Laboratory evolution, transcriptomics, and modeling reveal mechanisms of paraquat tolerance

Rychel, Kevin; Tan, Justin; Patel, Arjun; Lamoureux, Cameron; Hefner, Ying; Szubin, Richard; Johnsen, Josefin; Mohamed, Elsayed Tharwat Tolba; Phaneuf, Patrick V.; Anand, Amitesh; Olson, Connor A.; Park, Joon Ho; Sastry, Anand V.; Yang, Laurence; Feist, Adam M.; Palsson, Bernhard O.

doi:10.1016/j.celrep.2023.113105

Title: Laboratory evolution, transcriptomics, and modeling reveal mechanisms of paraquat tolerance

Journal Article · 19 September 2023 · Cell Reports

DOI: https://doi.org/10.1016/j.celrep.2023.113105 · OSTI ID:2001157

^[1]; Tan, Justin ^[1]; Patel, Arjun ^[1]; Lamoureux, Cameron ^[1]; Hefner, Ying ^[1]; Szubin, Richard ^[1]; Johnsen, Josefin ^[2]; Mohamed, Elsayed Tharwat Tolba ^[2]; Phaneuf, Patrick V. ^[2]; Anand, Amitesh ^[3]; Olson, Connor A. ^[1]; Park, Joon Ho ^[4]; Sastry, Anand V. ^[1]; Yang, Laurence ^[5]; Feist, Adam M. ^[6];

^[6]

Univ. of California, San Diego, CA (United States)
Technical Univ. of Denmark, Lyngby (Denmark)
Tata Institute of Fundamental Research (India)
Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
Queen's Univ., Kingston, ON (Canada)
Univ. of California, San Diego, CA (United States); Technical Univ. of Denmark, Lyngby (Denmark)

Relationships between the genome, transcriptome, and metabolome underlie all evolved phenotypes. However, it has proved difficult to elucidate these relationships because of the high number of variables measured. A recently developed data analytic method for characterizing the transcriptome can simplify interpretation by grouping genes into independently modulated sets (iModulons). Here, we demonstrate how iModulons reveal deep understanding of the effects of causal mutations and metabolic rewiring. We use adaptive laboratory evolution to generate E. coli strains that tolerate high levels of the redox cycling compound paraquat, which produces reactive oxygen species (ROS). We combine resequencing, iModulons, and metabolic models to elucidate six interacting stress-tolerance mechanisms: (1) modification of transport, (2) activation of ROS stress responses, (3) use of ROS-sensitive iron regulation, (4) motility, (5) broad transcriptional reallocation toward growth, and (6) metabolic rewiring to decrease NADH production. This work thus demonstrates the power of iModulon knowledge mapping for evolution analysis.

View Journal Article

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); USDOE

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2001157

Alternate ID(s):: OSTI ID: 2422991

Journal Information:: Cell Reports, Vol. 42, Issue 9; ISSN 2211-1247

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (76)

MultiQC: summarize analysis results for multiple tools and samples in a single report Ewels, Philip; Magnusson, Måns; Lundin, Sverker Bioinformatics, Vol. 32, Issue 19 https://doi.org/10.1093/bioinformatics/btw354	journal	June 2016
Intracellular production of superoxide radical and of hydrogen peroxide by redox active compounds Hassan, H. Moustafa; Fridovich, Irwin Archives of Biochemistry and Biophysics, Vol. 196, Issue 2 https://doi.org/10.1016/0003-9861(79)90289-3	journal	September 1979
Determining the Control Circuitry of Redox Metabolism at the Genome-Scale Federowicz, Stephen; Kim, Donghyuk; Ebrahim, Ali PLoS Genetics, Vol. 10, Issue 4 https://doi.org/10.1371/journal.pgen.1004264	journal	April 2014
Machine Learning Uncovers a Data-Driven Transcriptional Regulatory Network for the Crenarchaeal Thermoacidophile Sulfolobus acidocaldarius Chauhan, Siddharth M.; Poudel, Saugat; Rychel, Kevin Frontiers in Microbiology, Vol. 12 https://doi.org/10.3389/fmicb.2021.753521	journal	October 2021
Cutadapt removes adapter sequences from high-throughput sequencing reads Martin, Marcel EMBnet.journal, Vol. 17, Issue 1 https://doi.org/10.14806/ej.17.1.200	journal	May 2011
Tools for developing tolerance to toxic chemicals in microbial systems and perspectives on moving the field forward and into the industrial setting Peabody, George L.; Winkler, James; Kao, Katy C. Current Opinion in Chemical Engineering, Vol. 6 https://doi.org/10.1016/j.coche.2014.08.001	journal	November 2014
Bacterial fitness landscapes stratify based on proteome allocation associated with discrete aero-types Chen, Ke; Anand, Amitesh; Olson, Connor PLOS Computational Biology, Vol. 17, Issue 1 https://doi.org/10.1371/journal.pcbi.1008596	journal	January 2021
RSeQC: quality control of RNA-seq experiments Wang, Liguo; Wang, Shengqin; Li, Wei Bioinformatics, Vol. 28, Issue 16 https://doi.org/10.1093/bioinformatics/bts356	journal	June 2012
Optimal dimensionality selection for independent component analysis of transcriptomic data McConn, John Luke; Lamoureux, Cameron R.; Poudel, Saugat BMC Bioinformatics, Vol. 22, Issue 1 https://doi.org/10.1186/s12859-021-04497-7	journal	December 2021
Electron transfer in di(deoxy)nucleoside phosphates in aqueous solution: rapid migration of oxidative damage (via adenine) to guanine Candeias, Luis Pedro; Steenken, Steen Journal of the American Chemical Society, Vol. 115, Issue 6 https://doi.org/10.1021/ja00059a044	journal	March 1993
Defining bacterial regulons using ChIP-seq Myers, Kevin S.; Park, Dan M.; Beauchene, Nicole A. Methods, Vol. 86 https://doi.org/10.1016/j.ymeth.2015.05.022	journal	September 2015
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome Langmead, Ben; Trapnell, Cole; Pop, Mihai Genome Biology, Vol. 10, Issue 3 https://doi.org/10.1186/gb-2009-10-3-r25	journal	January 2009
Micromolar Intracellular Hydrogen Peroxide Disrupts Metabolism by Damaging Iron-Sulfur Enzymes Jang, Soojin; Imlay, James A. Journal of Biological Chemistry, Vol. 282, Issue 2 https://doi.org/10.1074/jbc.M607646200	journal	November 2006
Biotin Sensing: Universal Influence of Biotin Status on Transcription Beckett, Dorothy Annual Review of Genetics, Vol. 41, Issue 1 https://doi.org/10.1146/annurev.genet.41.042007.170450	journal	December 2007
Laboratory evolution of synthetic electron transport system variants reveals a larger metabolic respiratory system and its plasticity Anand, Amitesh; Patel, Arjun; Chen, Ke Nature Communications, Vol. 13, Issue 1 https://doi.org/10.1038/s41467-022-30877-5	journal	June 2022
The FeoC [4Fe–4S] Cluster Is Redox-Active and Rapidly Oxygen-Sensitive Smith, Aaron T.; Linkous, Richard O.; Max, Nathan J. Biochemistry, Vol. 58, Issue 49 https://doi.org/10.1021/acs.biochem.9b00745	journal	November 2019
The novel structure and chemistry of iron–sulfur clusters in the adenosylmethionine-dependent radical enzyme biotin synthase Jarrett, Joseph T. Archives of Biochemistry and Biophysics, Vol. 433, Issue 1 https://doi.org/10.1016/j.abb.2004.10.003	journal	January 2005
Linearization and transposition of circular molecules of insertion sequence IS3 Sekine, Yasuhiko; Aihara, Kotaro; Ohtsubo, Eiichi Journal of Molecular Biology, Vol. 294, Issue 1 https://doi.org/10.1006/jmbi.1999.3181	journal	November 1999
Adaptive evolution reveals a tradeoff between growth rate and oxidative stress during naphthoquinone-based aerobic respiration Anand, Amitesh; Chen, Ke; Yang, Laurence Proceedings of the National Academy of Sciences, Vol. 116, Issue 50 https://doi.org/10.1073/pnas.1909987116	journal	November 2019
iModulonDB: a knowledgebase of microbial transcriptional regulation derived from machine learning Rychel, Kevin; Decker, Katherine; Sastry, Anand V. Nucleic Acids Research, Vol. 49, Issue D1 https://doi.org/10.1093/nar/gkaa810	journal	October 2020
Use of Adaptive Laboratory Evolution To Discover Key Mutations Enabling Rapid Growth of Escherichia coli K-12 MG1655 on Glucose Minimal Medium LaCroix, Ryan A.; Sandberg, Troy E.; O'Brien, Edward J. Applied and Environmental Microbiology, Vol. 81, Issue 1 https://doi.org/10.1128/AEM.02246-14	journal	October 2014
Identification of a quinone-sensitive redox switch in the ArcB sensor kinase Malpica, R.; Franco, B.; Rodriguez, C. Proceedings of the National Academy of Sciences, Vol. 101, Issue 36 https://doi.org/10.1073/pnas.0403064101	journal	August 2004
Function, Evolution, and Composition of the RpoS Regulon in Escherichia coli Schellhorn, Herb E. Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.560099	journal	September 2020
Machine Learning of All Mycobacterium tuberculosis H37Rv RNA-seq Data Reveals a Structured Interplay between Metabolism, Stress Response, and Infection Yoo, Reo; Rychel, Kevin; Poudel, Saugat mSphere, Vol. 7, Issue 2 https://doi.org/10.1128/msphere.00033-22	journal	April 2022
featureCounts: an efficient general purpose program for assigning sequence reads to genomic features Liao, Y.; Smyth, G. K.; Shi, W. Bioinformatics, Vol. 30, Issue 7 https://doi.org/10.1093/bioinformatics/btt656	journal	November 2013
Machine-learning from Pseudomonas putida KT2440 transcriptomes reveals its transcriptional regulatory network Lim, Hyun Gyu; Rychel, Kevin; Sastry, Anand V. Metabolic Engineering, Vol. 72 https://doi.org/10.1016/j.ymben.2022.04.004	journal	July 2022
The Escherichia coli transcriptome mostly consists of independently regulated modules Sastry, Anand V.; Gao, Ye; Szubin, Richard Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-13483-w	journal	December 2019
Experimental Evolution Reveals Unifying Systems-Level Adaptations but Diversity in Driving Genotypes Kavvas, Erol S.; Long, Christopher P.; Sastry, Anand mSystems, Vol. 7, Issue 6 https://doi.org/10.1128/msystems.00165-22	journal	December 2022
Global Rebalancing of Cellular Resources by Pleiotropic Point Mutations Illustrates a Multi-scale Mechanism of Adaptive Evolution Utrilla, Jose; O’Brien, Edward J.; Chen, Ke Cell Systems, Vol. 2, Issue 4 https://doi.org/10.1016/j.cels.2016.04.003	journal	April 2016
A streamlined ribosome profiling protocol for the characterization of microorganisms Latif, Haythem; Szubin, Richard; Tan, Justin BioTechniques, Vol. 58, Issue 6 https://doi.org/10.2144/000114302	journal	June 2015
OxyS small RNA induces cell cycle arrest to allow DNA damage repair Barshishat, Shir; Elgrably‐Weiss, Maya; Edelstein, Jonathan The EMBO Journal, Vol. 37, Issue 3 https://doi.org/10.15252/embj.201797651	journal	December 2017
FlhD/FlhC Is a Regulator of Anaerobic Respiration and the Entner-Doudoroff Pathway through Induction of the Methyl-Accepting Chemotaxis Protein Aer Pruss, B. M.; Campbell, J. W.; Van Dyk, T. K. Journal of Bacteriology, Vol. 185, Issue 2 https://doi.org/10.1128/JB.185.2.534-543.2003	journal	January 2003
Paraquat and Escherichia coli. Mechanism of production of extracellular superoxide radical. Hassan, H. M.; Fridovich, I. Journal of Biological Chemistry, Vol. 254, Issue 21 https://doi.org/10.1016/S0021-9258(19)86598-5	journal	November 1979
Variation in Stress Responses within a Bacterial Species and the Indirect Costs of Stress Resistance Ferenci, T.; Spira, B. Annals of the New York Academy of Sciences, Vol. 1113, Issue 1 https://doi.org/10.1196/annals.1391.003	journal	May 2007
Cellular responses to reactive oxygen species are predicted from molecular mechanisms Yang, Laurence; Mih, Nathan; Anand, Amitesh Proceedings of the National Academy of Sciences, Vol. 116, Issue 28 https://doi.org/10.1073/pnas.1905039116	journal	July 2019
Mechanism of cytotoxicity of paraquat Fukushima, T.; Yamada, K.; Isobe, A. Experimental and Toxicologic Pathology, Vol. 45, Issue 5-6 https://doi.org/10.1016/S0940-2993(11)80424-0	journal	January 1993
Genome-scale Analysis of Escherichia coli FNR Reveals Complex Features of Transcription Factor Binding Myers, Kevin S.; Yan, Huihuang; Ong, Irene M. PLoS Genetics, Vol. 9, Issue 6 https://doi.org/10.1371/journal.pgen.1003565	journal	June 2013
Path to improving the life cycle and quality of genome-scale models of metabolism Seif, Yara; Palsson, Bernhard Ørn Cell Systems, Vol. 12, Issue 9 https://doi.org/10.1016/j.cels.2021.06.005	journal	September 2021
Machine learning uncovers independently regulated modules in the Bacillus subtilis transcriptome Rychel, Kevin; Sastry, Anand V.; Palsson, Bernhard O. Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-20153-9	journal	December 2020
Trouble is coming: Signaling pathways that regulate general stress responses in bacteria Gottesman, Susan Journal of Biological Chemistry, Vol. 294, Issue 31 https://doi.org/10.1074/jbc.REV119.005593	journal	June 2019
Advanced transcriptomic analysis reveals the role of efflux pumps and media composition in antibiotic responses of Pseudomonas aeruginosa Rajput, Akanksha; Tsunemoto, Hannah; Sastry, Anand V. Nucleic Acids Research, Vol. 50, Issue 17 https://doi.org/10.1093/nar/gkac743	journal	September 2022
Thermosensitivity of growth is determined by chaperone-mediated proteome reallocation Chen, Ke; Gao, Ye; Mih, Nathan Proceedings of the National Academy of Sciences, Vol. 114, Issue 43 https://doi.org/10.1073/pnas.1705524114	journal	October 2017
Genome-scale model of metabolism and gene expression provides a multi-scale description of acid stress responses in Escherichia coli Du, Bin; Yang, Laurence; Lloyd, Colton J. PLOS Computational Biology, Vol. 15, Issue 12 https://doi.org/10.1371/journal.pcbi.1007525	journal	December 2019
Regulation of inducible peroxide stress responses Mongkolsuk, Skorn; Helmann, John D. Molecular Microbiology, Vol. 45, Issue 1 https://doi.org/10.1046/j.1365-2958.2002.03015.x	journal	July 2002
Evolutionary consequences of drug resistance: shared principles across diverse targets and organisms Hughes, Diarmaid; Andersson, Dan I. Nature Reviews Genetics, Vol. 16, Issue 8 https://doi.org/10.1038/nrg3922	journal	July 2015
Pseudogene repair driven by selection pressure applied in experimental evolution Anand, Amitesh; Olson, Connor A.; Yang, Laurence Nature Microbiology, Vol. 4, Issue 3 https://doi.org/10.1038/s41564-018-0340-2	journal	January 2019
EmrE, an Escherichia coli 12-kDa Multidrug Transporter, Exchanges Toxic Cations and H ⁺ and Is Soluble in Organic Solvents Yerushalmi, Hagit; Lebendiker, Mario; Schuldiner, Shimon Journal of Biological Chemistry, Vol. 270, Issue 12 https://doi.org/10.1074/jbc.270.12.6856	journal	March 1995
Machine learning from Pseudomonas aeruginosa transcriptomes identifies independently modulated sets of genes associated with known transcriptional regulators Rajput, Akanksha; Tsunemoto, Hannah; Sastry, Anand V. Nucleic Acids Research, Vol. 50, Issue 7 https://doi.org/10.1093/nar/gkac187	journal	March 2022
AfterQC: automatic filtering, trimming, error removing and quality control for fastq data Chen, Shifu; Huang, Tanxiao; Zhou, Yanqing BMC Bioinformatics, Vol. 18, Issue S3 https://doi.org/10.1186/s12859-017-1469-3	journal	March 2017
Oxidative Stress in Bacteria and the Central Dogma of Molecular Biology Fasnacht, Michel; Polacek, Norbert Frontiers in Molecular Biosciences, Vol. 8 https://doi.org/10.3389/fmolb.2021.671037	journal	May 2021
Machine Learning of Bacterial Transcriptomes Reveals Responses Underlying Differential Antibiotic Susceptibility Sastry, Anand V.; Dillon, Nicholas; Anand, Amitesh mSphere, Vol. 6, Issue 4 https://doi.org/10.1128/mSphere.00443-21	journal	August 2021
Generation of a platform strain for ionic liquid tolerance using adaptive laboratory evolution Mohamed, Elsayed T.; Wang, Shizeng; Lennen, Rebecca M. Microbial Cell Factories, Vol. 16, Issue 1 https://doi.org/10.1186/s12934-017-0819-1	journal	November 2017
Two systems for the uptake of phosphate in Escherichia coli Rosenberg, H.; Gerdes, R. G.; Chegwidden, K. Journal of Bacteriology, Vol. 131, Issue 2 https://doi.org/10.1128/jb.131.2.505-511.1977	journal	August 1977
Diagnosing oxidative stress in bacteria: not as easy as you might think Imlay, James A. Current Opinion in Microbiology, Vol. 24 https://doi.org/10.1016/j.mib.2015.01.004	journal	April 2015
ROS Function in Redox Signaling and Oxidative Stress Schieber, Michael; Chandel, Navdeep S. Current Biology, Vol. 24, Issue 10 https://doi.org/10.1016/j.cub.2014.03.034	journal	May 2014
Paraquat diaphorases in Escherichia coli Liochev, Stefan I.; Fridovich, Irwin Free Radical Biology and Medicine, Vol. 16, Issue 5 https://doi.org/10.1016/0891-5849(94)90055-8	journal	May 1994
Revealing 29 sets of independently modulated genes in Staphylococcus aureus , their regulators, and role in key physiological response Poudel, Saugat; Tsunemoto, Hannah; Seif, Yara Proceedings of the National Academy of Sciences, Vol. 117, Issue 29 https://doi.org/10.1073/pnas.2008413117	journal	July 2020
Identification of Mutations in Laboratory-Evolved Microbes from Next-Generation Sequencing Data Using breseq Deatherage, Daniel E.; Barrick, Jeffrey E. Methods in Molecular Biology https://doi.org/10.1007/978-1-4939-0554-6_12	book	January 2014
OxyR Is a Convergent Target for Mutations Acquired during Adaptation to Oxidative Stress-Prone Metabolic States Anand, Amitesh; Chen, Ke; Catoiu, Edward Molecular Biology and Evolution, Vol. 37, Issue 3 https://doi.org/10.1093/molbev/msz251	journal	October 2019
Restoration of fitness lost due to dysregulation of the pyruvate dehydrogenase complex is triggered by ribosomal binding site modifications Anand, Amitesh; Olson, Connor A.; Sastry, Anand V. Cell Reports, Vol. 35, Issue 1 https://doi.org/10.1016/j.celrep.2021.108961	journal	April 2021
The emergence of adaptive laboratory evolution as an efficient tool for biological discovery and industrial biotechnology Sandberg, Troy E.; Salazar, Michael J.; Weng, Liam L. Metabolic Engineering, Vol. 56 https://doi.org/10.1016/j.ymben.2019.08.004	journal	December 2019
ALEdb 1.0: a database of mutations from adaptive laboratory evolution experimentation Phaneuf, Patrick V.; Gosting, Dennis; Palsson, Bernhard O. Nucleic Acids Research, Vol. 47, Issue D1 https://doi.org/10.1093/nar/gky983	journal	October 2018
The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium Imlay, James A. Nature Reviews Microbiology, Vol. 11, Issue 7 https://doi.org/10.1038/nrmicro3032	journal	May 2013
A Model for Designing Adaptive Laboratory Evolution Experiments LaCroix, Ryan A.; Palsson, Bernhard O.; Feist, Adam M. Applied and Environmental Microbiology, Vol. 83, Issue 8 https://doi.org/10.1128/AEM.03115-16	journal	February 2017
Local and global regulation of transcription initiation in bacteria Browning, Douglas F.; Busby, Stephen J. W. Nature Reviews Microbiology, Vol. 14, Issue 10 https://doi.org/10.1038/nrmicro.2016.103	journal	August 2016
Evolution of Escherichia coli to 42 °C and Subsequent Genetic Engineering Reveals Adaptive Mechanisms and Novel Mutations Sandberg, Troy E.; Pedersen, Margit; LaCroix, Ryan A. Molecular Biology and Evolution, Vol. 31, Issue 10 https://doi.org/10.1093/molbev/msu209	journal	July 2014
A comprehensive evaluation of module detection methods for gene expression data Saelens, Wouter; Cannoodt, Robrecht; Saeys, Yvan Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-03424-4	journal	March 2018
Pan-Genome Analysis of Transcriptional Regulation in Six Salmonella enterica Serovar Typhimurium Strains Reveals Their Different Regulatory Structures Yuan, Yuan; Seif, Yara; Rychel, Kevin mSystems, Vol. 7, Issue 6 https://doi.org/10.1128/msystems.00467-22	journal	December 2022
iML1515, a knowledgebase that computes Escherichia coli traits Monk, Jonathan M.; Lloyd, Colton J.; Brunk, Elizabeth Nature Biotechnology, Vol. 35, Issue 10 https://doi.org/10.1038/nbt.3956	journal	October 2017
RegulonDB v 10.5: tackling challenges to unify classic and high throughput knowledge of gene regulation in E. coli K-12 Santos-Zavaleta, Alberto; Salgado, Heladia; Gama-Castro, Socorro Nucleic Acids Research, Vol. 47, Issue D1 https://doi.org/10.1093/nar/gky1077	journal	November 2018
Mitochondrial NADH–Quinone Oxidoreductase of the Outer Membrane Is Responsible for Paraquat Cytotoxicity in Rat Livers Shimada, Hiroki; Hirai, Kei-Ichi; Simamura, Eriko Archives of Biochemistry and Biophysics, Vol. 351, Issue 1 https://doi.org/10.1006/abbi.1997.0557	journal	March 1998
Oxidation of the Guanine Nucleotide Pool Underlies Cell Death by Bactericidal Antibiotics Foti, J. J.; Devadoss, B.; Winkler, J. A. Science, Vol. 336, Issue 6079 https://doi.org/10.1126/science.1219192	journal	April 2012
Where in the world do bacteria experience oxidative stress?: Oxidative stress in natural environments Imlay, James A. Environmental Microbiology, Vol. 21, Issue 2 https://doi.org/10.1111/1462-2920.14445	journal	November 2018
LeuO Expression in Response to Starvation for Branched-chain Amino Acids Majumder, Arundhati; Fang, Ming; Tsai, Kan-Jen Journal of Biological Chemistry, Vol. 276, Issue 22 https://doi.org/10.1074/jbc.M100945200	journal	June 2001
Causal mutations from adaptive laboratory evolution are outlined by multiple scales of genome annotations and condition-specificity Phaneuf, Patrick V.; Yurkovich, James T.; Heckmann, David BMC Genomics, Vol. 21, Issue 1 https://doi.org/10.1186/s12864-020-06920-4	journal	July 2020
Microbial competition: Escherichia coli mutants that take over stationary phase cultures Zambrano, M.; Siegele, D.; Almiron, M. Science, Vol. 259, Issue 5102 https://doi.org/10.1126/science.7681219	journal	March 1993

Similar Records

Systems Engineering of Rhodococcus opacus to Enable Production of Drop-in Fuels from Lignocellulose

Technical Report · 2023 · OSTI ID:1894624

Dantas, Gautam

Machine-learning from Pseudomonas putida KT2440 transcriptomes reveals its transcriptional regulatory network

Journal Article · 2022 · Metabolic Engineering · OSTI ID:1868499

Lim, Hyun Gyu; Rychel, Kevin; Sastry, Anand V.; +11 more

Tools and Models for Integrating Multiple Cellular Networks

Technical Report · 2015 · OSTI ID:1225189

Gerstein, Mark

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
systems biology
adaptive laboratory evolution
oxidative stress
paraquat
transcriptomics
transcriptional regulatory networks
computational biology
big data analytics

Title: Laboratory evolution, transcriptomics, and modeling reveal mechanisms of paraquat tolerance

Citation Formats

References (76)

Similar Records

Related Subjects