[en] Fatty acid hydroperoxides (HPO) are free phyto-oxylipins known for their crucial role as signalling molecules during plant defense mechanisms. They were also demonstrated to have direct biocidal activities against plant pathogens including gram negative bacteria. In the present work, the biocidal effect of one linolenic fatty acid hydroperoxide, namely 13-HPOT has been investigated on three plant pathogen gram negative bacteria: Pectobacterium carotovorum, Pseudomonas syringae and Xanthomonas translucens. We showed that 13-HPOT has a strong dose response effect on those phytopathogens.
In a second part, the molecular mechanism behind the antibacterial effect of 13-HPOT was investigated at a molecular level using an integrative biophysical approach combining in vitro and in silico methods. Since other antimicrobial amphiphilic molecules have been shown to target the lipid membrane of the organisms they act on, we focused our study on the interaction of 13-HPOT with biomimetic membranes. In a first step, we hypothesized that the inner membrane of the bacteria was the main site of action of 13-HPOT and hence we used lipids representative of this membrane to form our models. Our results indicated that 13-HPOT can interact with the lipid representative of the inner bacterial plasma membrane. A strong membrane insertion is suggested but no major permeabilization of the membrane is observed. Phosphatidylethanolamine (PE) and cardiolipin (CL), present in the bacterial plasma membrane, appear to play important roles in this interaction. We suggest that the mode of action of 13-HPOT should involve either subtle changes in membrane properties, such as its lateral organization and distribution, and/or interactions
with membrane proteins.
Wasternack, C., Feussner, I., The oxylipin pathways: biochemistry and function (2018) Annu. Rev. Plant Biol., 69, pp. 363-386
Blée, E., Phytooxylipins and plant defense (1998) Prog. lipid Reseach, 37, pp. 33-72
Genva, M., New insights into the biosynthesis of esterified oxylipins and their involvement in plant defense and developmental mechanisms (2019) Phytochem. Rev., 8, pp. 343-359
Wasternack, C., Strnad, M., Jasmonates: News on Occurrence, Biosynthesis, Metabolism and Action of an Ancient Group of Signaling Compounds (2018) Int. J. Mol. Sci., 19, p. 2539
Blée, E., Impact of phyto-oxylipins in plant defense (2002) Trends Plant Sci., 7, pp. 315-321
Koo, A.J., Metabolism of the plant hormone jasmonate: a sentinel for tissue damage and master regulator of stress response (2018) Phytochem. Rev., 17, pp. 51-80
Griffiths, G., Biosynthesis and analysis of plant oxylipins (2015) Free Radic. Res., 49, pp. 565-582
Howe, G.A., Plant hormones: Metabolic end run to jasmonate (2018) Nat. Chem. Biol., 14, pp. 109-110
Savchenko, T.V., Zastrijnaja, O.M., Klimov, V.V., Oxylipins and plant abiotic stress resistance (2014) Biochem., 79, pp. 362-375
Fauconnier, M.L., Marlier, M., Revue bibliographique: Les lipoxygenases du soja (1997) Biotechnol., Agron. Soc. Environ., 1, pp. 125-141
Porta, H., Rocha-Sosa, M., Plant Lipoxygenases. Physiological and Molecular Features (2002) Plant Physiol., 130, pp. 15-21
Mosblech, A., Feussner, I., Heilmann, I., Oxylipins: Structurally diverse metabolites from fatty acid oxidation (2009) Plant Physiol. Biochem., 47, pp. 511-517
Andreou, A., Feussner, I., Lipoxygenases - Structure and reaction mechanism (2009) Phytochemistry, 70, pp. 1504-1510
Howe, G.A., Schilmiller, A.L., Oxylipin metabolism in response to stress (2002) Curr. Opin. Plant Biol., 5, pp. 230-236
Fauconnier, M.L., Welti, R., Blée, E., Marlier, M., Lipid and oxylipin profiles during aging and sprout development in potato tubers (Solanum tuberosum L.) (2003) Biochim. Biophys. Acta - Mol. Cell Biol. Lipids, 1633, pp. 118-126
Ghanem, M.E., Organ-dependent oxylipin signature in leaves and roots of salinized tomato plants (Solanum lycopersicum) (2012) J. Plant Physiol., 169, pp. 1090-1101
Prost, I., Evaluation of the Antimicrobial Activities of Plant Oxylipins Supports Their Involvement in Defense against Pathogens (2005) Plant Physiol., 139, pp. 1902-1913
Granér, G., Hamberg, M., Meijer, J., Screening of oxylipins for control of oilseed rape (Brassica napus) fungal pathogens (2003) Phytochemistry, 63, pp. 89-95
Zieniuk, B., Fabiszewska, A., Yarrowia lipolytica : a beneficious yeast in biotechnology as a rare opportunistic fungal pathogen : a minireview (2019) World J. Microbiol. Biotechnol., 35, pp. 1-8
(1768), pp. 2256-2262. , Tran Thanh, H. et al. Toxicity of fatty acid hydroperoxides towards Yarrowia lipolytica: Implication of their membrane fluidizing action. Biochim. Biophys. Acta - Biomembr 2007
Deboever, E., Deleu, M., Lins, L., Plant – Pathogen Interactions : Underestimated Roles of Phyto-oxylipins (2019) Trends Plant Sci.
Newman, M., Priming, induction and modulation of plant defence responses by bacterial lipopolysaccharides (2007) J. Endotoxin Res., 13, pp. 69-84
Sautrey, G., Negatively charged lipids as a potential target for new amphiphilic aminoglycoside antibiotics: A biophysical study (2016) J. Biol. Chem., 291, pp. 13864-13874
Deleu, M., Linoleic and linolenic acid hydroperoxides interact differentially with biomimetic plant membranes in a lipid specific manner (2018) Colloids Surf. B Biointerf.
Jermy, A., Bacterial physiology: Bacterial lipid rafts discovered (2010) Nat. Rev. Microbiol., 8, p. 2455
Barák, I., Muchová, K., The Role of Lipid Domains in Bacterial Cell Processes (2013) Int. J. Mol. Sci., 14, pp. 4050-4065
Lopez, D., Koch, G., Exploring functional membrane microdomains in bacteria : an overview (2017) Curr. Opin. Microbiol., 49, pp. 76-84
Mingeot-Leclercq, M.P., Décout, J.L., Bacterial lipid membranes as promising targets to fight antimicrobial resistance, molecular foundations and illustration through the renewal of aminoglycoside antibiotics and emergence of amphiphilic aminoglycosides (2016) Med. Chem. Commun., 7, pp. 586-611
Aktas, M., Narberhaus, F., Unconventional membrane lipid biosynthesis in Xanthomonas campestris (2015) Environ. Microbiol., 17, pp. 3116-3124
Sohlenkamp, C., Geiger, O., Bacterial membrane lipids: Diversity in structures and pathways (2015) FEMS Microbiol. Rev., 40, pp. 133-159
Henderson, J.C., The Power of Asymmetry : Architecture and Assembly of the Gram-Negative Outer Membrane Lipid Bilayer (2016) Annu. Rev. Microbiol., 70, pp. 255-278
Lin, T., Weibel, D.B., Organization and function of anionic phospholipids in bacteria (2016) Appl. Microbiol. Biotechnol., 100, pp. 4255-4267
Franche, A., Amphiphilic azobenzenes : Antibacterial activities and biophysical investigation of their interaction with bacterial membrane lipids (2019) Bioorg. Chem., 103399
Khoury, M.E., Targeting Bacterial Cardiolipin Enriched Microdomains : An Antimicrobial Strategy Used by Amphiphilic Aminoglycoside Antibiotics (2017) Sci. Rep., 1-12
Eeman, M., Penetration of surfactin into phospholipid monolayers: Nanoscale interfacial organization (2006) Langmuir, 22, pp. 11337-11345
Sautrey, G., New amphiphilic neamine derivatives active against resistant Pseudomonas aeruginosa and their interactions with lipopolysaccharides (2014) Antimicrob. Agents Chemother., 58, pp. 4420-4430
Deleu, M., Effects of surfactin on membrane models displaying lipid phase separation (2013) Biochim. Biophys. Acta - Biomembr., 1828, pp. 801-815
Tsuchiya, H., Membrane Interactions of Phytochemicals as Their Molecular Mechanism Applicable to the Discovery of Drug Leads from Plants (2015) Molecules, 20, pp. 18923-18966
Selvaraj, S., Krishnaswamy, S., Devashya, V., Sethuraman, S., Krishnan, U.M., Progress in Lipid Research Influence of membrane lipid composition on flavonoid – membrane interactions : Implications on their biological activity (2015) Prog. Lipid Res., 58, pp. 1-13
Ouberai, M., The Pseudomonas aeruginosa membranes: A target for a new amphiphilic aminoglycoside derivative? (2011) Biochim. Biophys. Acta - Biomembr., 1808, pp. 1716-1727
Epand, R.F., Savage, P.B., Epand, R.M., Bacterial lipid composition and the antimicrobial efficacy of cationic steroid compounds (Ceragenins) (2007) Biochim. Biophys. Acta - Biomembr., 1768, pp. 2500-2509
Fauconnier, M.L., Marlier, M., An efficient procedure for the production of fatty acid hydroperoxides from hydrolyzed flax seed oil and soybean lipoxygenase (1996) Biotechnol. Tech., 10, pp. 839-844
Ducarme, P., Rahman, M., Brasseur, R., IMPALA: A simple restraint field to simulate the biological membrane in molecular structure studies (1998) Proteins Struct. Funct. Genet., 30, pp. 357-371
Lins, L., Charloteaux, B., Thomas, A., Brasseur, R., Computational study of lipid-destabilizing protein fragments: Towards a comprehensive view of tilted peptides (2001) Proteins Struct. Funct. Genet., 44, pp. 435-447
Heerklotz, H., Seelig, J., Titration calorimetry of surfactant-membrane partitioning and membrane solubilization (2000) Biochim. Biophys. Acta - Biomembr., 1508, pp. 69-85
Razafindralambo, H., Dufour, S., Paquot, M., Deleu, M., Thermodynamic studies of the binding interactions of surfactin analogues to lipid vesicles (2009) J. Therm. Anal. Calorim., 95, pp. 817-821
Zakanda, F.N., Interaction of hexadecylbetainate chloride with biological relevant lipids (2012) Langmuir, 28, pp. 3524-3533
Deleu, M., Crowet, J.M., Nasir, M.N., Lins, L., Complementary biophysical tools to investigate lipid specificity in the interaction between bioactive molecules and the plasma membrane: A review (2014) Biochim. Biophys. Acta - Biomembr., 1838, pp. 3171-3190
Nasir, M.N., Interactions of sugar-based bolaamphiphiles with biomimetic systems of plasma membranes (2016) Biochimie, 130, pp. 23-32
Fu, F.N., Singh, B.R., Calcein permeability of liposomes mediated by type a botulinum neurotoxin and its light and heavy chains (1999) J. Protein Chem., 18, pp. 701-707
Bartlett, G.R., Calorimetric Assay Phosphorylated for Free Glyceric Acids (1958) J. Biol. Chem., 234, pp. 469-471
Shimanouchi, T., Ishii, H., Yoshimoto, N., Umakoshi, H., Kuboi, R., Calcein permeation across phosphatidylcholine bilayer membrane: Effects of membrane fluidity, liposome size, and immobilization (2009) Colloids Surf. B Biointerf., 73, pp. 156-160
Calvez, P., Demers, E., Boisselier, E., Salesse, C., Analysis of the contribution of saturated and polyunsaturated phospholipid monolayers to the binding of proteins (2011) Langmuir, 27, pp. 1373-1379
Brasseur, R., Killian, J.A., De Kruijff, B., Ruysschaert, J.M., Conformational analysis of gramicidin-gramicidin interactions at the air/water interface suggests that gramicidin aggregates into tube-like structures similar as found in the gramicidin-induced hexagonal HIIphase (1987) BBA - Biomembr., 903, pp. 11-17
Claereboudt, E.J.S., Eeckhaut, I., Lins, L., Deleu, M., How different sterols contribute to saponin tolerant plasma membranes in sea cucumbers (2018) Sci. Rep., 8, pp. 1-11
Lins, L., Brasseur, R., The hydrophobic effect in protein folding (1995) FASEB J., 9, pp. 535-540
Parasassi, T., Gratton, E., Membrane lipid domains and dynamics as detected by Laurdan fluorescence (1995) J. Fluoresc., 5, pp. 59-69
Harris, F.M., Best, K.B., Bell, J.D., Use of laurdan fluorescence intensity and polarization to distinguish between changes in membrane fluidity and phospholipid order (2002) Biochim. Biophys. Acta - Biomembr., 1565, pp. 123-128
Parasassi, T., De Stasio, G., Ravagnan, G., Rusch, R.M., Gratton, E., Quantitation of lipid phases in phospholipid vesicles by the generalized polarization of Laurdan fluorescence (1991) Biophys. J., 60, pp. 179-189
Ouberai, M., The Pseudomonas aeruginosa membranes : A target for a new amphiphilic aminoglycoside derivative ? (2011) BBA - Biomembr., 1808, pp. 1716-1727
Ladbury, J.E., Chowdhry, B.Z., Sensing the heat: the application of isothermal titration calorimetry to thermodynamic stidies of biomolecular interactions (1996) Chem. Biol., 3, pp. 791-801
Bechinger, B., Lohner, K., Detergent-like actions of linear amphipathic cationic antimicrobial peptides (2006) BBA - Biomembr., 1758, pp. 1529-1539
Bramkamp, M., Lopez, D., Exploring the Existence of Lipid Rafts in Bacteria (2015) Microbiol. Mol. Biol. Rev., 79, pp. 81-100
Toledo, A., Lipid rafts can be form in the inner and outer membranes of Borrelia burgdorferi and have different properties and associated proteins (2019) Mol. Microbiol., 108, pp. 63-76
Brezesinski, G., Möhwald, H., Langmuir monolayers to study interactions at model membrane surfaces (2003) Adv. Colloid Interface Sci., 100-102, pp. 563-584
Stefaniu, C., Brezesinski, G., Möhwald, H., Langmuir monolayers as models to study processes at membrane surfaces (2014) Adv. Colloid Interface Sci., 208, pp. 197-213
Marsh, D., Lateral pressure in membranes (1996) BBA, 1286, pp. 183-223
Mantil, E., Buznytska, I., Daly, G., Ianoul, A., Avis, T.J., Role of Lipid Composition in the Interaction and Activity of the Antimicrobial Compound Fengycin with Complex Membrane Models (2019) J. Membr. Biol.
Sanchez, S.A., Tricerri, M.A., Gunther, G., Gratton, E., Laurdan Generalized Polarization : from cuvette to microscope (2007) Mod. Res. Educ. Top. Microsc., 1007-1014
Lebecque, S., Lins, L., Dayan, F.E., Fauconnier, M., Interactions Between Natural Herbicides and Lipid Bilayers Mimicking the Plant Plasma Membrane (2019) Front. Pharmacol., 10, pp. 1-11
Kondakova, T., Glycerophospholipid synthesis and functions in Pseudomonas (2015) Chem. Phys. Lipids, 190, pp. 27-42
Lewis, R.N.A.H., Mcelhaney, R.N., The physicochemical properties of cardiolipin bilayers and cardiolipin-containing lipid membranes ☆ (2009) BBA - Biomembr., 1788, pp. 2069-2079
Arias-cartin, R., Grimaldi, S., Arnoux, P., Guigliarelli, B., Magalon, A., Cardiolipin binding in bacterial respiratory complexes : Structural and functional implications (2012) BBA - Bioenerg., 1817, pp. 1937-1949
Arnarez, C., Marrink, S.J., Periole, X., Identification of cardiolipin binding sites on cytochrome c oxidase at the entrance of proton channels (2013) Sci. Rep., 3, pp. 1-9
Sperandeo, P., Martorana, A.M., Polissi, A., Lipopolysaccharide biogenesis and transport at the outer membrane of Gram-negative bacteria (2017) BBA - Mol. celle Biol. lipids, 1862, pp. 1451-1460
Molinaro, A., Newman, M., Lanzetta, R., Parrilli, M., The Structures of Lipopolysaccharides from Plant-Associated Gram-Negative Bacteria (2009) European J. Org. Chem., 5887-5896
Erbs, G., Newman, M., The role of lipopolysaccharide and peptidoglycan, two glycosylated bacterial microbe-associated molecular patterns (MAMPs), in plant innate immunity (2012) Mol. Plant Pathol., 13, pp. 95-104