Chitosan and carboxylic acids, impact on membrane permeability and DNA integrity of Pseudomonas syringae: interest for biocontrol applications

Abstract Background Pseudomonas syringae causes major damage to a wide variety of plants and is a good model for antibacterial activity assessment. It is important to understand to the fullest extent the mechanisms underlying biobased antimicrobials so as to finely tune them as biocontrol treatments...

Full description

Saved in:
Bibliographic Details
Main Authors: Solène Meynaud, Davide Danzi, Elodie Vandelle, Christian Gardrat, Fabrice Coloma, Cindy Morris, Véronique Coma
Format: Article
Language:English
Published: SpringerOpen 2025-06-01
Series:Chemical and Biological Technologies in Agriculture
Subjects:
Online Access:https://doi.org/10.1186/s40538-025-00783-1
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850100569443663872
author Solène Meynaud
Davide Danzi
Elodie Vandelle
Christian Gardrat
Fabrice Coloma
Cindy Morris
Véronique Coma
author_facet Solène Meynaud
Davide Danzi
Elodie Vandelle
Christian Gardrat
Fabrice Coloma
Cindy Morris
Véronique Coma
author_sort Solène Meynaud
collection DOAJ
description Abstract Background Pseudomonas syringae causes major damage to a wide variety of plants and is a good model for antibacterial activity assessment. It is important to understand to the fullest extent the mechanisms underlying biobased antimicrobials so as to finely tune them as biocontrol treatments. Chitosan and carboxylic acids (solubilizing agents) are known to be active against phytopathogenic bacteria but the underlying mechanisms are not fully understood. The objective of this study was to assess the impact of pH, concentration, time and the association of chitosan and two types of carboxylic acids—acetic and tartaric acids—on membrane permeability and DNA alteration and the impact on cell inhibition. Results A standard method using 1-N-phenylnaphthalen-1-amine (NPN) and propidium iodide (PI) was used to measure membrane permeability and to assess DNA integrity. Chitosan exhibited a protective effect on permeabilization at higher concentration but was still effective in inhibiting bacteria. The study of pH and concentration showed a wider pH range of permeabilization for acetic acid than pH effect alone, but tartaric acid exhibited a faster DNA alteration at pH3 (30 vs. 90 min for acetic acid, visualized by a decrease in PI fluorescence). The combination of the different molecules showed an additive effect with a decrease of chitosan protection and DNA alteration by tartaric acid even at pH 4. The DNA alteration from the contact with tartaric acid revealed itself to be pH reversible in just an hour. Furthermore, the use of DAPI (4′,6-diamidino-2-phenylindole) showed an opposite effect than with PI in marking DNA of cells exposed to tartaric acid. Conclusions Tartaric and acetic acids showed different kinetics of action on P. syringae. Their mix, together or with chitosan, further highlights the importance of combining different bioactive molecules to have a large range of pH and concentration and limit protective effects due to hindrance of chitosan in high concentration solutions. They also exhibited pH reversible DNA alteration, most likely correlated with the change in conformation, that could lead to a biostatic effect. Graphical Abstract
format Article
id doaj-art-edcf2c7be2784d2d837fb6cc6579e6cc
institution DOAJ
issn 2196-5641
language English
publishDate 2025-06-01
publisher SpringerOpen
record_format Article
series Chemical and Biological Technologies in Agriculture
spelling doaj-art-edcf2c7be2784d2d837fb6cc6579e6cc2025-08-20T02:40:15ZengSpringerOpenChemical and Biological Technologies in Agriculture2196-56412025-06-0112111510.1186/s40538-025-00783-1Chitosan and carboxylic acids, impact on membrane permeability and DNA integrity of Pseudomonas syringae: interest for biocontrol applicationsSolène Meynaud0Davide Danzi1Elodie Vandelle2Christian Gardrat3Fabrice Coloma4Cindy Morris5Véronique Coma6Univ. Bordeaux, CNRS, Bordeaux INP, LCPO, UMR 5629Dipartimento di Biotecnologie, Università degli Studi di VeronaDipartimento di Biotecnologie, Università degli Studi di VeronaUniv. Bordeaux, CNRS, Bordeaux INP, LCPO, UMR 5629FAUREINRAE, Pathologie VégétaleUniv. Bordeaux, CNRS, Bordeaux INP, LCPO, UMR 5629Abstract Background Pseudomonas syringae causes major damage to a wide variety of plants and is a good model for antibacterial activity assessment. It is important to understand to the fullest extent the mechanisms underlying biobased antimicrobials so as to finely tune them as biocontrol treatments. Chitosan and carboxylic acids (solubilizing agents) are known to be active against phytopathogenic bacteria but the underlying mechanisms are not fully understood. The objective of this study was to assess the impact of pH, concentration, time and the association of chitosan and two types of carboxylic acids—acetic and tartaric acids—on membrane permeability and DNA alteration and the impact on cell inhibition. Results A standard method using 1-N-phenylnaphthalen-1-amine (NPN) and propidium iodide (PI) was used to measure membrane permeability and to assess DNA integrity. Chitosan exhibited a protective effect on permeabilization at higher concentration but was still effective in inhibiting bacteria. The study of pH and concentration showed a wider pH range of permeabilization for acetic acid than pH effect alone, but tartaric acid exhibited a faster DNA alteration at pH3 (30 vs. 90 min for acetic acid, visualized by a decrease in PI fluorescence). The combination of the different molecules showed an additive effect with a decrease of chitosan protection and DNA alteration by tartaric acid even at pH 4. The DNA alteration from the contact with tartaric acid revealed itself to be pH reversible in just an hour. Furthermore, the use of DAPI (4′,6-diamidino-2-phenylindole) showed an opposite effect than with PI in marking DNA of cells exposed to tartaric acid. Conclusions Tartaric and acetic acids showed different kinetics of action on P. syringae. Their mix, together or with chitosan, further highlights the importance of combining different bioactive molecules to have a large range of pH and concentration and limit protective effects due to hindrance of chitosan in high concentration solutions. They also exhibited pH reversible DNA alteration, most likely correlated with the change in conformation, that could lead to a biostatic effect. Graphical Abstracthttps://doi.org/10.1186/s40538-025-00783-1ChitosanAcetic acidTartaric acidPseudomonas syringaeMembrane permeabilityBiocontrol
spellingShingle Solène Meynaud
Davide Danzi
Elodie Vandelle
Christian Gardrat
Fabrice Coloma
Cindy Morris
Véronique Coma
Chitosan and carboxylic acids, impact on membrane permeability and DNA integrity of Pseudomonas syringae: interest for biocontrol applications
Chemical and Biological Technologies in Agriculture
Chitosan
Acetic acid
Tartaric acid
Pseudomonas syringae
Membrane permeability
Biocontrol
title Chitosan and carboxylic acids, impact on membrane permeability and DNA integrity of Pseudomonas syringae: interest for biocontrol applications
title_full Chitosan and carboxylic acids, impact on membrane permeability and DNA integrity of Pseudomonas syringae: interest for biocontrol applications
title_fullStr Chitosan and carboxylic acids, impact on membrane permeability and DNA integrity of Pseudomonas syringae: interest for biocontrol applications
title_full_unstemmed Chitosan and carboxylic acids, impact on membrane permeability and DNA integrity of Pseudomonas syringae: interest for biocontrol applications
title_short Chitosan and carboxylic acids, impact on membrane permeability and DNA integrity of Pseudomonas syringae: interest for biocontrol applications
title_sort chitosan and carboxylic acids impact on membrane permeability and dna integrity of pseudomonas syringae interest for biocontrol applications
topic Chitosan
Acetic acid
Tartaric acid
Pseudomonas syringae
Membrane permeability
Biocontrol
url https://doi.org/10.1186/s40538-025-00783-1
work_keys_str_mv AT solenemeynaud chitosanandcarboxylicacidsimpactonmembranepermeabilityanddnaintegrityofpseudomonassyringaeinterestforbiocontrolapplications
AT davidedanzi chitosanandcarboxylicacidsimpactonmembranepermeabilityanddnaintegrityofpseudomonassyringaeinterestforbiocontrolapplications
AT elodievandelle chitosanandcarboxylicacidsimpactonmembranepermeabilityanddnaintegrityofpseudomonassyringaeinterestforbiocontrolapplications
AT christiangardrat chitosanandcarboxylicacidsimpactonmembranepermeabilityanddnaintegrityofpseudomonassyringaeinterestforbiocontrolapplications
AT fabricecoloma chitosanandcarboxylicacidsimpactonmembranepermeabilityanddnaintegrityofpseudomonassyringaeinterestforbiocontrolapplications
AT cindymorris chitosanandcarboxylicacidsimpactonmembranepermeabilityanddnaintegrityofpseudomonassyringaeinterestforbiocontrolapplications
AT veroniquecoma chitosanandcarboxylicacidsimpactonmembranepermeabilityanddnaintegrityofpseudomonassyringaeinterestforbiocontrolapplications