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Spatiotemporal analysis of Escherichia coli membrane permeabilization and uptake kinetics induced by a single microbubble cavitation event
ID Drab, Mitja (Author), ID Iglič, Aleš (Author), ID Stopar, David (Author), ID Pandur, Žiga (Author)

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Abstract
A single cavitation microbubble can transiently disrupt the cellular membrane, providing a chemicalfree, targeted drug delivery mechanism. Here, we investigate the spatiotemporal dynamics of membrane permeabilization in an Escherichia coli (E. coli) monolayer exposed to a single cavitation event. Using high-resolution fluorescence microscopy and propidium iodide (PI) uptake as a marker of membrane disruption, we tracked the response of 5565 individual cells around the center of the cavitation event over timescales from microseconds to minutes and spatial scales from 1 to 165 µm. PI uptake rates exhibited a strong spatial dependence, with cells closer to the cavitation center showing rapid and extensive permeabilization. A modified Goldman equation describing PI concentrations inside and outside the cells was used and related to the spatiotemporal measurements of fluorescence intensity. The model accurately captured the first-order PI uptake kinetics, which resulted in saturated fluorescence intensity profiles. Additionally, the model predicted an exponential decay of permeability post-cavitation, implicitly suggesting that pore-resealing dynamics were taking place. Membrane permeability decreased with distance as 1/r, with a characteristic decay time of approximately 3.4 min. Our model thus predicts cell damage induced by a single cavitation event in both space and time. In the present case, where the cavitation bubble reached maximum radius of 29.7 µm, we found that at a distance of 11 µm from the cavitation center,~50% of cell membranes are damaged and permeable to PI, but a pore-resealing mechanism reduces this damage to~1% after 10 min. Our results are consistent with existing sonoporation studies and offer novel insights for optimizing cavitationassisted drug delivery and biofilm disruption strategies.

Language:English
Keywords:cavitation, bacterial cells, poration, propidium iodide uptake, Goldman equation
Work type:Article
Typology:1.01 - Original Scientific Article
Organization:FE - Faculty of Electrical Engineering
FS - Faculty of Mechanical Engineering
BF - Biotechnical Faculty
Publication status:Published
Publication version:Version of Record
Year:2025
Number of pages:12 str.
Numbering:15, art. 42593
PID:20.500.12556/RUL-176478 This link opens in a new window
UDC:577
ISSN on article:2045-2322
DOI:10.1038/s41598-025-26554-4 This link opens in a new window
COBISS.SI-ID:259523587 This link opens in a new window
Publication date in RUL:02.12.2025
Views:486
Downloads:172
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Record is a part of a journal

Title:Scientific reports
Shortened title:Sci. rep.
Publisher:Springer Nature
ISSN:2045-2322
COBISS.SI-ID:18727432 This link opens in a new window

Licences

License:CC BY 4.0, Creative Commons Attribution 4.0 International
Link:http://creativecommons.org/licenses/by/4.0/
Description:This is the standard Creative Commons license that gives others maximum freedom to do what they want with the work as long as they credit the author.

Secondary language

Language:Slovenian
Keywords:kavitacija, bakterijske celice, poracija, privzem propidijevega jodida, Goldmanova enačba

Projects

Funder:ARIS - Slovenian Research and Innovation Agency
Project number:Z2-60174
Name:Skaliranje kavitacije od posameznega mehurčka v kavitacijski oblak za povečanje inaktivacije bakterij

Funder:ARIS - Slovenian Research and Innovation Agency
Project number:J2-60032
Name:Večnivojski in integralni pristop k razumevanju kavitacije (MICKA)

Funder:ARIS - Slovenian Research and Innovation Agency
Project number:J2-4447
Name:Vpliv mehanike in topologije membrane na celično ujetje bakterij, virionov in anorganskih delcev

Funder:ARIS - Slovenian Research and Innovation Agency
Project number:J3-60063
Name:Avtologni krvni pripravki z zunajceličnimi delci in hibridosomi za regeneracijo

Funder:ARIS - Slovenian Research and Innovation Agency
Project number:P2-0232
Name:Analiza biomedicinskih slik in signalov

Funder:ARIS - Slovenian Research and Innovation Agency
Project number:P2-0422
Name:Funkcionalne tekočine za napredne energetske sisteme

Funder:ARIS - Slovenian Research and Innovation Agency
Project number:802-12
Name:Nanostructurome

Funder:EC - European Commission
Project number:101131175
Name:Plant EV farming
Acronym:FarmEVs

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