Streptococcus gordonii Modulates Candida albicans Biofilm Formation through Intergeneric Communication

Abstract

The fungus Candida albicans colonizes human oral cavity surfaces in conjunction with a complex microflora. C. albicans SC5314 formed biofilms on saliva-coated surfaces that in early stages of development consisted of ϳ30% hyphal forms. In mixed biofilms with the oral bacterium Streptococcus gordonii DL1, hyphal development by C. albicans was enhanced so that biofilms consisted of ϳ60% hyphal forms. Cell-cell contact between S. gordonii and C. albicans involved Streptococcus cell wall-anchored proteins SspA and SspB (antigen I/II family polypeptides). Repression of C. albicans hyphal filament and biofilm production by the quorum-sensing molecule farnesol was relieved by S. gordonii. The ability of a luxS mutant of S. gordonii deficient in production of autoinducer 2 to induce C. albicans hyphal formation was reduced, and this mutant suppressed farnesol inhibition of hyphal formation less effectively. Coincubation of the two microbial species led to activation of C. albicans mitogen-activated protein kinase Cek1p, inhibition of Mkc1p activation by H 2 O 2 , and enhanced activation of Hog1p by farnesol, which were direct effects of streptococci on morphogenetic signaling. These results suggest that interactions between C. albicans and S. gordonii involve physical (adherence) and chemical (diffusible) signals that influence the development of biofilm communities. Thus, bacteria may play a significant role in modulating Candida carriage and infection processes in the oral cavity.

Streptococcus gordonii comCDE (competence) operon modulates biofilm formation with Candida albicans

“…Dual species biofilms of S. gordonii and C. albicans generally had denser morphologies and increased biomass compared to the single species biofilms (Fig. 1) (Bamford et al, 2009). The DcomC and DcomCDE mutant strains had significantly increased dual species biofilm biomass values compared to wild-type (Fig.…”

“…These species of streptococci interact with a range of other oral microorganisms, thus establishing a foundation for the building of biofilm communities (Wright et al, 2013). S. gordonii forms biofilms with Porphyromonas gingivalis (Lamont et al, 2002), Actinomyces oris (Palmer et al, 2003), Fusobacterium nucleatum (Foster & Kolenbrander, 2004) and Aggregatibacter actinomycetemcomitans in dual or mixed species systems, and also produces dual species biofilms with the fungus Candida albicans (Bamford et al, 2009;Dutton et al, 2014).…”

“…The SspB-Als3 interaction is involved in biofilm development in which bacteria and fungi cooperate at the cellular and molecular level to generate a robust mixed microbial community (Whitmore & Lamont, 2011). Community composition may be regulated by extracellular signalling molecules such as autoinducer-2 (AI-2) (McNab et al, 2003;Bamford et al, 2009), farnesol (Bamford et al, 2009;Lu et al, 2014), Nacetyl-D-glucosamine (Naseem et al, 2011) and homoserine lactones (Hogan et al, 2004). In addition, the quorum-sensing (QS) molecule, competence stimulating peptide (CSP), produced by Streptococcus mutans inhibits hypha formation by C. albicans (Jarosz et al, 2009).…”

Fungi at the Scene of the Crime: Innocent Bystanders or Accomplices in Oral Infections?

“…The emergence of these datasets has been the catalyst for a number of studies investigating the importance of fungi within oral biofilm infections. This has fuelled the concept of interkingdom communities, which continues to grow above and beyond our traditional viewpoint of bacterial-bacterial interactions [12][13][14]. Indeed, the advancement in sequencing technologies has facilitated the characterisation of the fungal oral microbiome [11, 15•, 16].…”

Cross-feeding and interkingdom communication in dual-species biofilms of Streptococcus mutans and Candida albicans

“…Interaction between C. albicans and streptococci can contribute to enhanced biofilm formation. Oral streptococci produce cell wall-anchored proteins facilitating binding to C. albicans (Bamford et al, 2009). The S. gordonii cell wall-associated polypeptide SspB3 interacts directly with the C. albicans hyphae-specific agglutinin-like sequence 3 .…”