Cited by 147Bacterial Genetics and BiotechnologyRNA and protein synthesis mechanismsCell death mechanisms and regulation

Magnesium Flux Modulates Ribosomes to Increase Bacterial Survival

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Lee, Dong-yeon D., Galera-Laporta, Leticia, Bialecka-Fornal, Maja, Moon, Eun Chae, Shen, Zhouxin, Briggs, Steven P., Garcia-Ojalvo, Jordi, Süel, Gürol M.·2019·Cell

Abstract

Bacteria exhibit cell-to-cell variability in their resilience to stress, for example, following antibiotic exposure. Higher resilience is typically ascribed to "dormant" non-growing cellular states. Here, by measuring membrane potential dynamics of Bacillus subtilis cells, we show that actively growing bacteria can cope with ribosome-targeting antibiotics through an alternative mechanism based on ion flux modulation. Specifically, we observed two types of cellular behavior: growth-defective cells exhibited a mathematically predicted transient increase in membrane potential (hyperpolarization), followed by cell death, whereas growing cells lacked hyperpolarization events and showed elevated survival. Using structural perturbations of the ribosome and proteomic analysis, we uncovered that stress resilience arises from magnesium influx, which prevents hyperpolarization. Thus, ion flux modulation provides a distinct mechanism to cope with ribosomal stress. These results suggest new approaches to increase the effectiveness of ribosome-targeting antibiotics and reveal an intriguing connection between ribosomes and the membrane potential, two fundamental properties of cells.

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Crossref · 10.1016/j.cell.2019.01.042

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  • A decrease in Mg2+ during osmoadaptation could impair translation and thereby delay the resumption of growth.

    “These data, together with recent publications highlighting the connection between Mg2+ homeostasis and translation (29, 33, 34), support the idea that a decrease in Mg2+ during osmoadaptation could impair translation and thereby delay the resumption of growth.”

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Authors
Lee, D.-Y. D., Galera-Laporta, L., Bialecka-Fornal, M., Moon, E. C., Shen, Z., Briggs, S. P., Garcia-Ojalvo, J., & Süel, G. M.
Affiliations
  • University of California San Diego (US)
  • Universitat Pompeu Fabra (ES)
Corresponding author
Süel, Gürol M.
Venue
Cell
Publisher
Elsevier BV
Published
2019-04
Volume
177
Issue
2
Pages
352-360.e13
ISSN
0092-8674 (ISSN-L)
OpenAlex
W2922356758
Cited by
147
References
46
Citations by year
2026: 27 · 2025: 24 · 2024: 20 · 2023: 15 · 2022: 24 · 2021: 23 · 2020: 7 · 2019: 7
FWCI
9.18
Type
journal article
Language
en
Open access
Locations
  • Cell (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • Repositori digital de la UPF (Universitat Pompeu Fabra) (acceptedVersion)
  • RECERCAT (Consorci de Serveis Universitaris de Catalunya) (submittedVersion)
Funders
  • Spanish Ministry of Economy and Competitiveness
  • FEDER (FIS2015-66503-C3-1-P)
  • ICREA
  • Maria de Maeztu Program for Units of Excellence in Research and Development (MDM-2014-0370)
  • San Diego Center for Systems Biology
  • NIH (P50 GM085764)
  • National Institute of General Medical Sciences (R01 GM121888)
  • Howard Hughes Medical Institute
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
Keywords
magnesium influx, ribosome-targeting antibiotics, membrane hyperpolarization, Bacillus subtilis, cell-to-cell variability, antibiotic tolerance
MeSH terms
Bacterial Outer Membrane, Bacillus subtilis, Bacterial Proteins, Magnesium, Ribosomal Proteins, Ribosomes, Proteomics

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