Directed Evolution Reveals Unexpected Epistatic Interactions That Alter Metabolic Regulation and Enable Anaerobic Xylose Use by Saccharomyces cerevisiae
Abstract
The inability of native Saccharomyces cerevisiae to convert xylose from plant biomass into biofuels remains a major challenge for the production of renewable bioenergy. Despite extensive knowledge of the regulatory networks controlling carbon metabolism in yeast, little is known about how to reprogram S. cerevisiae to ferment xylose at rates comparable to glucose. Here we combined genome sequencing, proteomic profiling, and metabolomic analyses to identify and characterize the responsible mutations in a series of evolved strains capable of metabolizing xylose aerobically or anaerobically. We report that rapid xylose conversion by engineered and evolved S. cerevisiae strains depends upon epistatic interactions among genes encoding a xylose reductase (GRE3), a component of MAP Kinase (MAPK) signaling (HOG1), a regulator of Protein Kinase A (PKA) signaling (IRA2), and a scaffolding protein for mitochondrial iron-sulfur (Fe-S) cluster biogenesis (ISU1). Interestingly, the mutation in IRA2 only impacted anaerobic xylose consumption and required the loss of ISU1 function, indicating a previously unknown connection between PKA signaling, Fe-S cluster biogenesis, and anaerobiosis. Proteomic and metabolomic comparisons revealed that the xylose-metabolizing mutant strains exhibit altered metabolic pathways relative to the parental strain when grown in xylose. Further analyses revealed that interacting mutations in HOG1 and ISU1 unexpectedly elevatedmore »
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- Publication Date:
- Research Org.:
- Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1338424
- Alternate Identifier(s):
- OSTI ID: 1363955
- Grant/Contract Number:
- FC02-07ER64494
- Resource Type:
- Published Article
- Journal Name:
- PLoS Genetics
- Additional Journal Information:
- Journal Name: PLoS Genetics Journal Volume: 12 Journal Issue: 10; Journal ID: ISSN 1553-7404
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Sato, Trey K., Tremaine, Mary, Parreiras, Lucas S., Hebert, Alexander S., Myers, Kevin S., Higbee, Alan J., Sardi, Maria, McIlwain, Sean J., Ong, Irene M., Breuer, Rebecca J., Avanasi Narasimhan, Ragothaman, McGee, Mick A., Dickinson, Quinn, La Reau, Alex, Xie, Dan, Tian, Mingyuan, Reed, Jennifer L., Zhang, Yaoping, Coon, Joshua J., Hittinger, Chris Todd, Gasch, Audrey P., Landick, Robert, and Caudy, ed., Amy. Directed Evolution Reveals Unexpected Epistatic Interactions That Alter Metabolic Regulation and Enable Anaerobic Xylose Use by Saccharomyces cerevisiae. United States: N. p., 2016.
Web. doi:10.1371/journal.pgen.1006372.
Sato, Trey K., Tremaine, Mary, Parreiras, Lucas S., Hebert, Alexander S., Myers, Kevin S., Higbee, Alan J., Sardi, Maria, McIlwain, Sean J., Ong, Irene M., Breuer, Rebecca J., Avanasi Narasimhan, Ragothaman, McGee, Mick A., Dickinson, Quinn, La Reau, Alex, Xie, Dan, Tian, Mingyuan, Reed, Jennifer L., Zhang, Yaoping, Coon, Joshua J., Hittinger, Chris Todd, Gasch, Audrey P., Landick, Robert, & Caudy, ed., Amy. Directed Evolution Reveals Unexpected Epistatic Interactions That Alter Metabolic Regulation and Enable Anaerobic Xylose Use by Saccharomyces cerevisiae. United States. https://doi.org/10.1371/journal.pgen.1006372
Sato, Trey K., Tremaine, Mary, Parreiras, Lucas S., Hebert, Alexander S., Myers, Kevin S., Higbee, Alan J., Sardi, Maria, McIlwain, Sean J., Ong, Irene M., Breuer, Rebecca J., Avanasi Narasimhan, Ragothaman, McGee, Mick A., Dickinson, Quinn, La Reau, Alex, Xie, Dan, Tian, Mingyuan, Reed, Jennifer L., Zhang, Yaoping, Coon, Joshua J., Hittinger, Chris Todd, Gasch, Audrey P., Landick, Robert, and Caudy, ed., Amy. Fri .
"Directed Evolution Reveals Unexpected Epistatic Interactions That Alter Metabolic Regulation and Enable Anaerobic Xylose Use by Saccharomyces cerevisiae". United States. https://doi.org/10.1371/journal.pgen.1006372.
@article{osti_1338424,
title = {Directed Evolution Reveals Unexpected Epistatic Interactions That Alter Metabolic Regulation and Enable Anaerobic Xylose Use by Saccharomyces cerevisiae},
author = {Sato, Trey K. and Tremaine, Mary and Parreiras, Lucas S. and Hebert, Alexander S. and Myers, Kevin S. and Higbee, Alan J. and Sardi, Maria and McIlwain, Sean J. and Ong, Irene M. and Breuer, Rebecca J. and Avanasi Narasimhan, Ragothaman and McGee, Mick A. and Dickinson, Quinn and La Reau, Alex and Xie, Dan and Tian, Mingyuan and Reed, Jennifer L. and Zhang, Yaoping and Coon, Joshua J. and Hittinger, Chris Todd and Gasch, Audrey P. and Landick, Robert and Caudy, ed., Amy},
abstractNote = {The inability of native Saccharomyces cerevisiae to convert xylose from plant biomass into biofuels remains a major challenge for the production of renewable bioenergy. Despite extensive knowledge of the regulatory networks controlling carbon metabolism in yeast, little is known about how to reprogram S. cerevisiae to ferment xylose at rates comparable to glucose. Here we combined genome sequencing, proteomic profiling, and metabolomic analyses to identify and characterize the responsible mutations in a series of evolved strains capable of metabolizing xylose aerobically or anaerobically. We report that rapid xylose conversion by engineered and evolved S. cerevisiae strains depends upon epistatic interactions among genes encoding a xylose reductase (GRE3), a component of MAP Kinase (MAPK) signaling (HOG1), a regulator of Protein Kinase A (PKA) signaling (IRA2), and a scaffolding protein for mitochondrial iron-sulfur (Fe-S) cluster biogenesis (ISU1). Interestingly, the mutation in IRA2 only impacted anaerobic xylose consumption and required the loss of ISU1 function, indicating a previously unknown connection between PKA signaling, Fe-S cluster biogenesis, and anaerobiosis. Proteomic and metabolomic comparisons revealed that the xylose-metabolizing mutant strains exhibit altered metabolic pathways relative to the parental strain when grown in xylose. Further analyses revealed that interacting mutations in HOG1 and ISU1 unexpectedly elevated mitochondrial respiratory proteins and enabled rapid aerobic respiration of xylose and other non-fermentable carbon substrates. Lastly, our findings suggest a surprising connection between Fe-S cluster biogenesis and signaling that facilitates aerobic respiration and anaerobic fermentation of xylose, underscoring how much remains unknown about the eukaryotic signaling systems that regulate carbon metabolism.},
doi = {10.1371/journal.pgen.1006372},
journal = {PLoS Genetics},
number = 10,
volume = 12,
place = {United States},
year = {Fri Oct 14 00:00:00 EDT 2016},
month = {Fri Oct 14 00:00:00 EDT 2016}
}
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