Bacterial persisters are a stochastically formed subpopulation of low-energy cells
Persisters represent a small subpopulation of non- or slow-growing bacterial cells that are tolerant to killing by antibiotics. Despite their prominent role in the recalcitrance of chronic infections to antibiotic therapy, the mechanism of their formation has remained elusive. We show that sorted ce...
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| Published in | PLoS biology Vol. 19; no. 4; p. e3001194 |
|---|---|
| Main Authors | , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
19.04.2021
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1545-7885 1544-9173 1545-7885 |
| DOI | 10.1371/journal.pbio.3001194 |
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| Abstract | Persisters represent a small subpopulation of non- or slow-growing bacterial cells that are tolerant to killing by antibiotics. Despite their prominent role in the recalcitrance of chronic infections to antibiotic therapy, the mechanism of their formation has remained elusive. We show that sorted cells of
Escherichia coli
with low levels of energy-generating enzymes are better able to survive antibiotic killing. Using microfluidics time-lapse microscopy and a fluorescent reporter for in vivo ATP measurements, we find that a subpopulation of cells with a low level of ATP survives killing by ampicillin. We propose that these low ATP cells are formed stochastically as a result of fluctuations in the abundance of energy-generating components. These findings point to a general “low energy” mechanism of persister formation. |
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| AbstractList | Persisters represent a small subpopulation of non- or slow-growing bacterial cells that are tolerant to killing by antibiotics. Despite their prominent role in the recalcitrance of chronic infections to antibiotic therapy, the mechanism of their formation has remained elusive. We show that sorted cells of
Escherichia coli
with low levels of energy-generating enzymes are better able to survive antibiotic killing. Using microfluidics time-lapse microscopy and a fluorescent reporter for in vivo ATP measurements, we find that a subpopulation of cells with a low level of ATP survives killing by ampicillin. We propose that these low ATP cells are formed stochastically as a result of fluctuations in the abundance of energy-generating components. These findings point to a general “low energy” mechanism of persister formation. Persisters represent a small subpopulation of non- or slow-growing bacterial cells that are tolerant to killing by antibiotics. Despite their prominent role in the recalcitrance of chronic infections to antibiotic therapy, the mechanism of their formation has remained elusive. We show that sorted cells of Escherichia coli with low levels of energy-generating enzymes are better able to survive antibiotic killing. Using microfluidics time-lapse microscopy and a fluorescent reporter for in vivo ATP measurements, we find that a subpopulation of cells with a low level of ATP survives killing by ampicillin. We propose that these low ATP cells are formed stochastically as a result of fluctuations in the abundance of energy-generating components. These findings point to a general “low energy” mechanism of persister formation. Persisters represent a small subpopulation of non- or slow-growing bacterial cells that are tolerant to killing by antibiotics. Despite their prominent role in the recalcitrance of chronic infections to antibiotic therapy, the mechanism of their formation has remained elusive. We show that sorted cells of Escherichia coli with low levels of energy-generating enzymes are better able to survive antibiotic killing. Using microfluidics time-lapse microscopy and a fluorescent reporter for in vivo ATP measurements, we find that a subpopulation of cells with a low level of ATP survives killing by ampicillin. We propose that these low ATP cells are formed stochastically as a result of fluctuations in the abundance of energy-generating components. These findings point to a general “low energy” mechanism of persister formation. Persisters represent a small subpopulation of non- or slow-growing bacterial cells that are tolerant to killing by antibiotics, but the mechanism of their formation has remained elusive. This study of E. coli shows that stochastic heterogeneity in levels of energy-generating enzymes results in a subpopulation of cells with low ATP that are tolerant to antibiotics. Abbreviations: ADEP, acyldepsipeptide; CFU, colony forming unit; DIC, differential interference contrast; FACS, fluorescence-activated cell sorting; Icd, isocitrate dehydrogenase; TA, toxin-antitoxin; WT, wild type Main text In Escherichia coli, the RNA-degrading interferase-type toxin/antitoxins (TA) emerged as the main component involved in persister formation [1]. The HipA toxin is a glutamyl-tRNA kinase [7,8], and its gain-of-function mutants produce high levels of persisters by inhibiting translation in patients with relapsing urinary tract infection [9] while its absence leads to a decrease in the level of persisters in Caulobacter crescentus [10]. Stationary phase cells have lower ATP levels, and we found that persisters in a growing population of Staphylococcus aureus have elevated levels of expression of stationary phase markers, suggesting that those cells would also have a lower level of ATP [2]. CFU, colony forming unit; FACS, fluorescence-activated cell sorting; YFP, yellow fluorescent protein. https://doi.org/10.1371/journal.pbio.3001194.g001 We then examined whether impaired Krebs cycle activity in single cells of a wild type (WT) population would lead to persister formation. Persisters represent a small subpopulation of non- or slow-growing bacterial cells that are tolerant to killing by antibiotics. Despite their prominent role in the recalcitrance of chronic infections to antibiotic therapy, the mechanism of their formation has remained elusive. We show that sorted cells of Escherichia coli with low levels of energy-generating enzymes are better able to survive antibiotic killing. Using microfluidics time-lapse microscopy and a fluorescent reporter for in vivo ATP measurements, we find that a subpopulation of cells with a low level of ATP survives killing by ampicillin. We propose that these low ATP cells are formed stochastically as a result of fluctuations in the abundance of energy-generating components. These findings point to a general "low energy" mechanism of persister formation.Persisters represent a small subpopulation of non- or slow-growing bacterial cells that are tolerant to killing by antibiotics. Despite their prominent role in the recalcitrance of chronic infections to antibiotic therapy, the mechanism of their formation has remained elusive. We show that sorted cells of Escherichia coli with low levels of energy-generating enzymes are better able to survive antibiotic killing. Using microfluidics time-lapse microscopy and a fluorescent reporter for in vivo ATP measurements, we find that a subpopulation of cells with a low level of ATP survives killing by ampicillin. We propose that these low ATP cells are formed stochastically as a result of fluctuations in the abundance of energy-generating components. These findings point to a general "low energy" mechanism of persister formation. Abbreviations: ADEP, acyldepsipeptide; CFU, colony forming unit; DIC, differential interference contrast; FACS, fluorescence-activated cell sorting; Icd, isocitrate dehydrogenase; TA, toxin-antitoxin; WT, wild type Main text In Escherichia coli, the RNA-degrading interferase-type toxin/antitoxins (TA) emerged as the main component involved in persister formation [1]. The HipA toxin is a glutamyl-tRNA kinase [7,8], and its gain-of-function mutants produce high levels of persisters by inhibiting translation in patients with relapsing urinary tract infection [9] while its absence leads to a decrease in the level of persisters in Caulobacter crescentus [10]. Stationary phase cells have lower ATP levels, and we found that persisters in a growing population of Staphylococcus aureus have elevated levels of expression of stationary phase markers, suggesting that those cells would also have a lower level of ATP [2]. CFU, colony forming unit; FACS, fluorescence-activated cell sorting; YFP, yellow fluorescent protein. https://doi.org/10.1371/journal.pbio.3001194.g001 We then examined whether impaired Krebs cycle activity in single cells of a wild type (WT) population would lead to persister formation. |
| Audience | Academic |
| Author | Manuse, Sylvie Lewis, Kim Shan, Yue Sun, Wei-Sheng Canas-Duarte, Silvia J. Bakshi, Somenath Mori, Hirotada Paulsson, Johan |
| AuthorAffiliation | 3 Graduate School of Biological Sciences, Nara Institute of Science and Technology, Nara, Japan 2 Department of Systems Biology, Harvard Medical School, Boston, Massachusetts, United States of America 1 Antimicrobial Discovery Center, Department of Biology, Northeastern University, Boston, Massachusetts, United States of America Universitat zu Koln, GERMANY |
| AuthorAffiliation_xml | – name: 3 Graduate School of Biological Sciences, Nara Institute of Science and Technology, Nara, Japan – name: 2 Department of Systems Biology, Harvard Medical School, Boston, Massachusetts, United States of America – name: Universitat zu Koln, GERMANY – name: 1 Antimicrobial Discovery Center, Department of Biology, Northeastern University, Boston, Massachusetts, United States of America |
| Author_xml | – sequence: 1 givenname: Sylvie surname: Manuse fullname: Manuse, Sylvie – sequence: 2 givenname: Yue surname: Shan fullname: Shan, Yue – sequence: 3 givenname: Silvia J. orcidid: 0000-0001-5705-0023 surname: Canas-Duarte fullname: Canas-Duarte, Silvia J. – sequence: 4 givenname: Somenath orcidid: 0000-0003-3864-2546 surname: Bakshi fullname: Bakshi, Somenath – sequence: 5 givenname: Wei-Sheng surname: Sun fullname: Sun, Wei-Sheng – sequence: 6 givenname: Hirotada orcidid: 0000-0003-3855-778X surname: Mori fullname: Mori, Hirotada – sequence: 7 givenname: Johan surname: Paulsson fullname: Paulsson, Johan – sequence: 8 givenname: Kim orcidid: 0000-0002-1335-9982 surname: Lewis fullname: Lewis, Kim |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/33872303$$D View this record in MEDLINE/PubMed https://hal.science/hal-05005375$$DView record in HAL |
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| ContentType | Journal Article |
| Copyright | COPYRIGHT 2021 Public Library of Science 2021 Manuse et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. Attribution 2021 Manuse et al 2021 Manuse et al |
| Copyright_xml | – notice: COPYRIGHT 2021 Public Library of Science – notice: 2021 Manuse et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. – notice: Attribution – notice: 2021 Manuse et al 2021 Manuse et al |
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| DOI | 10.1371/journal.pbio.3001194 |
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| Keywords | acyldepsipeptide CFU isocitrate dehydrogenase differential interference contrast toxin-antitoxin fluorescence-activated cell sorting acyldepsipeptide Icd FACS TA colony forming unit DIC ADEP fluorescence-activated cell sorting Icd CFU differential interference contrast FACS colony forming unit isocitrate dehydrogenase TA toxin-antitoxin WT wild type WT DIC |
| Language | English |
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| Notes | new_version ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 The authors have declared that no competing interests exist. Current address: Department of Engineering, Cambridge University, Cambridge, United Kingdom |
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| Snippet | Persisters represent a small subpopulation of non- or slow-growing bacterial cells that are tolerant to killing by antibiotics. Despite their prominent role in... Abbreviations: ADEP, acyldepsipeptide; CFU, colony forming unit; DIC, differential interference contrast; FACS, fluorescence-activated cell sorting; Icd,... |
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| SubjectTerms | Abbreviations Ampicillin Analysis Anti-Bacterial Agents - pharmacology Antibiotics Antitoxins ATP Bacteria - drug effects Bacteria - genetics Bacteria - growth & development Bacteria - metabolism Bacterial Physiological Phenomena - drug effects Bacteriology Biology and Life Sciences Carbon Cellular Biology Citric Acid Cycle - drug effects Colonies Computer and Information Sciences Dehydrogenases Drug Resistance, Multiple, Bacterial - drug effects E coli Energy Energy Metabolism - drug effects Energy Metabolism - physiology Engineering and Technology Enzymes Escherichia coli Escherichia coli - drug effects Escherichia coli - growth & development Escherichia coli - metabolism Flow cytometry Fluorescence Isocitrate dehydrogenase Kinases Krebs cycle Life Sciences Medicine and Health Sciences Methods Microbial Sensitivity Tests Microbial Viability - drug effects Microbiology and Parasitology Microfluidics Organisms, Genetically Modified Physical Sciences Physiological aspects Population Properties Protein transport Research and Analysis Methods Short Reports Stationary phase Subcellular Processes Toxins Tricarboxylic acid cycle tRNA Urinary tract Yellow fluorescent protein |
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| Title | Bacterial persisters are a stochastically formed subpopulation of low-energy cells |
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