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Transcriptomic Responses to Coaggregation between Streptococcus gordonii and Streptococcus oralis.

ABSTRACT: Cell-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 minutes, RNA was extracted for Dual RNASeq 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 coaggregation with other oral bacteria. Targeting the key genes that are upregulated during interspecies interactions may be a powerful approach to control the developing biofilm and maintain oral health.

SUBMITTER: Choo SW

PROVIDER: S-EPMC8552878 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Oral streptococci, including Streptococcus gordonii, and Actinomyces naeslundii, are consistently found to be the most abundant bacteria in the early stages of dental plaque accumulation. These organisms interact physically (coaggregate) in vitro and in vivo. We hypothesized that coaggregation between S. gordonii and A. naeslundii leads to changes in gene expression in the partner organisms. Furthermore, we predicted that coaggregation-induced changes in phenotype contribute to the success of streptococci and actinomyces in dental plaque. To assess the responses of S. gordonii to coaggregation with A. naeslundii, RNA was extracted from S. gordonii cells 3 h after inducing coaggregation with A. naeslundii or from equivalent S. gordonii monocultures. The two RNA populations were reverse transcribed and compared by competitive hybridization with an S. gordonii genomic microarray. The most striking feature of the response to coaggregation was a profound change in expression of S. gordonii genes involved in arginine biosynthesis and transport. Subsequent experiments demonstrated that coaggregation with A. naeslundii stabilizes arginine biosynthesis in S. gordonii and enables growth under low-arginine conditions, such as those present in human saliva. Keywords: Cell-cell interaction The S. gordonii microarrays consist of 2195 70-mer oligonucleotides representing 2151 open reading frames, each repeated six times on the array. Chemically defined medium (CDM), was based in Tereleckyj’s FMC with minor modifications (Jakubovics et al., 2008). For coaggregate cultures, concentrated suspensions of S. gordonii DL1 (Challis) and A. naeslundii MG1 in CDM were mixed, vortexed and diluted to 1 x 108 cfu/ml. Monocultures were set up identically, except that A. naeslundii cells were omitted. Cultures were incubated at 37oC for 3 h prior to harvesting and extraction of total RNA. Purified RNA was reverse transcribed and cDNAs were labelled with Cy3 or Cy5 dye. cDNAs from coaggregate cultures and from S. gordonii monocultures were competitively hybridized with the S. gordonii microarray. Three independent sets of cultures were used, and flip dye pairs were included for two of the biological replicates (ie 5 hybridizations in total). In control experiments, cDNA derived from A.naeslundii monocultures did not hybridize with the S. gordonii microarrays. Data represent the ratios of gene expression in coaggregated S. gordonii compared with S. gordonii monocultured cells.

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Transcriptomic Responses to Coaggregation between Streptococcus gordonii and Streptococcus oralis.

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