Mutations in global regulators lead to metabolic selection during adaptation to complex environments
Abstract
Adaptation to ecologically complex environments can provide insights into the evolutionary dynamics and functional constraints encountered by organisms during natural selection. Unlike adaptation to a single limiting resource, adaptation to a new environment with abundant and varied resources can be difficult to achieve by small incremental changes since many mutations are required to achieve even modest gains in fitness. Since changing complex environments are quite common in nature, we investigated how such an epistatic bottleneck can be avoided to allow rapid adaptation. We show that adaptive mutations arise repeatedly in independently evolved populations in the context of greatly increased genetic and phenotypic diversity. We go on to show that weak selection requiring substantial metabolic reprogramming can be readily achieved by mutations in the global response regulator arcA and the stress response regulator rpoS. We identified 46 unique single-nucleotide variants of arcA and 18 mutations in rpoS, nine of which resulted in stop codons or large deletions, suggesting that a subtle modulation of ArcA function and knockouts of rpoS are largely responsible for the metabolic shifts leading to adaptation. These mutations allow a higher order “metabolic selection” that eliminates epistatic bottlenecks, which could occur when many changes would be required. Proteomicmore »
- Authors:
-
- Rice Univ., Houston, TX (United States)
- United States Army Edgewood Chemical Biological Center, Aberdeen Proving Ground, MD (United States); EXCET, Inc., Springfield, VA (United Kingdom)
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
- Northern Arizona Univ., Flagstaff, AZ (United States)
- United States Army Edgewood Chemical Biological Center, Aberdeen Proving Ground, MD (United States)
- Univ. Paris Descartes (France)
- Publication Date:
- Research Org.:
- Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1166862
- Report Number(s):
- PNNL-SA-106551
Journal ID: ISSN 1553-7404; 400403909
- Grant/Contract Number:
- AC05-76RL01830
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS Genetics
- Additional Journal Information:
- Journal Volume: 10; Journal Issue: 12; Journal ID: ISSN 1553-7404
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; proteomics; genome analysis; serial passage; laboratory evolution; Escherichia coli; adaptation
Citation Formats
Saxer, Gerda, Krepps, Michael D., Merkley, Eric D., Ansong, Charles, Deatherage Kaiser, Brooke L., Valovska, Marie -Thérèse, Ristic, Nikola, Yeh, Ping T., Prakash, Vittal P., Leiser, Owen P., Nakhleh, Luay, Gibbons, Henry S., Kreuzer, Helen W., Shamoo, Yousif, and Matic, Ivan. Mutations in global regulators lead to metabolic selection during adaptation to complex environments. United States: N. p., 2014.
Web. doi:10.1371/journal.pgen.1004872.
Saxer, Gerda, Krepps, Michael D., Merkley, Eric D., Ansong, Charles, Deatherage Kaiser, Brooke L., Valovska, Marie -Thérèse, Ristic, Nikola, Yeh, Ping T., Prakash, Vittal P., Leiser, Owen P., Nakhleh, Luay, Gibbons, Henry S., Kreuzer, Helen W., Shamoo, Yousif, & Matic, Ivan. Mutations in global regulators lead to metabolic selection during adaptation to complex environments. United States. https://doi.org/10.1371/journal.pgen.1004872
Saxer, Gerda, Krepps, Michael D., Merkley, Eric D., Ansong, Charles, Deatherage Kaiser, Brooke L., Valovska, Marie -Thérèse, Ristic, Nikola, Yeh, Ping T., Prakash, Vittal P., Leiser, Owen P., Nakhleh, Luay, Gibbons, Henry S., Kreuzer, Helen W., Shamoo, Yousif, and Matic, Ivan. Thu .
"Mutations in global regulators lead to metabolic selection during adaptation to complex environments". United States. https://doi.org/10.1371/journal.pgen.1004872. https://www.osti.gov/servlets/purl/1166862.
@article{osti_1166862,
title = {Mutations in global regulators lead to metabolic selection during adaptation to complex environments},
author = {Saxer, Gerda and Krepps, Michael D. and Merkley, Eric D. and Ansong, Charles and Deatherage Kaiser, Brooke L. and Valovska, Marie -Thérèse and Ristic, Nikola and Yeh, Ping T. and Prakash, Vittal P. and Leiser, Owen P. and Nakhleh, Luay and Gibbons, Henry S. and Kreuzer, Helen W. and Shamoo, Yousif and Matic, Ivan},
abstractNote = {Adaptation to ecologically complex environments can provide insights into the evolutionary dynamics and functional constraints encountered by organisms during natural selection. Unlike adaptation to a single limiting resource, adaptation to a new environment with abundant and varied resources can be difficult to achieve by small incremental changes since many mutations are required to achieve even modest gains in fitness. Since changing complex environments are quite common in nature, we investigated how such an epistatic bottleneck can be avoided to allow rapid adaptation. We show that adaptive mutations arise repeatedly in independently evolved populations in the context of greatly increased genetic and phenotypic diversity. We go on to show that weak selection requiring substantial metabolic reprogramming can be readily achieved by mutations in the global response regulator arcA and the stress response regulator rpoS. We identified 46 unique single-nucleotide variants of arcA and 18 mutations in rpoS, nine of which resulted in stop codons or large deletions, suggesting that a subtle modulation of ArcA function and knockouts of rpoS are largely responsible for the metabolic shifts leading to adaptation. These mutations allow a higher order “metabolic selection” that eliminates epistatic bottlenecks, which could occur when many changes would be required. Proteomic and carbohydrate analysis of adapting E. coli populations revealed an up-regulation of enzymes associated with the TCA cycle and amino acid metabolism and an increase in the secretion of putrescine. The overall effect of adaptation across populations is to redirect and efficiently utilize uptake and catabolism of abundant amino acids. Concomitantly, there is a pronounced spread of more ecologically limited strains that results from specialization through metabolic erosion. Remarkably, the global regulators arcA and rpoS can provide a “one-step” mechanism of adaptation to a novel environment, which highlights the importance of global resource management as a powerful strategy to adaptation.},
doi = {10.1371/journal.pgen.1004872},
journal = {PLoS Genetics},
number = 12,
volume = 10,
place = {United States},
year = {Thu Dec 11 00:00:00 EST 2014},
month = {Thu Dec 11 00:00:00 EST 2014}
}
Web of Science
Figures / Tables:
Works referenced in this record:
Long-Term Dynamics of Adaptation in Asexual Populations
journal, November 2013
- Wiser, M. J.; Ribeck, N.; Lenski, R. E.
- Science, Vol. 342, Issue 6164
Polyamines in microorganisms.
journal, January 1985
- Tabor, C. W.; Tabor, H.
- Microbiological Reviews, Vol. 49, Issue 1
Purification and phosphorylation of the Arc regulatory components of Escherichia coli.
journal, September 1992
- Iuchi, S.; Lin, E. C.
- Journal of Bacteriology, Vol. 174, Issue 17
Efflux pumps of Gram-negative bacteria: what they do, how they do it, with what and how to deal with them
journal, January 2014
- Amaral, Leonard; Martins, Ana; Spengler, Gabriella
- Frontiers in Pharmacology, Vol. 4
EFFECTS OF TEMPERATURE ON THE FITNESS COST OF RESISTANCE TO BACTERIOPHAGE T4 IN ESCHERICHIA COLI.
journal, June 2009
- Quance, Michael A.; Travisano, Michael
- Evolution, Vol. 63, Issue 6
Long-term survival during stationary phase: evolution and the GASP phenotype
journal, February 2006
- Finkel, Steven E.
- Nature Reviews Microbiology, Vol. 4, Issue 2
Synonymous but not the same: the causes and consequences of codon bias
journal, November 2010
- Plotkin, Joshua B.; Kudla, Grzegorz
- Nature Reviews Genetics, Vol. 12, Issue 1
Small changes in enzyme function can lead to surprisingly large fitness effects during adaptive evolution of antibiotic resistance
journal, December 2012
- Walkiewicz, K.; Benitez Cardenas, A. S.; Sun, C.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 52
Long-Term Experimental Evolution in Escherichia coli. I. Adaptation and Divergence During 2,000 Generations
journal, December 1991
- Lenski, Richard E.; Rose, Michael R.; Simpson, Suzanne C.
- The American Naturalist, Vol. 138, Issue 6
Role of RpoS in Virulence of Pathogens
journal, November 2009
- Dong, T.; Schellhorn, H. E.
- Infection and Immunity, Vol. 78, Issue 3
Adaptation of Enterococcus faecalis to Daptomycin Reveals an Ordered Progression to Resistance
journal, December 2013
- Miller, Corwin; Kong, Jiayi; Tran, Truc T.
- Antimicrobial Agents and Chemotherapy, Vol. 58, Issue 1
Comparative genomics and transcriptomics analysis of experimentally evolved Escherichia coli MC1000 in complex environments : Omics of evolved
journal, August 2013
- Puentes-Téllez, Pilar Eliana; Kovács, Ákos T.; Kuipers, Oscar P.
- Environmental Microbiology, Vol. 16, Issue 3
The Genetic Basis of Thermal Reaction Norm Evolution in Lab and Natural Phage Populations
journal, June 2006
- Knies, Jennifer L.; Izem, Rima; Supler, Katie L.
- PLoS Biology, Vol. 4, Issue 7
Short-Chain Fatty Acids and Human Colonic Function: Roles of Resistant Starch and Nonstarch Polysaccharides
journal, July 2001
- Topping, David L.; Clifton, Peter M.
- Physiological Reviews, Vol. 81, Issue 3
Putrescine catabolism is a metabolic response to several stresses in Escherichia coli : Putrescine catabolism and stress
journal, March 2013
- Schneider, Barbara L.; Hernandez, V. James; Reitzer, Larry
- Molecular Microbiology, Vol. 88, Issue 3
Stress-Induced Mutagenesis in Bacteria
journal, January 2007
- Foster, Patricia L.
- Critical Reviews in Biochemistry and Molecular Biology, Vol. 42, Issue 5
Genome-wide Mutational Diversity in an Evolving Population of Escherichia coli
journal, January 2009
- Barrick, J. E.; Lenski, R. E.
- Cold Spring Harbor Symposia on Quantitative Biology, Vol. 74, Issue 0
The RAST Server: Rapid Annotations using Subsystems Technology
journal, January 2008
- Aziz, Ramy K.; Bartels, Daniela; Best, Aaron A.
- BMC Genomics, Vol. 9, Issue 1, Article No. 75
Diminishing Returns Epistasis Among Beneficial Mutations Decelerates Adaptation
journal, June 2011
- Chou, H. -H.; Chiu, H. -C.; Delaney, N. F.
- Science, Vol. 332, Issue 6034
Spontaneous Mutation Accumulation Studies in Evolutionary Genetics
journal, December 2009
- Halligan, Daniel L.; Keightley, Peter D.
- Annual Review of Ecology, Evolution, and Systematics, Vol. 40, Issue 1
Clonal Adaptive Radiation in a Constant Environment
journal, July 2006
- Maharjan, R.
- Science, Vol. 313, Issue 5786
Codon preferences in free-living microorganisms.
journal, January 1990
- Andersson, S. G.; Kurland, C. G.
- Microbiological Reviews, Vol. 54, Issue 2
Partitioning of Resources and the Outcome of Interspecific Competition: A Model and Some General Considerations
journal, March 1973
- Stewart, Frank M.; Levin, Bruce R.
- The American Naturalist, Vol. 107, Issue 954
Polyamines Are Not Required for Aerobic Growth of Escherichia coli: Preparation of a Strain with Deletions in All of the Genes for Polyamine Biosynthesis
journal, June 2009
- Chattopadhyay, M. K.; Tabor, C. W.; Tabor, H.
- Journal of Bacteriology, Vol. 191, Issue 17
The Genetic Basis of Thermal Reaction Norm Evolution in Lab and Natural Phage Populations
text, January 2006
- Rima, Izem,; L., Supler, Katie; G., Kingsolver, Joel
- The University of North Carolina at Chapel Hill University Libraries
Global metabolic regulation analysis for Escherichia coli K12 based on protein expression by 2-dimensional electrophoresis and enzyme activity measurement
journal, January 2003
- Peng, L.; Shimizu, K.
- Applied Microbiology and Biotechnology, Vol. 61, Issue 2, p. 163-178
The effect of population structure on the adaptive radiation of microbial populations evolving in spatially structured environments: Spatial structure and adaptive radiation
journal, August 2006
- Habets, Michelle G. J. L.; Rozen, Daniel E.; Hoekstra, Rolf F.
- Ecology Letters, Vol. 9, Issue 9
The RpoS-Mediated General Stress Response in Escherichia coli
journal, October 2011
- Battesti, Aurelia; Majdalani, Nadim; Gottesman, Susan
- Annual Review of Microbiology, Vol. 65, Issue 1
Identity and Function of a Large Gene Network Underlying Mutagenic Repair of DNA Breaks
journal, December 2012
- Al Mamun, A. A. M.; Lombardo, M. -J.; Shee, C.
- Science, Vol. 338, Issue 6112
Pervasive genetic hitchhiking and clonal interference in forty evolving yeast populations
journal, July 2013
- Lang, Gregory I.; Rice, Daniel P.; Hickman, Mark J.
- Nature, Vol. 500, Issue 7464
Evidence that putrescine acts as an extracellular signal required for swarming in Proteus mirabilis: Role of putrescine in swarming
journal, January 2004
- Sturgill, Gwen; Rather, Philip N.
- Molecular Microbiology, Vol. 51, Issue 2
Effect of oxygen on theEscherichia coli ArcA and FNR regulation systems and metabolic responses
journal, January 2005
- Shalel Levanon, Sagit; San, Ka-Yiu; Bennett, George N.
- Biotechnology and Bioengineering, Vol. 89, Issue 5
Structural Analysis and Solution Studies of the Activated Regulatory Domain of the Response Regulator ArcA: A Symmetric Dimer Mediated by the α4-β5-α5 Face
journal, May 2005
- Toro-Roman, Alejandro; Mack, Timothy R.; Stock, Ann M.
- Journal of Molecular Biology, Vol. 349, Issue 1
Epistasis and Allele Specificity in the Emergence of a Stable Polymorphism in Escherichia coli
journal, March 2014
- Plucain, J.; Hindre, T.; Le Gac, M.
- Science, Vol. 343, Issue 6177
Experimental Evidence for Sympatric Ecological Diversification due to Frequency-Dependent Competition in Escherichia coli
journal, January 2004
- Friesen, Maren L.; Saxer, Gerda; Travisano, Michael
- Evolution, Vol. 58, Issue 2
The population genetics of ecological specialization in evolving Escherichia coli populations
journal, October 2000
- Cooper, Vaughn S.; Lenski, Richard E.
- Nature, Vol. 407, Issue 6805
A Regulatory Trade-Off as a Source of Strain Variation in the Species Escherichia coli
journal, August 2004
- King, T.; Ishihama, A.; Kori, A.
- Journal of Bacteriology, Vol. 186, Issue 17
Parallel Evolutionary Dynamics of Adaptive Diversification in Escherichia coli
journal, February 2013
- Herron, Matthew D.; Doebeli, Michael
- PLoS Biology, Vol. 11, Issue 2
Adaptive radiation in a heterogeneous environment
journal, July 1998
- Rainey, Paul B.; Travisano, Michael
- Nature, Vol. 394, Issue 6688
Experimental Evidence for Sympatric Ecological Diversification due to Frequency-Dependent Competition in Escherichia coli
journal, February 2004
- Friesen, Maren L.; Saxer, Gerda; Travisano, Michael
- Evolution, Vol. 58, Issue 2
DAnTE: a statistical tool for quantitative analysis of -omics data
journal, May 2008
- Polpitiya, A. D.; Qian, W. -J.; Jaitly, N.
- Bioinformatics, Vol. 24, Issue 13
Evolution of global regulatory networks during a long-term experiment withEscherichia coli
journal, January 2007
- Philippe, Nadège; Crozat, Estelle; Lenski, Richard E.
- BioEssays, Vol. 29, Issue 9
Contingency and Determinism in Replicated Adaptive Radiations of Island Lizards
journal, March 1998
- Losos, J. B.
- Science, Vol. 279, Issue 5359
Parallel changes in gene expression after 20,000 generations of evolution in Escherichia coli
journal, January 2003
- Cooper, T. F.; Rozen, D. E.; Lenski, R. E.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 3
Characterizing and measuring bias in sequence data
journal, January 2013
- Ross, Michael G.; Russ, Carsten; Costello, Maura
- Genome Biology, Vol. 14, Issue 5
Stress-induced Mutagenesis in Bacteria
book, November 2011
- Foster, Patricia L.
- Encyclopedia of Life Sciences
Nutritional Basis for Colonization Resistance by Human Commensal Escherichia coli Strains HS and Nissle 1917 against E. coli O157:H7 in the Mouse Intestine
journal, January 2013
- Maltby, Rosalie; Leatham-Jensen, Mary P.; Gibson, Terri
- PLoS ONE, Vol. 8, Issue 1
The predictability of molecular evolution during functional innovation
journal, February 2014
- Blank, D.; Wolf, L.; Ackermann, M.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 8
Evolution of the mutation rate
journal, August 2010
- Lynch, Michael
- Trends in Genetics, Vol. 26, Issue 8
Maintaining a healthy SPANC balance through regulatory and mutational adaptation: Stress resistance and metabolic capability
journal, May 2005
- Ferenci, Thomas
- Molecular Microbiology, Vol. 57, Issue 1
The influence of cellular physiology on the initiation of mutational pathways in Escherichia coli populations
journal, April 2003
- Notley–McRobb, Lucinda; Seeto, Shona; Ferenci, Thomas
- Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 270, Issue 1517
Whole Genome Sequencing of Mutation Accumulation Lines Reveals a Low Mutation Rate in the Social Amoeba Dictyostelium discoideum
journal, October 2012
- Saxer, Gerda; Havlak, Paul; Fox, Sara A.
- PLoS ONE, Vol. 7, Issue 10
Evolutionary fates within a microbial population highlight an essential role for protein folding during natural selection
journal, January 2010
- Peña, Matthew I.; Davlieva, Milya; Bennett, Matthew R.
- Molecular Systems Biology, Vol. 6, Issue 1
Effect ofrpoS gene knockout on the metabolism ofEscherichia coli during exponential growth phase and early stationary phase based on gene expressions, enzyme activities and intracellular metabolite concentrations
journal, June 2006
- Rahman, Mahbuba; Hasan, Mohammad Rubayet; Oba, Takahiro
- Biotechnology and Bioengineering, Vol. 94, Issue 3
Advances in proteomics data analysis and display using an accurate mass and time tag approach
journal, January 2006
- Zimmer, Jennifer S. D.; Monroe, Matthew E.; Qian, Wei-Jun
- Mass Spectrometry Reviews, Vol. 25, Issue 3
Long‐Term Experimental Evolution in Escherichia coli . VIII. Dynamics of a Balanced Polymorphism
journal, January 2000
- Rozen, Daniel E.; Lenski, Richard E.
- The American Naturalist, Vol. 155, Issue 1
The Bacterial Response Regulator ArcA Uses a Diverse Binding Site Architecture to Regulate Carbon Oxidation Globally
journal, October 2013
- Park, Dan M.; Akhtar, Md. Sohail; Ansari, Aseem Z.
- PLoS Genetics, Vol. 9, Issue 10
The Molecular Diversity of Adaptive Convergence
journal, January 2012
- Tenaillon, O.; Rodriguez-Verdugo, A.; Gaut, R. L.
- Science, Vol. 335, Issue 6067, p. 457-461
Nitrogen Assimilation and Global Regulation in Escherichia coli
journal, October 2003
- Reitzer, Larry
- Annual Review of Microbiology, Vol. 57, Issue 1
Dynamics of adaptation and diversification: a 10,000-generation experiment with bacterial populations.
journal, July 1994
- Lenski, R. E.; Travisano, M.
- Proceedings of the National Academy of Sciences, Vol. 91, Issue 15
Identification of Mutations in Laboratory-Evolved Microbes from Next-Generation Sequencing Data Using breseq
book, January 2014
- Deatherage, Daniel E.; Barrick, Jeffrey E.
- Methods in Molecular Biology
Negative Epistasis Between Beneficial Mutations in an Evolving Bacterial Population
journal, June 2011
- Khan, A. I.; Dinh, D. M.; Schneider, D.
- Science, Vol. 332, Issue 6034
Growth of Escherichia coli MG1655 on LB medium: monitoring utilization of amino acids, peptides, and nucleotides with transcriptional microarrays
journal, March 2006
- Baev, Mark V.; Baev, Dmitry; Jansco Radek, Agnes
- Applied Microbiology and Biotechnology, Vol. 71, Issue 3
Biogenic ammonia modifies antibiotic resistance at a distance in physically separated bacteria: Ammonia modifies antibiotic resistance at a distance
journal, June 2011
- Bernier, Steve P.; Létoffé, Sylvie; Delepierre, Muriel
- Molecular Microbiology, Vol. 81, Issue 3
Evolutionary paths to antibiotic resistance under dynamically sustained drug selection
journal, December 2011
- Toprak, Erdal; Veres, Adrian; Michel, Jean-Baptiste
- Nature Genetics, Vol. 44, Issue 1, p. 101-105
Natural Selection and Parallel Speciation in Sympatric Sticklebacks
journal, January 2000
- Rundle, H. D.
- Science, Vol. 287, Issue 5451
Signal Decay through a Reverse Phosphorelay in the Arc Two-component Signal Transduction System
journal, December 1998
- Georgellis, Dimitris; Kwon, Ohsuk; De Wulf, Peter
- Journal of Biological Chemistry, Vol. 273, Issue 49
The Evolution of Ecological Specialization
journal, November 1988
- Futuyma, D. J.; Moreno, G.
- Annual Review of Ecology and Systematics, Vol. 19, Issue 1
Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation
journal, June 2003
- Elena, Santiago F.; Lenski, Richard E.
- Nature Reviews Genetics, Vol. 4, Issue 6
The response to selection on major and minor mutations affecting a metrical trait
journal, February 1983
- Lande, Russell
- Heredity, Vol. 50, Issue 1
Metabolic Erosion Primarily Through Mutation Accumulation, and Not Tradeoffs, Drives Limited Evolution of Substrate Specificity in Escherichia coli
journal, February 2014
- Leiby, Nicholas; Marx, Christopher J.
- PLoS Biology, Vol. 12, Issue 2
Spatial structure leads to ecological breakdown and loss of diversity
journal, March 2009
- Saxer, Gerda; Doebeli, Michael; Travisano, Michael
- Proceedings of the Royal Society B: Biological Sciences, Vol. 276, Issue 1664
An adaptive mutation in adenylate kinase that increases organismal fitness is linked to stability-activity trade-offs
journal, December 2007
- Counago, R.; Wilson, C. J.; Pena, M. I.
- Protein Engineering Design and Selection, Vol. 21, Issue 1
Growth of Escherichia coli MG1655 on LB medium: monitoring utilization of sugars, alcohols, and organic acids with transcriptional microarrays
journal, April 2006
- Baev, Mark V.; Baev, Dmitry; Radek, Agnes Jancso
- Applied Microbiology and Biotechnology, Vol. 71, Issue 3
The SEED: a peer-to-peer environment for genome annotation
journal, November 2004
- Overbeek, Ross; Disz, Terry; Stevens, Rick
- Communications of the ACM, Vol. 47, Issue 11
Biosynthetic arginine decarboxylase in Escherichia coli is synthesized as a precursor and located in the cell envelope.
journal, January 1985
- Buch, J. K.; Boyle, S. M.
- Journal of Bacteriology, Vol. 163, Issue 2
Evolution of Escherichia coli During Growth in a Constant Environment
journal, July 1987
- Helling, Robert B.; Vargas, Christopher N.; Adams, Julian
- Genetics, Vol. 116, Issue 3
Microbial evolution in a simple unstructured environment: genetic differentiation in Escherichia coli.
journal, August 1994
- Rosenzweig, R. F.; Sharp, R. R.; Treves, D. S.
- Genetics, Vol. 137, Issue 4
Data from: Mutations in global regulators lead to metabolic selection during adaptation to complex environments
dataset, December 2014
- Saxer, Gerda; Krepps, Michael D.; Merkley, Eric D.
- Dryad Digital Repository-Supplementary information for journal article at DOI: 10.1371/journal.pgen.1004872, 6 files
Data from: Mutations in global regulators lead to metabolic selection during adaptation to complex environments
dataset, December 2014
- Saxer, Gerda; Krepps, Michael D.; Merkley, Eric D.
- Dryad Digital Repository-Supplementary information for journal article at DOI: 10.1371/journal.pgen.1004872, 6 files
Effect of oxygen on theEscherichia coli ArcA and FNR regulation systems and metabolic responses
journal, January 2005
- Shalel Levanon, Sagit; San, Ka-Yiu; Bennett, George N.
- Biotechnology and Bioengineering, Vol. 89, Issue 5
Effect ofrpoS gene knockout on the metabolism ofEscherichia coli during exponential growth phase and early stationary phase based on gene expressions, enzyme activities and intracellular metabolite concentrations
journal, June 2006
- Rahman, Mahbuba; Hasan, Mohammad Rubayet; Oba, Takahiro
- Biotechnology and Bioengineering, Vol. 94, Issue 3
Identification of Mutations in Laboratory-Evolved Microbes from Next-Generation Sequencing Data Using breseq
book, January 2014
- Deatherage, Daniel E.; Barrick, Jeffrey E.
- Methods in Molecular Biology
Growth of Escherichia coli MG1655 on LB medium: monitoring utilization of amino acids, peptides, and nucleotides with transcriptional microarrays
journal, March 2006
- Baev, Mark V.; Baev, Dmitry; Jansco Radek, Agnes
- Applied Microbiology and Biotechnology, Vol. 71, Issue 3
Structural Analysis and Solution Studies of the Activated Regulatory Domain of the Response Regulator ArcA: A Symmetric Dimer Mediated by the α4-β5-α5 Face
journal, May 2005
- Toro-Roman, Alejandro; Mack, Timothy R.; Stock, Ann M.
- Journal of Molecular Biology, Vol. 349, Issue 1
Evolution of the mutation rate
journal, August 2010
- Lynch, Michael
- Trends in Genetics, Vol. 26, Issue 8
Adaptive radiation in a heterogeneous environment
journal, July 1998
- Rainey, Paul B.; Travisano, Michael
- Nature, Vol. 394, Issue 6688
Pervasive genetic hitchhiking and clonal interference in forty evolving yeast populations
journal, July 2013
- Lang, Gregory I.; Rice, Daniel P.; Hickman, Mark J.
- Nature, Vol. 500, Issue 7464
Evolutionary paths to antibiotic resistance under dynamically sustained drug selection
journal, December 2011
- Toprak, Erdal; Veres, Adrian; Michel, Jean-Baptiste
- Nature Genetics, Vol. 44, Issue 1, p. 101-105
Long-term survival during stationary phase: evolution and the GASP phenotype
journal, February 2006
- Finkel, Steven E.
- Nature Reviews Microbiology, Vol. 4, Issue 2
Something in the air
journal, August 2011
- Sanchez, Cesar
- Nature Reviews Microbiology, Vol. 9, Issue 8
Small changes in enzyme function can lead to surprisingly large fitness effects during adaptive evolution of antibiotic resistance
journal, December 2012
- Walkiewicz, K.; Benitez Cardenas, A. S.; Sun, C.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 52
The predictability of molecular evolution during functional innovation
journal, February 2014
- Blank, D.; Wolf, L.; Ackermann, M.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 8
Dynamics of adaptation and diversification: a 10,000-generation experiment with bacterial populations.
journal, July 1994
- Lenski, R. E.; Travisano, M.
- Proceedings of the National Academy of Sciences, Vol. 91, Issue 15
The influence of cellular physiology on the initiation of mutational pathways in Escherichia coli populations
journal, April 2003
- Notley–McRobb, Lucinda; Seeto, Shona; Ferenci, Thomas
- Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 270, Issue 1517
Genome-wide Mutational Diversity in an Evolving Population of Escherichia coli
journal, January 2009
- Barrick, J. E.; Lenski, R. E.
- Cold Spring Harbor Symposia on Quantitative Biology, Vol. 74, Issue 0
Experimental Evidence for Sympatric Ecological Diversification due to Frequency-Dependent Competition in Escherichia coli
journal, February 2004
- Friesen, Maren L.; Saxer, Gerda; Travisano, Michael
- Evolution, Vol. 58, Issue 2
Clonal Adaptive Radiation in a Constant Environment
journal, July 2006
- Maharjan, R.
- Science, Vol. 313, Issue 5786
Diminishing Returns Epistasis Among Beneficial Mutations Decelerates Adaptation
journal, June 2011
- Chou, H. -H.; Chiu, H. -C.; Delaney, N. F.
- Science, Vol. 332, Issue 6034
Long-Term Dynamics of Adaptation in Asexual Populations
journal, November 2013
- Wiser, M. J.; Ribeck, N.; Lenski, R. E.
- Science, Vol. 342, Issue 6164
Epistasis and Allele Specificity in the Emergence of a Stable Polymorphism in Escherichia coli
journal, March 2014
- Plucain, J.; Hindre, T.; Le Gac, M.
- Science, Vol. 343, Issue 6177
Contingency and Determinism in Replicated Adaptive Radiations of Island Lizards
journal, March 1998
- Losos, J. B.
- Science, Vol. 279, Issue 5359
Natural Selection and Parallel Speciation in Sympatric Sticklebacks
journal, January 2000
- Rundle, H. D.
- Science, Vol. 287, Issue 5451
Adaptation of Enterococcus faecalis to Daptomycin Reveals an Ordered Progression to Resistance
journal, August 2013
- Miller, Corwin; Kong, Jiayi; Tran, Truc T.
- Antimicrobial Agents and Chemotherapy, Vol. 57, Issue 11
Adaptation and Heterogeneity of Escherichia coli MC1000 Growing in Complex Environments
journal, November 2012
- Puentes-Téllez, Pilar Eliana; Hansen, Martin Asser; Sørensen, Søren Johannes
- Applied and Environmental Microbiology, Vol. 79, Issue 3
The Global Regulator ArcA Modulates Expression of Virulence Factors in Vibrio cholerae
journal, September 2003
- Sengupta, N.; Paul, K.; Chowdhury, R.
- Infection and Immunity, Vol. 71, Issue 10
Purification and phosphorylation of the Arc regulatory components of Escherichia coli.
journal, September 1992
- Iuchi, S.; Lin, E. C.
- Journal of Bacteriology, Vol. 174, Issue 17
Impact of Global Transcriptional Regulation by ArcA, ArcB, Cra, Crp, Cya, Fnr, and Mlc on Glucose Catabolism in Escherichia coli
journal, April 2005
- Perrenoud, A.; Sauer, U.
- Journal of Bacteriology, Vol. 187, Issue 9
Polyamines in microorganisms.
journal, January 1985
- Tabor, C. W.; Tabor, H.
- Microbiological Reviews, Vol. 49, Issue 1
Codon preferences in free-living microorganisms
journal, June 1990
- Andersson, S. G.; Kurland, C. G.
- Microbiological Reviews, Vol. 54, Issue 2
The SEED: a peer-to-peer environment for genome annotation
journal, November 2004
- Overbeek, Ross; Disz, Terry; Stevens, Rick
- Communications of the ACM, Vol. 47, Issue 11
The RpoS-Mediated General Stress Response in Escherichia coli
journal, October 2011
- Battesti, Aurelia; Majdalani, Nadim; Gottesman, Susan
- Annual Review of Microbiology, Vol. 65, Issue 1
Characterizing and measuring bias in sequence data
journal, January 2013
- Ross, Michael G.; Russ, Carsten; Costello, Maura
- Genome Biology, Vol. 14, Issue 5
The Genetic Basis of Thermal Reaction Norm Evolution in Lab and Natural Phage Populations
journal, June 2006
- Knies, Jennifer L.; Izem, Rima; Supler, Katie L.
- PLoS Biology, Vol. 4, Issue 7
Metabolic Erosion Primarily Through Mutation Accumulation, and Not Tradeoffs, Drives Limited Evolution of Substrate Specificity in Escherichia coli
journal, February 2014
- Leiby, Nicholas; Marx, Christopher J.
- PLoS Biology, Vol. 12, Issue 2
The Bacterial Response Regulator ArcA Uses a Diverse Binding Site Architecture to Regulate Carbon Oxidation Globally
journal, October 2013
- Park, Dan M.; Akhtar, Md. Sohail; Ansari, Aseem Z.
- PLoS Genetics, Vol. 9, Issue 10
The Repeatability of Adaptive Radiation During Long-Term Experimental Evolution of Escherichia coli in a Multiple Nutrient Environment
journal, December 2010
- Saxer, Gerda; Doebeli, Michael; Travisano, Michael
- PLoS ONE, Vol. 5, Issue 12
Escherichia coli Lacking RpoS Are Rare in Natural Populations of Non-Pathogens
journal, November 2012
- Snyder, Emily; Gordon, David M.; Stoebel, Daniel M.
- G3 Genes|Genomes|Genetics, Vol. 2, Issue 11
Efflux pumps of Gram-negative bacteria: what they do, how they do it, with what and how to deal with them
journal, January 2014
- Amaral, Leonard; Martins, Ana; Spengler, Gabriella
- Frontiers in Pharmacology, Vol. 4
Works referencing / citing this record:
The essential role of hypermutation in rapid adaptation to antibiotic stress
posted_content, September 2018
- Mehta, Heer H.; Prater, Amy G.; Beabout, Kathryn
- bioRxiv
Metabolism at Evolutionary Optimal States
journal, June 2015
- Rabbers, Iraes; van Heerden, Johan; Nordholt, Niclas
- Metabolites, Vol. 5, Issue 2
Generation of mutation hotspots in ageing bacterial colonies
journal, December 2016
- Sekowska, Agnieszka; Wendel, Sofie; Fischer, Emil C.
- Scientific Reports, Vol. 6, Issue 1
The Essential Role of Hypermutation in Rapid Adaptation to Antibiotic Stress
journal, April 2019
- Mehta, Heer H.; Prater, Amy G.; Beabout, Kathryn
- Antimicrobial Agents and Chemotherapy, Vol. 63, Issue 7
Rampant loss of social traits during domestication of a Bacillus subtilis natural isolate
posted_content, January 2019
- Barreto, Hugo C.; Cordeiro, Tiago N.; Henriques, Adriano O.
- bioRxiv
A variable DNA recognition site organization establishes the LiaR-mediated cell envelope stress response of enterococci to daptomycin
journal, April 2015
- Davlieva, Milya; Shi, Yiwen; Leonard, Paul G.
- Nucleic Acids Research, Vol. 43, Issue 9
Genome Plasticity of agr -Defective Staphylococcus aureus during Clinical Infection
journal, July 2018
- Altman, Deena R.; Sullivan, Mitchell J.; Chacko, Kieran I.
- Infection and Immunity, Vol. 86, Issue 10
Modularity of the life cycle
journal, July 2019
- Libby, Eric
- Nature Ecology & Evolution, Vol. 3, Issue 8
Laboratory strains of Bacillus anthracis exhibit pervasive alteration in expression of proteins related to sporulation under laboratory conditions relative to genetically related wild strains
journal, December 2018
- Leiser, Owen P.; Blackburn, Jason K.; Hadfield, Ted L.
- PLOS ONE, Vol. 13, Issue 12
Rampant loss of social traits during domestication of a Bacillus subtilis natural isolate
journal, November 2020
- Barreto, Hugo C.; Cordeiro, Tiago N.; Henriques, Adriano O.
- Scientific Reports, Vol. 10, Issue 1
Development of rapid and simple experimental and in silico serotyping systems for Citrobacter
journal, October 2018
- Qian, Chengqian; Du, Yuhui; Li, Huiying
- Future Microbiology, Vol. 13, Issue 13
Data from: Mutations in global regulators lead to metabolic selection during adaptation to complex environments
dataset, December 2014
- Saxer, Gerda; Krepps, Michael D.; Merkley, Eric D.
- Dryad Digital Repository-Supplementary information for journal article at DOI: 10.1371/journal.pgen.1004872, 6 files
Genetic Adaptation to Growth Under Laboratory Conditions in Escherichia coli and Salmonella enterica
journal, April 2018
- Knöppel, Anna; Knopp, Michael; Albrecht, Lisa M.
- Frontiers in Microbiology, Vol. 9
Disadvantages and benefits of evolved unicellularity versus multicellularity in budding yeast
journal, July 2019
- Kuzdzal‐Fick, Jennie J.; Chen, Lin; Balázsi, Gábor
- Ecology and Evolution, Vol. 9, Issue 15
Pathogenic Nocardia cyriacigeorgica and Nocardia nova Evolve To Resist Trimethoprim-Sulfamethoxazole by both Expected and Unexpected Pathways
journal, April 2018
- Mehta, H.; Weng, J.; Prater, A.
- Antimicrobial Agents and Chemotherapy, Vol. 62, Issue 7
Horizontal transfer of a pathway for coumarate catabolism unexpectedly inhibits purine nucleotide biosynthesis
journal, October 2019
- Close, Dan M.; Cooper, Connor J.; Wang, Xingyou
- Molecular Microbiology, Vol. 112, Issue 6
Evolution of a global regulator: Lrp in four orders of γ-Proteobacteria
journal, May 2016
- Unoarumhi, Yvette; Blumenthal, Robert M.; Matson, Jyl S.
- BMC Evolutionary Biology, Vol. 16, Issue 1
Natural Escherichia coli isolates rapidly acquire genetic changes upon laboratory domestication
journal, January 2017
- Liu, Bin; Eydallin, Gustavo; Maharjan, Ram P.
- Microbiology, Vol. 163, Issue 1
Data from: Mutations in global regulators lead to metabolic selection during adaptation to complex environments
dataset, December 2014
- Saxer, Gerda; Krepps, Michael D.; Merkley, Eric D.
- Dryad Digital Repository-Supplementary information for journal article at DOI: 10.1371/journal.pgen.1004872, 6 files
Disadvantages and benefits of evolved unicellularity versus multicellularity in budding yeast
journal, July 2019
- Kuzdzal‐Fick, Jennie J.; Chen, Lin; Balázsi, Gábor
- Ecology and Evolution, Vol. 9, Issue 15
Rampant loss of social traits during domestication of a Bacillus subtilis natural isolate
journal, November 2020
- Barreto, Hugo C.; Cordeiro, Tiago N.; Henriques, Adriano O.
- Scientific Reports, Vol. 10, Issue 1
Piggybacking on Niche Adaptation Improves the Maintenance of Multidrug-Resistance Plasmids
journal, March 2021
- Kloos, Julia; Gama, João A.; Hegstad, Joachim
- Molecular Biology and Evolution, Vol. 38, Issue 8
Evolution of a global regulator: Lrp in four orders of γ-Proteobacteria
journal, May 2016
- Unoarumhi, Yvette; Blumenthal, Robert M.; Matson, Jyl S.
- BMC Evolutionary Biology, Vol. 16, Issue 1
Acinetobacter baumannii Repeatedly Evolves a Hypermutator Phenotype in Response to Tigecycline That Effectively Surveys Evolutionary Trajectories to Resistance
journal, October 2015
- Hammerstrom, Troy G.; Beabout, Kathryn; Clements, Thomas P.
- PLOS ONE, Vol. 10, Issue 10
Investigation of Yersinia pestis Laboratory Adaptation through a Combined Genomics and Proteomics Approach
journal, November 2015
- Leiser, Owen P.; Merkley, Eric D.; Clowers, Brian H.
- PLOS ONE, Vol. 10, Issue 11
Laboratory strains of Bacillus anthracis exhibit pervasive alteration in expression of proteins related to sporulation under laboratory conditions relative to genetically related wild strains
journal, December 2018
- Leiser, Owen P.; Blackburn, Jason K.; Hadfield, Ted L.
- PLOS ONE, Vol. 13, Issue 12
Development of rapid and simple experimental and in silico serotyping systems for Citrobacter
journal, October 2018
- Qian, Chengqian; Du, Yuhui; Li, Huiying
- Future Microbiology, Vol. 13, Issue 13
The Bacterial Two-Hybrid System Uncovers the Involvement of Acetylation in Regulating of Lrp Activity in Salmonella Typhimurium
journal, November 2016
- Qin, Ran; Sang, Yu; Ren, Jie
- Frontiers in Microbiology, Vol. 7
Genetic Adaptation to Growth Under Laboratory Conditions in Escherichia coli and Salmonella enterica
journal, April 2018
- Knöppel, Anna; Knopp, Michael; Albrecht, Lisa M.
- Frontiers in Microbiology, Vol. 9