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

Rauch, Cyril; Cherkaoui-Rbati, Mohammed; Egan, Sharon A.; Leigh, James A.

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.

Citation

Rauch, C., Cherkaoui-Rbati, M., Egan, S. A., & Leigh, J. A. (2017). The bio-physics of condensation of divalent cations into the bacterial wall has implications for growth of Gram-positive bacteria. BBA - Biomembranes, 1859(2), https://doi.org/10.1016/j.bbamem.2016.12.002

• Journal Article Type: Article
• Acceptance Date: Aug 6, 2016
• Online Publication Date: Dec 7, 2016
• Publication Date: Feb 1, 2017
• Deposit Date: Dec 6, 2016
• Publicly Available Date: Dec 7, 2016
• Journal: BBA - Biomembranes
• Print ISSN: 0005-2736
• Electronic ISSN: 1879-2642
• Publisher: Elsevier
• Peer Reviewed: Peer Reviewed
• Volume: 1859
• Issue: 2
• DOI: https://doi.org/10.1016/j.bbamem.2016.12.002
• Keywords: Gram-positive bacteria; teichoic acid; cell wall; metal cations; polyelectrolytes; Manning’s Theory
• Public URL: https://nottingham-repository.worktribe.com/output/970733
• Publisher URL: http://www.sciencedirect.com/science/article/pii/S000527361630387X
• Contract Date: Dec 6, 2016