Electric double layer interactions in bacterial adhesion to surfaces

Abstract

The DLVO (Derjaguin, Landau, Verwey, Overbeek) theory was originally developed to describe interactions between non-biological lyophobic colloids such as polystyrene particles, but is also used to describe bacterial adhesion to surfaces. Despite the differences between the surface of bacteria and that of non-biological particles, DLVO-descriptions of bacterial adhesion have nearly always treated bacteria as if they were non-biological particles and consequently in many cases these descriptions have failed to describe bacterial adhesion adequately. This review summarizes recent advances in colloid and surface science regarding the electrokinetic characterization of biological colloids, most notably bacteria, and their electric double layer interactions with surfaces.

Introduction

Adhesion of colloidal particles may be described by the DLVO (Derjaguin, Landau, Verwey, Overbeek) theory. According to this theory, particle adhesion is governed by long-range interactions between the adhering particle and the macroscopic substratum surface. These interactions include Lifshitz–van der Waals interactions and interactions resulting from overlapping electric double layers (also referred to as electrostatic interactions). The two types of interactions are assumed to be additive allowing the total Gibbs energy of adhesion to be expressed as a function of the distance between the particle and the macroscopic substratum surface. Recently [1], the so-called XDLVO theory has been forwarded, which in addition to classical DLVO interactions, accounts for short-range Lewis acid–base or hydration interactions. The DLVO theory has also been applied to describe bacterial adhesion² [3], [4], [5] in a wide range of applications, involving microbial adhesion on food processing equipment [6], [7], biomaterials implants [8], surfaces in the oral cavity [9], on grains of sand [10] and on bioreactor supports [11], [12]. Also, the DLVO theory has been used to describe the stability of bacteria in suspension [13].

The bacterial cell surface carries a net negative charge under most physiological conditions, with a few exceptions [14], [15]. As most natural surfaces are negatively charged as well, bacteria generally experience electric double layer repulsion when approaching these surfaces. Experimental studies have shown the importance of electric double layer interactions in bacterial adhesion [16], [17], [18], [19], but have also revealed discrepancies between observations and theoretical expectations, some of which are reviewed in Table 1.

The bacterial cell surface is a highly dynamic surface responding strongly to environmental changes through adsorption of ions and macromolecular components. Charged groups may associate or dissociate upon changes in pH or ionic strength of the suspending fluid, but also upon approach of a charged surface, either of another bacterium or a substratum. This, in addition, may induce changes in the conformation of different kinds of surface appendages, such as fibrils, fimbriae or flagellae [28]. Moreover, the bacterial cell surface may be penetrable to solvents and solutes, in particular ions, either due to the presence of a peptidoglycan layer [29], [30] as on Gram-positive bacteria, the presence of surface appendages [31] or a slime capsule [32]. Inside the bacterial cell wall, charged groups are present and the distribution of these charges influences electric double layer interactions in bacterial adhesion [29], [32], unlike for many synthetic colloids for which the electric charges in the plane of the outer surface determines their interaction with other surfaces.

Summarizing, the bacterial cell wall is structurally and chemically more complex and heterogeneous than the surface of synthetic colloidal particles and this has an impact on bacterial adhesion to surfaces. Yang et al. [33] have shown, for instance, that adhesion of polystyrene particles is not an appropriate model for bacterial adhesion because of differences in surface structure between bacteria and polystyrene particles. In an attempt to account for the presence of polymeric structures on bacterial cell surfaces, steric interactions have been introduced in addition to DLVO interactions [16], [26], [27], [34]. However, little attention has been paid to the effect of the bacterial cell surface structure on DLVO interactions and as far as electric double layer interactions are concerned, bacteria have mostly been treated as model colloidal particles [2], [3].

The electric potential at the bacterial cell surface is usually inferred from measured electrophoretic mobilities, i.e. the velocity of suspended bacteria in an aqueous phase under the influence of an applied electric field. Derivation of the bacterial cell surface potential from the electrophoretic mobility is not straightforward and strongly depends on the model used to describe the cell surface. Bacterial cell surfaces have hitherto in most cases been modeled as ion-impenetrable and non-conducting [35], but this simplification neglects effects of surface conductivity [29] and of penetrability of the bacterial cell surface to fluid flow [31], [36]. Apart from influencing the electrophoretic mobility, penetrability of the bacterial cell wall is also expected to influence electric double layer interactions in bacterial adhesion to surfaces [32], [37].

The aim of this paper is to summarize recent advances in colloid and surface science regarding electric double layer interactions, which help better to understand mechanisms of bacterial adhesion. To this end, first a description is given of bacterial cell surfaces as compared with the surface of model colloidal particles. Second, the impact of specific characteristics of bacteria on their electrochemical properties and their electric double layer interactions with surfaces as follows from the DLVO theory, is discussed in relation to existing literature on bacterial adhesion.