Role of Neuraminidase-Producing Bacteria in Exposing Cryptic Carbohydrate Receptors for Streptococcus gordonii Adherence

Abstract

<i>Streptococcus gordonii</i> is an early colonizer of the oral cavity. Although a variety of <i>S. gordonii</i> adherence mechanisms have been described, current dogma is that the major receptor for <i>S. gordonii</i> is sialic acid. However, as many bacterial species in the oral cavity produce neuraminidase that can cleave terminal sialic acid, it is unclear whether <i>S. gordonii</i> relies on sialic acid for adherence to oral surfaces or if this species has developed alternative binding strategies. Previous studies have examined adherence to immobilized glycoconjugates and identified binding to additional glycans, but no prior studies have defined the contribution of these different glycan structures in adherence to oral epithelial cells. We determined that the majority of <i>S. gordonii</i> strains tested did not rely on sialic acid for efficient adherence. In fact, adherence of some strains was significantly increased following neuraminidase treatment. Further investigation of representative strains that do not rely on sialic acid for adherence revealed binding not only to sialic acid via the serine-rich repeat protein GspB but also to β-1,4-linked galactose. Adherence to this carbohydrate occurs via an unknown adhesin distinct from those utilized by <i>Streptococcus oralis</i> and <i>Streptococcus pneumoniae</i> Demonstrating the potential biological relevance of binding to this cryptic receptor, we established that <i>S. oralis</i> increases <i>S. gordonii</i> adherence in a neuraminidase-dependent manner. These data suggest that <i>S. gordonii</i> has evolved to simultaneously utilize both terminal and cryptic receptors in response to the production of neuraminidase by other species in the oral environment.