Force microscopic and thermodynamic analysis of the adhesion between Pseudomonas aeruginosa and Candida albicans

Abstract

Pseudomonas aeruginosa expresses a plethora of virulence factors and many species have developed warning systems to detect and evade P. aeruginosa. Candida albicans detects P. aeruginosa by sensing the secreted bacterial quorum sensing molecule 3OC12HSL and responds by reverting to the yeast morphology, resistant to killing by P. aeruginosa. The aim of this study was to investigate the nature of the adhesion forces between P. aeruginosa and different C. albicans morphologies, based on surface thermodynamics and atomic force microscopy. Adhesion of P. aeruginosa to hyphae was always accompanied by strong adhesion forces, but did not occur to yeast cells. Surface thermodynamics and Poisson analyses of adhesion forces indicated that the outermost mannoprotein-layer on hyphal surfaces created favorable acid–base conditions for adhesion, allowing close approach of P. aeruginosa. Removal of these proteins caused unfavorable acid–base conditions, preventing adhesion of P. aeruginosa. Yet, favorable acid–base conditions alone are insufficient for mediating adhesion of P. aeruginosa to hyphae. P. aeruginosa PA14 lasI, unable to produce 3OC12HSL, showed favorable acid–base conditions, but was considerably less adherent to hyphae. However, growth in the presence of 3OC12HSL restored adhesion. Concluding, the mannoprotein-layer on the hyphal surface ensures favorable interaction conditions through attractive Lifshitz–Van der Waals and acid–base forces, allowing P. aeruginosa to closely approach the hyphal surface and interact stereo-chemically with the fungal cell wall for actual adhesion forces to occur. Interestingly, whereas on the one hand 3OC12HSL allows the bacterium to interact with hyphae, the same molecule induces changes in acid–base properties of the fungal outermost mannoprotein-layer during transition from hyphal to yeast morphology, preventing this interaction and allowing C. albicans to co-exist with P. aeruginosa.