Spatiotemporal dynamics of ionic reorganization near biological membrane interfaces

Row, Hyeongjoo; Fernandes, Joshua B.; Mandadapu, Kranthi K.; Shekhar, Karthik

doi:10.1103/PhysRevResearch.7.013185

Title: Spatiotemporal dynamics of ionic reorganization near biological membrane interfaces

Journal Article · 20 February 2025 · Physical Review Research

DOI: https://doi.org/10.1103/PhysRevResearch.7.013185 · OSTI ID:2522116

; Fernandes, Joshua B.; Mandadapu, Kranthi K.;

Electrical signals in excitable cells involve spatially localized ionic fluxes through ion channels and pumps on cellular lipid membranes. Common approaches to understand how these fluxes spread assume that the membrane and the surrounding electrolyte comprise an equivalent circuit of capacitors and resistors, which ignores the localized nature of transmembrane ion transport, the resulting ionic gradients and electric fields, and their spatiotemporal relaxation. Here, we consider a model of localized ion pumping across a lipid membrane, and use theory and simulation to investigate how the electrochemical signal propagates spatiotemporally in and out of plane along the membrane. The localized pumping generates long-ranged electric fields with three distinct scaling regimes along the membrane: a constant potential near-field region, an intermediate monopolar region, and a far-field dipolar region. Upon sustained pumping, the monopolar region expands radially in plane with a steady speed that is enhanced by the dielectric mismatch and the finite thickness of the lipid membrane. For unmyelinated lipid membranes in physiological settings, we find remarkably fast propagation speeds of $\sim 40 m / s$ , allowing faster ionic reorganization compared to bare diffusion. Together, our paper shows that transmembrane ionic fluxes induce transient long-ranged electric fields in electrolyte solutions, which may play hitherto unappreciated roles in biological signaling. Published by the American Physical Society 2025

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Sponsoring Organization:: USDOE Office of Science (SC), Advanced Scientific Computing Research (ASCR); USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC02-05CH11231; SC0023112

OSTI ID:: 2522116

Journal Information:: Physical Review Research, Journal Name: Physical Review Research Journal Issue: 1 Vol. 7; ISSN PPRHAI; ISSN 2643-1564

Publisher:: American Physical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

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