Effects of structure on the interactions between five natural antimicrobial compounds and phospholipids of bacterial cell membrane on model monolayers

Authors: NOWOTARSKA, WONG - Queens University - United Kingdom; NOWOTARKI, KRZYSZTOF - Queens University - United Kingdom; Friedman, Mendel; SITU, CHEN - Queens University - United Kingdom

Submitted to: Molecules
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/3/2014
Publication Date: 6/6/2014
Citation: Nowotarska, W.S., Nowotarki, K.J., Friedman, M., Situ, C. 2014. Effects of structure on the interactions between five natural antimicrobial compounds and phospholipids of bacterial cell membrane on model monolayers. Molecules. 19:7497-7515. DOI: 10.3390/molecules19067497.

Interpretive Summary: Many naturally-occurring compounds including secondary metabolites and photochemicals have been extensively evaluated for antimicrobial activity against foodborne pathogenic bacteria. Some have exhibited activity against antibiotic-resistant pathogens and inhibited the growth of the bacteria on contaminated food, including leafy greens, meat, and seafood. In previous publications (Journal of. Agricultural and Food Chemistry, 56, 7750, 2008; 57, 6720, 2009, and 59, 3780, 2011) we describe molecular dynamic computer simulations of binding of green tea catechins and black tea theaflavins to lipid bilayers as models for effects in microbial cell membranes. A major objective of the present collaborative study with the Institute of Agri-Food and Land Use, Queen’s University, Belfast, UK is to further extend these studies with the aid of an experimental physico-chemical technique that allowed us to focus on the influence of five naturally-occurring, structurally different antimicrobial compounds to interact with three different phospholipid models mimicking bacterial membranes. The model membrane studies created quantitative thermodynamic parameters that indicate that the antimicrobial compounds could modify the lipid monolayer structure by incorporating into the monolayer, forming aggregates of antimicrobials and lipids. The results offer insights in the mechanism of interaction between antimicrobials and cell membrane lipids. The method has the potential to predict bioactivities of natural compounds against microbial cells.

Technical Abstract: Monolayers composed of bacterial phospholipids were used as model membranes to study interactions of naturally occurring phenolic compounds 2,5-dihydroxybenzaldehyde, 2-hydroxy-5-methoxybenzaldehyde and the plant essential oil compounds carvacrol, cinnamaldehyde, and geraniol, previously found to be active against both Gram-positive and Gram-negative foodborne pathogenic microorganisms, with lipid monolayers 1,2-dihexadecanoyl-sn-glycero-3-phosphoethanolamine (DPPE), 1,2-dihexadecanoyl-sn-glycero-3-phospho-(1'-rac-glycerol) (DPPG), and 1,1',2,2'-tetratetradecanoyl cardiolipin (cardiolipin). Surface pressure–area (p-A) and surface potential–area (''-A) isotherms were measured to monitor changes in the thermodynamic and physical properties of the monolayers. The monolayer reciprocal isothermal compressibility (Cs 1) was calculated from the p-A data. The five compounds modified the three lipid monolayer structures by integrating into the monolayer, forming aggregates/rafts of antimicrobial–lipid complexes, reducing the packing effectiveness of the lipids, increasing the membrane fluidity, and altering the total dipole moment in the monolayer membrane model. The interactions of the five antimicrobial compounds with bacterial phospholipids depended on both the structure of the antimicrobial and the composition of the monolayers. The observed experimental results provide insight into the mechanism of the molecular interactions between naturally-occurring antimicrobial compounds and phospholipids of the bacterial cell membrane that govern activities. The significance of the results to microbial food safety is discussed.