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

David Peris, Ryan V. Moriarty, William G. Alexander, Emily Clare Baker, Kayla Sylvester, Maria Sardi, Quinn K. Langdon, Diego Libkind, Qi Ming Wang, Feng Yan Bai, Jean Baptiste Leducq, Guillaume Charron, Christian R. Landry, José Paulo Sampaio, Paula Gonçalves, Katie E. Hyma, Justin C. Fay, Trey K. Sato, Chris Todd Hittinger

Research output: Contribution to journalArticle

28 Citations (Scopus)

Abstract

Background: 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. Results: To investigate the efficacy of this approach for traits relevant to lignocellulosic biofuel production, we generated synthetic hybrids by crossing engineered xylose-fermenting strains of S. cerevisiae with wild strains from various Saccharomyces species. These interspecies hybrids retained important parental traits, such as xylose consumption and stress tolerance, while displaying intermediate kinetic parameters and, in some cases, heterosis (hybrid vigor). Next, we exposed them to adaptive evolution in ammonia fiber expansion-pretreated corn stover hydrolysate and recovered strains with improved fermentative traits. Genome sequencing showed that the genomes of these evolved synthetic hybrids underwent rearrangements, duplications, and deletions. To determine whether the genus Saccharomyces contains additional untapped potential, we screened a genetically diverse collection of more than 500 wild, non-engineered Saccharomyces isolates and uncovered a wide range of capabilities for traits relevant to cellulosic biofuel production. Notably, Saccharomyces mikatae strains have high innate tolerance to hydrolysate toxins, while some Saccharomyces species have a robust native capacity to consume xylose. Conclusions: This research demonstrates that hybridization is a viable method to combine industrially relevant traits from diverse yeast species and that members of the genus Saccharomyces beyond S. cerevisiae may offer advantageous genes and traits of interest to the lignocellulosic biofuel industry.

Original languageEnglish
Article number78
JournalBiotechnology for Biofuels
Volume10
Issue number1
DOIs
Publication statusPublished - 27 Mar 2017

Fingerprint

Saccharomyces
Biofuels
biofuel
Yeast
Xylose
Saccharomyces cerevisiae
fermentation
Fermentation
Biomass
tolerance
Hybrid Vigor
Genes
yeast
biomass
genome
heterosis
Research
Genome
Beer
vigor

Keywords

  • AFEX-pretreated corn stover hydrolysate (ACSH)
  • Ammonia fiber expansion (AFEX)
  • Biodiversity
  • Bioethanol
  • Hybridization
  • Hydrolysate toxins
  • Saccharomyces
  • Xylose

Cite this

Peris, D., Moriarty, R. V., Alexander, W. G., Baker, E. C., Sylvester, K., Sardi, M., ... Hittinger, C. T. (2017). Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production. Biotechnology for Biofuels, 10(1), [78]. https://doi.org/10.1186/s13068-017-0763-7
Peris, David ; Moriarty, Ryan V. ; Alexander, William G. ; Baker, Emily Clare ; 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. In: Biotechnology for Biofuels. 2017 ; Vol. 10, No. 1.
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abstract = "Background: 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. Results: To investigate the efficacy of this approach for traits relevant to lignocellulosic biofuel production, we generated synthetic hybrids by crossing engineered xylose-fermenting strains of S. cerevisiae with wild strains from various Saccharomyces species. These interspecies hybrids retained important parental traits, such as xylose consumption and stress tolerance, while displaying intermediate kinetic parameters and, in some cases, heterosis (hybrid vigor). Next, we exposed them to adaptive evolution in ammonia fiber expansion-pretreated corn stover hydrolysate and recovered strains with improved fermentative traits. Genome sequencing showed that the genomes of these evolved synthetic hybrids underwent rearrangements, duplications, and deletions. To determine whether the genus Saccharomyces contains additional untapped potential, we screened a genetically diverse collection of more than 500 wild, non-engineered Saccharomyces isolates and uncovered a wide range of capabilities for traits relevant to cellulosic biofuel production. Notably, Saccharomyces mikatae strains have high innate tolerance to hydrolysate toxins, while some Saccharomyces species have a robust native capacity to consume xylose. Conclusions: This research demonstrates that hybridization is a viable method to combine industrially relevant traits from diverse yeast species and that members of the genus Saccharomyces beyond S. cerevisiae may offer advantageous genes and traits of interest to the lignocellulosic biofuel industry.",
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author = "David Peris and Moriarty, {Ryan V.} and Alexander, {William G.} and Baker, {Emily Clare} and Kayla Sylvester and Maria Sardi and Langdon, {Quinn K.} and Diego Libkind and Wang, {Qi Ming} and Bai, {Feng Yan} and Leducq, {Jean Baptiste} and Guillaume Charron and Landry, {Christian R.} and Sampaio, {Jos{\'e} Paulo} and Paula Gon{\cc}alves and Hyma, {Katie E.} and Fay, {Justin C.} and Sato, {Trey K.} and Hittinger, {Chris Todd}",
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Peris, D, Moriarty, RV, Alexander, WG, Baker, EC, Sylvester, K, Sardi, M, Langdon, QK, Libkind, D, Wang, QM, Bai, FY, Leducq, JB, Charron, G, Landry, CR, Sampaio, JP, Gonçalves, P, Hyma, KE, Fay, JC, Sato, TK & Hittinger, CT 2017, 'Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production', Biotechnology for Biofuels, vol. 10, no. 1, 78. https://doi.org/10.1186/s13068-017-0763-7

Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production. / Peris, David; Moriarty, Ryan V.; Alexander, William G.; Baker, Emily Clare; 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.

In: Biotechnology for Biofuels, Vol. 10, No. 1, 78, 27.03.2017.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production

AU - Peris, David

AU - Moriarty, Ryan V.

AU - Alexander, William G.

AU - Baker, Emily Clare

AU - Sylvester, Kayla

AU - Sardi, Maria

AU - Langdon, Quinn K.

AU - Libkind, Diego

AU - Wang, Qi Ming

AU - Bai, Feng Yan

AU - Leducq, Jean Baptiste

AU - Charron, Guillaume

AU - Landry, Christian R.

AU - Sampaio, José Paulo

AU - Gonçalves, Paula

AU - Hyma, Katie E.

AU - Fay, Justin C.

AU - Sato, Trey K.

AU - Hittinger, Chris Todd

N1 - Sem PDF. DOE Great Lakes Bioenergy Research Center (DOE Office of Science BER) (DE-FC02-07ER64494) National Science Foundation (DEB-1253634) USDA National Institute of Food and Agriculture Hatch Project (1003258) ANPCyT (PICT 2542) CONICET (PIP 0392) UNComahue Grant (B171) National Natural Science Foundation of China (31470150) NSERC Discovery Grant National Institutes of Health (GM080669; 5 T32 GM007133-40) National Science Foundation Graduate Research Fellowship (DGE-1256259) Predoctoral Training Program in Genetics - A aguardar informação sobre financiamento NIH Genome Analysis Training Grant - A aguardar informação sobre financiamento Pew Charitable Trusts - A aguardar informação sobre financiamento

PY - 2017/3/27

Y1 - 2017/3/27

N2 - Background: 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. Results: To investigate the efficacy of this approach for traits relevant to lignocellulosic biofuel production, we generated synthetic hybrids by crossing engineered xylose-fermenting strains of S. cerevisiae with wild strains from various Saccharomyces species. These interspecies hybrids retained important parental traits, such as xylose consumption and stress tolerance, while displaying intermediate kinetic parameters and, in some cases, heterosis (hybrid vigor). Next, we exposed them to adaptive evolution in ammonia fiber expansion-pretreated corn stover hydrolysate and recovered strains with improved fermentative traits. Genome sequencing showed that the genomes of these evolved synthetic hybrids underwent rearrangements, duplications, and deletions. To determine whether the genus Saccharomyces contains additional untapped potential, we screened a genetically diverse collection of more than 500 wild, non-engineered Saccharomyces isolates and uncovered a wide range of capabilities for traits relevant to cellulosic biofuel production. Notably, Saccharomyces mikatae strains have high innate tolerance to hydrolysate toxins, while some Saccharomyces species have a robust native capacity to consume xylose. Conclusions: This research demonstrates that hybridization is a viable method to combine industrially relevant traits from diverse yeast species and that members of the genus Saccharomyces beyond S. cerevisiae may offer advantageous genes and traits of interest to the lignocellulosic biofuel industry.

AB - Background: 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. Results: To investigate the efficacy of this approach for traits relevant to lignocellulosic biofuel production, we generated synthetic hybrids by crossing engineered xylose-fermenting strains of S. cerevisiae with wild strains from various Saccharomyces species. These interspecies hybrids retained important parental traits, such as xylose consumption and stress tolerance, while displaying intermediate kinetic parameters and, in some cases, heterosis (hybrid vigor). Next, we exposed them to adaptive evolution in ammonia fiber expansion-pretreated corn stover hydrolysate and recovered strains with improved fermentative traits. Genome sequencing showed that the genomes of these evolved synthetic hybrids underwent rearrangements, duplications, and deletions. To determine whether the genus Saccharomyces contains additional untapped potential, we screened a genetically diverse collection of more than 500 wild, non-engineered Saccharomyces isolates and uncovered a wide range of capabilities for traits relevant to cellulosic biofuel production. Notably, Saccharomyces mikatae strains have high innate tolerance to hydrolysate toxins, while some Saccharomyces species have a robust native capacity to consume xylose. Conclusions: This research demonstrates that hybridization is a viable method to combine industrially relevant traits from diverse yeast species and that members of the genus Saccharomyces beyond S. cerevisiae may offer advantageous genes and traits of interest to the lignocellulosic biofuel industry.

KW - AFEX-pretreated corn stover hydrolysate (ACSH)

KW - Ammonia fiber expansion (AFEX)

KW - Biodiversity

KW - Bioethanol

KW - Hybridization

KW - Hydrolysate toxins

KW - Saccharomyces

KW - Xylose

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