Superior Membrane Permeabilization and Solubilization Properties of Biosurfactants may be Explained by Heterogeneous Perturbation

Abstract

Biosurfactants such as antimicrobial lipopeptides, saponins, and bile salts often show a superior performance to permeabilize and lyse membranes and/or a better suitability for membrane protein solubilization than classical, synthetic detergents. We propose a classification of surfactants into those that are homogeneously disordering versus heterogeneously perturbing a given membrane to help explaining and predicting this behaviour. Typical synthetic detergents such as C12EO8, octyl glucoside, SDS, and lauryl maltoside were identified as homogeneously disordering by the limiting fluorescence anisotropy of several DPH derivatives reaching a characteristic, low level at the onset of solubilization. The biosurfactants surfactin, fengycin, iturin, digitonin, and lysophosphatidylcholine along with the synthetic CHAPS belong to another class that initiates membrane lysis without critical disordering the whole membrane. They disrupt the membrane locally due to a spontaneous segregation from the lipid and/or an ordering effect that induces packing defects. This may account for enhanced activity, selectivity, and mutual synergism of antimicrobial biosurfactants. They should also be prone to form partially-demixed, asymmetric micelles (or bicelles) with a relatively lipid- (and sterol?) rich core surrounding a solubilized protein. Triton shows the pattern of a segregating surfactant in the presence of cholesterol. Zeta potential measurements of liposomes exposed to surfactin show strong peptide-peptide interactions already at a few mol-% in the membrane.