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Direct interactions with commensal streptococci modify intercellular communication behaviors of Streptococcus mutans.

ABSTRACT: The formation of dental caries is a complex process that ultimately leads to damage of the tooth enamel from acids produced by microbes in attached biofilms. The bacterial interactions occurring within these biofilms between cariogenic bacteria, such as the mutans streptococci, and health-associated commensal streptococci, are thought to be critical determinants of health and disease. To better understand these interactions, a Streptococcus mutans reporter strain that actively monitors cell-cell communication via peptide signaling was cocultured with different commensal streptococci. Signaling by S. mutans, normally highly active in monoculture, was completely inhibited by several species of commensals, but only when the bacteria were in direct contact with S. mutans. We identified a novel gene expression pattern that occurred in S. mutans when cultured directly with these commensals. Finally, mutant derivatives of commensals lacking previously shown antagonistic gene products displayed wild-type levels of signal inhibition in cocultures. Collectively, these results reveal a novel pathway(s) in multiple health-associated commensal streptococci that blocks peptide signaling and induces a common contact-dependent pattern of differential gene expression in S. mutans. Understanding the molecular basis for this inhibition will assist in the rational design of new risk assessments, diagnostics, and treatments for the most pervasive oral infectious diseases.

SUBMITTER: Kaspar JR

PROVIDER: S-EPMC8027600 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND: Hundreds of bacterial species coexist within the human oral cavity, where complex interactions can occur. Recent evidence has shown that the commensal oral streptococci that populate supragingival biofilms on the tooth surface produce extracellular proteases that degrade cell-cell signaling molecules of their disease-causing competitors, Streptococcus mutans. To further explore these interactions, we performed transcriptome analysis of S. mutans cocultured with different oral streptococci and found that cell-cell signaling was complety inhibited, but only when the bacteria were directly cocultured together. METHODS: RNA-Seq was utilized to compare the transcriptomes of S. mutans wild-type strain UA159 cocultured in its own supernatant (3 replicates), UA159 cocultured in S. sp. A12 supernatant (3 replicates) and directly cocultured with S. sp. A12 (3 replicates). Strains were grown to OD600 nm = 0.5 in CDM medium before harvest. Deep sequencing was performed at the University of Florida ICBR facilities (Gainesville, FL). Approximately 15 million short-reads were obtained for each sample. After removing adapter sequences from each short-read and trimming of the 3’-ends by quality scores, the resulting sequences were mapped onto the reference genome of strain UA159 (GenBank accession no. AE014133) using the short-read aligner. Mapped short-read alignments were then converted into readable formats using SAMTOOLS. RESULTS: Using an optimzed data analysis workflow, we mapped 13-16 million reads per sample to the genome of UA159. For viewing of the mapped reads aligned to the genome, .bam files were uploaded into the Integrative Genomics Viewer (IGV – version 2.3.55). A .csv file containing raw read counts for each replicate (3) was then uploaded to Degust (http://degust.erc.monash.edu/) and edgeR analysis performed to determine Log2 fold change and a false discovery rate (FDR). When comparing the growth of S. mutans in its own spent supernatant against competitor spent supernatants, we found 88 genes differentially expressed (Log2 fold change > (-)1.5, -log10 P-value > 4) which included upregulation of the zinc transport system and several amino acid ABC transporters, along with downregulation of the TnSmu1 genomic island. A more substantial effect was seen when we compared growth of S. mutans in competitor spent supernatant compared to growth directly with a competitor. Here, 140 genes were differentially expressed and included upregulation of one of the CRISPR genetic clusters as well as downregulation of the entire genetic competence regulon, as expected. Principal component analysis (PCA) of transcriptome data from these three conditions displayed a wide variation and separation among the tested groups, further confirming a unique transcriptome response for S. mutans between growth in the supernatant of a competitor and directly with a competitor. CONCLUSIONS: We believe that these measured transcriptomic changes represent a conserved S. mutans response to competitors that has not been previously captured in RNA-Seq experiments of monocultures alone. Together, these results highlight a previously undocumented transcriptomic alteration by S. mutans when challenged by health-associated oral streptococci.

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Direct interactions with commensal streptococci modify intercellular communication behaviors of Streptococcus mutans.

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