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abstract:
- lang: eng
text: Active regulation of gene expression, orchestrated by complex interactions
of activators and repressors at promoters, controls the fate of organisms. In
contrast, basal expression at uninduced promoters is considered to be a dynamically
inert mode of nonfunctional “promoter leakiness,” merely a byproduct of transcriptional
regulation. Here, we investigate the basal expression mode of the mar operon,
the main regulator of intrinsic multiple antibiotic resistance in Escherichia
coli, and link its dynamic properties to the noncanonical, yet highly conserved
start codon of marR across Enterobacteriaceae. Real-time, single-cell measurements
across tens of generations reveal that basal expression consists of rare stochastic
gene expression pulses, which maximize variability in wildtype and, surprisingly,
transiently accelerate cellular elongation rates. Competition experiments show
that basal expression confers fitness advantages to wildtype across several transitions
between exponential and stationary growth by shortening lag times. The dynamically
rich basal expression of the mar operon has likely been evolutionarily maintained
for its role in growth homeostasis of Enterobacteria within the gut environment,
thereby allowing other ancillary gene regulatory roles to evolve, e.g., control
of costly-to-induce multidrug efflux pumps. Understanding the complex selection
forces governing genetic systems involved in intrinsic multidrug resistance is
crucial for effective public health measures.
acknowledged_ssus:
- _id: Bio
acknowledgement: K.J. thanks B. Wu, I. Tomanek, K. Tomasek for detailed discussions
on the manuscript, all other members from the Guet laboratory for valuable feedback,
R. Chait, & Imaging and Optics Facility, Institute of Science and Technology Austria
for helping with microscopy, Dr. Sudha Rao and Dr. Raja Mugasimangalam, Genotypic
Technology India for allowing time off to address the revisions. K.J. acknowledges
Institute of Science and Technology fellowship IC1006FELL02, R.H. was supported
in part by Chan Zuckerberg Initiative and Donor Advised-Fund grant 2020-225401 (https://doi.org/10.37921/120055ratwvi),
O.O.B. acknowledges Fonds Zur Förderung der Wissenschaftlichen Forschung (FWF) Grant
ESP253-B, R.R. acknowledges FWF Grant 10.55776/ESP219, C.C.G. acknowledges FWF I5127-B.
article_number: e2413709122
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full_name: Jain, Kirti
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last_name: Jain
orcid: 0000-0002-3809-0449
- first_name: Robert
full_name: Hauschild, Robert
id: 4E01D6B4-F248-11E8-B48F-1D18A9856A87
last_name: Hauschild
orcid: 0000-0001-9843-3522
- first_name: Olga
full_name: Bochkareva, Olga
id: C4558D3C-6102-11E9-A62E-F418E6697425
last_name: Bochkareva
orcid: 0000-0003-1006-6639
- first_name: Roderich
full_name: Römhild, Roderich
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last_name: Römhild
orcid: 0000-0001-9480-5261
- first_name: Gašper
full_name: Tkačik, Gašper
id: 3D494DCA-F248-11E8-B48F-1D18A9856A87
last_name: Tkačik
orcid: 0000-0002-6699-1455
- first_name: Calin C
full_name: Guet, Calin C
id: 47F8433E-F248-11E8-B48F-1D18A9856A87
last_name: Guet
orcid: 0000-0001-6220-2052
citation:
ama: Jain K, Hauschild R, Bochkareva O, Römhild R, Tkačik G, Guet CC. Pulsatile
basal gene expression as a fitness determinant in bacteria. Proceedings of
the National Academy of Sciences. 2025;122(15). doi:10.1073/pnas.2413709122
apa: Jain, K., Hauschild, R., Bochkareva, O., Römhild, R., Tkačik, G., & Guet,
C. C. (2025). Pulsatile basal gene expression as a fitness determinant in bacteria.
Proceedings of the National Academy of Sciences. National Academy of Sciences.
https://doi.org/10.1073/pnas.2413709122
chicago: Jain, Kirti, Robert Hauschild, Olga Bochkareva, Roderich Römhild, Gašper
Tkačik, and Calin C Guet. “Pulsatile Basal Gene Expression as a Fitness Determinant
in Bacteria.” Proceedings of the National Academy of Sciences. National
Academy of Sciences, 2025. https://doi.org/10.1073/pnas.2413709122.
ieee: K. Jain, R. Hauschild, O. Bochkareva, R. Römhild, G. Tkačik, and C. C. Guet,
“Pulsatile basal gene expression as a fitness determinant in bacteria,” Proceedings
of the National Academy of Sciences, vol. 122, no. 15. National Academy of
Sciences, 2025.
ista: Jain K, Hauschild R, Bochkareva O, Römhild R, Tkačik G, Guet CC. 2025. Pulsatile
basal gene expression as a fitness determinant in bacteria. Proceedings of the
National Academy of Sciences. 122(15), e2413709122.
mla: Jain, Kirti, et al. “Pulsatile Basal Gene Expression as a Fitness Determinant
in Bacteria.” Proceedings of the National Academy of Sciences, vol. 122,
no. 15, e2413709122, National Academy of Sciences, 2025, doi:10.1073/pnas.2413709122.
short: K. Jain, R. Hauschild, O. Bochkareva, R. Römhild, G. Tkačik, C.C. Guet, Proceedings
of the National Academy of Sciences 122 (2025).
corr_author: '1'
date_created: 2025-04-27T22:02:13Z
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date_updated: 2026-05-20T08:33:08Z
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doi: 10.1073/pnas.2413709122
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title: Pulsatile basal gene expression as a fitness determinant in bacteria
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abstract:
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text: Active regulation of gene expression, orchestrated by complex interactions
of activators and repressors at promoters, controls the fate of organisms. In
contrast, basal expression at uninduced promoters is considered to be a dynamically
inert mode of non-functional “promoter leakiness”, merely a byproduct of transcriptional
regulation. Here, we investigate the basal expression mode of the mar operon,
the main regulator of intrinsic multiple antibiotic resistance in Escherichia
coli, and link its dynamic properties to the non-canonical, yet highly conserved
start codon of marR across Enterobacteriaceae. Real-time, single-cell measurements
across tens of generations reveal that basal expression consists of rare stochastic
gene expression pulses, which maximize variability in wildtype and, surprisingly,
transiently accelerate cellular elongation rates. Competition experiments show
that basal expression confers fitness advantages to wildtype across several transitions
between exponential and stationary growth by shortening lag times. The dynamically
rich basal expression of the mar operon has likely been evolutionarily maintained
for its role in growth homeostasis of Enterobacteria within the gut environment,
thereby allowing other ancillary gene regulatory roles to evolve, e.g. control
of costly-to-induce multi-drug efflux pumps. Understanding the complex selection
forces governing genetic systems involved in intrinsic multi-drug resistance is
crucial for effective public health measures.
article_processing_charge: No
author:
- first_name: Kirti
full_name: Jain, Kirti
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full_name: Guet, Calin C
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citation:
ama: Jain K, Hauschild R, Bochkareva O, Römhild R, Tkačik G, Guet CC. Data for “Pulsatile
basal gene expression as a fitness determinant in bacteria.” 2025. doi:10.15479/AT:ISTA:19294
apa: Jain, K., Hauschild, R., Bochkareva, O., Römhild, R., Tkačik, G., & Guet,
C. C. (2025). Data for “Pulsatile basal gene expression as a fitness determinant
in bacteria.” Institute of Science and Technology Austria. https://doi.org/10.15479/AT:ISTA:19294
chicago: Jain, Kirti, Robert Hauschild, Olga Bochkareva, Roderich Römhild, Gašper
Tkačik, and Calin C Guet. “Data for ‘Pulsatile Basal Gene Expression as a Fitness
Determinant in Bacteria.’” Institute of Science and Technology Austria, 2025.
https://doi.org/10.15479/AT:ISTA:19294.
ieee: K. Jain, R. Hauschild, O. Bochkareva, R. Römhild, G. Tkačik, and C. C. Guet,
“Data for ‘Pulsatile basal gene expression as a fitness determinant in bacteria.’”
Institute of Science and Technology Austria, 2025.
ista: Jain K, Hauschild R, Bochkareva O, Römhild R, Tkačik G, Guet CC. 2025. Data
for ‘Pulsatile basal gene expression as a fitness determinant in bacteria’, Institute
of Science and Technology Austria, 10.15479/AT:ISTA:19294.
mla: Jain, Kirti, et al. Data for “Pulsatile Basal Gene Expression as a Fitness
Determinant in Bacteria.” Institute of Science and Technology Austria, 2025,
doi:10.15479/AT:ISTA:19294.
short: K. Jain, R. Hauschild, O. Bochkareva, R. Römhild, G. Tkačik, C.C. Guet, (2025).
corr_author: '1'
date_created: 2025-03-04T13:27:21Z
date_published: 2025-03-04T00:00:00Z
date_updated: 2026-05-20T08:33:07Z
day: '04'
ddc:
- '570'
department:
- _id: CaGu
- _id: Bio
- _id: FyKo
- _id: GaTk
doi: 10.15479/AT:ISTA:19294
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image: /images/cc_by.png
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type: research_data
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year: '2025'
...
---
_id: '10812'
abstract:
- lang: eng
text: Several promising strategies based on combining or cycling different antibiotics
have been proposed to increase efficacy and counteract resistance evolution, but
we still lack a deep understanding of the physiological responses and genetic
mechanisms that underlie antibiotic interactions and the clinical applicability
of these strategies. In antibiotic-exposed bacteria, the combined effects of physiological
stress responses and emerging resistance mutations (occurring at different time
scales) generate complex and often unpredictable dynamics. In this Review, we
present our current understanding of bacterial cell physiology and genetics of
responses to antibiotics. We emphasize recently discovered mechanisms of synergistic
and antagonistic drug interactions, hysteresis in temporal interactions between
antibiotics that arise from microbial physiology and interactions between antibiotics
and resistance mutations that can cause collateral sensitivity or cross-resistance.
We discuss possible connections between the different phenomena and indicate relevant
research directions. A better and more unified understanding of drug and genetic
interactions is likely to advance antibiotic therapy.
acknowledgement: The authors thank B. Kavčič and H. Schulenburg for constructive feedback
on the manuscript.
article_processing_charge: No
article_type: review
author:
- first_name: Roderich
full_name: Römhild, Roderich
id: 68E56E44-62B0-11EA-B963-444F3DDC885E
last_name: Römhild
orcid: 0000-0001-9480-5261
- first_name: Mark Tobias
full_name: Bollenbach, Mark Tobias
id: 3E6DB97A-F248-11E8-B48F-1D18A9856A87
last_name: Bollenbach
orcid: 0000-0003-4398-476X
- first_name: Dan I.
full_name: Andersson, Dan I.
last_name: Andersson
citation:
ama: Römhild R, Bollenbach MT, Andersson DI. The physiology and genetics of bacterial
responses to antibiotic combinations. Nature Reviews Microbiology. 2022;20:478-490.
doi:10.1038/s41579-022-00700-5
apa: Römhild, R., Bollenbach, M. T., & Andersson, D. I. (2022). The physiology
and genetics of bacterial responses to antibiotic combinations. Nature Reviews
Microbiology. Springer Nature. https://doi.org/10.1038/s41579-022-00700-5
chicago: Römhild, Roderich, Mark Tobias Bollenbach, and Dan I. Andersson. “The Physiology
and Genetics of Bacterial Responses to Antibiotic Combinations.” Nature Reviews
Microbiology. Springer Nature, 2022. https://doi.org/10.1038/s41579-022-00700-5.
ieee: R. Römhild, M. T. Bollenbach, and D. I. Andersson, “The physiology and genetics
of bacterial responses to antibiotic combinations,” Nature Reviews Microbiology,
vol. 20. Springer Nature, pp. 478–490, 2022.
ista: Römhild R, Bollenbach MT, Andersson DI. 2022. The physiology and genetics
of bacterial responses to antibiotic combinations. Nature Reviews Microbiology.
20, 478–490.
mla: Römhild, Roderich, et al. “The Physiology and Genetics of Bacterial Responses
to Antibiotic Combinations.” Nature Reviews Microbiology, vol. 20, Springer
Nature, 2022, pp. 478–90, doi:10.1038/s41579-022-00700-5.
short: R. Römhild, M.T. Bollenbach, D.I. Andersson, Nature Reviews Microbiology
20 (2022) 478–490.
date_created: 2022-03-04T04:33:49Z
date_published: 2022-08-01T00:00:00Z
date_updated: 2023-08-02T14:41:44Z
day: '01'
department:
- _id: CaGu
doi: 10.1038/s41579-022-00700-5
external_id:
isi:
- '000763891900001'
pmid:
- '35241807'
intvolume: ' 20'
isi: 1
keyword:
- General Immunology and Microbiology
- Microbiology
- Infectious Diseases
language:
- iso: eng
month: '08'
oa_version: None
page: 478-490
pmid: 1
publication: Nature Reviews Microbiology
publication_identifier:
eissn:
- 1740-1534
issn:
- 1740-1526
publication_status: published
publisher: Springer Nature
quality_controlled: '1'
scopus_import: '1'
status: public
title: The physiology and genetics of bacterial responses to antibiotic combinations
type: journal_article
user_id: 4359f0d1-fa6c-11eb-b949-802e58b17ae8
volume: 20
year: '2022'
...
---
_id: '9046'
acknowledgement: Our work was supported by the Swedish Research Council (grant 2017-01527)
to DIA
article_number: e1009172
article_processing_charge: No
article_type: original
author:
- first_name: Roderich
full_name: Römhild, Roderich
id: 68E56E44-62B0-11EA-B963-444F3DDC885E
last_name: Römhild
orcid: 0000-0001-9480-5261
- first_name: Dan I.
full_name: Andersson, Dan I.
last_name: Andersson
citation:
ama: Römhild R, Andersson DI. Mechanisms and therapeutic potential of collateral
sensitivity to antibiotics. PLoS Pathogens. 2021;17(1). doi:10.1371/journal.ppat.1009172
apa: Römhild, R., & Andersson, D. I. (2021). Mechanisms and therapeutic potential
of collateral sensitivity to antibiotics. PLoS Pathogens. Public Library
of Science. https://doi.org/10.1371/journal.ppat.1009172
chicago: Römhild, Roderich, and Dan I. Andersson. “Mechanisms and Therapeutic Potential
of Collateral Sensitivity to Antibiotics.” PLoS Pathogens. Public Library
of Science, 2021. https://doi.org/10.1371/journal.ppat.1009172.
ieee: R. Römhild and D. I. Andersson, “Mechanisms and therapeutic potential of collateral
sensitivity to antibiotics,” PLoS Pathogens, vol. 17, no. 1. Public Library
of Science, 2021.
ista: Römhild R, Andersson DI. 2021. Mechanisms and therapeutic potential of collateral
sensitivity to antibiotics. PLoS Pathogens. 17(1), e1009172.
mla: Römhild, Roderich, and Dan I. Andersson. “Mechanisms and Therapeutic Potential
of Collateral Sensitivity to Antibiotics.” PLoS Pathogens, vol. 17, no.
1, e1009172, Public Library of Science, 2021, doi:10.1371/journal.ppat.1009172.
short: R. Römhild, D.I. Andersson, PLoS Pathogens 17 (2021).
date_created: 2021-01-31T23:01:21Z
date_published: 2021-01-14T00:00:00Z
date_updated: 2025-07-10T12:01:33Z
day: '14'
ddc:
- '570'
department:
- _id: CaGu
doi: 10.1371/journal.ppat.1009172
external_id:
isi:
- '000610190400007'
pmid:
- '33444399'
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has_accepted_license: '1'
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isi: 1
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- iso: eng
month: '01'
oa: 1
oa_version: Published Version
pmid: 1
publication: PLoS Pathogens
publication_identifier:
eissn:
- 1553-7374
issn:
- 1553-7366
publication_status: published
publisher: Public Library of Science
quality_controlled: '1'
scopus_import: '1'
status: public
title: Mechanisms and therapeutic potential of collateral sensitivity to antibiotics
tmp:
image: /images/cc_by.png
legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
short: CC BY (4.0)
type: journal_article
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 17
year: '2021'
...
---
_id: '9746'
abstract:
- lang: eng
text: Evolutionary adaptation is a major source of antibiotic resistance in bacterial
pathogens. Evolution-informed therapy aims to constrain resistance by accounting
for bacterial evolvability. Sequential treatments with antibiotics that target
different bacterial processes were previously shown to limit adaptation through
genetic resistance trade-offs and negative hysteresis. Treatment with homogeneous
sets of antibiotics is generally viewed to be disadvantageous, as it should rapidly
lead to cross-resistance. We here challenged this assumption by determining the
evolutionary response of Pseudomonas aeruginosa to experimental sequential treatments
involving both heterogenous and homogeneous antibiotic sets. To our surprise,
we found that fast switching between only β-lactam antibiotics resulted in increased
extinction of bacterial populations. We demonstrate that extinction is favored
by low rates of spontaneous resistance emergence and low levels of spontaneous
cross-resistance among the antibiotics in sequence. The uncovered principles may
help to guide the optimized use of available antibiotics in highly potent, evolution-informed
treatment designs.
acknowledgement: We would like to thank Leif Tueffers and João Botelho for discussions
and suggestions as well as Kira Haas and Julia Bunk for technical support. We acknowledge
financial support from the German Science Foundation (grant SCHU 1415/12-2 to HS,
and funding under Germany’s Excellence Strategy EXC 2167–390884018 as well as the
Research Training Group 2501 TransEvo to HS and SN), the Max Planck Society (IMPRS
scholarship to AB; Max-Planck fellowship to HS), and the Leibniz Science Campus
Evolutionary Medicine of the Lung (EvoLUNG, to HS and SN). This work was further
supported by the German Science Foundation Research Infrastructure NGS_CC (project
407495230) as part of the Next Generation Sequencing Competence Network (project
423957469). NGS analyses were carried out at the Competence Centre for Genomic Analysis
Kiel (CCGA Kiel).
article_number: e68876
article_processing_charge: No
article_type: original
author:
- first_name: Aditi
full_name: Batra, Aditi
last_name: Batra
- first_name: Roderich
full_name: Römhild, Roderich
id: 68E56E44-62B0-11EA-B963-444F3DDC885E
last_name: Römhild
orcid: 0000-0001-9480-5261
- first_name: Emilie
full_name: Rousseau, Emilie
last_name: Rousseau
- first_name: Sören
full_name: Franzenburg, Sören
last_name: Franzenburg
- first_name: Stefan
full_name: Niemann, Stefan
last_name: Niemann
- first_name: Hinrich
full_name: Schulenburg, Hinrich
last_name: Schulenburg
citation:
ama: Batra A, Römhild R, Rousseau E, Franzenburg S, Niemann S, Schulenburg H. High
potency of sequential therapy with only beta-lactam antibiotics. eLife.
2021;10. doi:10.7554/elife.68876
apa: Batra, A., Römhild, R., Rousseau, E., Franzenburg, S., Niemann, S., & Schulenburg,
H. (2021). High potency of sequential therapy with only beta-lactam antibiotics.
ELife. eLife Sciences Publications. https://doi.org/10.7554/elife.68876
chicago: Batra, Aditi, Roderich Römhild, Emilie Rousseau, Sören Franzenburg, Stefan
Niemann, and Hinrich Schulenburg. “High Potency of Sequential Therapy with Only
Beta-Lactam Antibiotics.” ELife. eLife Sciences Publications, 2021. https://doi.org/10.7554/elife.68876.
ieee: A. Batra, R. Römhild, E. Rousseau, S. Franzenburg, S. Niemann, and H. Schulenburg,
“High potency of sequential therapy with only beta-lactam antibiotics,” eLife,
vol. 10. eLife Sciences Publications, 2021.
ista: Batra A, Römhild R, Rousseau E, Franzenburg S, Niemann S, Schulenburg H. 2021.
High potency of sequential therapy with only beta-lactam antibiotics. eLife. 10,
e68876.
mla: Batra, Aditi, et al. “High Potency of Sequential Therapy with Only Beta-Lactam
Antibiotics.” ELife, vol. 10, e68876, eLife Sciences Publications, 2021,
doi:10.7554/elife.68876.
short: A. Batra, R. Römhild, E. Rousseau, S. Franzenburg, S. Niemann, H. Schulenburg,
ELife 10 (2021).
date_created: 2021-07-28T13:36:57Z
date_published: 2021-07-28T00:00:00Z
date_updated: 2023-08-11T10:26:29Z
day: '28'
department:
- _id: CaGu
doi: 10.7554/elife.68876
external_id:
isi:
- '000692027800001'
pmid:
- '34318749'
intvolume: ' 10'
isi: 1
language:
- iso: eng
main_file_link:
- open_access: '1'
url: https://doi.org/10.7554/eLife.68876
month: '07'
oa: 1
oa_version: Published Version
pmid: 1
publication: eLife
publication_identifier:
eissn:
- 2050-084X
publication_status: published
publisher: eLife Sciences Publications
quality_controlled: '1'
scopus_import: '1'
status: public
title: High potency of sequential therapy with only beta-lactam antibiotics
type: journal_article
user_id: 4359f0d1-fa6c-11eb-b949-802e58b17ae8
volume: 10
year: '2021'
...