Abstract
ABSTRACTCell-cell adhesion between oral bacteria plays a key role in the development of polymicrobial communities such as dental plaque. Oral streptococci such as Streptococcus gordonii and Streptococcus oralis are important early colonizers of dental plaque and bind to a wide range of different oral microorganisms, forming multispecies clumps or “coaggregates.” S. gordonii actively responds to coaggregation by regulating gene expression. To further understand these responses, we assessed gene regulation in S. gordonii and S. oralis following coaggregation in 25% human saliva. Coaggregates were formed by mixing, and after 30 min, RNA was extracted for dual transcriptome sequencing (RNA-Seq) analysis. In S. oralis, 18 genes (6 upregulated and 12 downregulated) were regulated by coaggregation. Significantly downregulated genes encoded functions such as amino acid and antibiotic biosynthesis, ribosome, and central carbon metabolism. In total, 28 genes were differentially regulated in Streptococcus gordonii (25 upregulated and 3 downregulated). Many genes associated with transporters and a two-component (NisK/SpaK) regulatory system were upregulated following coaggregation. Our comparative analyses of S. gordonii-S. oralis with different previously published S. gordonii pairings (S. gordonii-Fusobacterium nucleatum and S. gordonii-Veillonella parvula) suggest that the gene regulation is specific to each pairing, and responses do not appear to be conserved. This ability to distinguish between neighboring bacteria may be important for S. gordonii to adapt appropriately during the development of complex biofilms such as dental plaque.IMPORTANCE Dental plaque is responsible for two of the most prevalent diseases in humans, dental caries and periodontitis. Controlling the formation of dental plaque and preventing the transition from oral health to disease requires a detailed understanding of microbial colonization and biofilm development. Streptococci are among the most common colonizers of dental plaque. This study identifies key genes that are regulated when oral streptococci bind to one another, as they do in the early stages of dental plaque formation. We show that specific genes are regulated in two different oral streptococci following the formation of mixed-species aggregates. The specific responses of S. gordonii to coaggregation with S. oralis are different from those to coaggregation with other oral bacteria. Targeting the key genes that are upregulated during interspecies interactions may be a powerful approach to control the development of biofilm and maintain oral health.
Highlights
Cell-cell adhesion between oral bacteria plays a key role in the development of polymicrobial communities such as dental plaque
We have identified a number of genes that are regulated in S. gordonii in response to coaggregation with Fusobacterium nucleatum or Veillonella parvula [17, 18]
This work builds on and improves our understanding of the interactions between S. gordonii and S. oralis and provides insights into their potential roles during the formation of mixed-species biofilms. We compared these genes with the sets of genes that we identified in the interactions between S. gordonii and other bacterial species (e.g., F. nucleatum and V. parvula) in order to examine whether
Summary
Cell-cell adhesion between oral bacteria plays a key role in the development of polymicrobial communities such as dental plaque. In an attempt to standardize this approach, we have developed a simple method for studying coaggregation-mediated gene regulation by mixing suspensions of different bacteria in 25% human saliva to form coaggregates, incubating for 30 min, extracting RNA, and assessing gene expression by dual transcriptome sequencing (RNA-Seq). Using this approach, we have identified a number of genes that are regulated in S. gordonii in response to coaggregation with Fusobacterium nucleatum or Veillonella parvula [17, 18]
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