Cited by 12Electrostatics and Colloid InteractionsBacterial Genetics and BiotechnologyAntimicrobial agents and applications

The bio-physics of condensation of divalent cations into the bacterial wall has implications for growth of Gram-positive bacteria

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Rauch, Cyril, Cherkaoui, Mohammed, Egan, Sharon, Leigh, James·2017·Biochimica et Biophysica Acta (BBA) - Biomembranes

Abstract

Background The anionic-polyelectrolyte nature of the wall of Gram-positive bacteria has long been suspected to be involved in homeostasis of essential cations and bacterial growth. A better understanding of the coupling between the biophysics and the biology of the wall is essential to understand some key features at play in ion-homeostasis in this living system. Methods We consider the wall as a polyelectrolyte gel and balance the long-range electrostatic repulsion within this structure against the penalty entropy required to condense cations around wall polyelectrolytes. The resulting equations define how cations interact physically with the wall and the characteristic time required for a cation to leave the wall and enter into the bacterium to enable its usage for bacterial metabolism and growth. Results The model was challenged against experimental data regarding growth of Gram-positive bacteria in the presence of varying concentration of divalent ions. The model explains qualitatively and quantitatively how divalent cations interact with the wall as well as how the biophysical properties of the wall impact on bacterial growth (in particular the initiation of bacterial growth). Conclusion The interplay between polymer biophysics and the biology of Gram positive bacteria is defined for the first time as a new set of variables that contribute to the kinetics of bacterial growth. General significance Providing an understanding of how bacteria capture essential metal cations in way that does not follow usual binding laws has implications when considering the control of such organisms and their ability to survive and grow in extreme environments.

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Crossref · 10.1016/j.bbamem.2016.12.002

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  • The thick cell walls of Gram-positive bacteria have an enormous ion-binding capacity, with near equal contributions from peptidoglycan and teichoic acids.

    “Similarly, the thick cell walls of Gram-positive bacteria have an enormous ion-binding capacity,61 with near equal contributions from peptidoglycan and teichoic acids.62”

    From Metals in Motion: Understanding Labile Metal Pools in Bacteria (2025) · cites this paper as [61]

    Citation 62 is attached specifically to the claim of near-equal ion-binding contributions from peptidoglycan and teichoic acids. The Introduction says teichoic acids may constitute up to 60% of the wall’s mass and describes their role in binding cations, but neither that passage nor the passages retrieved for equal contributions and binding capacity compares the two components’ ion-binding contributions. (LLM, conf=0.74)

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Research works printed but not linked: 9

  1. U. Ilangovan, H. Ton-That, J. Iwahara, O. Schneewind, R.T. Clubb, Structure of sortase, the transpeptidase that anchors proteins to the cell wall of Staphylococcus aureus, Proceedings of the National Academy of Sciences of the United States of America, 98 (2001) 6056-6061.
  2. M.T. Naik, N. Suree, U. Ilangovan, C.K. Liew, W. Thieu, D.O. Campbell, J.J. Clemens, M.E. Jung, R.T. Clubb, Staphylococcus aureus Sortase A transpeptidase. Calcium promotes sorting signal binding by altering the mobility and structure of an active site loop, The Journal of biological chemistry, 281 (2006) 1817-1826.
  3. M. Webb, The influence of magnesium on cell division. V. The effect of magnesium on the growth of bacteria in chemically-defined media of varying complexity, Journal of general microbiology, 5 (1951) 485-495.
  4. K.J. Thomas, 3rd, C.V. Rice, Revised model of calcium and magnesium binding to the bacterial cell wall, Biometals : an international journal on the role of metal ions in biology, biochemistry, and medicine, 27 (2014) 1361-1370.
  5. G.S. Manning, Limiting Laws and Counterion Condensation in Polyelectrolyte Solutions .2. Self-Diffusion of Small Ions, Journal of Chemical Physics, 51 (1969) 934-&.
  6. G.S. Manning, Limiting Laws and Counterion Condensation in Polyelectrolyte Solutions .3. An Analysis Based on Mayer Ionic Solution Theory, Journal of Chemical Physics, 51 (1969) 3249-&.
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  8. J. Monod, The Growth of Bacterial Cultures, Annual Review of Microbiology, 3 (1949) 371-394.
  9. R. Zwanzig, Generalized Verhulst Laws for Population-Growth, Proceedings of the National Academy of Sciences of the United States of America, 70 (1973) 3048-3051.

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Authors
Rauch, C., Cherkaoui, M., Egan, S., & Leigh, J.
Affiliations
University of Nottingham (GB)
Corresponding author
Rauch, Cyril
Venue
Biochimica et Biophysica Acta (BBA) - Biomembranes
Publisher
Elsevier BV
Published
2017-02
Volume
1859
Issue
2
Pages
282-288
ISSN
0005-2736 (ISSN-L)
OpenAlex
W2560783062
Cited by
12
References
0
Citations by year
2026: 3 · 2025: 1 · 2023: 3 · 2022: 1 · 2021: 1 · 2020: 2 · 2018: 1
FWCI
0.21
Type
journal article
Language
en
Open access
Locations
  • Biochimica et Biophysica Acta (BBA) - Biomembranes (publishedVersion)
  • PubMed (publishedVersion)
  • Repository@Nottingham (University of Nottingham) (acceptedVersion, other-oa)
  • Repository@Nottingham (University of Nottingham) (submittedVersion, cc-by-nc-nd)
  • Nottingham ePrints (University of Nottingham) (submittedVersion, cc-by-nc-nd)
Funders
University of Nottingham
Topics
  • Physical Sciences › Chemistry › Physical and Theoretical Chemistry › Electrostatics and Colloid Interactions
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Physical Sciences › Chemistry › Organic Chemistry › Antimicrobial agents and applications
Keywords
Gram-positive bacterial cell wall, divalent cations, polyelectrolyte gels, electrostatic repulsion, entropy penalty, ion homeostasis, bacterial growth kinetics, cation binding, growth initiation
MeSH terms
Polyelectrolytes, Biophysics, Cations, Divalent, Cell Wall, Gram-Positive Bacteria, Homeostasis, Metals, Polymers, Static Electricity

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