Oleaginicity of the yeast strain Saccharomyces cerevisiae D5A
Abstract
Here, the model yeast, Saccharomyces cerevisiae, is not known to be oleaginous. However, an industrial wild-type strain, D5A, was shown to accumulate over 20% storage lipids from glucose when growth is nitrogen-limited compared to no more than 7% lipid accumulation without nitrogen stress. To elucidate the mechanisms of S. cerevisiae D5A oleaginicity, we compared physiological and metabolic changes; as well as the transcriptional profiles of the oleaginous industrial strain, D5A, and a non-oleaginous laboratory strain, BY4741, under normal and nitrogen-limited conditions using analytic techniques and next-generation sequencing-based RNA-Seq transcriptomics. Transcriptional levels for genes associated with fatty acid biosynthesis, nitrogen metabolism, amino acid catabolism, as well as the pentose phosphate pathway and ethanol oxidation in central carbon (C) metabolism, were up-regulated in D5A during nitrogen deprivation. Despite increased carbon flux to lipids, most gene-encoding enzymes involved in triacylglycerol (TAG) assembly were expressed at similar levels regardless of the varying nitrogen concentrations in the growth media and strain backgrounds. Phospholipid turnover also contributed to TAG accumulation through increased precursor production with the down-regulation of subsequent phospholipid synthesis steps. Our results also demonstrated that nitrogen assimilation via the glutamate-glutamine pathway and amino acid metabolism, as well as the fluxes of carbon and reductantsmore »
- Authors:
- Publication Date:
- Research Org.:
- National Renewable Energy Laboratory (NREL), Golden, CO (United States)
- Sponsoring Org.:
- USDOE Office of Energy Efficiency and Renewable Energy (EERE), Sustainable Transportation Office. Bioenergy Technologies Office
- OSTI Identifier:
- 1618737
- Alternate Identifier(s):
- OSTI ID: 1476705
- Report Number(s):
- NREL/JA-5100-71803
Journal ID: ISSN 1754-6834; 258; PII: 1256
- Grant/Contract Number:
- AC36-08GO28308; 2018ACA149
- Resource Type:
- Published Article
- Journal Name:
- Biotechnology for Biofuels
- Additional Journal Information:
- Journal Name: Biotechnology for Biofuels Journal Volume: 11 Journal Issue: 1; Journal ID: ISSN 1754-6834
- Publisher:
- Springer Science + Business Media
- Country of Publication:
- Netherlands
- Language:
- English
- Subject:
- 09 BIOMASS FUELS; oleaginous yeast; Saccharomyces cerevisiae; transcriptomics; RNA-Seq; lipid accumulation; triacylglycerol (TAG); nitrogen assimilation
Citation Formats
He, Qiaoning, Yang, Yongfu, Yang, Shihui, Donohoe, Bryon S., Van Wychen, Stefanie, Zhang, Min, Himmel, Michael E., and Knoshaug, Eric P. Oleaginicity of the yeast strain Saccharomyces cerevisiae D5A. Netherlands: N. p., 2018.
Web. doi:10.1186/s13068-018-1256-z.
He, Qiaoning, Yang, Yongfu, Yang, Shihui, Donohoe, Bryon S., Van Wychen, Stefanie, Zhang, Min, Himmel, Michael E., & Knoshaug, Eric P. Oleaginicity of the yeast strain Saccharomyces cerevisiae D5A. Netherlands. https://doi.org/10.1186/s13068-018-1256-z
He, Qiaoning, Yang, Yongfu, Yang, Shihui, Donohoe, Bryon S., Van Wychen, Stefanie, Zhang, Min, Himmel, Michael E., and Knoshaug, Eric P. Mon .
"Oleaginicity of the yeast strain Saccharomyces cerevisiae D5A". Netherlands. https://doi.org/10.1186/s13068-018-1256-z.
@article{osti_1618737,
title = {Oleaginicity of the yeast strain Saccharomyces cerevisiae D5A},
author = {He, Qiaoning and Yang, Yongfu and Yang, Shihui and Donohoe, Bryon S. and Van Wychen, Stefanie and Zhang, Min and Himmel, Michael E. and Knoshaug, Eric P.},
abstractNote = {Here, the model yeast, Saccharomyces cerevisiae, is not known to be oleaginous. However, an industrial wild-type strain, D5A, was shown to accumulate over 20% storage lipids from glucose when growth is nitrogen-limited compared to no more than 7% lipid accumulation without nitrogen stress. To elucidate the mechanisms of S. cerevisiae D5A oleaginicity, we compared physiological and metabolic changes; as well as the transcriptional profiles of the oleaginous industrial strain, D5A, and a non-oleaginous laboratory strain, BY4741, under normal and nitrogen-limited conditions using analytic techniques and next-generation sequencing-based RNA-Seq transcriptomics. Transcriptional levels for genes associated with fatty acid biosynthesis, nitrogen metabolism, amino acid catabolism, as well as the pentose phosphate pathway and ethanol oxidation in central carbon (C) metabolism, were up-regulated in D5A during nitrogen deprivation. Despite increased carbon flux to lipids, most gene-encoding enzymes involved in triacylglycerol (TAG) assembly were expressed at similar levels regardless of the varying nitrogen concentrations in the growth media and strain backgrounds. Phospholipid turnover also contributed to TAG accumulation through increased precursor production with the down-regulation of subsequent phospholipid synthesis steps. Our results also demonstrated that nitrogen assimilation via the glutamate-glutamine pathway and amino acid metabolism, as well as the fluxes of carbon and reductants from central C metabolism, are integral to the general oleaginicity of D5A, which resulted in the enhanced lipid storage during nitrogen deprivation. This work demonstrated the disequilibrium and rebalance of carbon and nitrogen contribution to the accumulation of lipids in the oleaginous yeast S. cerevisiae D5A. Rather than TAG assembly from acyl groups, the major switches for the enhanced lipid accumulation of D5A (i.e., fatty acid biosynthesis) are the increases of cytosolic pools of acetyl-CoA and NADPH, as well as alternative nitrogen assimilation.},
doi = {10.1186/s13068-018-1256-z},
journal = {Biotechnology for Biofuels},
number = 1,
volume = 11,
place = {Netherlands},
year = {Mon Sep 24 00:00:00 EDT 2018},
month = {Mon Sep 24 00:00:00 EDT 2018}
}
https://doi.org/10.1186/s13068-018-1256-z
Web of Science
Works referenced in this record:
Microbial lipid-based lignocellulosic biorefinery: feasibility and challenges
journal, January 2015
- Jin, Mingjie; Slininger, Patricia J.; Dien, Bruce S.
- Trends in Biotechnology, Vol. 33, Issue 1
Biodiesel production from oleaginous microorganisms
journal, January 2009
- Meng, Xin; Yang, Jianming; Xu, Xin
- Renewable Energy, Vol. 34, Issue 1
Metabolism and Regulation of Glycerolipids in the Yeast Saccharomyces cerevisiae
journal, February 2012
- Henry, Susan A.; Kohlwein, Sepp D.; Carman, George M.
- Genetics, Vol. 190, Issue 2, p. 317-349
Fatty Acid-Derived Biofuels and Chemicals Production in Saccharomyces cerevisiae
journal, September 2014
- Zhou, Yongjin J.; Buijs, Nicolaas A.; Siewers, Verena
- Frontiers in Bioengineering and Biotechnology, Vol. 2
Advances in ethanol production
journal, June 2011
- Geddes, Claudia C.; Nieves, Ismael U.; Ingram, Lonnie O.
- Current Opinion in Biotechnology, Vol. 22, Issue 3
TCA cycle-independent acetate metabolism via the glyoxylate cycle in Saccharomyces cerevisiae
journal, November 2010
- Lee, Yong Joo; Jang, Jin Won; Kim, Kyung Jin
- Yeast, Vol. 28, Issue 2
Regulation of amino-acid metabolism controls flux to lipid accumulation in Yarrowia lipolytica
journal, March 2016
- Kerkhoven, Eduard J.; Pomraning, Kyle R.; Baker, Scott E.
- npj Systems Biology and Applications, Vol. 2, Issue 1
Overexpression of genes of the fatty acid biosynthetic pathway leads to accumulation of sterols in Saccharomyces cerevisiae: Sterol accumulation by overexpression of fatty acid synthesis genes
journal, August 2012
- Shin, Ga-Hee; Veen, Markus; Stahl, Ulf
- Yeast, Vol. 29, Issue 9
The alcohol dehydrogenases of Saccharomyces cerevisiae: a comprehensive review
journal, November 2008
- de Smidt, Olga; du Preez, James C.; Albertyn, Jacobus
- FEMS Yeast Research, Vol. 8, Issue 7, p. 967-978
Comparative proteomic analysis of Rhodosporidium toruloides during lipid accumulation
journal, October 2009
- Liu, Hongwei; Zhao, Xin; Wang, Fangjun
- Yeast, Vol. 26, Issue 10
Engineering the fatty acid metabolic pathway in Saccharomyces cerevisiae for advanced biofuel production
journal, December 2015
- Tang, Xiaoling; Lee, Jaslyn; Chen, Wei Ning
- Metabolic Engineering Communications, Vol. 2
Yarrowia lipolytica as a model for bio-oil production
journal, November 2009
- Beopoulos, Athanasios; Cescut, Julien; Haddouche, Ramdane
- Progress in Lipid Research, Vol. 48, Issue 6, p. 375-387
DGA1 (diacylglycerol acyltransferase gene) overexpression and leucine biosynthesis significantly increase lipid accumulation in the Δsnf2 disruptant of Saccharomyces cerevisiae
journal, November 2007
- Kamisaka, Yasushi; Tomita, Nao; Kimura, Kazuyoshi
- Biochemical Journal, Vol. 408, Issue 1, p. 61-68
Glutamate synthase levels in Neurospora crassa mutants altered with respect to nitrogen metabolism.
journal, February 1981
- Dunn-Coleman, N. S.; Robey, E. A.; Tomsett, A. B.
- Molecular and Cellular Biology, Vol. 1, Issue 2
Transcriptomic and metabolomic profiling of Zymomonas mobilis during aerobic and anaerobic fermentations
journal, January 2009
- Yang, Shihui; Tschaplinski, Timothy J.; Engle, Nancy L.
- BMC Genomics, Vol. 10, Issue 1
Combined algal processing: A novel integrated biorefinery process to produce algal biofuels and bioproducts
journal, November 2016
- Dong, Tao; Knoshaug, Eric P.; Davis, Ryan
- Algal Research, Vol. 19
Next-generation biofuels: a new challenge for yeast: Next-generation biofuels: a new challenge for yeast
journal, July 2015
- Petrovič, Uroš
- Yeast, Vol. 32, Issue 9
Oleaginous yeasts: Promising platforms for the production of oleochemicals and biofuels: Microbial Production of Oleochemicals and Biofuels
journal, May 2017
- Adrio, José L.
- Biotechnology and Bioengineering, Vol. 114, Issue 9
Glycerol stress in S accharomyces cerevisiae : Cellular responses and evolved adaptations : Glycerol Stress in
journal, January 2017
- Mattenberger, Florian; Sabater-Muñoz, Beatriz; Hallsworth, John E.
- Environmental Microbiology, Vol. 19, Issue 3
Regulation of Sensing, Transportation, and Catabolism of Nitrogen Sources in Saccharomyces cerevisiae
journal, February 2018
- Zhang, Weiping; Du, Guocheng; Zhou, Jingwen
- Microbiology and Molecular Biology Reviews, Vol. 82, Issue 1
Lipid accumulation from glucose and xylose in an engineered, naturally oleaginous strain of Saccharomyces cerevisiae
journal, June 2018
- Knoshaug, Eric P.; Van Wychen, Stefanie; Singh, Arjun
- Biofuel Research Journal, Vol. 5, Issue 2
Fatty acid synthesis and elongation in yeast
journal, March 2007
- Tehlivets, Oksana; Scheuringer, Kim; Kohlwein, Sepp D.
- Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, Vol. 1771, Issue 3, p. 255-270
Comprehensive Metabolomic, Lipidomic and Microscopic Profiling of Yarrowia lipolytica during Lipid Accumulation Identifies Targets for Increased Lipogenesis
journal, April 2015
- Pomraning, Kyle R.; Wei, Siwei; Karagiosis, Sue A.
- PLOS ONE, Vol. 10, Issue 4
Integrated analysis of transcriptome and lipid profiling reveals the co-influences of inositol–choline and Snf1 in controlling lipid biosynthesis in yeast
journal, May 2012
- Chumnanpuen, Pramote; Zhang, Jie; Nookaew, Intawat
- Molecular Genetics and Genomics, Vol. 287, Issue 7
The Techno-Economic Basis for Coproduct Manufacturing To Enable Hydrocarbon Fuel Production from Lignocellulosic Biomass
journal, May 2016
- Biddy, Mary J.; Davis, Ryan; Humbird, David
- ACS Sustainable Chemistry & Engineering, Vol. 4, Issue 6
Engineering lipid overproduction in the oleaginous yeast Yarrowia lipolytica
journal, May 2015
- Qiao, Kangjian; Imam Abidi, Syed Hussain; Liu, Hongjuan
- Metabolic Engineering, Vol. 29, p. 56-65
Lipids of oleaginous yeasts. Part I: Biochemistry of single cell oil production
journal, June 2011
- Papanikolaou, Seraphim; Aggelis, George
- European Journal of Lipid Science and Technology, Vol. 113, Issue 8
The oxidative pentose phosphate pathway is the primary source of NADPH for lipid overproduction from glucose in Yarrowia lipolytica
journal, July 2015
- Wasylenko, Thomas M.; Ahn, Woo Suk; Stephanopoulos, Gregory
- Metabolic Engineering, Vol. 30
Overproduction and secretion of free fatty acids through disrupted neutral lipid recycle in Saccharomyces cerevisiae
journal, March 2015
- Leber, Christopher; Polson, Brian; Fernandez-Moya, Ruben
- Metabolic Engineering, Vol. 28
The novel zinc cluster regulator Tog1 plays important roles in oleate utilization and oxidative stress response in Saccharomyces cerevisiae
journal, August 2014
- Thepnok, Piyasuda; Ratanakhanokchai, Khanok; Soontorngun, Nitnipa
- Biochemical and Biophysical Research Communications, Vol. 450, Issue 4
Nitrogen-Sparing Mechanisms in Chlamydomonas Affect the Transcriptome, the Proteome, and Photosynthetic Metabolism
journal, April 2014
- Schmollinger, Stefan; Mühlhaus, Timo; Boyle, Nanette R.
- The Plant Cell, Vol. 26, Issue 4
Profiling of Cytosolic and Peroxisomal Acetyl-CoA Metabolism in Saccharomyces cerevisiae
journal, August 2012
- Chen, Yun; Siewers, Verena; Nielsen, Jens
- PLoS ONE, Vol. 7, Issue 8
Nitrogen regulation in Saccharomyces cerevisiae
journal, May 2002
- Magasanik, Boris; Kaiser, Chris A.
- Gene, Vol. 290, Issue 1-2
Sufficient utilization of natural fluctuating light intensity is an effective approach of promoting lipid productivity in oleaginous microalgal cultivation outdoors
journal, March 2015
- He, Qiaoning; Yang, Haijian; Xu, Liangliang
- Bioresource Technology, Vol. 180
Synthesis of FAEEs from glycerol in engineered Saccharomyces cerevisiae using endogenously produced ethanol by heterologous expression of an unspecific bacterial acyltransferase
journal, August 2011
- Yu, Kyung Ok; Jung, Ju; Kim, Seung Wook
- Biotechnology and Bioengineering, Vol. 109, Issue 1
The proteome analysis of oleaginous yeast Lipomyces starkeyi: Comparative proteomic analysis of Lipomyces starkeyi
journal, October 2010
- Liu, Hongwei; Zhao, Xin; Wang, Fangjun
- FEMS Yeast Research, Vol. 11, Issue 1
Not just a circle: flux modes in the plant TCA cycle
journal, August 2010
- Sweetlove, Lee J.; Beard, Katherine F. M.; Nunes-Nesi, Adriano
- Trends in Plant Science, Vol. 15, Issue 8
Systems-Level Analysis of Nitrogen Starvation-Induced Modifications of Carbon Metabolism in a Chlamydomonas reinhardtii Starchless Mutant
journal, November 2013
- Blaby, I. K.; Glaesener, A. G.; Mettler, T.
- The Plant Cell, Vol. 25, Issue 11
Regulation of lipid accumulation in oleaginous micro-organisms
journal, November 2002
- Ratledge, C.
- Biochemical Society Transactions, Vol. 30, Issue 6, p. 1047-1050
Metabolic engineering of Saccharomyces cerevisiae to produce a reduced viscosity oil from lignocellulose
journal, March 2017
- Tran, Tam N. T.; Breuer, Rebecca J.; Avanasi Narasimhan, Ragothaman
- Biotechnology for Biofuels, Vol. 10, Issue 1
Lipid production in Nannochloropsis gaditana is doubled by decreasing expression of a single transcriptional regulator
journal, June 2017
- Ajjawi, Imad; Verruto, John; Aqui, Moena
- Nature Biotechnology, Vol. 35, Issue 7
Improved production of fatty acid ethyl esters in Saccharomyces cerevisiae through up-regulation of the ethanol degradation pathway and expression of the heterologous phosphoketolase pathway
journal, January 2014
- de Jong, Bouke Wim; Shi, Shuobo; Siewers, Verena
- Microbial Cell Factories, Vol. 13, Issue 1
Lipid recovery from wet oleaginous microbial biomass for biofuel production: A critical review
journal, September 2016
- Dong, Tao; Knoshaug, Eric P.; Pienkos, Philip T.
- Applied Energy, Vol. 177
Systems biology of lipid metabolism: From yeast to human
journal, October 2009
- Nielsen, Jens
- FEBS Letters, Vol. 583, Issue 24
Improvement of Ethanol Yield from Glycerol via Conversion of Pyruvate to Ethanol in Metabolically Engineered Saccharomyces cerevisiae
journal, December 2011
- Yu, Kyung Ok; Jung, Ju; Ramzi, Ahmad Bazli
- Applied Biochemistry and Biotechnology, Vol. 166, Issue 4
Manipulation of culture conditions alters lipid content and fatty acid profiles of a wide variety of known and new oleaginous yeast species
journal, September 2013
- Sitepu, Irnayuli R.; Sestric, Ryan; Ignatia, Laura
- Bioresource Technology, Vol. 144
Butanol Tolerance in a Selection of Microorganisms
journal, December 2008
- Knoshaug, Eric P.; Zhang, Min
- Applied Biochemistry and Biotechnology, Vol. 153, Issue 1-3
Transcriptomic Analyses during the Transition from Biomass Production to Lipid Accumulation in the Oleaginous Yeast Yarrowia lipolytica
journal, November 2011
- Morin, Nicolas; Cescut, Julien; Beopoulos, Athanasios
- PLoS ONE, Vol. 6, Issue 11, Article No. e27966
Enhanced amino acid utilization sustains growth of cells lacking Snf1/AMPK
journal, July 2015
- Nicastro, Raffaele; Tripodi, Farida; Guzzi, Cinzia
- Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1853, Issue 7
Remodeling of intermediate metabolism in the diatom Phaeodactylum tricornutum under nitrogen stress
journal, December 2014
- Levitan, Orly; Dinamarca, Jorge; Zelzion, Ehud
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 2
Combined “de novo” and “ex novo” lipid fermentation in a mix-medium of corncob acid hydrolysate and soybean oil by Trichosporon dermatis
journal, June 2017
- Huang, Chao; Luo, Mu-Tan; Chen, Xue-Fang
- Biotechnology for Biofuels, Vol. 10, Issue 1
Comparative metabolic profiling of the lipid-producing green microalga Chlorella reveals that nitrogen and carbon metabolic pathways contribute to lipid metabolism
journal, June 2017
- Chen, Hui; Zheng, Yanli; Zhan, Jiao
- Biotechnology for Biofuels, Vol. 10, Issue 1
Fatty alcohol production in Lipomyces starkeyi and Yarrowia lipolytica
journal, October 2016
- Wang, Wei; Wei, Hui; Knoshaug, Eric
- Biotechnology for Biofuels, Vol. 9, Issue 1
Engineering Rhodosporidium toruloides for increased lipid production : Engineering
journal, November 2015
- Zhang, Shuyan; Skerker, Jeffrey M.; Rutter, Charles D.
- Biotechnology and Bioengineering, Vol. 113, Issue 5
Multi-omics analysis reveals regulators of the response to nitrogen limitation in Yarrowia lipolytica
journal, February 2016
- Pomraning, Kyle R.; Kim, Young-Mo; Nicora, Carrie D.
- BMC Genomics, Vol. 17, Issue 1
Saccharomyces cerevisiae Mutants Resistant to Catabolite Repression: Use in Cheese Whey Hydrolysate Fermentation
journal, January 1982
- Bailey, Richard B.; Benitez, Tahia; Woodward, Anne
- Applied and Environmental Microbiology, Vol. 44, Issue 3
Overexpression of OLE1 enhances stress tolerance and constitutively activates the MAPK HOG pathway in Saccharomyces cerevisiae : Enhanced Stress Tolerance by
journal, November 2016
- Nasution, Olviyani; Lee, Young Mi; Kim, Eunjung
- Biotechnology and Bioengineering, Vol. 114, Issue 3
Metabolic engineering of yeast for production of fuels and chemicals
journal, June 2013
- Nielsen, Jens; Larsson, Christer; van Maris, Antonius
- Current Opinion in Biotechnology, Vol. 24, Issue 3
Oily yeasts as oleaginous cell factories
journal, April 2011
- Ageitos, Jose Manuel; Vallejo, Juan Andres; Veiga-Crespo, Patricia
- Applied Microbiology and Biotechnology, Vol. 90, Issue 4
Choreography of Transcriptomes and Lipidomes of Nannochloropsis Reveals the Mechanisms of Oil Synthesis in Microalgae
journal, April 2014
- Li, Jing; Han, Danxiang; Wang, Dongmei
- The Plant Cell, Vol. 26, Issue 4
Metabolic engineering of Saccharomyces cerevisiae for production of fatty acid-derived biofuels and chemicals
journal, January 2014
- Runguphan, Weerawat; Keasling, Jay D.
- Metabolic Engineering, Vol. 21
Advancing oleaginous microorganisms to produce lipid via metabolic engineering technology
journal, October 2013
- Liang, Ming-Hua; Jiang, Jian-Guo
- Progress in Lipid Research, Vol. 52, Issue 4, p. 395-408
Overproduction of fatty acids in engineered Saccharomyces cerevisiae
journal, April 2014
- Li, Xiaowei; Guo, Daoyi; Cheng, Yongbo
- Biotechnology and Bioengineering, Vol. 111, Issue 9, p. 1841-1852
The Response of Diatom Central Carbon Metabolism to Nitrogen Starvation Is Different from That of Green Algae and Higher Plants
journal, November 2011
- Hockin, Nicola Louise; Mock, Thomas; Mulholland, Francis
- Plant Physiology, Vol. 158, Issue 1
Genome-wide location analysis reveals an important overlap between the targets of the yeast transcriptional regulators Rds2 and Adr1
journal, July 2012
- Soontorngun, Nitnipa; Baramee, Sirilak; Tangsombatvichit, Chalinee
- Biochemical and Biophysical Research Communications, Vol. 423, Issue 4
A multi-omic map of the lipid-producing yeast Rhodosporidium toruloides
journal, January 2012
- Zhu, Zhiwei; Zhang, Sufang; Liu, Hongwei
- Nature Communications, Vol. 3, Issue 1
Oleaginous yeasts for biodiesel: Current and future trends in biology and production
journal, November 2014
- Sitepu, Irnayuli R.; Garay, Luis A.; Sestric, Ryan
- Biotechnology Advances, Vol. 32, Issue 7
Engineering increased triacylglycerol accumulation in Saccharomyces cerevisiae using a modified type 1 plant diacylglycerol acyltransferase
journal, December 2014
- Greer, Michael S.; Truksa, Martin; Deng, Wei
- Applied Microbiology and Biotechnology, Vol. 99, Issue 5
Works referencing / citing this record:
Insights into the Metabolism of Oleaginous Rhodococcus spp.
journal, July 2019
- Alvarez, Héctor M.; Herrero, O. Marisa; Silva, Roxana A.
- Applied and Environmental Microbiology, Vol. 85, Issue 18