Cellular responses to reactive oxygen species are predicted from molecular mechanisms
Abstract
Catalysis using iron–sulfur clusters and transition metals can be traced back to the last universal common ancestor. The damage to metalloproteins caused by reactive oxygen species (ROS) can prevent cell growth and survival when unmanaged, thus eliciting an essential stress response that is universal and fundamental in biology. Here we develop a computable multiscale description of the ROS stress response in Escherichia coli, called OxidizeME. We use OxidizeME to explain four key responses to oxidative stress: 1) ROS-induced auxotrophy for branched-chain, aromatic, and sulfurous amino acids; 2) nutrient-dependent sensitivity of growth rate to ROS; 3) ROS-specific differential gene expression separate from global growth-associated differential expression; and 4) coordinated expression of iron–sulfur cluster (ISC) and sulfur assimilation (SUF) systems for iron–sulfur cluster biosynthesis. These results show that we can now develop fundamental and quantitative genotype–phenotype relationships for stress responses on a genome-wide basis.
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC); Univ. of California, Oakland, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1577615
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Proceedings of the National Academy of Sciences of the United States of America
- Additional Journal Information:
- Journal Volume: 116; Journal Issue: 28; Journal ID: ISSN 0027-8424
- Publisher:
- National Academy of Sciences
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Science & Technology; reactive oxygen species; oxidative stress; metabolism; protein expression; genome-scale model
Citation Formats
Cellular responses to reactive oxygen species are predicted from molecular mechanisms. United States: N. p., 2019.
Web. doi:10.1073/pnas.1905039116.
Cellular responses to reactive oxygen species are predicted from molecular mechanisms. United States. doi:https://doi.org/10.1073/pnas.1905039116
Wed .
"Cellular responses to reactive oxygen species are predicted from molecular mechanisms". United States. doi:https://doi.org/10.1073/pnas.1905039116. https://www.osti.gov/servlets/purl/1577615.
@article{osti_1577615,
title = {Cellular responses to reactive oxygen species are predicted from molecular mechanisms},
author = {None, None},
abstractNote = {Catalysis using iron–sulfur clusters and transition metals can be traced back to the last universal common ancestor. The damage to metalloproteins caused by reactive oxygen species (ROS) can prevent cell growth and survival when unmanaged, thus eliciting an essential stress response that is universal and fundamental in biology. Here we develop a computable multiscale description of the ROS stress response in Escherichia coli, called OxidizeME. We use OxidizeME to explain four key responses to oxidative stress: 1) ROS-induced auxotrophy for branched-chain, aromatic, and sulfurous amino acids; 2) nutrient-dependent sensitivity of growth rate to ROS; 3) ROS-specific differential gene expression separate from global growth-associated differential expression; and 4) coordinated expression of iron–sulfur cluster (ISC) and sulfur assimilation (SUF) systems for iron–sulfur cluster biosynthesis. These results show that we can now develop fundamental and quantitative genotype–phenotype relationships for stress responses on a genome-wide basis.},
doi = {10.1073/pnas.1905039116},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 28,
volume = 116,
place = {United States},
year = {2019},
month = {7}
}
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Works referenced in this record:
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- Ranquet, Caroline; Ollagnier-de-Choudens, Sandrine; Loiseau, Laurent
- Journal of Biological Chemistry, Vol. 282, Issue 42
A domino effect in antifolate drug action in Escherichia coli
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- Kwon, Yun Kyung; Lu, Wenyun; Melamud, Eugene
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Genome-Scale Reconstruction of Escherichia coli's Transcriptional and Translational Machinery: A Knowledge Base, Its Mathematical Formulation, and Its Functional Characterization
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Thermosensitivity of growth is determined by chaperone-mediated proteome reallocation
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- Proceedings of the National Academy of Sciences, Vol. 114, Issue 43
Bacterial persistence is an active σ S stress response to metabolic flux limitation
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- Molecular Systems Biology, Vol. 12, Issue 9
A role for tetrahydrofolates in the metabolism of iron-sulfur clusters in all domains of life
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DynamicME: dynamic simulation and refinement of integrated models of metabolism and protein expression
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Coordinate Regulation of the Suf and Isc Fe-S Cluster Biogenesis Pathways by IscR Is Essential for Viability of Escherichia coli
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- Mettert, E. L.; Kiley, P. J.
- Journal of Bacteriology, Vol. 196, Issue 24
HtrA Stress Protein Is Involved in Intramacrophagic Replication of Adherent and Invasive Escherichia coli Strain LF82 Isolated from a Patient with Crohn's Disease
journal, January 2005
- Bringer, M. -A.; Barnich, N.; Glasser, A. -L.
- Infection and Immunity, Vol. 73, Issue 2
The iron-sulfur clusters of dehydratases are primary intracellular targets of copper toxicity
journal, May 2009
- Macomber, L.; Imlay, J. A.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 20
Oxidative stress and disruption of labile iron generate specific auxotrophic requirements in Salmonella enterica
journal, January 2009
- Thorgersen, Michael P.; Downs, Diana M.
- Microbiology, Vol. 155, Issue 1
Modeling the multi-scale mechanisms of macromolecular resource allocation
journal, October 2018
- Yang, Laurence; Yurkovich, James T.; King, Zachary A.
- Current Opinion in Microbiology, Vol. 45
Superoxide Imposes Leakage of Sulfite fromEscherichia coli
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- Benov, Ludmil; Fridovich, Irwin
- Archives of Biochemistry and Biophysics, Vol. 347, Issue 2
Iron homeostasis in Mycobacterium tuberculosis is essential for persistence
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- Pandey, Manitosh; Talwar, Sakshi; Bose, Sutapa
- Scientific Reports, Vol. 8, Issue 1
Potentiating antibacterial activity by predictably enhancing endogenous microbial ROS production
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- Brynildsen, Mark P.; Winkler, Jonathan A.; Spina, Catherine S.
- Nature Biotechnology, Vol. 31, Issue 2
Studies of IscR reveal a unique mechanism for metal-dependent regulation of DNA binding specificity
journal, May 2013
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Bacterial persistence from a system-level perspective
journal, August 2017
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- Current Opinion in Biotechnology, Vol. 46
Multiscale Modeling of Metabolism and Macromolecular Synthesis in E. coli and Its Application to the Evolution of Codon Usage
journal, September 2012
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Reliable and efficient solution of genome-scale models of Metabolism and macromolecular Expression
journal, January 2017
- Ma, Ding; Yang, Laurence; Fleming, Ronan M. T.
- Scientific Reports, Vol. 7, Issue 1
The power to reduce: pyridine nucleotides – small molecules with a multitude of functions
journal, February 2007
- Pollak, Nadine; Dölle, Christian; Ziegler, Mathias
- Biochemical Journal, Vol. 402, Issue 2
COBRAme: A computational framework for genome-scale models of metabolism and gene expression
journal, July 2018
- Lloyd, Colton J.; Ebrahim, Ali; Yang, Laurence
- PLOS Computational Biology, Vol. 14, Issue 7
Genome‐scale models of metabolism and gene expression extend and refine growth phenotype prediction
journal, January 2013
- O'Brien, Edward J.; Lerman, Joshua A.; Chang, Roger L.
- Molecular Systems Biology, Vol. 9, Issue 1
Intracellular Hydrogen Peroxide and Superoxide Poison 3-Deoxy-D-Arabinoheptulosonate 7-Phosphate Synthase, the First Committed Enzyme in the Aromatic Biosynthetic Pathway of Escherichia coli
journal, March 2014
- Sobota, J. M.; Gu, M.; Imlay, J. A.
- Journal of Bacteriology, Vol. 196, Issue 11
Evolutionary adaptations that enable enzymes to tolerate oxidative stress
journal, August 2019
- Imlay, James A.; Sethu, Ramakrishnan; Rohaun, Sanjay Kumar
- Free Radical Biology and Medicine, Vol. 140
Iron enzyme ribulose-5-phosphate 3-epimerase in Escherichia coli is rapidly damaged by hydrogen peroxide but can be protected by manganese
journal, March 2011
- Sobota, J. M.; Imlay, J. A.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 13
Use of Adaptive Laboratory Evolution To Discover Key Mutations Enabling Rapid Growth of Escherichia coli K-12 MG1655 on Glucose Minimal Medium
journal, October 2014
- LaCroix, Ryan A.; Sandberg, Troy E.; O'Brien, Edward J.
- Applied and Environmental Microbiology, Vol. 81, Issue 1
Atmospheric oxygenation three billion years ago
journal, September 2013
- Crowe, Sean A.; Døssing, Lasse N.; Beukes, Nicolas J.
- Nature, Vol. 501, Issue 7468
The Mismetallation of Enzymes during Oxidative Stress
journal, August 2014
- Imlay, James A.
- Journal of Biological Chemistry, Vol. 289, Issue 41
ALEdb 1.0: a database of mutations from adaptive laboratory evolution experimentation
journal, October 2018
- Phaneuf, Patrick V.; Gosting, Dennis; Palsson, Bernhard O.
- Nucleic Acids Research, Vol. 47, Issue D1
The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium
journal, May 2013
- Imlay, James A.
- Nature Reviews Microbiology, Vol. 11, Issue 7
The Mechanism of the Auxotrophy for Sulfur-containing Amino Acids Imposed upon Escherichia coli by Superoxide
journal, August 1996
- Benov, Ludmil; Kredich, Nicholas M.; Fridovich, Irwin
- Journal of Biological Chemistry, Vol. 271, Issue 35
Mycobacteria and the Intraphagosomal Environment: Take It With a Pinch of Salt(s)!: Sensing and Regulation of the Intraphagosomal Environment
journal, April 2012
- Soldati, Thierry; Neyrolles, Olivier
- Traffic, Vol. 13, Issue 8
The quantitative and condition-dependent Escherichia coli proteome
journal, December 2015
- Schmidt, Alexander; Kochanowski, Karl; Vedelaar, Silke
- Nature Biotechnology, Vol. 34, Issue 1
Why Superoxide Imposes an Aromatic Amino Acid Auxotrophy on Escherichia coli : THE TRANSKETOLASE CONNECTION
journal, February 1999
- Benov, Ludmil; Fridovich, Irwin
- Journal of Biological Chemistry, Vol. 274, Issue 7
Reprint of: Iron/sulfur proteins biogenesis in prokaryotes: Formation, regulation and diversity
journal, August 2013
- Roche, Béatrice; Aussel, Laurent; Ezraty, Benjamin
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 8-9
iML1515, a knowledgebase that computes Escherichia coli traits
journal, October 2017
- Monk, Jonathan M.; Lloyd, Colton J.; Brunk, Elizabeth
- Nature Biotechnology, Vol. 35, Issue 10
Iron-sulphur clusters and the problem with oxygen
journal, February 2006
- Imlay, James A.
- Molecular Microbiology, Vol. 59, Issue 4
Escherichia coli RIC Is Able to Donate Iron to Iron-Sulfur Clusters
journal, April 2014
- Nobre, Lígia S.; Garcia-Serres, Ricardo; Todorovic, Smilja
- PLoS ONE, Vol. 9, Issue 4
solveME: fast and reliable solution of nonlinear ME models
journal, September 2016
- Yang, Laurence; Ma, Ding; Ebrahim, Ali
- BMC Bioinformatics, Vol. 17, Issue 1
Where in the world do bacteria experience oxidative stress?: Oxidative stress in natural environments
journal, November 2018
- Imlay, James A.
- Environmental Microbiology, Vol. 21, Issue 2
SoxRS-Regulated Expression and Genetic Analysis of the yggX Gene of Escherichia coli
journal, October 2003
- Pomposiello, P. J.; Koutsolioutsou, A.; Carrasco, D.
- Journal of Bacteriology, Vol. 185, Issue 22
NADPH: ferredoxin oxidoreductase acts as a paraquat diaphorase and is a member of the soxRS regulon.
journal, February 1994
- Liochev, S. I.; Hausladen, A.; Beyer, W. F.
- Proceedings of the National Academy of Sciences, Vol. 91, Issue 4
The physiology and habitat of the last universal common ancestor
journal, July 2016
- Weiss, Madeline C.; Sousa, Filipa L.; Mrnjavac, Natalia
- Nature Microbiology, Vol. 1, Issue 9
The Identification of Primary Sites of Superoxide and Hydrogen Peroxide Formation in the Aerobic Respiratory Chain and Sulfite Reductase Complex of Escherichia coli
journal, April 1999
- Messner, Kevin R.; Imlay, James A.
- Journal of Biological Chemistry, Vol. 274, Issue 15
A role of ygfZ in the Escherichia coli response to plumbagin challenge
journal, January 2010
- Lin, Ching-Nan; Syu, Wan-Jr; Sun, Wei-Sheng W.
- Journal of Biomedical Science, Vol. 17, Issue 1
Works referencing / citing this record:
Superoxide Imposes Leakage of Sulfite fromEscherichia coli
journal, November 1997
- Benov, Ludmil; Fridovich, Irwin
- Archives of Biochemistry and Biophysics, Vol. 347, Issue 2
Reprint of: Iron/sulfur proteins biogenesis in prokaryotes: Formation, regulation and diversity
journal, August 2013
- Roche, Béatrice; Aussel, Laurent; Ezraty, Benjamin
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 8-9
Bacterial persistence from a system-level perspective
journal, August 2017
- Radzikowski, Jakub Leszek; Schramke, Hannah; Heinemann, Matthias
- Current Opinion in Biotechnology, Vol. 46
Evolutionary adaptations that enable enzymes to tolerate oxidative stress
journal, August 2019
- Imlay, James A.; Sethu, Ramakrishnan; Rohaun, Sanjay Kumar
- Free Radical Biology and Medicine, Vol. 140
Modeling the multi-scale mechanisms of macromolecular resource allocation
journal, October 2018
- Yang, Laurence; Yurkovich, James T.; King, Zachary A.
- Current Opinion in Microbiology, Vol. 45
Genome‐scale models of metabolism and gene expression extend and refine growth phenotype prediction
journal, January 2013
- O'Brien, Edward J.; Lerman, Joshua A.; Chang, Roger L.
- Molecular Systems Biology, Vol. 9, Issue 1
Atmospheric oxygenation three billion years ago
journal, September 2013
- Crowe, Sean A.; Døssing, Lasse N.; Beukes, Nicolas J.
- Nature, Vol. 501, Issue 7468
Potentiating antibacterial activity by predictably enhancing endogenous microbial ROS production
journal, January 2013
- Brynildsen, Mark P.; Winkler, Jonathan A.; Spina, Catherine S.
- Nature Biotechnology, Vol. 31, Issue 2
The quantitative and condition-dependent Escherichia coli proteome
journal, December 2015
- Schmidt, Alexander; Kochanowski, Karl; Vedelaar, Silke
- Nature Biotechnology, Vol. 34, Issue 1
iML1515, a knowledgebase that computes Escherichia coli traits
journal, October 2017
- Monk, Jonathan M.; Lloyd, Colton J.; Brunk, Elizabeth
- Nature Biotechnology, Vol. 35, Issue 10
A domino effect in antifolate drug action in Escherichia coli
journal, August 2008
- Kwon, Yun Kyung; Lu, Wenyun; Melamud, Eugene
- Nature Chemical Biology, Vol. 4, Issue 10
The physiology and habitat of the last universal common ancestor
journal, July 2016
- Weiss, Madeline C.; Sousa, Filipa L.; Mrnjavac, Natalia
- Nature Microbiology, Vol. 1, Issue 9
The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium
journal, May 2013
- Imlay, James A.
- Nature Reviews Microbiology, Vol. 11, Issue 7
Studies of IscR reveal a unique mechanism for metal-dependent regulation of DNA binding specificity
journal, May 2013
- Rajagopalan, Senapathy; Teter, Sarah J.; Zwart, Petrus H.
- Nature Structural & Molecular Biology, Vol. 20, Issue 6
Iron homeostasis in Mycobacterium tuberculosis is essential for persistence
journal, November 2018
- Pandey, Manitosh; Talwar, Sakshi; Bose, Sutapa
- Scientific Reports, Vol. 8, Issue 1
Reliable and efficient solution of genome-scale models of Metabolism and macromolecular Expression
journal, January 2017
- Ma, Ding; Yang, Laurence; Fleming, Ronan M. T.
- Scientific Reports, Vol. 7, Issue 1
The power to reduce: pyridine nucleotides – small molecules with a multitude of functions
journal, February 2007
- Pollak, Nadine; Dölle, Christian; Ziegler, Mathias
- Biochemical Journal, Vol. 402, Issue 2
The iron-sulfur clusters of dehydratases are primary intracellular targets of copper toxicity
journal, May 2009
- Macomber, L.; Imlay, J. A.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 20
A role for tetrahydrofolates in the metabolism of iron-sulfur clusters in all domains of life
journal, May 2010
- Waller, J. C.; Alvarez, S.; Naponelli, V.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 23
Iron enzyme ribulose-5-phosphate 3-epimerase in Escherichia coli is rapidly damaged by hydrogen peroxide but can be protected by manganese
journal, March 2011
- Sobota, J. M.; Imlay, J. A.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 13
Thermosensitivity of growth is determined by chaperone-mediated proteome reallocation
journal, October 2017
- Chen, Ke; Gao, Ye; Mih, Nathan
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 43
NADPH: ferredoxin oxidoreductase acts as a paraquat diaphorase and is a member of the soxRS regulon.
journal, February 1994
- Liochev, S. I.; Hausladen, A.; Beyer, W. F.
- Proceedings of the National Academy of Sciences, Vol. 91, Issue 4
The Mechanism of the Auxotrophy for Sulfur-containing Amino Acids Imposed upon Escherichia coli by Superoxide
journal, August 1996
- Benov, Ludmil; Kredich, Nicholas M.; Fridovich, Irwin
- Journal of Biological Chemistry, Vol. 271, Issue 35
The Identification of Primary Sites of Superoxide and Hydrogen Peroxide Formation in the Aerobic Respiratory Chain and Sulfite Reductase Complex of Escherichia coli
journal, April 1999
- Messner, Kevin R.; Imlay, James A.
- Journal of Biological Chemistry, Vol. 274, Issue 15
Why Superoxide Imposes an Aromatic Amino Acid Auxotrophy on Escherichia coli : THE TRANSKETOLASE CONNECTION
journal, February 1999
- Benov, Ludmil; Fridovich, Irwin
- Journal of Biological Chemistry, Vol. 274, Issue 7
Cobalt Stress in Escherichia coli
journal, July 2007
- Ranquet, Caroline; Ollagnier-de-Choudens, Sandrine; Loiseau, Laurent
- Journal of Biological Chemistry, Vol. 282, Issue 42
The Mismetallation of Enzymes during Oxidative Stress
journal, August 2014
- Imlay, James A.
- Journal of Biological Chemistry, Vol. 289, Issue 41
ALEdb 1.0: a database of mutations from adaptive laboratory evolution experimentation
journal, October 2018
- Phaneuf, Patrick V.; Gosting, Dennis; Palsson, Bernhard O.
- Nucleic Acids Research, Vol. 47, Issue D1
Oxidative stress and disruption of labile iron generate specific auxotrophic requirements in Salmonella enterica
journal, January 2009
- Thorgersen, Michael P.; Downs, Diana M.
- Microbiology, Vol. 155, Issue 1
Where in the world do bacteria experience oxidative stress?: Oxidative stress in natural environments
journal, November 2018
- Imlay, James A.
- Environmental Microbiology, Vol. 21, Issue 2
Iron-sulphur clusters and the problem with oxygen
journal, February 2006
- Imlay, James A.
- Molecular Microbiology, Vol. 59, Issue 4
Mycobacteria and the Intraphagosomal Environment: Take It With a Pinch of Salt(s)!: Sensing and Regulation of the Intraphagosomal Environment
journal, April 2012
- Soldati, Thierry; Neyrolles, Olivier
- Traffic, Vol. 13, Issue 8
Use of Adaptive Laboratory Evolution To Discover Key Mutations Enabling Rapid Growth of Escherichia coli K-12 MG1655 on Glucose Minimal Medium
journal, October 2014
- LaCroix, Ryan A.; Sandberg, Troy E.; O'Brien, Edward J.
- Applied and Environmental Microbiology, Vol. 81, Issue 1
HtrA Stress Protein Is Involved in Intramacrophagic Replication of Adherent and Invasive Escherichia coli Strain LF82 Isolated from a Patient with Crohn's Disease
journal, January 2005
- Bringer, M. -A.; Barnich, N.; Glasser, A. -L.
- Infection and Immunity, Vol. 73, Issue 2
Intracellular Hydrogen Peroxide and Superoxide Poison 3-Deoxy-D-Arabinoheptulosonate 7-Phosphate Synthase, the First Committed Enzyme in the Aromatic Biosynthetic Pathway of Escherichia coli
journal, March 2014
- Sobota, J. M.; Gu, M.; Imlay, J. A.
- Journal of Bacteriology, Vol. 196, Issue 11
Coordinate Regulation of the Suf and Isc Fe-S Cluster Biogenesis Pathways by IscR Is Essential for Viability of Escherichia coli
journal, September 2014
- Mettert, E. L.; Kiley, P. J.
- Journal of Bacteriology, Vol. 196, Issue 24
SoxRS-Regulated Expression and Genetic Analysis of the yggX Gene of Escherichia coli
journal, October 2003
- Pomposiello, P. J.; Koutsolioutsou, A.; Carrasco, D.
- Journal of Bacteriology, Vol. 185, Issue 22
A role of ygfZ in the Escherichia coli response to plumbagin challenge
journal, January 2010
- Lin, Ching-Nan; Syu, Wan-Jr; Sun, Wei-Sheng W.
- Journal of Biomedical Science, Vol. 17, Issue 1
solveME: fast and reliable solution of nonlinear ME models
journal, September 2016
- Yang, Laurence; Ma, Ding; Ebrahim, Ali
- BMC Bioinformatics, Vol. 17, Issue 1
DynamicME: dynamic simulation and refinement of integrated models of metabolism and protein expression
journal, January 2019
- Yang, Laurence; Ebrahim, Ali; Lloyd, Colton J.
- BMC Systems Biology, Vol. 13, Issue 1
Genome-Scale Reconstruction of Escherichia coli's Transcriptional and Translational Machinery: A Knowledge Base, Its Mathematical Formulation, and Its Functional Characterization
journal, March 2009
- Thiele, Ines; Jamshidi, Neema; Fleming, Ronan M. T.
- PLoS Computational Biology, Vol. 5, Issue 3
COBRAme: A computational framework for genome-scale models of metabolism and gene expression
journal, July 2018
- Lloyd, Colton J.; Ebrahim, Ali; Yang, Laurence
- PLOS Computational Biology, Vol. 14, Issue 7
Multiscale Modeling of Metabolism and Macromolecular Synthesis in E. coli and Its Application to the Evolution of Codon Usage
journal, September 2012
- Thiele, Ines; Fleming, Ronan M. T.; Que, Richard
- PLoS ONE, Vol. 7, Issue 9
Escherichia coli RIC Is Able to Donate Iron to Iron-Sulfur Clusters
journal, April 2014
- Nobre, Lígia S.; Garcia-Serres, Ricardo; Todorovic, Smilja
- PLoS ONE, Vol. 9, Issue 4
Bacterial persistence is an active σ S stress response to metabolic flux limitation
journal, September 2016
- Radzikowski, Jakub Leszek; Vedelaar, Silke; Siegel, David
- Molecular Systems Biology, Vol. 12, Issue 9
Adaptive evolution reveals a tradeoff between growth rate and oxidative stress during naphthoquinone-based aerobic respiration
journal, November 2019
- Anand, Amitesh; Chen, Ke; Yang, Laurence
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 50