Path-dependency of the interaction between coaggregating and between non-coaggregating oral bacterial pairs—a thermodynamic approach

Abstract

Coaggregation, i.e. specific recognition between bacteria from different species, is a well-described phenomenon in the human oral cavity but remains physically poorly understood. With our study we aimed at elucidating some aspects of the mechanism of the coaggregation between the oral bacteria Streptococcus oralis J22 and Actinomyces naeslundii 147, in particular with respect to the driving force for coaggregation and its pathway-dependency. To that end, the macroscopic turbidity of the bacterial suspension, the morphology of the coaggregates, binding isotherms and heats of interaction were compared between the above-mentioned coaggregating bacterial pair and a non-coaggregating pair, Streptococcus sanguis PK1889 and A. naeslundii 147. The coaggregating pair forms large aggregates, which rapidly sediment from the suspension while the non-coaggregating pair forms only very small coaggregates that remain homogeneously suspended. Coaggregation is further characterized by a high affinity between the partner cells that bind to each other in a strong cooperative mode. The interactions between both pairs occur under the release of heat and are thus enthalpically favorable. More heat is released for the coaggregating than for the non-coaggregating pair. Adding the coaggregating bacteria in steps to each other leads to saturation of enthalpically favorable binding sites. This is observed when the streptococcus is added to the actinomyces as well as when the addition is done the other way around. It is concluded that the cooperativity of the coaggregation process is based on an increase of entropy. It is furthermore shown that the density of the coaggregates as well as the heat effect of formation of these coaggregates depend on the number of steps in which the partner cells are added to each other. Adding S. oralis J22 in three steps to A. naeslundii 147 results in the formation of denser coaggregates under the release of less heat, as compared to that of addition in one step. These differences point to a larger entropy increase when in a step-wise mixing the coaggregating bacteria are allowed to form more densely-packed coaggregates.