Global network reorganization during dynamic adaptations of Bacillus subtilis metabolism

Joerg Martin Buescher; Wolfram Liebermeister; Matthieu Jules; Markus Uhr; Jan Muntel; Eric Botella; Bernd Hessling; Roelco Jacobus Kleijn; Ludovic Le Chat; François Lecointe; Ulrike Mäder; Pierre Nicolas; Sjouke Piersma; Frank Rügheimer; Dörte Becher; Philippe Bessieres; Elena Bidnenko; Emma L Denham; Etienne Dervyn; Kevin M Devine; Geoff Doherty; Samuel Drulhe; Liza Felicori; Mark J Fogg; Anne Goelzer; Annette Hansen; Colin R Harwood; Michael Hecker; Sebastian Hubner; Claus Hultschig; Hanne Jarmer; Edda Klipp; Aurélie Leduc; Peter Lewis; Frank Molina; Philippe Noirot; Sabine Peres; Nathalie Pigeonneau; Susanne Pohl; Simon Rasmussen; Bernd Rinn; Marc Schaffer; Julian Schnidder; Benno Schwikowski; Jan Maarten Van Dijl; Patrick Veiga; Sean Walsh; Anthony J Wilkinson; Jörg Stelling; Stéphane Aymerich

doi:10.1126/science.1206871

Global network reorganization during dynamic adaptations of Bacillus subtilis metabolism

Joerg Martin Buescher, Wolfram Liebermeister, Matthieu Jules, Markus Uhr, Jan Muntel, Eric Botella, Bernd Hessling, Roelco Jacobus Kleijn, Ludovic Le Chat, François Lecointe, Ulrike Mäder, Pierre Nicolas, Sjouke Piersma, Frank Rügheimer, Dörte Becher, Philippe Bessieres, Elena Bidnenko, Emma L Denham, Etienne Dervyn, Kevin M DevineGeoff Doherty, Samuel Drulhe, Liza Felicori, Mark J Fogg, Anne Goelzer, Annette Hansen, Colin R Harwood, Michael Hecker, Sebastian Hubner, Claus Hultschig, Hanne Jarmer, Edda Klipp, Aurélie Leduc, Peter Lewis, Frank Molina, Philippe Noirot, Sabine Peres, Nathalie Pigeonneau, Susanne Pohl, Simon Rasmussen, Bernd Rinn, Marc Schaffer, Julian Schnidder, Benno Schwikowski, Jan Maarten Van Dijl, Patrick Veiga, Sean Walsh, Anthony J Wilkinson, Jörg Stelling, Stéphane Aymerich

Department of Clinical Medicine

191 Citations (Scopus)

Abstract

Adaptation of cells to environmental changes requires dynamic interactions between metabolic and regulatory networks, but studies typically address only one or a few layers of regulation. For nutritional shifts between two preferred carbon sources of Bacillus subtilis, we combined statistical and model-based data analyses of dynamic transcript, protein, and metabolite abundances and promoter activities. Adaptation to malate was rapid and primarily controlled posttranscriptionally compared with the slow, mainly transcriptionally controlled adaptation to glucose that entailed nearly half of the known transcription regulation network. Interactions across multiple levels of regulation were involved in adaptive changes that could also be achieved by controlling single genes. Our analysis suggests that global trade-offs and evolutionary constraints provide incentives to favor complex control programs.

Original language	English
Journal	Science (New York, N.Y.)
Volume	335
Issue number	6072
Pages (from-to)	1099-103
Number of pages	5
ISSN	0036-8075
DOIs	https://doi.org/10.1126/science.1206871
Publication status	Published - 2 Mar 2012

Keywords

Adaptation, Physiological
Algorithms
Bacillus subtilis/genetics
Bacterial Proteins/metabolism
Computer Simulation
Data Interpretation, Statistical
Gene Expression Regulation, Bacterial
Gene Regulatory Networks
Genome, Bacterial
Glucose/metabolism
Malates/metabolism
Metabolic Networks and Pathways/genetics
Metabolome
Metabolomics
Models, Biological
Operon
Promoter Regions, Genetic
Transcription Factors/metabolism
Transcription, Genetic

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10.1126/science.1206871

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Buescher, J. M., Liebermeister, W., Jules, M., Uhr, M., Muntel, J., Botella, E., Hessling, B., Kleijn, R. J., Le Chat, L., Lecointe, F., Mäder, U., Nicolas, P., Piersma, S., Rügheimer, F., Becher, D., Bessieres, P., Bidnenko, E., Denham, E. L., Dervyn, E., ... Aymerich, S. (2012). Global network reorganization during dynamic adaptations of Bacillus subtilis metabolism. Science (New York, N.Y.), 335(6072), 1099-103. https://doi.org/10.1126/science.1206871

Buescher, JM, Liebermeister, W, Jules, M, Uhr, M, Muntel, J, Botella, E, Hessling, B, Kleijn, RJ, Le Chat, L, Lecointe, F, Mäder, U, Nicolas, P, Piersma, S, Rügheimer, F, Becher, D, Bessieres, P, Bidnenko, E, Denham, EL, Dervyn, E, Devine, KM, Doherty, G, Drulhe, S, Felicori, L, Fogg, MJ, Goelzer, A, Hansen, A, Harwood, CR, Hecker, M, Hubner, S, Hultschig, C, Jarmer, H, Klipp, E, Leduc, A, Lewis, P, Molina, F, Noirot, P, Peres, S, Pigeonneau, N, Pohl, S, Rasmussen, S, Rinn, B, Schaffer, M, Schnidder, J, Schwikowski, B, Van Dijl, JM, Veiga, P, Walsh, S, Wilkinson, AJ, Stelling, J & Aymerich, S 2012, 'Global network reorganization during dynamic adaptations of Bacillus subtilis metabolism', Science (New York, N.Y.), vol. 335, no. 6072, pp. 1099-103. https://doi.org/10.1126/science.1206871

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title = "Global network reorganization during dynamic adaptations of Bacillus subtilis metabolism",

abstract = "Adaptation of cells to environmental changes requires dynamic interactions between metabolic and regulatory networks, but studies typically address only one or a few layers of regulation. For nutritional shifts between two preferred carbon sources of Bacillus subtilis, we combined statistical and model-based data analyses of dynamic transcript, protein, and metabolite abundances and promoter activities. Adaptation to malate was rapid and primarily controlled posttranscriptionally compared with the slow, mainly transcriptionally controlled adaptation to glucose that entailed nearly half of the known transcription regulation network. Interactions across multiple levels of regulation were involved in adaptive changes that could also be achieved by controlling single genes. Our analysis suggests that global trade-offs and evolutionary constraints provide incentives to favor complex control programs.",

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author = "Buescher, {Joerg Martin} and Wolfram Liebermeister and Matthieu Jules and Markus Uhr and Jan Muntel and Eric Botella and Bernd Hessling and Kleijn, {Roelco Jacobus} and {Le Chat}, Ludovic and Fran{\c c}ois Lecointe and Ulrike M{\"a}der and Pierre Nicolas and Sjouke Piersma and Frank R{\"u}gheimer and D{\"o}rte Becher and Philippe Bessieres and Elena Bidnenko and Denham, {Emma L} and Etienne Dervyn and Devine, {Kevin M} and Geoff Doherty and Samuel Drulhe and Liza Felicori and Fogg, {Mark J} and Anne Goelzer and Annette Hansen and Harwood, {Colin R} and Michael Hecker and Sebastian Hubner and Claus Hultschig and Hanne Jarmer and Edda Klipp and Aur{\'e}lie Leduc and Peter Lewis and Frank Molina and Philippe Noirot and Sabine Peres and Nathalie Pigeonneau and Susanne Pohl and Simon Rasmussen and Bernd Rinn and Marc Schaffer and Julian Schnidder and Benno Schwikowski and {Van Dijl}, {Jan Maarten} and Patrick Veiga and Sean Walsh and Wilkinson, {Anthony J} and J{\"o}rg Stelling and St{\'e}phane Aymerich",

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doi = "10.1126/science.1206871",

language = "English",

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T1 - Global network reorganization during dynamic adaptations of Bacillus subtilis metabolism

AU - Buescher, Joerg Martin

AU - Liebermeister, Wolfram

AU - Jules, Matthieu

AU - Uhr, Markus

AU - Muntel, Jan

AU - Botella, Eric

AU - Hessling, Bernd

AU - Kleijn, Roelco Jacobus

AU - Le Chat, Ludovic

AU - Lecointe, François

AU - Mäder, Ulrike

AU - Nicolas, Pierre

AU - Piersma, Sjouke

AU - Rügheimer, Frank

AU - Becher, Dörte

AU - Bessieres, Philippe

AU - Bidnenko, Elena

AU - Denham, Emma L

AU - Dervyn, Etienne

AU - Devine, Kevin M

AU - Doherty, Geoff

AU - Drulhe, Samuel

AU - Felicori, Liza

AU - Fogg, Mark J

AU - Goelzer, Anne

AU - Hansen, Annette

AU - Harwood, Colin R

AU - Hecker, Michael

AU - Hubner, Sebastian

AU - Hultschig, Claus

AU - Jarmer, Hanne

AU - Klipp, Edda

AU - Leduc, Aurélie

AU - Lewis, Peter

AU - Molina, Frank

AU - Noirot, Philippe

AU - Peres, Sabine

AU - Pigeonneau, Nathalie

AU - Pohl, Susanne

AU - Rasmussen, Simon

AU - Rinn, Bernd

AU - Schaffer, Marc

AU - Schnidder, Julian

AU - Schwikowski, Benno

AU - Van Dijl, Jan Maarten

AU - Veiga, Patrick

AU - Walsh, Sean

AU - Wilkinson, Anthony J

AU - Stelling, Jörg

AU - Aymerich, Stéphane

PY - 2012/3/2

Y1 - 2012/3/2

N2 - Adaptation of cells to environmental changes requires dynamic interactions between metabolic and regulatory networks, but studies typically address only one or a few layers of regulation. For nutritional shifts between two preferred carbon sources of Bacillus subtilis, we combined statistical and model-based data analyses of dynamic transcript, protein, and metabolite abundances and promoter activities. Adaptation to malate was rapid and primarily controlled posttranscriptionally compared with the slow, mainly transcriptionally controlled adaptation to glucose that entailed nearly half of the known transcription regulation network. Interactions across multiple levels of regulation were involved in adaptive changes that could also be achieved by controlling single genes. Our analysis suggests that global trade-offs and evolutionary constraints provide incentives to favor complex control programs.

AB - Adaptation of cells to environmental changes requires dynamic interactions between metabolic and regulatory networks, but studies typically address only one or a few layers of regulation. For nutritional shifts between two preferred carbon sources of Bacillus subtilis, we combined statistical and model-based data analyses of dynamic transcript, protein, and metabolite abundances and promoter activities. Adaptation to malate was rapid and primarily controlled posttranscriptionally compared with the slow, mainly transcriptionally controlled adaptation to glucose that entailed nearly half of the known transcription regulation network. Interactions across multiple levels of regulation were involved in adaptive changes that could also be achieved by controlling single genes. Our analysis suggests that global trade-offs and evolutionary constraints provide incentives to favor complex control programs.

KW - Adaptation, Physiological

KW - Algorithms

KW - Bacillus subtilis/genetics

KW - Bacterial Proteins/metabolism

KW - Computer Simulation

KW - Data Interpretation, Statistical

KW - Gene Expression Regulation, Bacterial

KW - Gene Regulatory Networks

KW - Genome, Bacterial

KW - Glucose/metabolism

KW - Malates/metabolism

KW - Metabolic Networks and Pathways/genetics

KW - Metabolome

KW - Metabolomics

KW - Models, Biological

KW - Operon

KW - Promoter Regions, Genetic

KW - Transcription Factors/metabolism

KW - Transcription, Genetic

U2 - 10.1126/science.1206871

DO - 10.1126/science.1206871

M3 - Journal article

C2 - 22383848

SN - 0036-8075

VL - 335

SP - 1099

EP - 1103

JO - Science (New York, N.Y.)

JF - Science (New York, N.Y.)

IS - 6072

ER -

Global network reorganization during dynamic adaptations of Bacillus subtilis metabolism

Abstract

Keywords

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