Deciphering cyanobacterial phenotypes for fast photoautotrophic growth via isotopically nonstationary metabolic flux analysis
Abstract
Synechococcus elongatus UTEX 2973 is the fastest growing cyanobacterium characterized to date. Its genome was found to be 99.8% identical to S. elongatus 7942 yet it grows twice as fast. Current genome-to-phenome mapping is still poorly performed for non-model organisms. Even for species with identical genomes, cell phenotypes can be strikingly different. To understand Synechococcus 2973’s fast-growth phenotype and its metabolic features advantageous to photo-biorefineries, 13C isotopically nonstationary metabolic flux analysis (INST-MFA), biomass compositional analysis, gene knockouts, and metabolite profiling were performed on both strains under various growth conditions.
- Authors:
- Publication Date:
- Research Org.:
- Washington Univ., St. Louis, MO (United States). Donald Danforth Plant Science Center
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1618702
- Alternate Identifier(s):
- OSTI ID: 1504898
- Grant/Contract Number:
- DESC0012722; AE-AR0000202; AR0000202; SC0012722
- Resource Type:
- Published Article
- Journal Name:
- Biotechnology for Biofuels
- Additional Journal Information:
- Journal Name: Biotechnology for Biofuels Journal Volume: 10 Journal Issue: 1; Journal ID: ISSN 1754-6834
- Publisher:
- Springer Science + Business Media
- Country of Publication:
- Netherlands
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 13C labeling experiments; Channeling; Glycogen; Metabolites; Photobioreactor; Energy charge
Citation Formats
Abernathy, Mary H., Yu, Jingjie, Ma, Fangfang, Liberton, Michelle, Ungerer, Justin, Hollinshead, Whitney D., Gopalakrishnan, Saratram, He, Lian, Maranas, Costas D., Pakrasi, Himadri B., Allen, Doug K., and Tang, Yinjie J. Deciphering cyanobacterial phenotypes for fast photoautotrophic growth via isotopically nonstationary metabolic flux analysis. Netherlands: N. p., 2017.
Web. doi:10.1186/s13068-017-0958-y.
Abernathy, Mary H., Yu, Jingjie, Ma, Fangfang, Liberton, Michelle, Ungerer, Justin, Hollinshead, Whitney D., Gopalakrishnan, Saratram, He, Lian, Maranas, Costas D., Pakrasi, Himadri B., Allen, Doug K., & Tang, Yinjie J. Deciphering cyanobacterial phenotypes for fast photoautotrophic growth via isotopically nonstationary metabolic flux analysis. Netherlands. https://doi.org/10.1186/s13068-017-0958-y
Abernathy, Mary H., Yu, Jingjie, Ma, Fangfang, Liberton, Michelle, Ungerer, Justin, Hollinshead, Whitney D., Gopalakrishnan, Saratram, He, Lian, Maranas, Costas D., Pakrasi, Himadri B., Allen, Doug K., and Tang, Yinjie J. Thu .
"Deciphering cyanobacterial phenotypes for fast photoautotrophic growth via isotopically nonstationary metabolic flux analysis". Netherlands. https://doi.org/10.1186/s13068-017-0958-y.
@article{osti_1618702,
title = {Deciphering cyanobacterial phenotypes for fast photoautotrophic growth via isotopically nonstationary metabolic flux analysis},
author = {Abernathy, Mary H. and Yu, Jingjie and Ma, Fangfang and Liberton, Michelle and Ungerer, Justin and Hollinshead, Whitney D. and Gopalakrishnan, Saratram and He, Lian and Maranas, Costas D. and Pakrasi, Himadri B. and Allen, Doug K. and Tang, Yinjie J.},
abstractNote = {Synechococcus elongatus UTEX 2973 is the fastest growing cyanobacterium characterized to date. Its genome was found to be 99.8% identical to S. elongatus 7942 yet it grows twice as fast. Current genome-to-phenome mapping is still poorly performed for non-model organisms. Even for species with identical genomes, cell phenotypes can be strikingly different. To understand Synechococcus 2973’s fast-growth phenotype and its metabolic features advantageous to photo-biorefineries, 13C isotopically nonstationary metabolic flux analysis (INST-MFA), biomass compositional analysis, gene knockouts, and metabolite profiling were performed on both strains under various growth conditions.},
doi = {10.1186/s13068-017-0958-y},
journal = {Biotechnology for Biofuels},
number = 1,
volume = 10,
place = {Netherlands},
year = {Thu Nov 16 00:00:00 EST 2017},
month = {Thu Nov 16 00:00:00 EST 2017}
}
https://doi.org/10.1186/s13068-017-0958-y
Web of Science
Works referenced in this record:
INCA: a computational platform for isotopically non-stationary metabolic flux analysis
journal, January 2014
- Young, J. D.
- Bioinformatics, Vol. 30, Issue 9
The γ-aminobutyric acid shunt contributes to closing the tricarboxylic acid cycle in S ynechocystis sp. PCC 6803 : The γ-aminobutyric acid shunt in
journal, July 2014
- Xiong, Wei; Brune, Daniel; Vermaas, Wim F. J.
- Molecular Microbiology, Vol. 93, Issue 4
The potential of Synechococcus elongatus UTEX 2973 for sugar feedstock production
journal, April 2016
- Song, Kuo; Tan, Xiaoming; Liang, Yajing
- Applied Microbiology and Biotechnology, Vol. 100, Issue 18
Absolute quantitation of intracellular metabolite concentrations by an isotope ratio-based approach
journal, July 2008
- Bennett, Bryson D.; Yuan, Jie; Kimball, Elizabeth H.
- Nature Protocols, Vol. 3, Issue 8
Engineering the spatial organization of metabolic enzymes: mimicking nature's synergy
journal, October 2008
- Conrado, Robert J.; Varner, Jeffrey D.; DeLisa, Matthew P.
- Current Opinion in Biotechnology, Vol. 19, Issue 5
The Importance of Energy Balance in Improving Photosynthetic Productivity
journal, November 2010
- Kramer, David M.; Evans, John R.
- Plant Physiology, Vol. 155, Issue 1
The role of pH in the regulation of carbon fixation in the chloroplast stroma. Studies on CO2 fixation in the light and dark
journal, August 1975
- Werdan, Karl; Heldt, Hans W.; Milovancev, Mirjana
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 396, Issue 2
13 C-MFA delineates the photomixotrophic metabolism of Synechocystis sp. PCC 6803 under light- and carbon-sufficient conditions
journal, April 2014
- You, Le; Berla, Bert; He, Lian
- Biotechnology Journal, Vol. 9, Issue 5
Seawater cultivation of freshwater cyanobacterium Synechocystis sp. PCC 6803 drastically alters amino acid composition and glycogen metabolism
journal, April 2015
- Iijima, Hiroko; Nakaya, Yuka; Kuwahara, Ayuko
- Frontiers in Microbiology, Vol. 6
The plasticity of cyanobacterial metabolism supports direct CO2 conversion to ethylene
journal, April 2015
- Xiong, Wei; Morgan, John A.; Ungerer, Justin
- Nature Plants, Vol. 1, Issue 5
Isotope labelling of Rubisco subunits provides in vivo information on subcellular biosynthesis and exchange of amino acids between compartments: Probing subcellular metabolism in seeds
journal, February 2012
- Allen, Doug K.; Laclair, Russell W.; Ohlrogge, John B.
- Plant, Cell & Environment, Vol. 35, Issue 7
Enhancing photo-catalytic production of organic acids in the cyanobacterium S ynechocystis sp. PCC 6803 Δ glg C , a strain incapable of glycogen storage : Enhancing photo-catalytic production of organic acids
journal, January 2015
- Carrieri, Damian; Broadbent, Charlie; Carruth, David
- Microbial Biotechnology, Vol. 8, Issue 2
Quantitative Multilevel Analysis of Central Metabolism in Developing Oilseeds of Oilseed Rape during in Vitro Culture
journal, May 2015
- Schwender, Jörg; Hebbelmann, Inga; Heinzel, Nicolas
- Plant Physiology, Vol. 168, Issue 3
Introducing extra NADPH consumption ability significantly increases the photosynthetic efficiency and biomass production of cyanobacteria
journal, November 2016
- Zhou, Jie; Zhang, Fuliang; Meng, Hengkai
- Metabolic Engineering, Vol. 38
Kinetic flux profiling for quantitation of cellular metabolic fluxes
journal, July 2008
- Yuan, Jie; Bennett, Bryson D.; Rabinowitz, Joshua D.
- Nature Protocols, Vol. 3, Issue 8
Flux and reflux: metabolite reflux in plant suspension cells and its implications for isotope-assisted metabolic flux analysis
journal, January 2014
- Nargund, Shilpa; Misra, Ashish; Zhang, Xiaofeng
- Mol. BioSyst., Vol. 10, Issue 6
Metabolic flux analysis using 13 C peptide label measurements
journal, January 2014
- Mandy, Dominic E.; Goldford, Joshua E.; Yang, Hong
- The Plant Journal, Vol. 77, Issue 3
Stoichiometric model of Escherichia coli metabolism: Incorporation of growth-rate dependent biomass composition and mechanistic energy requirements
journal, November 1997
- Pramanik, J.; Keasling, J. D.
- Biotechnology and Bioengineering, Vol. 56, Issue 4, p. 398-421
Sampling of intracellular metabolites for stationary and non-stationary 13C metabolic flux analysis in Escherichia coli
journal, November 2014
- Millard, Pierre; Massou, Stéphane; Wittmann, Christoph
- Analytical Biochemistry, Vol. 465
Coordination of bacterial proteome with metabolism by cyclic AMP signalling
journal, August 2013
- You, Conghui; Okano, Hiroyuki; Hui, Sheng
- Nature, Vol. 500, Issue 7462
Microalgae for high-value compounds and biofuels production: A review with focus on cultivation under stress conditions
journal, December 2013
- Markou, Giorgos; Nerantzis, Elias
- Biotechnology Advances, Vol. 31, Issue 8
A roadmap for interpreting 13 C metabolite labeling patterns from cells
journal, August 2015
- Buescher, Joerg M.; Antoniewicz, Maciek R.; Boros, Laszlo G.
- Current Opinion in Biotechnology, Vol. 34
Resolution of Conflicting Signals at the Single-Cell Level in the Regulation of Cyanobacterial Photosynthesis and Nitrogen Fixation
journal, June 2013
- Mohr, Wiebke; Vagner, Tomas; Kuypers, Marcel M. M.
- PLoS ONE, Vol. 8, Issue 6
Characterization of a zwf mutant of Synechococcus sp. strain PCC 7942.
journal, May 1995
- Scanlan, D. J.; Sundaram, S.; Newman, J.
- Journal of Bacteriology, Vol. 177, Issue 9
The essential gene set of a photosynthetic organism
journal, October 2015
- Rubin, Benjamin E.; Wetmore, Kelly M.; Price, Morgan N.
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 48
Compartmentalization and Metabolic Channeling for Multienzymatic Biosynthesis: Practical Strategies and Modeling Approaches
book, January 2013
- Jandt, U.; You, C.; Zhang, Y. H. -P.
- Fundamentals and Application of New Bioproduction Systems
Microalgae: The Potential for Carbon Capture
journal, October 2010
- Sayre, Richard
- BioScience, Vol. 60, Issue 9
Quantitative analysis of the microbial metabolome by isotope dilution mass spectrometry using uniformly 13C-labeled cell extracts as internal standards
journal, January 2005
- Wu, Liang; Mashego, Mlawule R.; van Dam, Jan C.
- Analytical Biochemistry, Vol. 336, Issue 2
A carbon sink pathway increases carbon productivity in cyanobacteria
journal, May 2015
- Oliver, John W. K.; Atsumi, Shota
- Metabolic Engineering, Vol. 29
Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli
journal, June 2009
- Bennett, Bryson D.; Kimball, Elizabeth H.; Gao, Melissa
- Nature Chemical Biology, Vol. 5, Issue 8
Substrate channelling as an approach to cascade reactions
journal, March 2016
- Wheeldon, Ian; Minteer, Shelley D.; Banta, Scott
- Nature Chemistry, Vol. 8, Issue 4
The Malic Enzyme Is Required for Optimal Photoautotrophic Growth of Synechocystis sp. Strain PCC 6803 under Continuous Light but Not under a Diurnal Light Regimen
journal, November 2004
- Bricker, T. M.; Zhang, S.; Laborde, S. M.
- Journal of Bacteriology, Vol. 186, Issue 23
Isotopically nonstationary 13C flux analysis of cyanobacterial isobutyraldehyde production
journal, July 2017
- Jazmin, Lara J.; Xu, Yao; Cheah, Yi Ern
- Metabolic Engineering, Vol. 42
Unlocking the Constraints of Cyanobacterial Productivity: Acclimations Enabling Ultrafast Growth
journal, July 2016
- Bernstein, Hans C.; McClure, Ryan S.; Hill, Eric A.
- mBio, Vol. 7, Issue 4
Increased fructose 1,6-bisphosphate aldolase in plastids enhances growth and photosynthesis of tobacco plants
journal, February 2012
- Uematsu, Kimio; Suzuki, Nobuaki; Iwamae, Tomoko
- Journal of Experimental Botany, Vol. 63, Issue 8
Role of Light in the Regulation of Chloroplast Enzymes
journal, June 1980
- Buchanan, Bob B.
- Annual Review of Plant Physiology, Vol. 31, Issue 1
Sampling for Metabolome Analysis of Microorganisms
journal, May 2007
- Bolten, Christoph J.; Kiefer, Patrick; Letisse, Fabien
- Analytical Chemistry, Vol. 79, Issue 10
Energetics and carbon metabolism during growth of microalgal cells under photoautotrophic, mixotrophic and cyclic light-autotrophic/dark-heterotrophic conditions
journal, October 2000
- Yang, Chen; Hua, Qiang; Shimizu, Kazuyuki
- Biochemical Engineering Journal, Vol. 6, Issue 2
Effects of overexpressing photosynthetic carbon flux control enzymes in the cyanobacterium Synechocystis PCC 6803
journal, November 2016
- Liang, Feiyan; Lindblad, Peter
- Metabolic Engineering, Vol. 38
Analysis of Isotopic Labeling in Peptide Fragments by Tandem Mass Spectrometry
journal, March 2014
- Allen, Doug K.; Evans, Bradley S.; Libourel, Igor G. L.
- PLoS ONE, Vol. 9, Issue 3
Modulation of the Major Paths of Carbon in Photorespiratory Mutants of Synechocystis
journal, January 2011
- Huege, Jan; Goetze, Jan; Schwarz, Doreen
- PLoS ONE, Vol. 6, Issue 1
Metabolic Pathway Confirmation and Discovery Through <sup>13</sup>C-labeling of Proteinogenic Amino Acids
journal, January 2012
- You, Le; Page, Lawrence; Feng, Xueyang
- Journal of Visualized Experiments, Issue 59
Quantification of Peptide m / z Distributions from 13 C-Labeled Cultures with High-Resolution Mass Spectrometry
journal, January 2014
- Allen, Doug K.; Goldford, Joshua; Gierse, James K.
- Analytical Chemistry, Vol. 86, Issue 3
Carbon metabolism and energy conversion of Synechococcus sp. PCC 7942 under mixotrophic conditions: comparison with photoautotrophic condition
journal, May 2011
- Yan, Riming; Zhu, Du; Zhang, Zhibin
- Journal of Applied Phycology, Vol. 24, Issue 4
Simulating cyanobacterial phenotypes by integrating flux balance analysis, kinetics, and a light distribution function
journal, December 2015
- He, Lian; Wu, Stephen G.; Wan, Ni
- Microbial Cell Factories, Vol. 14, Issue 1
Mapping photoautotrophic metabolism with isotopically nonstationary 13C flux analysis
journal, November 2011
- Young, Jamey D.; Shastri, Avantika A.; Stephanopoulos, Gregory
- Metabolic Engineering, Vol. 13, Issue 6
Isotopically nonstationary 13 C flux analysis of changes in Arabidopsis thaliana leaf metabolism due to high light acclimation
journal, November 2014
- Ma, Fangfang; Jazmin, Lara J.; Young, Jamey D.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 47
Examining Escherichia coli glycolytic pathways, catabolite repression, and metabolite channeling using Δpfk mutants
journal, October 2016
- Hollinshead, Whitney D.; Rodriguez, Sarah; Martin, Hector Garcia
- Biotechnology for Biofuels, Vol. 9, Issue 1
Detailing the optimality of photosynthesis in cyanobacteria through systems biology analysis
journal, January 2012
- Nogales, J.; Gudmundsson, S.; Knight, E. M.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 7
Quantitative estimation of channeling from early glycolytic intermediates to CO2 in intact Escherichia coli: Quantitation of channeling in intact E. coli
journal, June 2005
- Shearer, Georgia; Lee, Jennifer C.; Koo, Jia-an
- FEBS Journal, Vol. 272, Issue 13
Identifying the Metabolic Differences of a Fast-Growth Phenotype in Synechococcus UTEX 2973
journal, January 2017
- Mueller, Thomas J.; Ungerer, Justin L.; Pakrasi, Himadri B.
- Scientific Reports, Vol. 7, Issue 1
Exploring metabolic engineering design principles for the photosynthetic production of lactic acid by Synechocystis sp. PCC6803
journal, January 2014
- Angermayr, S.; van der Woude, Aniek D.; Correddu, Danilo
- Biotechnology for Biofuels, Vol. 7, Issue 1
Applications of cyanobacteria in biotechnology
journal, January 2009
- Abed, R. M. M.; Dobretsov, S.; Sudesh, K.
- Journal of Applied Microbiology, Vol. 106, Issue 1
Engineering Cellular Metabolism
journal, March 2016
- Nielsen, Jens; Keasling, Jay D.
- Cell, Vol. 164, Issue 6
Synechococcus elongatus UTEX 2973, a fast growing cyanobacterial chassis for biosynthesis using light and CO2
journal, January 2015
- Yu, Jingjie; Liberton, Michelle; Cliften, Paul F.
- Scientific Reports, Vol. 5, Issue 1
Works referencing / citing this record:
A method to compute instantaneous oxygen evolution rates in cyanobacterial cultures grown in shake flasks
journal, January 2020
- Sengupta, Annesha; Wangikar, Pramod P.
- Engineering Reports, Vol. 2, Issue 1
Engineering cyanobacteria for production of terpenoids
journal, November 2018
- Lin, Po-Cheng; Pakrasi, Himadri B.
- Planta, Vol. 249, Issue 1
A Novel Cyanobacterium Synechococcus elongatus PCC 11802 has Distinct Genomic and Metabolomic Characteristics Compared to its Neighbor PCC 11801
journal, January 2020
- Jaiswal, Damini; Sengupta, Annesha; Sengupta, Shinjinee
- Scientific Reports, Vol. 10, Issue 1
Enhanced production of sucrose in the fast-growing cyanobacterium Synechococcus elongatus UTEX 2973
journal, January 2020
- Lin, Po-Cheng; Zhang, Fuzhong; Pakrasi, Himadri B.
- Scientific Reports, Vol. 10, Issue 1
Model metabolic strategy for heterotrophic bacteria in the cold ocean based on Colwellia psychrerythraea 34H
journal, November 2018
- Czajka, Jeffrey J.; Abernathy, Mary H.; Benites, Veronica T.
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 49
Navigating the fitness landscape using multiallele genome editing
journal, November 2018
- Miller, Neil T.; Burnap, Robert L.
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 50
Parallel isotope differential modeling for instationary 13C fluxomics at the genome scale
journal, June 2020
- Zhang, Zhengdong; Liu, Zhentao; Meng, Yafei
- Biotechnology for Biofuels, Vol. 13, Issue 1
Mass Isotopologue Distribution of dimer ion adducts of intracellular metabolites for potential applications in 13C Metabolic Flux Analysis
journal, August 2019
- Prasannan, Charulata B.; Mishra, Vivek; Jaiswal, Damini
- PLOS ONE, Vol. 14, Issue 8
New Applications of Synthetic Biology Tools for Cyanobacterial Metabolic Engineering
journal, February 2019
- Santos-Merino, María; Singh, Amit K.; Ducat, Daniel C.
- Frontiers in Bioengineering and Biotechnology, Vol. 7
Emerging Species and Genome Editing Tools: Future Prospects in Cyanobacterial Synthetic Biology
journal, September 2019
- Gale, Grant A. R.; Schiavon Osorio, Alejandra A.; Mills, Lauren A.
- Microorganisms, Vol. 7, Issue 10