Flux-Enabled Exploration of the Role of Sip1 in Galactose Yeast Metabolism

Shymansky, Christopher M.; Wang, George; Baidoo, Edward E. K.; Gin, Jennifer; Apel, Amanda Reider; Mukhopadhyay, Aindrila; Martin, Hector Garcia; Keasling, Jay D.

doi:10.3389/fbioe.2017.00031

Title: Flux-Enabled Exploration of the Role of Sip1 in Galactose Yeast Metabolism

Journal Article · Wed May 24 04:00:00 UTC 2017 · Frontiers in Bioengineering and Biotechnology

DOI: https://doi.org/10.3389/fbioe.2017.00031 · OSTI ID:1379658

Shymansky, Christopher M. ^[1]; Wang, George ^[2]; Baidoo, Edward E. K. ^[2]; Gin, Jennifer ^[2]; Apel, Amanda Reider ^[2]; Mukhopadhyay, Aindrila ^[2]; Martin, Hector Garcia ^[3]; Keasling, Jay D. ^[4]

Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Joint BioEnergy Institute, Emeryville, CA (United States); Univ. of California, Berkeley, CA (United States)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Joint BioEnergy Institute, Emeryville, CA (United States)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Joint BioEnergy Institute, Emeryville, CA (United States); DOE Agile Biofoundry, Emeryville, CA (United States); Basque Center for Applied Mathematics, Bilbao, Basque Country (Spain)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Joint BioEnergy Institute, Emeryville, CA (United States); Univ. of California, Berkeley, CA (United States); Technical Univ. of Denmark, Horsholm (Denmark)

¹³C metabolic flux analysis (¹³C MFA) is an important systems biology technique that has been used to investigate microbial metabolism for decades. The heterotrimer Snf1 kinase complex plays a key role in the preference Saccharomyces cerevisiae exhibits for glucose over galactose, a phenomenon known as glucose repression or carbon catabolite repression. The SIP1 gene, encoding a part of this complex, has received little attention, presumably, because its knockout lacks a growth phenotype. We present a fluxomic investigation of the relative effects of the presence of galactose in classically glucose-repressing media and/or knockout of SIP1 using a multi-scale variant of ¹³C MFA known as 2-Scale ¹³C metabolic flux analysis (2S-¹³C MFA). In this study, all strains have the galactose metabolism deactivated (gal1Δ background) so as to be able to separate the metabolic effects purely related to glucose repression from those arising from galactose metabolism. The resulting flux profiles reveal that the presence of galactose in classically glucose-repressing conditions, for a CEN.PK113-7D gal1Δ background, results in a substantial decrease in pentose phosphate pathway (PPP) flux and increased flow from cytosolic pyruvate and malate through the mitochondria toward cytosolic branched-chain amino acid biosynthesis. These fluxomic redistributions are accompanied by a higher maximum specific growth rate, both seemingly in violation of glucose repression. Deletion of SIP1 in the CEN.PK113-7D gal1Δ cells grown in mixed glucose/galactose medium results in a further increase. Knockout of this gene in cells grown in glucose-only medium results in no change in growth rate and a corresponding decrease in glucose and ethanol exchange fluxes and flux through pathways involved in aspartate/threonine biosynthesis. Glucose repression appears to be violated at a 1/10 ratio of galactose-to-glucose. Based on the scientific literature, we may have conducted our experiments near a critical sugar ratio that is known to allow galactose to enter the cell. Additionally, we report a number of fluxomic changes associated with these growth rate increases and unexpected flux profile redistributions resulting from deletion of SIP1 in glucose-only medium.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1379658

Journal Information:: Frontiers in Bioengineering and Biotechnology, Journal Name: Frontiers in Bioengineering and Biotechnology Vol. 5; ISSN 2296-4185

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

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Metabolic-Flux Profiling of the Yeasts Saccharomyces cerevisiae and Pichia stipitis Fiaux, Jocelyne; Çakar, Z. Petek; Sonderegger, Marco Eukaryotic Cell, Vol. 2, Issue 1 https://doi.org/10.1128/ec.2.1.170-180.2003	journal	February 2003
Network Identification and Flux Quantification in the Central Metabolism of Saccharomyces cerevisiae under Different Conditions of Glucose Repression Gombert, A. K.; Moreira dos Santos, M.; Christensen, B. Journal of Bacteriology, Vol. 183, Issue 4 https://doi.org/10.1128/jb.183.4.1441-1451.2001	journal	February 2001
How Saccharomyces Responds to Nutrients Zaman, Shadia; Lippman, Soyeon Im; Zhao, Xin Annual Review of Genetics, Vol. 42, Issue 1 https://doi.org/10.1146/annurev.genet.41.110306.130206	journal	December 2008
De novo sequencing, assembly and analysis of the genome of the laboratory strain Saccharomyces cerevisiae CEN.PK113-7D, a model for modern industrial biotechnology Nijkamp, Jurgen F.; van den Broek, Marcel; Datema, Erwin Microbial Cell Factories, Vol. 11, Issue 1 https://doi.org/10.1186/1475-2859-11-36	journal	January 2012
Characterization of the metabolic shift between oxidative and fermentative growth in Saccharomyces cerevisiae by comparative ¹³C flux analysis Frick, Oliver; Wittmann, Christoph Microbial Cell Factories, Vol. 4, Issue 1 https://doi.org/10.1186/1475-2859-4-30	journal	November 2005
Connecting extracellular metabolomic measurements to intracellular flux states in yeast Mo, Monica L.; Palsson, Bernhard Ø; Herrgård, Markus J. BMC Systems Biology, Vol. 3, Issue 1 https://doi.org/10.1186/1752-0509-3-37	journal	January 2009
Large-scale 13C-flux analysis reveals mechanistic principles of metabolic network robustness to null mutations in yeast Blank, Lars M.; Kuepfer, Lars; Sauer, Uwe Genome Biology, Vol. 6, Issue 6, p. R49 https://doi.org/10.1186/gb-2005-6-6-r49	journal	January 2005
Different Levels of Catabolite Repression Optimize Growth in Stable and Variable Environments New, Aaron M.; Cerulus, Bram; Govers, Sander K. PLoS Biology, Vol. 12, Issue 1 https://doi.org/10.1371/journal.pbio.1001764	journal	January 2014
Natural Variation in Preparation for Nutrient Depletion Reveals a Cost–Benefit Tradeoff Wang, Jue; Atolia, Esha; Hua, Bo PLOS Biology, Vol. 13, Issue 1 https://doi.org/10.1371/journal.pbio.1002041	journal	January 2015
Population Diversification in a Yeast Metabolic Program Promotes Anticipation of Environmental Shifts Venturelli, Ophelia S.; Zuleta, Ignacio; Murray, Richard M. PLOS Biology, Vol. 13, Issue 1 https://doi.org/10.1371/journal.pbio.1002042	journal	January 2015
A Method to Constrain Genome-Scale Models with 13C Labeling Data García Martín, Héctor; Kumar, Vinay Satish; Weaver, Daniel PLOS Computational Biology, Vol. 11, Issue 9 https://doi.org/10.1371/journal.pcbi.1004363	journal	September 2015
13C Metabolic Flux Analysis for Systematic Metabolic Engineering of S. cerevisiae for Overproduction of Fatty Acids Ghosh, Amit; Ando, David; Gin, Jennifer Frontiers in Bioengineering and Biotechnology, Vol. 4 https://doi.org/10.3389/fbioe.2016.00076	journal	October 2016
Achieving Metabolic Flux Analysis for S. cerevisiae at a Genome-Scale: Challenges, Requirements, and Considerations Gopalakrishnan, Saratram; Maranas, Costas Metabolites, Vol. 5, Issue 3 https://doi.org/10.3390/metabo5030521	journal	September 2015

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