35, Issue 1 https://doi.org/10.1002/yea.3283	journal	December 2017
Evaluation of divergent yeast genera for fermentation-associated stresses and identification of a robust sugarcane distillery waste isolate Saccharomyces cerevisiae NGY10 for lignocellulosic ethanol production in SHF and SSF Pandey, Ajay Kumar; Kumar, Mohit; Kumari, Sonam Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1379-x	journal	February 2019
Mitochondria-encoded genes contribute to evolution of heat and cold tolerance in yeast Li, Xueying C.; Peris, David; Hittinger, Chris Todd Science Advances, Vol. 5, Issue 1 https://doi.org/10.1126/sciadv.aav1848	journal	January 2019
Structural, Physiological and Regulatory Analysis of Maltose Transporter Genes in Saccharomyces eubayanus CBS 12357T Brickwedde, Anja; Brouwers, Nick; van den Broek, Marcel Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01786	journal	August 2018
Saccharomyces arboricola and Its Hybrids’ Propensity for Sake Production: Interspecific Hybrids Reveal Increased Fermentation Abilities and a Mosaic Metabolic Profile Winans, Matthew J.; Yamamoto, Yuki; Fujimaru, Yuki Fermentation, Vol. 6, Issue 1 https://doi.org/10.3390/fermentation6010014	journal	January 2020
Overcoming lignocellulose‐derived microbial inhibitors: advancing the Saccharomyces cerevisiae resistance toolbox Brandt, Bianca A.; Jansen, Trudy; Görgens, Johann F. Biofuels, Bioproducts and Biorefining, Vol. 13, Issue 6 https://doi.org/10.1002/bbb.2042	journal	August 2019
Inheritance of brewing-relevant phenotypes in constructed Saccharomyces cerevisiae × Saccharomyces eubayanus hybrids Krogerus, Kristoffer; Seppänen-Laakso, Tuulikki; Castillo, Sandra Microbial Cell Factories, Vol. 16, Issue 1 https://doi.org/10.1186/s12934-017-0679-8	journal	April 2017
Interspecific hybridization facilitates niche adaptation in beer yeast Gallone, Brigida; Steensels, Jan; Mertens, Stijn Nature Ecology & Evolution, Vol. 3, Issue 11 https://doi.org/10.1038/s41559-019-0997-9	journal	October 2019
Phylogeography of the wild Lager-brewing ancestor ( Saccharomyces eubayanus ) in Patagonia Eizaguirre, Juan I.; Peris, David; Rodríguez, María E. Environmental Microbiology, Vol. 20, Issue 10 https://doi.org/10.1111/1462-2920.14375	journal	October 2018
A Unique Saccharomyces cerevisiae × Saccharomyces uvarum Hybrid Isolated From Norwegian Farmhouse Beer: Characterization and Reconstruction Krogerus, Kristoffer; Preiss, Richard; Gibson, Brian Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.02253	journal	September 2018
Fitness benefits of loss of heterozygosity in Saccharomyces hybrids Lancaster, Samuel M.; Payen, Celia; Smukowski Heil, Caiti Genome Research, Vol. 29, Issue 10 https://doi.org/10.1101/gr.245605.118	journal	September 2019
Phenotype-Independent Isolation of Interspecies Saccharomyces Hybrids by Dual-Dye Fluorescent Staining and Fluorescence-Activated Cell Sorting Gorter de Vries, Arthur R.; Koster, Charlotte C.; Weening, Susan M. Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00871	journal	April 2019

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Related Subjects

09 BIOMASS FUELS
60 APPLIED LIFE SCIENCES
Saccharomyces
biodiversity
ammonia fiber expansion (AFEX)
AFEX-pretreated corn stover hydrolysate (ACSH)
hybridization
bioethanol
xylose
hydrolysate toxins

MOESM13 of Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production Peris, David; Moriarty, Ryan; Alexander, William https://doi.org/10.6084/m9.figshare.c.3727654_d4.v1 The current record is supplemented by this figure	figure	March 2017
MOESM6 of Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production Peris, David; Moriarty, Ryan; Alexander, William https://doi.org/10.6084/m9.figshare.c.3727654_d12.v1 The current record is supplemented by this dataset	dataset	March 2017
MOESM10 of Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production Peris, David; Moriarty, Ryan; Alexander, William https://doi.org/10.6084/m9.figshare.c.3727654_d1 The current record is supplemented by this audiovisual	audiovisual	January 2017
MOESM11 of Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production Peris, David; Moriarty, Ryan; Alexander, William https://doi.org/10.6084/m9.figshare.c.3727654_d2 The current record is supplemented by this audiovisual	audiovisual	January 2017
MOESM14 of Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production Peris, David; Moriarty, Ryan; Alexander, William https://doi.org/10.6084/m9.figshare.c.3727654_d5 The current record is supplemented by this audiovisual	audiovisual	January 2017
MOESM15 of Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production Peris, David; Moriarty, Ryan; Alexander, William https://doi.org/10.6084/m9.figshare.c.3727654_d6 The current record is supplemented by this dataset	dataset	January 2017
MOESM12 of Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production Peris, David; Moriarty, Ryan; Alexander, William https://doi.org/10.6084/m9.figshare.c.3727654_d3 The current record is supplemented by this audiovisual	audiovisual	January 2017
MOESM13 of Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production Peris, David; Moriarty, Ryan; Alexander, William https://doi.org/10.6084/m9.figshare.c.3727654_d4 The current record is supplemented by this audiovisual	audiovisual	January 2017
MOESM3 of Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production Peris, David; Moriarty, Ryan; Alexander, William https://doi.org/10.6084/m9.figshare.c.3727654_d9 The current record is supplemented by this audiovisual	audiovisual	January 2017
MOESM1 of Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production Peris, David; Moriarty, Ryan; Alexander, William https://doi.org/10.6084/m9.figshare.c.3727654_d7.v1 The current record is supplemented by this dataset	dataset	March 2017
MOESM1 of Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production Peris, David; Moriarty, Ryan; Alexander, William https://doi.org/10.6084/m9.figshare.c.3727654_d7 The current record is supplemented by this dataset	dataset	January 2017
MOESM2 of Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production Peris, David; Moriarty, Ryan; Alexander, William https://doi.org/10.6084/m9.figshare.c.3727654_d8 The current record is supplemented by this dataset	dataset	January 2017
MOESM9 of Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production Peris, David; Moriarty, Ryan; Alexander, William https://doi.org/10.6084/m9.figshare.c.3727654_d15.v1 The current record is supplemented by this dataset	dataset	March 2017
MOESM11 of Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production Peris, David; Moriarty, Ryan; Alexander, William https://doi.org/10.6084/m9.figshare.c.3727654_d2.v1 The current record is supplemented by this dataset	dataset	March 2017
MOESM4 of Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production Peris, David; Moriarty, Ryan; Alexander, William https://doi.org/10.6084/m9.figshare.c.3727654_d10.v1 The current record is supplemented by this dataset	dataset	March 2017
MOESM14 of Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production Peris, David; Moriarty, Ryan; Alexander, William https://doi.org/10.6084/m9.figshare.c.3727654_d5.v1 The current record is supplemented by this dataset	dataset	March 2017
Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production [Supplemental Data] Peris, David; Moriarty, Ryan; Alexander, William https://doi.org/10.6084/m9.figshare.c.3727654 The current record is supplemented by this dataset	dataset	March 2017
MOESM7 of Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production Peris, David; Moriarty, Ryan; Alexander, William https://doi.org/10.6084/m9.figshare.c.3727654_d13.v1 The current record is supplemented by this dataset	dataset	March 2017
MOESM4 of Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production Peris, David; Moriarty, Ryan; Alexander, William https://doi.org/10.6084/m9.figshare.c.3727654_d10 The current record is supplemented by this dataset	dataset	January 2017
MOESM5 of Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production Peris, David; Moriarty, Ryan; Alexander, William https://doi.org/10.6084/m9.figshare.c.3727654_d11 The current record is supplemented by this audiovisual	audiovisual	January 2017
MOESM2 of Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production Peris, David; Moriarty, Ryan; Alexander, William https://doi.org/10.6084/m9.figshare.c.3727654_d8.v1 The current record is supplemented by this dataset	dataset	March 2017
MOESM8 of Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production Peris, David; Moriarty, Ryan; Alexander, William https://doi.org/10.6084/m9.figshare.c.3727654_d14 The current record is supplemented by this audiovisual	audiovisual	January 2017
MOESM9 of Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production Peris, David; Moriarty, Ryan; Alexander, William https://doi.org/10.6084/m9.figshare.c.3727654_d15 The current record is supplemented by this dataset	dataset	January 2017
MOESM6 of Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production Peris, David; Moriarty, Ryan; Alexander, William https://doi.org/10.6084/m9.figshare.c.3727654_d12 The current record is supplemented by this audiovisual	audiovisual	January 2017
MOESM7 of Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production Peris, David; Moriarty, Ryan; Alexander, William https://doi.org/10.6084/m9.figshare.c.3727654_d13 The current record is supplemented by this audiovisual	audiovisual	January 2017
MOESM12 of Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production [Supplemental Data] Peris, David; Moriarty, Ryan; Alexander, William https://doi.org/10.6084/m9.figshare.c.3727654_d3.v1 The current record is supplemented by this dataset	dataset	March 2017
MOESM5 of Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production Peris, David; Moriarty, Ryan; Alexander, William https://doi.org/10.6084/m9.figshare.c.3727654_d11.v1 The current record is supplemented by this figure	figure	March 2017
MOESM15 of Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production Peris, David; Moriarty, Ryan; Alexander, William https://doi.org/10.6084/m9.figshare.c.3727654_d6.v1 The current record is supplemented by this dataset	dataset	March 2017
MOESM8 of Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production Peris, David; Moriarty, Ryan; Alexander, William https://doi.org/10.6084/m9.figshare.c.3727654_d14.v1 The current record is supplemented by this figure	figure	March 2017
Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production [Supplemental Data] Peris, David; Moriarty, Ryan; Alexander, William https://doi.org/10.6084/m9.figshare.c.3727654.v1 The current record is supplemented by this collection	collection	March 2017
MOESM3 of Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production Peris, David; Moriarty, Ryan; Alexander, William https://doi.org/10.6084/m9.figshare.c.3727654_d9.v1 The current record is supplemented by this figure	figure	March 2017
MOESM10 of Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production Peris, David; Moriarty, Ryan; Alexander, William https://doi.org/10.6084/m9.figshare.c.3727654_d1.v1 The current record is supplemented by this dataset	dataset	March 2017