ATP-Dependent Persister Formation in Escherichia coli
Open accessAbstract
Persisters are dormant variants that form a subpopulation of cells tolerant to antibiotics. Persisters are largely responsible for the recalcitrance of chronic infections to therapy. In Escherichia coli , one widely accepted model of persister formation holds that stochastic accumulation of ppGpp causes activation of the Lon protease that degrades antitoxins; active toxins then inhibit translation, resulting in dormant, drug-tolerant persisters. We found that various stresses induce toxin-antitoxin (TA) expression but that induction of TAs does not necessarily increase persisters. The 16S rRNA promoter rrnB P1 was proposed to be a persister reporter and an indicator of toxin activation regulated by ppGpp. Using fluorescence-activated cell sorting (FACS), we confirmed the enrichment for persisters in the fraction of rrnB P1 -gfp dim cells; however, this is independent of toxin-antitoxins. rrnB P1 is coregulated by ppGpp and ATP. We show that rrnB P1 can report persisters in a relA / spoT deletion background, suggesting that rrnB P1 is a persister marker responding to ATP. Consistent with this finding, decreasing the level of ATP by arsenate treatment causes drug tolerance. Lowering ATP slows translation and prevents the formation of DNA double-strand breaks upon fluoroquinolone treatment. We conclude that variation in ATP levels leads to persister formation by decreasing the activity of antibiotic targets. IMPORTANCE Persisters are a subpopulation of antibiotic-tolerant cells responsible for the recalcitrance of chronic infections. Our current understanding of persister formation is primarily based on studies of E. coli . The activation of toxin-antitoxin systems by ppGpp has become a widely accepted model for persister formation. In this study, we found that stress-induced activation of mRNA interferase-type toxins does not necessarily cause persister formation. We also found that the persister marker rrnB P1 reports persister cells because it detects a drop in cellular ATP levels. Consistent with this, lowering the ATP level decreases antibiotic target activity and, thus, leads to persister formation. We conclude that stochastic variation in ATP is the main mechanism of persister formation. A decrease in ATP provides a satisfactory explanation for the drug tolerance of persisters, since bactericidal antibiotics act by corrupting energy-dependent targets.
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Dormant state reduces exposure of antibiotic targets and helps bacterial cells tolerate a variety of antibiotics, a process linked to the toxin-antitoxin system.
“It has been well studied that dormant state reduces the exposure of antibiotic targets and helps bacterial cells tolerate a variety of antibiotics, a process linked to the toxin-antitoxin system [18,54].”
From Antifungal persistence: Clinical relevance and mechanisms (2025) · cites this paper as [54]
The Discussion says reduced ATP diminishes antibiotic-target activity and produces tolerance to several antibiotic classes. The Introduction links toxin-antitoxin modules to persister formation, but the Results and Discussion find their contribution limited and condition-dependent; the paper does not support presenting the general tolerance mechanism as toxin-antitoxin-driven. Page numbers are unavailable in our copy. (LLM, conf=0.84)
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- [27]Maisonneuve E, Castro-Camargo M, Gerdes K 2013 ppGpp controls bacterial persistence by stochastic induction of toxin-antitoxin activity. Cell 154: 1140– 1150. doi: 10.1016/j.cell.2013.07.048. 23993101 · DOI
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- Authors
- Shan, Y., Brown Gandt, A., Rowe, S. E., Deisinger, J. P., Conlon, B. P., & Lewis, K.
- Affiliations
- Northeastern University (US)
- Department of Biology, Antimicrobial Discovery Center, Northeastern University, Boston, Massachusetts, USA
- Corresponding author
- Lewis, Kim
- Venue
- mBio
- Publisher
- American Society for Microbiology
- Published
- 2017-03-08
- Volume
- 8
- Issue
- 1
- ISSN
- 2150-7511 (ISSN-L)
- 2161-2129
- PMC
- PMC5296605
- OpenAlex
- W2586386056
- Cited by
- 508
- References
- 71
- Citations by year
- 2026: 55 · 2025: 61 · 2024: 47 · 2023: 42 · 2022: 54 · 2021: 61 · 2020: 56 · 2019: 69 · 2018: 37 · 2017: 26
- FWCI
- 34.04
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- mBio (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- UNC Libraries
- Funders
- DH | National Institute for Health Research (R01AI110578)
- Charles A. King Trust (Fellowship)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Health Sciences › Medicine › Infectious Diseases › Antimicrobial Resistance in Staphylococcus
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
- Keywords
- persister cells, antibiotic tolerance, Escherichia coli, ATP levels, toxin-antitoxin systems, ppGpp, Lon protease, arsenate, protein synthesis inhibition, DNA double-strand breaks, fluoroquinolones, chronic infection
- MeSH terms
- Adenosine Triphosphate, Drug Tolerance, Escherichia coli, Gene Expression Regulation, Bacterial, Microbial Viability
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