Cross-Kingdom Cell-to-Cell Interactions in Cariogenic Biofilm Initiation

Candida albicansis known to form polymicrobial biofilms with variousStreptococcusspp., including mitis and mutans group streptococci.Streptococcus gordonii(mitis group) has been shown to bind avidly toC. albicanshyphae via direct cell-to-cell interaction, while the cariogenic pathogenStreptococcus mutans(mutans group) interacts with the fungal cells via extracellular glucans. However, the biophysical properties of these cross-kingdom interactions at the single-cell level during the early stage of biofilm formation remain understudied. Here, we examined the binding forces betweenS. mutans(orS. gordonii) andC. albicansin the presence and absence of in situ glucans on the fungal surface using single-cell atomic force microscopy and their influence on biofilm initiation and subsequent development under cariogenic conditions. The data show thatS. gordoniibinding force to theC. albicanssurface is significantly higher than that ofS. mutansto the fungal surface (similar to 2-fold). However,S. mutansbinding forces are dramatically enhanced when theC. albicanscell surface is locally coated with extracellular glucans (similar to 6-fold vs. uncoatedC. albicans), which vastly exceeds the forces betweenS. gordoniiandC. albicans. The enhanced binding affinity ofS. mutansto glucan-coatedC. albicansresulted in a larger structure during early biofilm initiation compared toS. gordonii-C. albicansbiofilms. Ultimately, this resulted inS. mutansdominance composition in the 3-species biofilm model under cariogenic conditions. This study provides a novel biophysical aspect ofCandida-streptococcal interaction whereby extracellular glucans may selectively favorS. mutansbinding interactions withC. albicansduring cariogenic biofilm development.

Automated summary

The study revealed differences in binding forces between S. gordonii and S. mutans with Candida albicans, with the latter exhibiting significantly enhanced binding forces when the fungal surface is coated with extracellular glucans. This enhanced binding affinity led to the formation of larger structures during early biofilm initiation and ultimately resulted in the dominance of S. mutans in the 3-species biofilm model under cariogenic conditions.