Cargando…

A Diffusion Model to Quantify Membrane Repair Process in Listeria monocytogenes Exposed to High Pressure Processing Based on Fluorescence Microscopy Data

The effects of environmental stresses on microorganisms have been well-studied, and cellular responses to stresses such as heat, cold, acids, and salts have been extensively discussed. Although high pressure processing (HPP) is becoming more popular as a preservation method in the food industry, the...

Descripción completa

Detalles Bibliográficos
Autores principales: Nikparvar, Bahareh, Subires, Alicia, Capellas, Marta, Hernandez-Herrero, Manuela, Crauwels, Peter, Riedel, Christian U., Bar, Nadav
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8155719/
https://www.ncbi.nlm.nih.gov/pubmed/34054742
http://dx.doi.org/10.3389/fmicb.2021.598739
_version_ 1783699269824282624
author Nikparvar, Bahareh
Subires, Alicia
Capellas, Marta
Hernandez-Herrero, Manuela
Crauwels, Peter
Riedel, Christian U.
Bar, Nadav
author_facet Nikparvar, Bahareh
Subires, Alicia
Capellas, Marta
Hernandez-Herrero, Manuela
Crauwels, Peter
Riedel, Christian U.
Bar, Nadav
author_sort Nikparvar, Bahareh
collection PubMed
description The effects of environmental stresses on microorganisms have been well-studied, and cellular responses to stresses such as heat, cold, acids, and salts have been extensively discussed. Although high pressure processing (HPP) is becoming more popular as a preservation method in the food industry, the characteristics of the cellular damage caused by high pressure are unclear, and the microbial response to this stress has not yet been well-explored. We exposed the pathogen Listeria monocytogenes to HPP (400 MPa, 8 min, 8°C) and found that the high pressure created plasma membrane pores. Using a common staining technique involving propidium iodide (PI) combined with high-frequency fluorescence microscopy, we monitored the rate of diffusion of PI molecules into hundreds of bacterial cells through these pores on days 0, 1, 2, 3, and 4 after pressurization. We also developed a mathematical dynamic model based on mass transfer and passive diffusion laws, calibrated using our microscopy experiments, to evaluate the response of bacteria to HPP. We found that the rate of diffusion of PI into the cells decreased over the 4 consecutive days after exposure to HPP, indicating repair of the pressure-created membrane pores. The model suggested a temporal change in the size of pores until closure. To the best of our knowledge, this is the first time that pressure-created membrane pores have been quantitatively described and shown to diminish with time. In addition, we found that the membrane repair rate in response to HPP was linear, and growth was temporarily arrested at the population level during the repair period. These results support the existence of a progressive repair process in some of the cells that take up PI, which can therefore be considered as being sub-lethally injured rather than dead. Hence, we showed that a subgroup of bacteria survived HPP and actively repaired their membrane pores.
format Online
Article
Text
id pubmed-8155719
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-81557192021-05-28 A Diffusion Model to Quantify Membrane Repair Process in Listeria monocytogenes Exposed to High Pressure Processing Based on Fluorescence Microscopy Data Nikparvar, Bahareh Subires, Alicia Capellas, Marta Hernandez-Herrero, Manuela Crauwels, Peter Riedel, Christian U. Bar, Nadav Front Microbiol Microbiology The effects of environmental stresses on microorganisms have been well-studied, and cellular responses to stresses such as heat, cold, acids, and salts have been extensively discussed. Although high pressure processing (HPP) is becoming more popular as a preservation method in the food industry, the characteristics of the cellular damage caused by high pressure are unclear, and the microbial response to this stress has not yet been well-explored. We exposed the pathogen Listeria monocytogenes to HPP (400 MPa, 8 min, 8°C) and found that the high pressure created plasma membrane pores. Using a common staining technique involving propidium iodide (PI) combined with high-frequency fluorescence microscopy, we monitored the rate of diffusion of PI molecules into hundreds of bacterial cells through these pores on days 0, 1, 2, 3, and 4 after pressurization. We also developed a mathematical dynamic model based on mass transfer and passive diffusion laws, calibrated using our microscopy experiments, to evaluate the response of bacteria to HPP. We found that the rate of diffusion of PI into the cells decreased over the 4 consecutive days after exposure to HPP, indicating repair of the pressure-created membrane pores. The model suggested a temporal change in the size of pores until closure. To the best of our knowledge, this is the first time that pressure-created membrane pores have been quantitatively described and shown to diminish with time. In addition, we found that the membrane repair rate in response to HPP was linear, and growth was temporarily arrested at the population level during the repair period. These results support the existence of a progressive repair process in some of the cells that take up PI, which can therefore be considered as being sub-lethally injured rather than dead. Hence, we showed that a subgroup of bacteria survived HPP and actively repaired their membrane pores. Frontiers Media S.A. 2021-05-13 /pmc/articles/PMC8155719/ /pubmed/34054742 http://dx.doi.org/10.3389/fmicb.2021.598739 Text en Copyright © 2021 Nikparvar, Subires, Capellas, Hernandez-Herrero, Crauwels, Riedel and Bar. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Nikparvar, Bahareh
Subires, Alicia
Capellas, Marta
Hernandez-Herrero, Manuela
Crauwels, Peter
Riedel, Christian U.
Bar, Nadav
A Diffusion Model to Quantify Membrane Repair Process in Listeria monocytogenes Exposed to High Pressure Processing Based on Fluorescence Microscopy Data
title A Diffusion Model to Quantify Membrane Repair Process in Listeria monocytogenes Exposed to High Pressure Processing Based on Fluorescence Microscopy Data
title_full A Diffusion Model to Quantify Membrane Repair Process in Listeria monocytogenes Exposed to High Pressure Processing Based on Fluorescence Microscopy Data
title_fullStr A Diffusion Model to Quantify Membrane Repair Process in Listeria monocytogenes Exposed to High Pressure Processing Based on Fluorescence Microscopy Data
title_full_unstemmed A Diffusion Model to Quantify Membrane Repair Process in Listeria monocytogenes Exposed to High Pressure Processing Based on Fluorescence Microscopy Data
title_short A Diffusion Model to Quantify Membrane Repair Process in Listeria monocytogenes Exposed to High Pressure Processing Based on Fluorescence Microscopy Data
title_sort diffusion model to quantify membrane repair process in listeria monocytogenes exposed to high pressure processing based on fluorescence microscopy data
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8155719/
https://www.ncbi.nlm.nih.gov/pubmed/34054742
http://dx.doi.org/10.3389/fmicb.2021.598739
work_keys_str_mv AT nikparvarbahareh adiffusionmodeltoquantifymembranerepairprocessinlisteriamonocytogenesexposedtohighpressureprocessingbasedonfluorescencemicroscopydata
AT subiresalicia adiffusionmodeltoquantifymembranerepairprocessinlisteriamonocytogenesexposedtohighpressureprocessingbasedonfluorescencemicroscopydata
AT capellasmarta adiffusionmodeltoquantifymembranerepairprocessinlisteriamonocytogenesexposedtohighpressureprocessingbasedonfluorescencemicroscopydata
AT hernandezherreromanuela adiffusionmodeltoquantifymembranerepairprocessinlisteriamonocytogenesexposedtohighpressureprocessingbasedonfluorescencemicroscopydata
AT crauwelspeter adiffusionmodeltoquantifymembranerepairprocessinlisteriamonocytogenesexposedtohighpressureprocessingbasedonfluorescencemicroscopydata
AT riedelchristianu adiffusionmodeltoquantifymembranerepairprocessinlisteriamonocytogenesexposedtohighpressureprocessingbasedonfluorescencemicroscopydata
AT barnadav adiffusionmodeltoquantifymembranerepairprocessinlisteriamonocytogenesexposedtohighpressureprocessingbasedonfluorescencemicroscopydata
AT nikparvarbahareh diffusionmodeltoquantifymembranerepairprocessinlisteriamonocytogenesexposedtohighpressureprocessingbasedonfluorescencemicroscopydata
AT subiresalicia diffusionmodeltoquantifymembranerepairprocessinlisteriamonocytogenesexposedtohighpressureprocessingbasedonfluorescencemicroscopydata
AT capellasmarta diffusionmodeltoquantifymembranerepairprocessinlisteriamonocytogenesexposedtohighpressureprocessingbasedonfluorescencemicroscopydata
AT hernandezherreromanuela diffusionmodeltoquantifymembranerepairprocessinlisteriamonocytogenesexposedtohighpressureprocessingbasedonfluorescencemicroscopydata
AT crauwelspeter diffusionmodeltoquantifymembranerepairprocessinlisteriamonocytogenesexposedtohighpressureprocessingbasedonfluorescencemicroscopydata
AT riedelchristianu diffusionmodeltoquantifymembranerepairprocessinlisteriamonocytogenesexposedtohighpressureprocessingbasedonfluorescencemicroscopydata
AT barnadav diffusionmodeltoquantifymembranerepairprocessinlisteriamonocytogenesexposedtohighpressureprocessingbasedonfluorescencemicroscopydata