Ameliorating the Metabolic Burden of the Co-expression of Secreted Fungal Cellulases in a High Lipid-Accumulating Yarrowia lipolytica Strain by Medium C/N Ratio and a Chemical Chaperone

Wei, Hui; Wang, Wei; Alper, Hal S.; Xu, Qi; Knoshaug, Eric P.; Van Wychen, Stefanie; Lin, Chien-Yuan; Luo, Yonghua; Decker, Stephen R.; Himmel, Michael E.; Zhang, Min

doi:10.3389/fmicb.2018.03276

Title: Ameliorating the Metabolic Burden of the Co-expression of Secreted Fungal Cellulases in a High Lipid-Accumulating Yarrowia lipolytica Strain by Medium C/N Ratio and a Chemical Chaperone

Journal Article · Wed Jan 09 00:00:00 EST 2019 · Frontiers in Microbiology

DOI:https://doi.org/10.3389/fmicb.2018.03276· OSTI ID:1490107

Wei, Hui; Wang, Wei; Alper, Hal S.; Xu, Qi; Knoshaug, Eric P.; Van Wychen, Stefanie; Lin, Chien-Yuan; Luo, Yonghua; Decker, Stephen R.; Himmel, Michael E.; Zhang, Min

Yarrowia lipolytica, known to accumulate lipids intracellularly, lacks the cellulolytic enzymes needed to break down solid biomass directly. This study aimed to evaluate the potential metabolic burden of expressing core cellulolytic enzymes in an engineered high lipid-accumulating strain of Y. lipolytica. Three fungal cellulases, Talaromyces emersonii-Trichoderma reesei chimeric cellobiohydrolase I (chimeric-CBH I), T. reesei cellobiohydrolase II (CBH II), and T. reesei endoglucanase II (EG II) were expressed using three constitutive strong promoters as a single integrative expression block in a recently engineered lipid hyper-accumulating strain of Y. lipolytica (HA1). In yeast extract-peptone-dextrose (YPD) medium, the resulting cellulase co-expressing transformant YL165-1 had the chimeric-CBH I, CBH II, and EG II secretion titers being 26, 17, and 132 mg L^-1, respectively. Cellulase co-expression in YL165-1 in culture media with a moderate C/N ratio of ~4.5 unexpectedly resulted in a nearly two-fold reduction in cellular lipid accumulation compared to the parental control strain, a sign of cellular metabolic drain. Such metabolic drain was ameliorated when grown in media with a high C/N ratio of 59 having a higher glucose utilization rate that led to approximately twofold more cell mass and threefold more lipid production per liter culture compared to parental control strain, suggesting cross-talk between cellulase and lipid production, both of which involve the endoplasmic reticulum (ER). Most importantly, we found that the chemical chaperone, trimethylamine N-oxide dihydride increased glucose utilization, cell mass and total lipid titer in the transformants, suggesting further amelioration of the metabolic drain. In conclusion, this is the first study examining lipid production in cellulase-expressing Y. lipolytica strains under various C/N ratio media and with a chemical chaperone highlighting the metabolic complexity for developing robust, cellulolytic and lipogenic yeast strains.

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Research Organization:: National Renewable Energy Laboratory (NREL), Golden, CO (United States)

Sponsoring Organization:: USDOE Office of Energy Efficiency and Renewable Energy (EERE), Sustainable Transportation Office. Bioenergy Technologies Office (BETO)

Grant/Contract Number:: AC36-08GO28308

OSTI ID:: 1490107

Alternate ID(s):: OSTI ID: 1491724

Report Number(s):: NREL/JA-2700-73065; 3276

Journal Information:: Frontiers in Microbiology, Journal Name: Frontiers in Microbiology Vol. 9; ISSN 1664-302X

Publisher:: Frontiers Media SACopyright Statement

Country of Publication:: Switzerland

Language:: English

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Cited by: 13 works

Citation information provided by
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References (108)

Cloning and Expression of Trichoderma reesei Cellobiohydrolase I in Pichia pastoris Godbole, S.; Decker, S. R.; Nieves, R. A. Biotechnology Progress, Vol. 15, Issue 5 https://doi.org/10.1021/bp9901116	journal	October 1999
Assembling a cellulase cocktail and a cellodextrin transporter into a yeast host for CBP ethanol production Chang, Jui-Jen; Ho, Feng-Ju; Ho, Cheng-Yu Biotechnology for Biofuels, Vol. 6, Issue 1 https://doi.org/10.1186/1754-6834-6-19	journal	January 2013
Cloning and sequencing of the alkaline extracellular protease gene of Yarrowia lipolytica. Davidow, L. S.; O'Donnell, M. M.; Kaczmarek, F. S. Journal of Bacteriology, Vol. 169, Issue 10 https://doi.org/10.1128/jb.169.10.4621-4629.1987	journal	October 1987
Conferring cellulose-degrading ability to Yarrowia lipolytica to facilitate a consolidated bioprocessing approach Guo, Zhong-peng; Duquesne, Sophie; Bozonnet, Sophie Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0819-8	journal	May 2017
Strategic enhancement of algal biomass, nutrient uptake and lipid through statistical optimization of nutrient supplementation in coupling Scenedesmus obliquus-like microalgae cultivation and municipal wastewater treatment Zhang, Chunmin; Zhang, Yalei; Zhuang, Baolu Bioresource Technology, Vol. 171 https://doi.org/10.1016/j.biortech.2014.07.060	journal	November 2014
Integrating Cellular and Bioprocess Engineering in the Non-Conventional Yeast Yarrowia lipolytica for Biodiesel Production: A Review Xie, Dongming Frontiers in Bioengineering and Biotechnology, Vol. 5 https://doi.org/10.3389/fbioe.2017.00065	journal	October 2017
Heterologous protein expression in Hypocrea jecorina: A historical perspective and new developments Singh, Arjun; Taylor, Larry E.; Vander Wall, Todd A. Biotechnology Advances, Vol. 33, Issue 1 https://doi.org/10.1016/j.biotechadv.2014.11.009	journal	January 2015
Analyzing real-time PCR data by the comparative CT method Schmittgen, Thomas D.; Livak, Kenneth J. Nature Protocols, Vol. 3, Issue 6 https://doi.org/10.1038/nprot.2008.73	journal	June 2008
Stimulation of Lignocellulosic Biomass Hydrolysis by Proteins of Glycoside Hydrolase Family 61 Structure and Function of a Large, Enigmatic Family Harris, Paul; Welner, Ditte; McFarland, K. Biochemistry, Vol. 49, Issue 15, p. 3305-3316 https://doi.org/10.1021/bi100009p	journal	April 2010
Genomic, Proteomic, and Biochemical Analyses of Oleaginous Mucor circinelloides: Evaluating Its Capability in Utilizing Cellulolytic Substrates for Lipid Production Wei, Hui; Wang, Wei; Yarbrough, John M. PLoS ONE, Vol. 8, Issue 9 https://doi.org/10.1371/journal.pone.0071068	journal	September 2013
Heterologous Expression of Xylanase Enzymes in Lipogenic Yeast Yarrowia lipolytica Wang, Wei; Wei, Hui; Alahuhta, Markus PLoS ONE, Vol. 9, Issue 12 https://doi.org/10.1371/journal.pone.0111443	journal	December 2014
Expression and secretion of fungal endoglucanase II and chimeric cellobiohydrolase I in the oleaginous yeast Lipomyces starkeyi Xu, Qi; Knoshaug, Eric P.; Wang, Wei Microbial Cell Factories, Vol. 16, Issue 1 https://doi.org/10.1186/s12934-017-0742-5	journal	July 2017
Influence of dry and wet ball milling on dispersion characteristics of the multi-walled carbon nanotubes in aqueous solution with and without surfactant Munkhbayar, B.; Nine, Md. J.; Jeoun, Jinseong Powder Technology, Vol. 234 https://doi.org/10.1016/j.powtec.2012.09.045	journal	January 2013
Protein production and induction of the unfolded protein response in Trichoderma reesei strain Rut-C30 and its transformant expressing endoglucanase I with a hydrophobic tag : Protein Production by Collén, Anna; Saloheimo, Markku; Bailey, Michael Biotechnology and Bioengineering, Vol. 89, Issue 3 https://doi.org/10.1002/bit.20350	journal	December 2004
Inhibition of growth of Zymomonas mobilis by model compounds found in lignocellulosic hydrolysates Franden, Mary Ann; Pilath, Heidi M.; Mohagheghi, Ali Biotechnology for Biofuels, Vol. 6, Issue 1 https://doi.org/10.1186/1754-6834-6-99	journal	January 2013
Consolidated bioprocessing of cellulosic biomass: an update Lynd, Lee R.; van Zyl, Willem H.; McBride, John E. Current Opinion in Biotechnology, Vol. 16, Issue 5, p. 577-583 https://doi.org/10.1016/j.copbio.2005.08.009	journal	October 2005
Characterization of Trichoderma reesei cellobiohydrolase Cel7A secreted from Pichia pastoris using two different promoters Boer, Harry; Teeri, Tuula T.; Koivula, Anu Biotechnology and Bioengineering, Vol. 69, Issue 5, p. 486-494 https://doi.org/10.1002/1097-0290(20000905)69:5<486::AID-BIT3>3.0.CO;2-N	journal	January 2000
Evaluation of single cell oil (SCO) from a tropical marine yeast Yarrowia lipolytica NCIM 3589 as a potential feedstock for biodiesel Katre, Gouri; Joshi, Chirantan; Khot, Mahesh AMB Express, Vol. 2, Issue 1 https://doi.org/10.1186/2191-0855-2-36	journal	January 2012
Muscle LIM protein/CSRP3: a mechanosensor with a role in autophagy Rashid, M. M.; Runci, A.; Polletta, L. Cell Death Discovery, Vol. 1, Issue 1 https://doi.org/10.1038/cddiscovery.2015.14	journal	August 2015
Production of oils and fats by oleaginous microorganisms with an emphasis given to the potential of the nonconventional yeast Yarrowia lipolytica Carsanba, E.; Papanikolaou, S.; Erten, H. Critical Reviews in Biotechnology, Vol. 38, Issue 8 https://doi.org/10.1080/07388551.2018.1472065	journal	April 2018
An evolutionary metabolic engineering approach for enhancing lipogenesis in Yarrowia lipolytica Liu, Leqian; Pan, Anny; Spofford, Caitlin Metabolic Engineering, Vol. 29 https://doi.org/10.1016/j.ymben.2015.02.003	journal	May 2015
Autophagy provides nutrients for nonassimilating fungal structures and is necessary for plant colonization but not for infection in the necrotrophic plant pathogen Fusarium graminearum Josefsen, Lone; Droce, Aida; Sondergaard, Teis Esben Autophagy, Vol. 8, Issue 3 https://doi.org/10.4161/auto.18705	journal	March 2012
SGAtools: one-stop analysis and visualization of array-based genetic interaction screens Wagih, Omar; Usaj, Matej; Baryshnikova, Anastasia Nucleic Acids Research, Vol. 41, Issue W1 https://doi.org/10.1093/nar/gkt400	journal	May 2013
Overexpression of native Saccharomyces cerevisiae ER-to-Golgi SNARE genes increased heterologous cellulase secretion Van Zyl, John Henry D.; Den Haan, Riaan; Van Zyl, Willem H. Applied Microbiology and Biotechnology, Vol. 100, Issue 1 https://doi.org/10.1007/s00253-015-7022-2	journal	October 2015
Magnesium Ions Improve Growth and Ethanol Production of Zymomonas mobilis under Heat or Ethanol Stress ., Pornthap Thanonkeo; ., Pattana Laopaiboon; ., Kaewta Sootsuwan Biotechnology(Faisalabad), Vol. 6, Issue 1 https://doi.org/10.3923/biotech.2007.112.119	journal	January 2007
Metabolic engineering of Yarrowia lipolytica to produce chemicals and fuels from xylose Ledesma-Amaro, Rodrigo; Lazar, Zbigniew; Rakicka, Magdalena Metabolic Engineering, Vol. 38 https://doi.org/10.1016/j.ymben.2016.07.001	journal	November 2016
Enzymatic hydrolysis of maize straw polysaccharides for the production of reducing sugars Chen, M.; Zhao, J.; Xia, L. Carbohydrate Polymers, Vol. 71, Issue 3 https://doi.org/10.1016/j.carbpol.2007.06.011	journal	February 2008
Development and physiological characterization of cellobiose-consuming Yarrowia lipolytica : Development and Physiological Characterization Lane, Stephan; Zhang, Shuyan; Wei, Na Biotechnology and Bioengineering, Vol. 112, Issue 5 https://doi.org/10.1002/bit.25499	journal	January 2015
Extra metabolic burden by displaying over secreting: Growth, fermentation and enzymatic activity in cellobiose of recombinant yeast expressing β-glucosidase Ding, Juanjuan; Liang, Guohong; Zhang, Kun Bioresource Technology, Vol. 254 https://doi.org/10.1016/j.biortech.2017.12.030	journal	April 2018
Efficient direct ethanol production from cellulose by cellulase- and cellodextrin transporter-co-expressing Saccharomyces cerevisiae Yamada, Ryosuke; Nakatani, Yuki; Ogino, Chiaki AMB Express, Vol. 3, Issue 1 https://doi.org/10.1186/2191-0855-3-34	journal	January 2013
The metabolic burden of cellulase expression by recombinant Saccharomyces cerevisiae Y294 in aerobic batch culture van Rensburg, Eugéne; den Haan, Riaan; Smith, Justin Applied Microbiology and Biotechnology, Vol. 96, Issue 1 https://doi.org/10.1007/s00253-012-4037-9	journal	April 2012
Activating and Elucidating Metabolism of Complex Sugars in Yarrowia lipolytica Ryu, Seunghyun; Hipp, Julie; Trinh, Cong T. Applied and Environmental Microbiology, Vol. 82, Issue 4 https://doi.org/10.1128/AEM.03582-15	journal	December 2015
Methods for measuring cellulase activities Wood, Thomas M.; Bhat, K. Mahalingeshwara Methods in Enzymology, Vol. 160, p. 87-112 https://doi.org/10.1016/0076-6879(88)60109-1	journal	January 1988
Acceleration of ethanol production from paper mill waste fiber by supplementation with β-glucosidase Xin, Zhao; Yinbo, Qu; Peiji, Gao Enzyme and Microbial Technology, Vol. 15, Issue 1 https://doi.org/10.1016/0141-0229(93)90117-K	journal	January 1993
Self-surface assembly of cellulosomes with two miniscaffoldins on Saccharomyces cerevisiae for cellulosic ethanol production Fan, L. -H.; Zhang, Z. -J.; Yu, X. -Y. Proceedings of the National Academy of Sciences, Vol. 109, Issue 33 https://doi.org/10.1073/pnas.1209856109	journal	August 2012
Carotenoid and fatty acid metabolism in nitrogen-starved Dunaliella salina, a unicellular green microalga Lamers, Packo P.; Janssen, Marcel; De Vos, Ric C. H. Journal of Biotechnology, Vol. 162, Issue 1 https://doi.org/10.1016/j.jbiotec.2012.04.018	journal	November 2012
Effects of nitrogen sources on cell growth and lipid accumulation of green alga Neochloris oleoabundans Li, Yanqun; Horsman, Mark; Wang, Bei Applied Microbiology and Biotechnology, Vol. 81, Issue 4 https://doi.org/10.1007/s00253-008-1681-1	journal	September 2008
Engineering xylose utilization in Yarrowia lipolytica by understanding its cryptic xylose pathway Rodriguez, Gabriel M.; Hussain, Murtaza Shabbir; Gambill, Lauren Biotechnology for Biofuels, Vol. 9, Issue 1 https://doi.org/10.1186/s13068-016-0562-6	journal	July 2016
Monitoring Rhodosporidium toruloides NCYC 921 batch fermentations growing under carbon and nitrogen limitation by flow cytometry Andrade, Raoni; Leal, Rodrigo; Roseiro, José World Journal of Microbiology and Biotechnology, Vol. 28, Issue 3 https://doi.org/10.1007/s11274-011-0920-2	journal	October 2011
Engineering towards a complete heterologous cellulase secretome in Yarrowia lipolytica reveals its potential for consolidated bioprocessing Wei, Hui; Wang, Wei; Alahuhta, Markus Biotechnology for Biofuels, Vol. 7, Issue 1 https://doi.org/10.1186/s13068-014-0148-0	journal	October 2014
Manipulation of culture conditions alters lipid content and fatty acid profiles of a wide variety of known and new oleaginous yeast species Sitepu, Irnayuli R.; Sestric, Ryan; Ignatia, Laura Bioresource Technology, Vol. 144 https://doi.org/10.1016/j.biortech.2013.06.047	journal	September 2013
Simultaneous production of citric acid and invertase by Yarrowia lipolytica SUC+ transformants Lazar, Zbigniew; Walczak, Ewa; Robak, Małgorzata Bioresource Technology, Vol. 102, Issue 13 https://doi.org/10.1016/j.biortech.2011.04.032	journal	July 2011
Tracking dynamics of plant biomass composting by changes in substrate structure, microbial community, and enzyme activity Wei, Hui; Tucker, Melvin P.; Baker, John O. Biotechnology for Biofuels, Vol. 5, Issue 1 https://doi.org/10.1186/1754-6834-5-20	journal	January 2012
Direct Conversion of Xylan to Ethanol by Recombinant Saccharomyces cerevisiae Strains Displaying an Engineered Minihemicellulosome Sun, Jie; Wen, Fei; Si, Tong Applied and Environmental Microbiology, Vol. 78, Issue 11 https://doi.org/10.1128/AEM.07679-11	journal	March 2012
Immobilization of Recombinant Invertase (re-INVB) from Zymomonas mobilis on d -Sorbitol Cinnamic Ester for Production of Invert Sugar Vallejo-Becerra, Vanessa; Marín-Zamora, María Elisa; Vásquez-Bahena, Jazmin Magdalena Journal of Agricultural and Food Chemistry, Vol. 56, Issue 4 https://doi.org/10.1021/jf072646h	journal	February 2008
Maximizing biodiesel production from Yarrowia lipolytica Po1g biomass using subcritical water pretreatment Tsigie, Yeshitila Asteraye; Huynh, Lien Huong; Ahmed, Ibrahim Nasser Bioresource Technology, Vol. 111 https://doi.org/10.1016/j.biortech.2012.02.052	journal	May 2012
Hydrolysis and fermentation of amorphous cellulose by recombinant Saccharomyces cerevisiae Den Haan, Riaan; Rose, Shaunita H.; Lynd, Lee R. Metabolic Engineering, Vol. 9, Issue 1, p. 87-94 https://doi.org/10.1016/j.ymben.2006.08.005	journal	January 2007
Enabling xylose utilization in Yarrowia lipolytica for lipid production Li, Haibo; Alper, Hal S. Biotechnology Journal, Vol. 11, Issue 9 https://doi.org/10.1002/biot.201600210	journal	July 2016
The Spatial Organization of Lipid Synthesis in the Yeast Saccharomyces cerevisiae Derived from Large Scale Green Fluorescent Protein Tagging and High Resolution Microscopy Natter, Klaus; Leitner, Peter; Faschinger, Alexander Molecular & Cellular Proteomics, Vol. 4, Issue 5 https://doi.org/10.1074/mcp.M400123-MCP200	journal	February 2005
Development of a high-throughput method to evaluate the impact of inhibitory compounds from lignocellulosic hydrolysates on the growth of Zymomonas mobilis Franden, Mary Ann; Pienkos, Philip T.; Zhang, Min Journal of Biotechnology, Vol. 144, Issue 4 https://doi.org/10.1016/j.jbiotec.2009.08.006	journal	December 2009
Yeast recombination: the association between double-strand gap repair and crossing-over. Orr-Weaver, T. L.; Szostak, J. W. Proceedings of the National Academy of Sciences, Vol. 80, Issue 14 https://doi.org/10.1073/pnas.80.14.4417	journal	July 1983
A novel strain of Yarrowia lipolytica as a platform for value-added product synthesis from glycerol Mirończuk, Aleksandra M.; Rzechonek, Dorota A.; Biegalska, Anna Biotechnology for Biofuels, Vol. 9, Issue 1 https://doi.org/10.1186/s13068-016-0593-z	journal	August 2016
A conserved family of proteins facilitates nascent lipid droplet budding from the ER Choudhary, Vineet; Ojha, Namrata; Golden, Andy The Journal of Cell Biology, Vol. 211, Issue 2 https://doi.org/10.1083/jcb.201505067	journal	October 2015
Simultaneous saccharification and fermentation of cellulose in ionic liquid for efficient production of α-ketoglutaric acid by Yarrowia lipolytica Ryu, Seunghyun; Labbé, Nicole; Trinh, Cong T. Applied Microbiology and Biotechnology, Vol. 99, Issue 10 https://doi.org/10.1007/s00253-015-6521-5	journal	March 2015
Comparison of the Heterologous Expression of Trichoderma reesei Endoglucanase II and Cellobiohydrolase II in the Yeasts Pichia pastoris and Yarrowia lipolytica Boonvitthya, Nassapat; Bozonnet, Sophie; Burapatana, Vorakan Molecular Biotechnology, Vol. 54, Issue 2 https://doi.org/10.1007/s12033-012-9557-0	journal	May 2012
Genetic suppression of HO-1 exacerbates renal damage: reversed by an increase in the antiapoptotic signaling pathway Olszanecki, Rafal; Rezzani, Rita; Omura, Shinji American Journal of Physiology-Renal Physiology, Vol. 292, Issue 1 https://doi.org/10.1152/ajprenal.00261.2006	journal	January 2007
Optimization of enzyme complexes for lignocellulose hydrolysis Berlin, Alex; Maximenko, Vera; Gilkes, Neil Biotechnology and Bioengineering, Vol. 97, Issue 2, p. 287-296 https://doi.org/10.1002/bit.21238	journal	January 2007
Unraveling fatty acid transport and activation mechanisms in Yarrowia lipolytica Dulermo, Rémi; Gamboa-Meléndez, Heber; Ledesma-Amaro, Rodrigo Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, Vol. 1851, Issue 9 https://doi.org/10.1016/j.bbalip.2015.04.004	journal	September 2015
Cellobiohydrolase secretion by yeast: Current state and prospects for improvement den Haan, Riaan; Kroukamp, Heinrich; van Zyl, John-Henry D. Process Biochemistry, Vol. 48, Issue 1 https://doi.org/10.1016/j.procbio.2012.11.015	journal	January 2013
Connecting lignin-degradation pathway with pre-treatment inhibitor sensitivity of Cupriavidus necator Wang, Wei; Yang, Shihui; Hunsinger, Glendon B. Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00247	journal	May 2014
Integration event induced changes in recombinant protein productivity in Pichia pastoris discovered by whole genome sequencing and derived vector optimization Schwarzhans, Jan-Philipp; Wibberg, Daniel; Winkler, Anika Microbial Cell Factories, Vol. 15, Issue 1 https://doi.org/10.1186/s12934-016-0486-7	journal	May 2016
Investigation of combined effect of nitrogen, phosphorus and iron on lipid productivity of microalgae Ankistrodesmus falcatus KJ671624 using response surface methodology Singh, Poonam; Guldhe, Abhishek; Kumari, Sheena Biochemical Engineering Journal, Vol. 94 https://doi.org/10.1016/j.bej.2014.10.019	journal	February 2015
Sorbitol required for cell growth and ethanol production by Zymomonas mobilis under heat, ethanol, and osmotic stresses Sootsuwan, Kaewta; Thanonkeo, Pornthap; Keeratirakha, Nawapote Biotechnology for Biofuels, Vol. 6, Issue 1 https://doi.org/10.1186/1754-6834-6-180	journal	January 2013
Yarrowia lipolytica as a biotechnological chassis to produce usual and unusual fatty acids Ledesma-Amaro, Rodrigo; Nicaud, Jean-Marc Progress in Lipid Research, Vol. 61 https://doi.org/10.1016/j.plipres.2015.12.001	journal	January 2016
High-throughput fermentation screening for the yeast Yarrowia lipolytica with real-time monitoring of biomass and lipid production Back, Alexandre; Rossignol, Tristan; Krier, François Microbial Cell Factories, Vol. 15, Issue 1 https://doi.org/10.1186/s12934-016-0546-z	journal	August 2016
Effect of different C/N ratios on carotenoid and lipid production by Rhodotorula glutinis Braunwald, Teresa; Schwemmlein, Lisa; Graeff-Hönninger, Simone Applied Microbiology and Biotechnology, Vol. 97, Issue 14 https://doi.org/10.1007/s00253-013-5005-8	journal	June 2013
Functional overexpression of genes involved in erythritol synthesis in the yeast Yarrowia lipolytica Mirończuk, Aleksandra M.; Biegalska, Anna; Dobrowolski, Adam Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0772-6	journal	March 2017
Reduction of trimethylamine N-oxide byEscherichia coli as anaerobic respiration Ishimoto, M.; Shimokawa, O. Zeitschrift für allgemeine Mikrobiologie, Vol. 18, Issue 3 https://doi.org/10.1002/jobm.3630180304	journal	January 1978
Lipid droplets are functionally connected to the endoplasmic reticulum in Saccharomyces cerevisiae Jacquier, N.; Choudhary, V.; Mari, M. Journal of Cell Science, Vol. 124, Issue 14 https://doi.org/10.1242/jcs.076836	journal	June 2011
Acidophilic Green Alga Pseudochlorella sp. YKT1 Accumulates High Amount of Lipid Droplets under a Nitrogen-Depleted Condition at a Low-pH Hirooka, Shunsuke; Higuchi, Sumio; Uzuka, Akihiro PLoS ONE, Vol. 9, Issue 9 https://doi.org/10.1371/journal.pone.0107702	journal	September 2014
Trends and novel strategies for enhancing lipid accumulation and quality in microalgae Singh, Poonam; Kumari, Sheena; Guldhe, Abhishek Renewable and Sustainable Energy Reviews, Vol. 55 https://doi.org/10.1016/j.rser.2015.11.001	journal	March 2016
Transfer hydrogenation of cellulose to sugar alcohols over supported ruthenium catalysts Kobayashi, Hirokazu; Matsuhashi, Hisateru; Komanoya, Tasuku Chem. Commun., Vol. 47, Issue 8 https://doi.org/10.1039/c0cc04311g	journal	January 2011
High level secretion of cellobiohydrolases by Saccharomyces cerevisiae Ilmén, Marja; den Haan, Riaan; Brevnova, Elena Biotechnology for Biofuels, Vol. 4, Issue 1 https://doi.org/10.1186/1754-6834-4-30	journal	January 2011
Biomass Recalcitrance: Engineering Plants and Enzymes for Biofuels Production Himmel, M. E.; Ding, S.-Y.; Johnson, D. K. Science, Vol. 315, Issue 5813, p. 804-807 https://doi.org/10.1126/science.1137016	journal	February 2007
Effects of wet ball-milling on particle dispersion and mechanical properties of particulate epoxy composites Hussain, M.; Oku, Y.; Nakahira, A. Materials Letters, Vol. 26, Issue 3 https://doi.org/10.1016/0167-577X(95)00223-5	journal	February 1996
Efficient conversion of crude glycerol from various industrial wastes into single cell oil by yeast Yarrowia lipolytica Dobrowolski, Adam; Mituła, Paweł; Rymowicz, Waldemar Bioresource Technology, Vol. 207 https://doi.org/10.1016/j.biortech.2016.02.039	journal	May 2016
Trimethylamine oxide reduction by Salmonella Kim, Kyung Eun; Chang, George W. Canadian Journal of Microbiology, Vol. 20, Issue 12 https://doi.org/10.1139/m74-269	journal	December 1974
Comparison of Nitrogen Depletion and Repletion on Lipid Production in Yeast and Fungal Species Yang, Shihui; Wang, Wei; Wei, Hui Energies, Vol. 9, Issue 9 https://doi.org/10.3390/en9090685	journal	August 2016
Genome-wide analysis of the endoplasmic reticulum stress response during lignocellulase production in Neurospora crassa Fan, Feiyu; Ma, Guoli; Li, Jingen Biotechnology for Biofuels, Vol. 8, Issue 1 https://doi.org/10.1186/s13068-015-0248-5	journal	April 2015
Comprehensive Metabolomic, Lipidomic and Microscopic Profiling of Yarrowia lipolytica during Lipid Accumulation Identifies Targets for Increased Lipogenesis Pomraning, Kyle R.; Wei, Siwei; Karagiosis, Sue A. PLOS ONE, Vol. 10, Issue 4 https://doi.org/10.1371/journal.pone.0123188	journal	April 2015
Secretory Protein Biogenesis and Traffic in the Early Secretory Pathway Barlowe, Charles K.; Miller, Elizabeth A. Genetics, Vol. 193, Issue 2 https://doi.org/10.1534/genetics.112.142810	journal	February 2013
Enzymatic properties of cellulases from Humicola insolens Schülein, Martin Journal of Biotechnology, Vol. 57, Issue 1-3, p. 71-81 https://doi.org/10.1016/S0168-1656(97)00090-4	journal	September 1997
High Lipid Induction in Microalgae for Biodiesel Production Sharma, Kalpesh K.; Schuhmann, Holger; Schenk, Peer M. Energies, Vol. 5, Issue 5 https://doi.org/10.3390/en5051532	journal	May 2012
Protocols and Programs for High-Throughput Growth and Aging Phenotyping in Yeast Jung, Paul P.; Christian, Nils; Kay, Daniel P. PLOS ONE, Vol. 10, Issue 3 https://doi.org/10.1371/journal.pone.0119807	journal	March 2015
Engineering the push and pull of lipid biosynthesis in oleaginous yeast Yarrowia lipolytica for biofuel production Tai, Mitchell; Stephanopoulos, Gregory Metabolic Engineering, Vol. 15, p. 1-9 https://doi.org/10.1016/j.ymben.2012.08.007	journal	January 2013
Expression of oleosin and perilipins in yeast promotes formation of lipid droplets from the endoplasmic reticulum Jacquier, N.; Mishra, S.; Choudhary, V. Journal of Cell Science, Vol. 126, Issue 22 https://doi.org/10.1242/jcs.131896	journal	September 2013
Recent progress in consolidated bioprocessing Olson, Daniel G.; McBride, John E.; Joe Shaw, A. Current Opinion in Biotechnology, Vol. 23, Issue 3, p. 396-405 https://doi.org/10.1016/j.copbio.2011.11.026	journal	June 2012
Chemicals to enhance microalgal growth and accumulation of high-value bioproducts Yu, Xinheng; Chen, Lei; Zhang, Weiwen Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00056	journal	February 2015
Understanding the metabolic burden of recombinant antibody production in Saccharomyces cerevisiae using a quantitative metabolomics approach de Ruijter, Jorg C.; Koskela, Essi V.; Nandania, Jatin Yeast, Vol. 35, Issue 4 https://doi.org/10.1002/yea.3298	journal	January 2018
Correlating the ability of lignocellulosic polymers to constrain water with the potential to inhibit cellulose saccharification Selig, Michael J.; Thygesen, Lisbeth G.; Felby, Claus Biotechnology for Biofuels, Vol. 7, Issue 1 https://doi.org/10.1186/s13068-014-0159-x	journal	November 2014
Overexpression of an exotic thermotolerant β-glucosidase in trichoderma reesei and its significant increase in cellulolytic activity and saccharification of barley straw Dashtban, Mehdi; Qin, Wensheng Microbial Cell Factories, Vol. 11, Issue 1 https://doi.org/10.1186/1475-2859-11-63	journal	January 2012
Metabolic engineering of Yarrowia lipolytica for industrial applications Zhu, Quinn; Jackson, Ethel N. Current Opinion in Biotechnology, Vol. 36 https://doi.org/10.1016/j.copbio.2015.08.010	journal	December 2015
Genetic engineering of Yarrowia lipolytica for enhanced production of trans-10, cis-12 conjugated linoleic acid Zhang, Baixi; Chen, Haiqin; Li, Min Microbial Cell Factories, Vol. 12, Issue 1 https://doi.org/10.1186/1475-2859-12-70	journal	January 2013
Yarrowia lipolytica as an Oleaginous Cell Factory Platform for Production of Fatty Acid-Based Biofuel and Bioproducts Abghari, Ali; Chen, Shulin Frontiers in Energy Research, Vol. 2 https://doi.org/10.3389/FENRG.2014.00021	journal	June 2014
The exopolysaccharides biosynthesis by Candida yeast depends on carbon sources Gientka, Iwona; Bzducha-Wróbel, Anna; Stasiak-Różańska, Lidia Electronic Journal of Biotechnology, Vol. 22 https://doi.org/10.1016/j.ejbt.2016.02.008	journal	July 2016
Metabolic engineering of yeasts by heterologous enzyme production for degradation of cellulose and hemicellulose from biomass: a perspective Kricka, William; Fitzpatrick, James; Bond, Ursula Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00174	journal	April 2014
Design and characterisation of synthetic operons for biohydrogen technology Lamont, Ciaran M.; Sargent, Frank Archives of Microbiology, Vol. 199, Issue 3 https://doi.org/10.1007/s00203-016-1322-5	journal	November 2016
Influence of ylHog1 MAPK kinase on Yarrowia lipolytica stress response and erythritol production Rzechonek, Dorota A.; Day, Alison M.; Quinn, Janet Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-33168-6	journal	October 2018
Metabolic engineering in the host Yarrowia lipolytica Abdel-Mawgoud, Ahmad M.; Markham, Kelly A.; Palmer, Claire M. Metabolic Engineering, Vol. 50 https://doi.org/10.1016/j.ymben.2018.07.016	journal	November 2018
Effects of varying media, temperature, and growth rates on the intracellular concentrations of yeast amino acids Martinez-Force, Enrique; Benitez, Tahia Biotechnology Progress, Vol. 11, Issue 4 https://doi.org/10.1021/bp00034a004	journal	July 1995
Development of cellobiose-degrading ability in Yarrowia lipolytica strain by overexpression of endogenous genes Guo, Zhongpeng; Duquesne, Sophie; Bozonnet, Sophie Biotechnology for Biofuels, Vol. 8, Issue 1 https://doi.org/10.1186/s13068-015-0289-9	journal	August 2015
Mixtures of Thermostable Enzymes Show High Performance in Biomass Saccharification Kallioinen, Anne; Puranen, Terhi; Siika-aho, Matti Applied Biochemistry and Biotechnology, Vol. 173, Issue 5 https://doi.org/10.1007/s12010-014-0893-3	journal	April 2014
The Biochemistry and Molecular Biology of Lipid Accumulation in Oleaginous Microorganisms Ratledge, Colin; Wynn, James P. Advances in Applied Microbiology https://doi.org/10.1016/S0065-2164(02)51000-5	book	January 2002
Yarrowia lipolytica and Its Multiple Applications in the Biotechnological Industry Gonçalves, F. A. G.; Colen, G.; Takahashi, J. A. The Scientific World Journal, Vol. 2014 https://doi.org/10.1155/2014/476207	journal	January 2014
Conditions of endoplasmic reticulum stress stimulate lipid droplet formation in Saccharomyces cerevisiae Fei, Weihua; Wang, Han; Fu, Xin Biochemical Journal, Vol. 424, Issue 1 https://doi.org/10.1042/BJ20090785	journal	October 2009
Quantitative analysis of fitness and genetic interactions in yeast on a genome scale Baryshnikova, Anastasia; Costanzo, Michael; Kim, Yungil Nature Methods, Vol. 7, Issue 12 https://doi.org/10.1038/nmeth.1534	journal	November 2010
Harnessing Yarrowia lipolytica lipogenesis to create a platform for lipid and biofuel production Blazeck, John; Hill, Andrew; Liu, Leqian Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4131	journal	January 2014
Oleaginous yeasts for biodiesel: Current and future trends in biology and production Sitepu, Irnayuli R.; Garay, Luis A.; Sestric, Ryan Biotechnology Advances, Vol. 32, Issue 7 https://doi.org/10.1016/j.biotechadv.2014.08.003	journal	November 2014

Cited By (1)

Metabolomic Alterations Do Not Induce Metabolic Burden in the Industrial Yeast M2n[pBKD2-Pccbgl1]-C1 Engineered by Multiple δ-Integration of a Fungal β-Glucosidase Gene Favaro, Lorenzo; Cagnin, Lorenzo; Corte, Laura Frontiers in Bioengineering and Biotechnology, Vol. 7 https://doi.org/10.3389/fbioe.2019.00376	journal	November 2019

Figures / Tables (11)

, YL101 expressing EG II. Lane 3, strain HA1 (transformed with empty vector). Lane 4, YL165-1. Loading amount was 22.5 μL supernatant per well. Cellulase titers (g L^-1) are indicated by numbers in the western blot images." data-ostiid="1490107">

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Related Subjects

09 BIOMASS FUELS
fungal cellulolytic enzymes
Yarrowia lipolytica
cellulosic biofuel
cellobiohydrolase I
endoglucanase II
lipid metabolism
endoplasmic reticulum stress
chemical chaperone