Genome-Wide Transcriptional Changes inStreptococcus gordoniiin Response to Competence Signaling Peptide

Abstract

Streptococcus gordonii is a primary colonizer of the multispecies biofilm on tooth surfaces forming dental plaque and a potential agent of endocarditis. The recent completion of the genome sequence of the naturally competent strain Challis allowed the design of a spotted oligonucleotide microarray to examine a genome-wide response of this organism to environmental stimuli such as signal peptides. Based on temporal responses to synthetic competence signaling peptide (CSP) as indicated by transformation frequencies, the S. gordonii transcriptome was analyzed at various time points after CSP exposure. Microarray analysis identified 35 candidate early genes and 127 candidate late genes that were up-regulated at 5 and 15 min, respectively; these genes were often grouped in clusters. Results supported published findings on S. gordonii competence, showing up-regulation of 12 of 16 genes that have been reported to affect transformation frequencies in this species. Comparison of CSP-induced S. gordonii transcriptomes to results published for Streptococcus pneumoniae strains identified both conserved and species-specific genes. Putative intergenic regulatory sites, such as the conserved combox sequence thought to be a binding site for competence sigma factor, were found preceding S. gordonii late responsive genes. In contrast, S. gordonii early CSP-responsive genes were not preceded by the direct repeats found in S. pneumoniae. These studies provide the first insights into a genome-wide transcriptional response of an oral commensal organism. They offer an extensive analysis of transcriptional changes that accompany competence in S. gordonii and form a basis for future intra- and interspecies comparative analyses of this ecologically important phenotype.

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

“…There is evidence that peptides produced by S. mutans (Jarosz et al, 2009) and Enterococcus faecalis (Cruz et al, 2013) are inhibitory to filamentation by C. albicans. The ComCDE systems in S. gordonii, S. pneumoniae and S. mutans function as QS autoregulatory control systems, modulating gene expression patterns in different ways for the three streptococcal species (Vickerman et al, 2007;Mashburn-Warren et al, 2010;Son et al, 2012;Merritt & Qi, 2012). Since S. gordonii and C. albicans form fully integrated dual species biofilm communities (Dutton et al, 2014) we investigated the possible role of the ComCDE system in their regulation.…”

“…The induction of competence for DNA uptake and transformation in S. gordonii involves a complex regulatory network similar to that in Streptococcus pneumoniae (Vickerman et al, 2007) and shares some similarities to that in S. mutans (Son et al, 2012). Competence regulation in these organisms employs a ComABCDE system that generates the CSP (comC gene product).…”

Glycosylation and biogenesis of a family of serine-rich bacterial adhesins

“…The sequencing of the large repetitive region was completed by using a transposon mutagenesis strategy which allows us to sequence one 400-600 bp repetitive region at a time and assemble them manually based on the exact transposition insertion sites (Wu & Fives-Taylor, 1999). The unusual repetitive nature of Fap1 was initially thought to be artificial; however, the discovery of Fap1-like proteins in other streptococci, such as Streptococcus gordonii strains M99 and DL1 (Bensing & Sullam, 2002;Takahashi et al, 2002;Vickerman et al, 2007), Streptococcus cristatus (Handley et al, 2005) and the sequenced genome of Streptococcus pneumoniae TIGR4 (Tettelin et al, 2001), has confirmed our findings and stimulated researchers' interest in the area.…”

Characterization of Streptococcus gordonii prophage PH15: complete genome sequence and functional analysis of phage-encoded integrase and endolysin

“…The genome from S. gordonii Challis CH1 (accession no. CP000725; Vickerman et al, 2007) contains a CRISPR array with repeats of 36 bp and a total of 26 spacers of 30 bp in size. The sequences of the repeats were identical to the repeats of CRISPR1 from different S. thermophilus strains (Barrangou et al, 2007).…”

“…The genome sequence of the virulent phage M102, which infects S. mutans, has recently been published (van der Ploeg, 2007). The sequenced genomes of three oral streptococcal strains, including S. gordonii CH1, do not appear to contain prophages (Ajdić et al, 2002;Tanzer et al, 2008;Vickerman et al, 2007;Xu et al, 2007). Temperate phages from Streptococcus mitis, an abundant inhabitant of the oral cavity, have been described (Romero et al, 2004a;Siboo et al, 2003).…”