DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: 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:
; ; ; ; ; ; ; ; ; ; ORCiD logo; ORCiD logo
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}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1186/s13068-017-0958-y

Citation Metrics:
Cited by: 70 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

INCA: a computational platform for isotopically non-stationary metabolic flux analysis
journal, January 2014


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
  • DOI: 10.1111/mmi.12699

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
  • DOI: 10.1007/s00253-016-7510-z

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
  • DOI: 10.1038/nprot.2008.107

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
  • DOI: 10.1016/j.copbio.2008.07.006

The Importance of Energy Balance in Improving Photosynthetic Productivity
journal, November 2010


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
  • DOI: 10.1016/0005-2728(75)90041-9

The plasticity of cyanobacterial metabolism supports direct CO2 conversion to ethylene
journal, April 2015


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
  • DOI: 10.1104/pp.15.00385

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
  • DOI: 10.1038/nprot.2008.131

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
  • DOI: 10.1039/C3MB70348G

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
  • DOI: 10.1111/tpj.12390

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
  • DOI: 10.1016/j.ab.2014.07.026

Coordination of bacterial proteome with metabolism by cyclic AMP signalling
journal, August 2013

  • You, Conghui; Okano, Hiroyuki; Hui, Sheng
  • Nature, Vol. 500, Issue 7462
  • DOI: 10.1038/nature12446

Microalgae for high-value compounds and biofuels production: A review with focus on cultivation under stress conditions
journal, December 2013


A roadmap for interpreting 13 C metabolite labeling patterns from cells
journal, August 2015


Characterization of a zwf mutant of Synechococcus sp. strain PCC 7942.
journal, May 1995


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
  • DOI: 10.1073/pnas.1519220112

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
  • DOI: 10.1007/10_2013_221

Microalgae: The Potential for Carbon Capture
journal, October 2010


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
  • DOI: 10.1016/j.ab.2004.09.001

A carbon sink pathway increases carbon productivity in cyanobacteria
journal, May 2015


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
  • DOI: 10.1038/nchembio.186

Substrate channelling as an approach to cascade reactions
journal, March 2016

  • Wheeldon, Ian; Minteer, Shelley D.; Banta, Scott
  • Nature Chemistry, Vol. 8, Issue 4
  • DOI: 10.1038/nchem.2459

Isotopically nonstationary 13C flux analysis of cyanobacterial isobutyraldehyde production
journal, July 2017


Unlocking the Constraints of Cyanobacterial Productivity: Acclimations Enabling Ultrafast Growth
journal, July 2016


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
  • DOI: 10.1093/jxb/ers004

Role of Light in the Regulation of Chloroplast Enzymes
journal, June 1980


Sampling for Metabolome Analysis of Microorganisms
journal, May 2007

  • Bolten, Christoph J.; Kiefer, Patrick; Letisse, Fabien
  • Analytical Chemistry, Vol. 79, Issue 10
  • DOI: 10.1021/ac0623888

Effects of overexpressing photosynthetic carbon flux control enzymes in the cyanobacterium Synechocystis PCC 6803
journal, November 2016


Analysis of Isotopic Labeling in Peptide Fragments by Tandem Mass Spectrometry
journal, March 2014


Modulation of the Major Paths of Carbon in Photorespiratory Mutants of Synechocystis
journal, January 2011


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
  • DOI: 10.3791/3583

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
  • DOI: 10.1021/ac403985w

Simulating cyanobacterial phenotypes by integrating flux balance analysis, kinetics, and a light distribution function
journal, December 2015


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
  • DOI: 10.1016/j.ymben.2011.08.002

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
  • DOI: 10.1073/pnas.1319485111

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
  • DOI: 10.1186/s13068-016-0630-y

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
  • DOI: 10.1073/pnas.1117907109

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
  • DOI: 10.1038/srep41569

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
  • DOI: 10.1186/1754-6834-7-99

Applications of cyanobacteria in biotechnology
journal, January 2009


Engineering Cellular Metabolism
journal, March 2016


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
  • DOI: 10.1038/srep08132

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
  • DOI: 10.1002/eng2.12094

Engineering cyanobacteria for production of terpenoids
journal, November 2018


A Novel Cyanobacterium Synechococcus elongatus PCC 11802 has Distinct Genomic and Metabolomic Characteristics Compared to its Neighbor PCC 11801
journal, January 2020


Enhanced production of sucrose in the fast-growing cyanobacterium Synechococcus elongatus UTEX 2973
journal, January 2020


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
  • DOI: 10.1073/pnas.1807804115

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
  • DOI: 10.1073/pnas.1818285115

Parallel isotope differential modeling for instationary 13C fluxomics at the genome scale
journal, June 2020


Mass Isotopologue Distribution of dimer ion adducts of intracellular metabolites for potential applications in 13C Metabolic Flux Analysis
journal, August 2019


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
  • DOI: 10.3389/fbioe.2019.00033

Emerging Species and Genome Editing Tools: Future Prospects in Cyanobacterial Synthetic Biology
journal, September 2019