Deciphering the distinct biocontrol activities of lipopeptides fengycin and surfactin through their differential impact on lipid membranes.

Gilliard, Guillaume; Demortier, Thomas; Boubsi, Farah; Jijakli, Haissam; Ongena, Marc; De Clerck, Caroline; Deleu, Magali

doi:10.1016/j.colsurfb.2024.113933

Article (Scientific journals)

Deciphering the distinct biocontrol activities of lipopeptides fengycin and surfactin through their differential impact on lipid membranes.

Gilliard, Guillaume; Demortier, Thomas; Boubsi, Farah et al.

2024 • In Colloids and Surfaces. B, Biointerfaces, 239, p. 113933

Peer Reviewed verified by ORBi

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https://hdl.handle.net/2268/322017

DOI
10.1016/j.colsurfb.2024.113933

PubMed
38729019

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Keywords :

Antifungal activity; Lipopeptides; Membrane activity; Plant immunity; fengycin; Peptides, Cyclic; Membrane Lipids; surfactin peptide; Antifungal Agents; Arabidopsis/metabolism; Cell Membrane/drug effects; Cell Membrane/metabolism; Antifungal Agents/pharmacology; Antifungal Agents/chemistry; Lipopeptides/pharmacology; Lipopeptides/chemistry; Peptides, Cyclic/pharmacology; Peptides, Cyclic/chemistry; Peptides, Cyclic/metabolism; Membrane Lipids/metabolism; Membrane Lipids/chemistry; Botrytis/drug effects; Antagonistic activity; Antifungal activities; Chemical pesticides; Fengycins; Lipid membranes; Plant immunities; Surfactins; Arabidopsis; Botrytis; Botrytis cinerea; Cell Membrane; Biotechnology; Surfaces and Interfaces; Physical and Theoretical Chemistry; Colloid and Surface Chemistry

Abstract :

[en] Lipopeptides produced by beneficial bacilli present promising alternatives to chemical pesticides for plant biocontrol purposes. Our research explores the distinct plant biocontrol activities of lipopeptides surfactin (SRF) and fengycin (FGC) by examining their interactions with lipid membranes. Our study shows that FGC exhibits a direct antagonistic activity against Botrytis cinerea and no marked immune-eliciting activity in Arabidopsis thaliana while SRF only demonstrates an ability to stimulate plant immunity. It also reveals that SRF and FGC exhibit diverse effects on membrane integrity and lipid packing. SRF primarily influences membrane physical state without significant membrane permeabilization, while FGC permeabilizes membranes without significantly affecting lipid packing. From our results, we can suggest that the direct antagonistic activity of lipopeptides is linked to their capacity to permeabilize lipid membrane while the stimulation of plant immunity is more likely the result of their ability to alter the mechanical properties of the membrane. Our work also explores how membrane lipid composition modulates the activities of SRF and FGC. Sterols negatively impact both lipopeptides' activities while sphingolipids mitigate the effects on membrane lipid packing but enhance membrane leakage. In conclusion, our findings emphasize the importance of considering both membrane lipid packing and leakage mechanisms in predicting the biological effects of lipopeptides. It also sheds light on the intricate interplay between the membrane composition and the effectiveness of the lipopeptides, providing insights for targeted biocontrol agent design.

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Gilliard, Guillaume ; Université de Liège - ULiège > Département GxABT > Chemistry for Sustainable Food and Environmental Systems (CSFES)

Demortier, Thomas ; Université de Liège - ULiège > Département GxABT > Biosystems Dynamics and Exchanges (BIODYNE)

Boubsi, Farah ; Université de Liège - ULiège > TERRA Research Centre

Jijakli, Haissam ; Université de Liège - ULiège > TERRA Research Centre > Gestion durable des bio-agresseurs

Ongena, Marc ; Université de Liège - ULiège > Département GxABT

De Clerck, Caroline ; Université de Liège - ULiège > TERRA Research Centre > Plant Sciences

Deleu, Magali ; Université de Liège - ULiège > TERRA Research Centre > Chemistry for Sustainable Food and Environmental Systems (CSFES)

Language :

English

Title :

Deciphering the distinct biocontrol activities of lipopeptides fengycin and surfactin through their differential impact on lipid membranes.

Publication date :

July 2024

Journal title :

Colloids and Surfaces. B, Biointerfaces

ISSN :

0927-7765

eISSN :

1873-4367

Publisher :

Elsevier B.V., Netherlands

Volume :

239

Pages :

113933

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

https://api.elsevier.com/content/article/PII:S0927776524001929?httpAccept=text/xml

Funders :

F.R.S.-FNRS - Fonds de la Recherche Scientifique

Funding text :

G.G. is recipient of a F.R.I.A. fellowship (F.R.S.-FNRS, grant n\u00B0 1.E.069.20 F), M.D. and M.O. are respectively senior research associate and research director at the F.R.S.-FNRS. The research was supported by the Feder program 2021-2027 (project PHENIX biocontrol Uliege-SPW) and the PDR Project Surfasymm (Belgian Fund for Scientific Research, F.R.S.-FNRS, grant T.0063.19).

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