Evaluating proteome allocation of Saccharomyces cerevisiae phenotypes with resource balance analysis

Dinh, Hoang V.; Maranas, Costas D.

doi:10.1016/j.ymben.2023.04.009

Title: Evaluating proteome allocation of Saccharomyces cerevisiae phenotypes with resource balance analysis

Journal Article · 18 April 2023 · Metabolic Engineering

DOI: https://doi.org/10.1016/j.ymben.2023.04.009 · OSTI ID:1993844

Dinh, Hoang V. ^[1];

^[2]

Pennsylvania State University, University Park, PA (United States); University of Illinois
Pennsylvania State University, University Park, PA (United States)

Saccharomyces cerevisiae is an important model organism and a workhorse in bioproduction. Here, we reconstructed a compact and tractable genome-scale resource balance analysis (RBA) model (i.e., named scRBA) to analyze metabolic fluxes and proteome allocation in a computationally efficient manner. Resource capacity models such as scRBA provide the quantitative means to identify bottlenecks in biosynthetic pathways due to enzyme, compartment size, and/or ribosome availability limitations. ATP maintenance rate and in vivo apparent turnover numbers (k_app) were regressed from metabolic flux and protein concentration data to capture observed physiological growth yield and proteome efficiency and allocation, respectively. Estimated parameter values were found to vary with oxygen and nutrient availability. Altogether, this work (i) provides condition-specific model parameters to recapitulate phenotypes corresponding to different extracellular environments, (ii) alludes to the enhancing effect of substrate channeling and post-translational activation on in vivo enzyme efficiency in glycolysis and electron transport chain, and (iii) reveals that the Crabtree effect is underpinned by specific limitations in mitochondrial proteome capacity and secondarily ribosome availability rather than overall proteome capacity.

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Research Organization:: Center for Advanced Bioenergy and Bioproducts Innovation (CABBI), Urbana, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: SC0018420

OSTI ID:: 1993844

Journal Information:: Metabolic Engineering, Journal Name: Metabolic Engineering Vol. 77; ISSN 1096-7176

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (116)

The proteasome: friend and foe of mitochondrial biogenesis Krämer, Lena; Groh, Carina; Herrmann, Johannes M. FEBS Letters, Vol. 595, Issue 8 https://doi.org/10.1002/1873-3468.14010	journal	December 2020
Yeast Systems Biology: Model Organism and Cell Factory Nielsen, Jens Biotechnology Journal, Vol. 14, Issue 9 https://doi.org/10.1002/biot.201800421	journal	May 2019
Statistical reconciliation of the elemental and molecular biomass composition ofSaccharomyces cerevisiae Lange, H. C.; Heijnen, J. J. Biotechnology and Bioengineering, Vol. 75, Issue 3 https://doi.org/10.1002/bit.10054	journal	January 2001
Toward “homolactic” fermentation of glucose and xylose by engineered Saccharomyces cerevisiae harboring a kinetically efficient l -lactate dehydrogenase within pdc1 - pdc5 deletion background: l -Lactic Acid Production From Glucose and Xylose Novy, Vera; Brunner, Bernd; Müller, Gerdt Biotechnology and Bioengineering, Vol. 114, Issue 1 https://doi.org/10.1002/bit.26048	journal	July 2016
Comprehensive understanding of Saccharomyces cerevisiae phenotypes with whole‐cell model WM_S288C Ye, Chao; Xu, Nan; Gao, Cong Biotechnology and Bioengineering, Vol. 117, Issue 5 https://doi.org/10.1002/bit.27298	journal	February 2020
Continuous measurement of ethanol production by aerobic yeast suspensions with an enzyme electrode Verduyn, Cornelis; Zomerdijk, Timotheus P. L.; van Dijken, Johannes P. Applied Microbiology and Biotechnology, Vol. 19, Issue 3 https://doi.org/10.1007/BF00256451	journal	March 1984
Metabolic engineering of Saccharomyces cerevisiae: a key cell factory platform for future biorefineries Hong, Kuk-Ki; Nielsen, Jens Cellular and Molecular Life Sciences, Vol. 69, Issue 16 https://doi.org/10.1007/s00018-012-0945-1	journal	March 2012
Saccharomyces cerevisiae: a potential host for carboxylic acid production from lignocellulosic feedstock? Sandström, Anders G.; Almqvist, Henrik; Portugal-Nunes, Diogo Applied Microbiology and Biotechnology, Vol. 98, Issue 17 https://doi.org/10.1007/s00253-014-5866-5	journal	June 2014
Enhanced production of para-hydroxybenzoic acid by genetically engineered Saccharomyces cerevisiae Averesch, Nils J. H.; Prima, Alex; Krömer, Jens O. Bioprocess and Biosystems Engineering, Vol. 40, Issue 8 https://doi.org/10.1007/s00449-017-1785-z	journal	May 2017
Construction of advanced producers of first- and second-generation ethanol in Saccharomyces cerevisiae and selected species of non-conventional yeasts (Scheffersomyces stipitis, Ogataea polymorpha) Ruchala, Justyna; Kurylenko, Olena O.; Dmytruk, Kostyantyn V. Journal of Industrial Microbiology & Biotechnology, Vol. 47, Issue 1 https://doi.org/10.1007/s10295-019-02242-x	journal	October 2019
The complete sequence of the mitochondrial genome of Saccharomyces cerevisiae Foury, Françoise; Roganti, Tiziana; Lecrenier, Nicolas FEBS Letters, Vol. 440, Issue 3 https://doi.org/10.1016/S0014-5793(98)01467-7	journal	December 1998
Mitochondrial biogenesis: The Tom and Tim machine Pfanner, Nikolaus; Meijer, Michiel Current Biology, Vol. 7, Issue 2 https://doi.org/10.1016/S0960-9822(06)00048-0	journal	February 1997
The economics of ribosome biosynthesis in yeast Warner, Jonathan R. Trends in Biochemical Sciences, Vol. 24, Issue 11 https://doi.org/10.1016/S0968-0004(99)01460-7	journal	November 1999
Cell design in bacteria as a convex optimization problem Goelzer, Anne; Fromion, Vincent; Scorletti, Gérard Automatica, Vol. 47, Issue 6 https://doi.org/10.1016/j.automatica.2011.02.038	journal	June 2011
Reprogramming Yeast Metabolism from Alcoholic Fermentation to Lipogenesis Yu, Tao; Zhou, Yongjin J.; Huang, Mingtao Cell, Vol. 174, Issue 6 https://doi.org/10.1016/j.cell.2018.07.013	journal	September 2018
Cell Factory Engineering Davy, Anne Mathilde; Kildegaard, Helene Faustrup; Andersen, Mikael Rørdam Cell Systems, Vol. 4, Issue 3 https://doi.org/10.1016/j.cels.2017.02.010	journal	March 2017
Absolute Quantification of Protein and mRNA Abundances Demonstrate Variability in Gene-Specific Translation Efficiency in Yeast Lahtvee, Petri-Jaan; Sánchez, Benjamín J.; Smialowska, Agata Cell Systems, Vol. 4, Issue 5 https://doi.org/10.1016/j.cels.2017.03.003	journal	May 2017
Building kinetic models for metabolic engineering Foster, Charles J.; Wang, Lin; Dinh, Hoang V. Current Opinion in Biotechnology, Vol. 67 https://doi.org/10.1016/j.copbio.2020.11.010	journal	February 2021
Production of reactive oxygen species and loss of viability in yeast mitochondrial mutants: protective effect of Bcl-x Trancikova, A.; Weisova, P.; Kissova, I. FEMS Yeast Research, Vol. 5, Issue 2 https://doi.org/10.1016/j.femsyr.2004.06.014	journal	November 2004
Advanced Strategies for Production of Natural Products in Yeast Chen, Ruibing; Yang, Shan; Zhang, Lei iScience, Vol. 23, Issue 3 https://doi.org/10.1016/j.isci.2020.100879	journal	March 2020
Metabolic engineering of microorganisms for biofuel production Majidian, Parastoo; Tabatabaei, Meisam; Zeinolabedini, Mehrshad Renewable and Sustainable Energy Reviews, Vol. 82 https://doi.org/10.1016/j.rser.2017.10.085	journal	February 2018
The Warburg Effect: How Does it Benefit Cancer Cells? Liberti, Maria V.; Locasale, Jason W. Trends in Biochemical Sciences, Vol. 41, Issue 3 https://doi.org/10.1016/j.tibs.2015.12.001	journal	March 2016
The effects of alternate optimal solutions in constraint-based genome-scale metabolic models Mahadevan, R.; Schilling, C. H. Metabolic Engineering, Vol. 5, Issue 4 https://doi.org/10.1016/j.ymben.2003.09.002	journal	October 2003
Metabolic engineering of Saccharomyces cerevisiae for the biotechnological production of succinic acid Raab, Andreas M.; Gebhardt, Gabi; Bolotina, Natalia Metabolic Engineering, Vol. 12, Issue 6 https://doi.org/10.1016/j.ymben.2010.08.005	journal	November 2010
Establishing a synthetic pathway for high-level production of 3-hydroxypropionic acid in Saccharomyces cerevisiae via β-alanine Borodina, Irina; Kildegaard, Kanchana R.; Jensen, Niels B. Metabolic Engineering, Vol. 27 https://doi.org/10.1016/j.ymben.2014.10.003	journal	January 2015
De novo production of resveratrol from glucose or ethanol by engineered Saccharomyces cerevisiae Li, Mingji; Kildegaard, Kanchana R.; Chen, Yun Metabolic Engineering, Vol. 32 https://doi.org/10.1016/j.ymben.2015.08.007	journal	November 2015
Engineering cofactor and transport mechanisms in Saccharomyces cerevisiae for enhanced acetyl-CoA and polyketide biosynthesis Cardenas, Javier; Da Silva, Nancy A. Metabolic Engineering, Vol. 36 https://doi.org/10.1016/j.ymben.2016.02.009	journal	July 2016
Multilevel engineering of the upstream module of aromatic amino acid biosynthesis in Saccharomyces cerevisiae for high production of polymer and drug precursors Suástegui, Miguel; Yu Ng, Chiam; Chowdhury, Anupam Metabolic Engineering, Vol. 42 https://doi.org/10.1016/j.ymben.2017.06.008	journal	July 2017
Connecting central carbon and aromatic amino acid metabolisms to improve de novo 2-phenylethanol production in Saccharomyces cerevisiae Hassing, Else-Jasmijn; de Groot, Philip A.; Marquenie, Vita R. Metabolic Engineering, Vol. 56 https://doi.org/10.1016/j.ymben.2019.09.011	journal	December 2019
Quantifying the propagation of parametric uncertainty on flux balance analysis Dinh, Hoang V.; Sarkar, Debolina; Maranas, Costas D. Metabolic Engineering, Vol. 69 https://doi.org/10.1016/j.ymben.2021.10.012	journal	January 2022
Synthetic Biology of Yeast Liu, Zihe; Zhang, Yueping; Nielsen, Jens Biochemistry, Vol. 58, Issue 11 https://doi.org/10.1021/acs.biochem.8b01236	journal	January 2019
Efficient Biosynthesis of (2S)-Naringenin from p-Coumaric Acid in Saccharomyces cerevisiae Gao, Song; Lyu, Yunbin; Zeng, Weizhu Journal of Agricultural and Food Chemistry, Vol. 68, Issue 4 https://doi.org/10.1021/acs.jafc.9b05218	journal	November 2019
Metabolic Engineering of Escherichia coli for High Yield Production of Succinic Acid Driven by Methanol Zhang, Wenming; Zhang, Ting; Song, Meng ACS Synthetic Biology, Vol. 7, Issue 12 https://doi.org/10.1021/acssynbio.8b00109	journal	October 2018
Improvement of cis , cis -Muconic Acid Production in Saccharomyces cerevisiae through Biosensor-Aided Genome Engineering Wang, Guokun; Øzmerih, Süleyman; Guerreiro, Rogério ACS Synthetic Biology, Vol. 9, Issue 3 https://doi.org/10.1021/acssynbio.9b00477	journal	February 2020
Proteome analysis of yeast response to various nutrient limitations Kolkman, Annemieke; Daran‐Lapujade, Pascale; Fullaondo, Asier Molecular Systems Biology, Vol. 2, Issue 1 https://doi.org/10.1038/msb4100069	journal	January 2006
Production of the antimalarial drug precursor artemisinic acid in engineered yeast Ro, Dae-Kyun; Paradise, Eric M.; Ouellet, Mario Nature, Vol. 440, Issue 7086, p. 940-943 https://doi.org/10.1038/nature04640	journal	April 2006
Overflow metabolism in Escherichia coli results from efficient proteome allocation Basan, Markus; Hui, Sheng; Okano, Hiroyuki Nature, Vol. 528, Issue 7580 https://doi.org/10.1038/nature15765	journal	December 2015
What is flux balance analysis? Orth, Jeffrey D.; Thiele, Ines; Palsson, Bernhard Ø Nature Biotechnology, Vol. 28, Issue 3 https://doi.org/10.1038/nbt.1614	journal	March 2010
An enzyme-coupled biosensor enables (S)-reticuline production in yeast from glucose DeLoache, William C.; Russ, Zachary N.; Narcross, Lauren Nature Chemical Biology, Vol. 11, Issue 7 https://doi.org/10.1038/nchembio.1816	journal	May 2015
A protocol for generating a high-quality genome-scale metabolic reconstruction Thiele, Ines; Palsson, Bernhard Ø Nature Protocols, Vol. 5, Issue 1 https://doi.org/10.1038/nprot.2009.203	journal	January 2010
Structure of the c10 ring of the yeast mitochondrial ATP synthase in the open conformation Symersky, Jindrich; Pagadala, Vijayakanth; Osowski, Daniel Nature Structural & Molecular Biology, Vol. 19, Issue 5 https://doi.org/10.1038/nsmb.2284	journal	April 2012
A consensus S. cerevisiae metabolic model Yeast8 and its ecosystem for comprehensively probing cellular metabolism Lu, Hongzhong; Li, Feiran; Sánchez, Benjamín J. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-11581-3	journal	August 2019
A proteome-integrated, carbon source dependent genetic regulatory network in Saccharomyces cerevisiae Garcia-Albornoz, M.; Holman, S. W.; Antonisse, T. Molecular Omics, Vol. 16, Issue 1 https://doi.org/10.1039/C9MO00136K	journal	January 2020
The diversity of protein turnover and abundance under nitrogen-limited steady-state conditions in Saccharomyces cerevisiae Helbig, Andreas O.; Daran-Lapujade, Pascale; van Maris, Antonius J. A. Molecular BioSystems, Vol. 7, Issue 12 https://doi.org/10.1039/c1mb05250k	journal	January 2011
Harnessing the yeast Saccharomyces cerevisiae for the production of fungal secondary metabolites Wang, Guokun; Kell, Douglas B.; Borodina, Irina Essays in Biochemistry, Vol. 65, Issue 2 https://doi.org/10.1042/EBC20200137	journal	July 2021
Polypeptide-chain-elongation rate in Escherichia coli B/r as a function of growth rate Young, R.; Bremer, H. Biochemical Journal, Vol. 160, Issue 2 https://doi.org/10.1042/bj1600185	journal	November 1976
Evidence for a high proportion of inactive ribosomes in slow-growing yeast cells Waldron, C.; Jund, R.; Lacroute, F. Biochemical Journal, Vol. 168, Issue 3 https://doi.org/10.1042/bj1680409	journal	December 1977
Global characterization of in vivo enzyme catalytic rates and their correspondence to in vitro k _cat measurements Davidi, Dan; Noor, Elad; Liebermeister, Wolfram Proceedings of the National Academy of Sciences, Vol. 113, Issue 12 https://doi.org/10.1073/pnas.1514240113	journal	March 2016
Absolute yeast mitochondrial proteome quantification reveals trade-off between biosynthesis and energy generation during diauxic shift Di Bartolomeo, Francesca; Malina, Carl; Campbell, Kate Proceedings of the National Academy of Sciences, Vol. 117, Issue 13 https://doi.org/10.1073/pnas.1918216117	journal	March 2020
Proteome reallocation from amino acid biosynthesis to ribosomes enables yeast to grow faster in rich media Björkeroth, Johan; Campbell, Kate; Malina, Carl Proceedings of the National Academy of Sciences, Vol. 117, Issue 35 https://doi.org/10.1073/pnas.1921890117	journal	August 2020
Kinetic profiling of metabolic specialists demonstrates stability and consistency of in vivo enzyme turnover numbers Heckmann, David; Campeau, Anaamika; Lloyd, Colton J. Proceedings of the National Academy of Sciences, Vol. 117, Issue 37 https://doi.org/10.1073/pnas.2001562117	journal	September 2020
Adaptations in metabolism and protein translation give rise to the Crabtree effect in yeast Malina, Carl; Yu, Rosemary; Björkeroth, Johan Proceedings of the National Academy of Sciences, Vol. 118, Issue 51 https://doi.org/10.1073/pnas.2112836118	journal	December 2021
The Respiratory Chain in Yeast Behaves as a Single Functional Unit Boumans, Hans; Grivell, Leslie A.; Berden, Jan A. Journal of Biological Chemistry, Vol. 273, Issue 9 https://doi.org/10.1074/jbc.273.9.4872	journal	February 1998
A Cross-linking Mass Spectrometry Approach Defines Protein Interactions in Yeast Mitochondria Linden, Andreas; Deckers, Markus; Parfentev, Iwan Molecular & Cellular Proteomics, Vol. 19, Issue 7 https://doi.org/10.1074/mcp.RA120.002028	journal	July 2020
Metabolic engineering strategies for sesquiterpene production in microorganism Liu, Chun-Li; Xue, Kai; Yang, Yankun Critical Reviews in Biotechnology, Vol. 42, Issue 1 https://doi.org/10.1080/07388551.2021.1924112	journal	July 2021
Laboratory-scale production of (S)-reticuline, an important intermediate of benzylisoquinoline alkaloids, using a bacterial-based method Matsumura, Eitaro; Nakagawa, Akira; Tomabechi, Yusuke Bioscience, Biotechnology, and Biochemistry, Vol. 81, Issue 2 https://doi.org/10.1080/09168451.2016.1243985	journal	February 2017
Revising the Representation of Fatty Acid, Glycerolipid, and Glycerophospholipid Metabolism in the Consensus Model of Yeast Metabolism Aung, Hnin W.; Henry, Susan A.; Walker, Larry P. Industrial Biotechnology, Vol. 9, Issue 4 https://doi.org/10.1089/ind.2013.0013	journal	August 2013
Growth-limiting Intracellular Metabolites in Yeast Growing under Diverse Nutrient Limitations Boer, Viktor M.; Crutchfield, Christopher A.; Bradley, Patrick H. Molecular Biology of the Cell, Vol. 21, Issue 1 https://doi.org/10.1091/mbc.e09-07-0597	journal	January 2010
Supercomplexes in the respiratory chains of yeast and mammalian mitochondria Schagger, H. The EMBO Journal, Vol. 19, Issue 8 https://doi.org/10.1093/emboj/19.8.1777	journal	April 2000
Genome-scale modeling of yeast metabolism: retrospectives and perspectives Chen, Yu; Li, Feiran; Nielsen, Jens FEMS Yeast Research, Vol. 22, Issue 1 https://doi.org/10.1093/femsyr/foac003	journal	January 2022
Saccharomyces cerevisiae: a nomadic yeast with no niche? Goddard, Matthew R.; Greig, Duncan FEMS Yeast Research, Vol. 15, Issue 3 https://doi.org/10.1093/femsyr/fov009	journal	February 2015
Genome-scale modeling of yeast: chronology, applications and critical perspectives Lopes, Helder; Rocha, Isabel FEMS Yeast Research, Vol. 17, Issue 5 https://doi.org/10.1093/femsyr/fox050	journal	July 2017
Linking genetic, metabolic, and phenotypic diversity among Saccharomyces cerevisiae strains using multi-omics associations Kang, Kang; Bergdahl, Basti; Machado, Daniel GigaScience, Vol. 8, Issue 4 https://doi.org/10.1093/gigascience/giz015	journal	January 2019
Structural basis of yeast aminoacyl-tRNA synthetase complex formation revealed by crystal structures of two binary sub-complexes Simader, Hannes; Hothorn, Michael; Köhler, Christine Nucleic Acids Research, Vol. 34, Issue 14 https://doi.org/10.1093/nar/gkl560	journal	August 2006
Saccharomyces Genome Database: the genomics resource of budding yeast Cherry, J. M.; Hong, E. L.; Amundsen, C. Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr1029	journal	November 2011
BiGG Models: A platform for integrating, standardizing and sharing genome-scale models King, Zachary A.; Lu, Justin; Dräger, Andreas Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1049	journal	October 2015
BRENDA in 2019: a European ELIXIR core data resource Jeske, Lisa; Placzek, Sandra; Schomburg, Ida Nucleic Acids Research, Vol. 47, Issue D1 https://doi.org/10.1093/nar/gky1048	journal	November 2018
Engineering Saccharomyces cerevisiae cells for production of fatty acid-derived biofuels and chemicals Hu, Yating; Zhu, Zhiwei; Nielsen, Jens Open Biology, Vol. 9, Issue 5 https://doi.org/10.1098/rsob.190049	journal	May 2019
Genome-Scale Reconstruction of the Saccharomyces cerevisiae Metabolic Network Forster, J. Genome Research, Vol. 13, Issue 2 https://doi.org/10.1101/gr.234503	journal	February 2003
Pyruvate decarboxylase activity is regulated by the Ser/Thr protein phosphatase Sit4p in the yeastSaccharomyces cerevisiae de Assis, Leandro José; Zingali, Russolina Benedeta; Masuda, Claudio Akio FEMS Yeast Research, Vol. 13, Issue 6 https://doi.org/10.1111/1567-1364.12052	journal	June 2013
Why, when, and how did yeast evolve alcoholic fermentation? Dashko, Sofia; Zhou, Nerve; Compagno, Concetta FEMS Yeast Research, Vol. 14, Issue 6 https://doi.org/10.1111/1567-1364.12161	journal	June 2014
Nutrient sensing and signaling in the yeast Saccharomyces cerevisiae Conrad, Michaela; Schothorst, Joep; Kankipati, Harish Nag FEMS Microbiology Reviews, Vol. 38, Issue 2 https://doi.org/10.1111/1574-6976.12065	journal	March 2014
A glycolytic metabolon inSaccharomyces cerevisiaeis stabilized by F-actin Araiza-Olivera, Daniela; Chiquete-Felix, Natalia; Rosas-Lemus, Mónica FEBS Journal, Vol. 280, Issue 16 https://doi.org/10.1111/febs.12387	journal	July 2013
EngineeredSaccharomyces cerevisiaethat produces 1,3-propanediol from d-glucose Rao, Z.; Ma, Z.; Shen, W. Journal of Applied Microbiology, Vol. 105, Issue 6 https://doi.org/10.1111/j.1365-2672.2008.03868.x	journal	December 2008
Intracellular characterization of aerobic glucose metabolism in seven yeast species by 13C flux analysis and metabolomics: Flux response to Crabtree effect in yeast species Christen, Stefan; Sauer, Uwe FEMS Yeast Research, Vol. 11, Issue 3 https://doi.org/10.1111/j.1567-1364.2010.00713.x	journal	January 2011
Identifying Pex21p as a protein that specifically interacts with yeast seryl-tRNA synthetase Rocak, Sanda; Landeka, Irena; Weygand-Durasevic, Ivana FEMS Microbiology Letters, Vol. 214, Issue 1 https://doi.org/10.1111/j.1574-6968.2002.tb11331.x	journal	August 2002
Quantitative Physiology of Saccharomyces cerevisiae at Near-Zero Specific Growth Rates Boender, Léonie G. M.; de Hulster, Erik A. F.; van Maris, Antonius J. A. Applied and Environmental Microbiology, Vol. 75, Issue 17 https://doi.org/10.1128/AEM.00429-09	journal	September 2009
Quantitative Physiology of Non-Energy-Limited Retentostat Cultures of Saccharomyces cerevisiae at Near-Zero Specific Growth Rates Liu, Yaya; el Masoudi, Anissa; Pronk, Jack T. Applied and Environmental Microbiology, Vol. 85, Issue 20 https://doi.org/10.1128/AEM.01161-19	journal	October 2019
Malic Acid Production by Saccharomyces cerevisiae: Engineering of Pyruvate Carboxylation, Oxaloacetate Reduction, and Malate Export Zelle, R. M.; de Hulster, E.; van Winden, W. A. Applied and Environmental Microbiology, Vol. 74, Issue 9 https://doi.org/10.1128/AEM.02591-07	journal	March 2008
Effect of Specific Growth Rate on Fermentative Capacity of Baker’s Yeast Van Hoek, Pim; Van Dijken, Johannes P.; Pronk, Jack T. Applied and Environmental Microbiology, Vol. 64, Issue 11 https://doi.org/10.1128/AEM.64.11.4226-4233.1998	journal	January 1998
Metabolic Engineering of Glycerol Production in Saccharomyces cerevisiae Overkamp, K. M.; Bakker, B. M.; Kotter, P. Applied and Environmental Microbiology, Vol. 68, Issue 6 https://doi.org/10.1128/AEM.68.6.2814-2821.2002	journal	June 2002
Prolonged Maltose-Limited Cultivation of Saccharomyces cerevisiae Selects for Cells with Improved Maltose Affinity and Hypersensitivity Jansen, M. L. A.; Daran-Lapujade, P.; de Winde, J. H. Applied and Environmental Microbiology, Vol. 70, Issue 4 https://doi.org/10.1128/AEM.70.4.1956-1963.2004	journal	April 2004
Next-Generation Genetic and Fermentation Technologies for Safe and Sustainable Production of Food Ingredients: Colors and Flavorings Seo, Seung-Oh; Jin, Yong-Su Annual Review of Food Science and Technology, Vol. 13, Issue 1 https://doi.org/10.1146/annurev-food-052720-012228	journal	March 2022
Combined metabolic engineering of precursor and co-factor supply to increase α-santalene production by Saccharomyces cerevisiae Scalcinati, Gionata; Partow, Siavash; Siewers, Verena Microbial Cell Factories, Vol. 11, Issue 1 https://doi.org/10.1186/1475-2859-11-117	journal	January 2012
Production of 2,3-butanediol in Saccharomyces cerevisiae by in silico aided metabolic engineering Ng, Chiam Yu; Jung, Moo-young; Lee, Jinwon Microbial Cell Factories, Vol. 11, Issue 1 https://doi.org/10.1186/1475-2859-11-68	journal	January 2012
COBRApy: COnstraints-Based Reconstruction and Analysis for Python Ebrahim, Ali; Lerman, Joshua A.; Palsson, Bernhard O. BMC Systems Biology, Vol. 7, Issue 1 https://doi.org/10.1186/1752-0509-7-74	journal	January 2013
Engineering of acetyl-CoA metabolism for the improved production of polyhydroxybutyrate in Saccharomyces cerevisiae Kocharin, Kanokarn; Chen, Yun; Siewers, Verena AMB Express, Vol. 2, Issue 1 https://doi.org/10.1186/2191-0855-2-52	journal	January 2012
Automatic construction of metabolic models with enzyme constraints Bekiaris, Pavlos Stephanos; Klamt, Steffen BMC Bioinformatics, Vol. 21, Issue 1 https://doi.org/10.1186/s12859-019-3329-9	journal	January 2020
SLIMEr: probing flexibility of lipid metabolism in yeast with an improved constraint-based modeling framework Sánchez, Benjamín J.; Li, Feiran; Kerkhoven, Eduard J. BMC Systems Biology, Vol. 13, Issue 1 https://doi.org/10.1186/s12918-018-0673-8	journal	January 2019
Rational and combinatorial approaches to engineering styrene production by Saccharomyces cerevisiae McKenna, Rebekah; Thompson, Brian; Pugh, Shawn Microbial Cell Factories, Vol. 13, Issue 1 https://doi.org/10.1186/s12934-014-0123-2	journal	August 2014
Engineering and systems-level analysis of Saccharomyces cerevisiae for production of 3-hydroxypropionic acid via malonyl-CoA reductase-dependent pathway Kildegaard, Kanchana R.; Jensen, Niels B.; Schneider, Konstantin Microbial Cell Factories, Vol. 15, Issue 1 https://doi.org/10.1186/s12934-016-0451-5	journal	March 2016
Production of para-aminobenzoic acid from different carbon-sources in engineered Saccharomyces cerevisiae Averesch, Nils J. H.; Winter, Gal; Krömer, Jens O. Microbial Cell Factories, Vol. 15, Issue 1 https://doi.org/10.1186/s12934-016-0485-8	journal	May 2016
Maintenance-energy requirements and robustness of Saccharomyces cerevisiae at aerobic near-zero specific growth rates Vos, Tim; Hakkaart, Xavier D. V.; de Hulster, Erik A. F. Microbial Cell Factories, Vol. 15, Issue 1 https://doi.org/10.1186/s12934-016-0501-z	journal	June 2016
Adaptation of central metabolite pools to variations in growth rate and cultivation conditions in Saccharomyces cerevisiae Kumar, Kanhaiya; Venkatraman, Vishwesh; Bruheim, Per Microbial Cell Factories, Vol. 20, Issue 1 https://doi.org/10.1186/s12934-021-01557-8	journal	March 2021
Engineering of Saccharomyces cerevisiae for the accumulation of high amounts of triacylglycerol Arhar, Simon; Gogg-Fassolter, Gabriela; Ogrizović, Mojca Microbial Cell Factories, Vol. 20, Issue 1 https://doi.org/10.1186/s12934-021-01640-0	journal	July 2021
Improving isobutanol production with the yeast Saccharomyces cerevisiae by successively blocking competing metabolic pathways as well as ethanol and glycerol formation Wess, Johannes; Brinek, Martin; Boles, Eckhard Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1486-8	journal	July 2019
OptForce: An Optimization Procedure for Identifying All Genetic Manipulations Leading to Targeted Overproductions Ranganathan, Sridhar; Suthers, Patrick F.; Maranas, Costas D. PLoS Computational Biology, Vol. 6, Issue 4 https://doi.org/10.1371/journal.pcbi.1000744	journal	April 2010
k-OptForce: Integrating Kinetics with Flux Balance Analysis for Strain Design Chowdhury, Anupam; Zomorrodi, Ali R.; Maranas, Costas D. PLoS Computational Biology, Vol. 10, Issue 2 https://doi.org/10.1371/journal.pcbi.1003487	journal	February 2014
Systematic Analysis of Transcriptional and Post-transcriptional Regulation of Metabolism in Yeast Gonçalves, Emanuel; Raguz Nakic, Zrinka; Zampieri, Mattia PLOS Computational Biology, Vol. 13, Issue 1 https://doi.org/10.1371/journal.pcbi.1005297	journal	January 2017
COBRAme: A computational framework for genome-scale models of metabolism and gene expression Lloyd, Colton J.; Ebrahim, Ali; Yang, Laurence PLOS Computational Biology, Vol. 14, Issue 7 https://doi.org/10.1371/journal.pcbi.1006302	journal	July 2018
Industrial Systems Biology of Saccharomyces cerevisiae Enables Novel Succinic Acid Cell Factory Otero, José Manuel; Cimini, Donatella; Patil, Kiran R. PLoS ONE, Vol. 8, Issue 1 https://doi.org/10.1371/journal.pone.0054144	journal	January 2013
Improving the phenotype predictions of a yeast genome‐scale metabolic model by incorporating enzymatic constraints Sánchez, Benjamín J.; Zhang, Cheng; Nilsson, Avlant Molecular Systems Biology, Vol. 13, Issue 8 https://doi.org/10.15252/msb.20167411	journal	August 2017
The Reference Genome Sequence of Saccharomyces cerevisiae : Then and Now Engel, Stacia R.; Dietrich, Fred S.; Fisk, Dianna G. G3: Genes\|Genomes\|Genetics, Vol. 4, Issue 3 https://doi.org/10.1534/g3.113.008995	journal	December 2013
Genome-Wide Transcriptional Response of Saccharomyces cerevisiae to Stress-Induced Perturbations Taymaz-Nikerel, Hilal; Cankorur-Cetinkaya, Ayca; Kirdar, Betul Frontiers in Bioengineering and Biotechnology, Vol. 4 https://doi.org/10.3389/fbioe.2016.00017	journal	February 2016
Metabolic Engineering of the Shikimate Pathway for Production of Aromatics and Derived Compounds—Present and Future Strain Construction Strategies Averesch, Nils J. H.; Krömer, Jens O. Frontiers in Bioengineering and Biotechnology, Vol. 6 https://doi.org/10.3389/fbioe.2018.00032	journal	March 2018
Quantitative Trait Nucleotides Impacting the Technological Performances of Industrial Saccharomyces cerevisiae Strains Peltier, Emilien; Friedrich, Anne; Schacherer, Joseph Frontiers in Genetics, Vol. 10 https://doi.org/10.3389/fgene.2019.00683	journal	July 2019
Oxidative Stress and Programmed Cell Death in Yeast Farrugia, Gianluca; Balzan, Rena Frontiers in Oncology, Vol. 2 https://doi.org/10.3389/fonc.2012.00064	journal	January 2012
Yeast Mitochondrial Interactosome Model: Metabolon Membrane Proteins Complex Involved in the Channeling of ADP/ATP Clémençon, Benjamin International Journal of Molecular Sciences, Vol. 13, Issue 2 https://doi.org/10.3390/ijms13021858	journal	February 2012
Saccharomyces cerevisiae and its industrial applications Parapouli, Maria; Vasileiadi, Anastasios; Afendra, Amalia-Sofia AIMS Microbiology, Vol. 6, Issue 1 https://doi.org/10.3934/microbiol.2020001	journal	January 2020
Production of biopharmaceutical proteins by yeast Nielsen, Jens Bioengineered, Vol. 4, Issue 4 https://doi.org/10.4161/bioe.22856	journal	July 2013
Whole-cell modeling in yeast predicts compartment-specific proteome constraints that drive metabolic strategies Elsemman, Ibrahim E.; Rodriguez Prado, Angelica; Grigaitis, Pranas Zenodo https://doi.org/10.5281/zenodo.5732995	dataset	January 2021
Production of para-aminobenzoic acid from different carbon-sources in engineered Saccharomyces cerevisiae Averesch, Nils; Winter, Gal; Krömer, Jens Figshare https://doi.org/10.6084/m9.figshare.c.3606545.v1	collection	January 2016
Maintenance-energy requirements and robustness of Saccharomyces cerevisiae at aerobic near-zero specific growth rates Vos, Tim; Hakkaart, Xavier; Hulster, Erik Figshare https://doi.org/10.6084/m9.figshare.c.3627827	collection	January 2016
Adaptation of central metabolite pools to variations in growth rate and cultivation conditions in Saccharomyces cerevisiae Kumar, Kanhaiya; Venkatraman, Vishwesh; Bruheim, Per figshare https://doi.org/10.6084/m9.figshare.c.5333115	collection	January 2021
Engineering of Saccharomyces cerevisiae for the accumulation of high amounts of triacylglycerol Arhar, Simon; Gogg-Fassolter, Gabriela; Ogrizović, Mojca figshare https://doi.org/10.6084/m9.figshare.c.5531131	collection	January 2021
Quantifying absolute gene expression profiles reveals distinct regulation of central carbon metabolism genes in yeast Yu, Rosemary; Vorontsov, Egor; Sihlbom, Carina eLife, Vol. 10 https://doi.org/10.7554/eLife.65722	journal	March 2021

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59 BASIC BIOLOGICAL SCIENCES
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Title: Evaluating proteome allocation of Saccharomyces cerevisiae phenotypes with resource balance analysis

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