The oligopeptide (<i>opp</i>) gene cluster of <i>Streptococcus mutans</i>: identification, prevalence, and characterization

Nepomuceno, R. S. L.; Tavares, Milene B.; Lemos, José A.; Griswold, Ann R.; Ribeiro, Júlia Lisboa; Balan, Andrea; Guimarães, K. S.; Cai, Silvana; Burne, Robert A.; Ferreira, Luís Carlos S.; Ferreira, Rita de Cássia Café

doi:10.1111/j.1399-302x.2007.00368.x

Cited by 15 publications

(18 citation statements)

References 44 publications

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“…Thus, the responses to CSP and XIP in S. mutans are similar to what has been reported for comX induction by ComS in Streptococcus thermophilus. Specifically, Gardan et al (50) reported that comX expression in a ComS-deficient strain of S. thermophilus was optimal when a synthetic ComS [17][18][19][20][21][22][23][24] peptide was added to cultures during early-or mid-exponential phase, but no comX expression was detected at the end of the exponentialgrowth phase (50). Further experiments measuring endogenous comS and comX expression showed that competence gene expression was independent of the initial OD 600 of the culture and that the ComRS system functions more as a timing device than as a quorum-sensing system (50).…”

Section: Discussionmentioning

confidence: 99%

“…The comS gene encodes a 17-aa propeptide that is secreted and appears in the supernatant fluid as the active sigX-inducing peptide (XIP), consisting of the seven C-terminal residues of ComS (ComS [11][12][13][14][15][16][17] ) (20). XIP is imported via the Opp oligopeptide permease system back into the cells (22), where it is bound by the cytoplasmic Rgg-type transcriptional regulator ComR (20). The ComRS complex can directly activate the transcription of comX and comS, constituting a positive-feedback loop (20).…”

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confidence: 99%

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Growth Phase and pH Influence Peptide Signaling for Competence Development in Streptococcus mutans

Guo

Ahn

Kaspar

et al. 2013

Journal of Bacteriology

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The development of competence by the dental caries pathogen Streptococcus mutans is mediated primarily through the alternative sigma factor ComX (SigX), which is under the control of multiple regulatory systems and activates the expression of genes involved in DNA uptake and recombination. Here we report that the induction of competence and competence gene expression by XIP (sigX-inducing peptide) and CSP (competence-stimulating peptide) is dependent on the growth phase and that environmental pH has a potent effect on the responses to XIP. A dramatic decline in comX and comS expression was observed in midand late-exponential-phase cells. XIP-mediated competence development and responses to XIP were optimal around a neutral pH, although mid-exponential-phase cells remained refractory to XIP treatment, and acidified late-exponential-phase cultures were resistant to killing by high concentrations of XIP. Changes in the expression of the genes for the oligopeptide permease (opp), which appears to be responsible for the internalization of XIP, could not entirely account for the behaviors observed. Interestingly, comS and comX expression was highly induced in response to endogenously overproduced XIP or ComS in mid-exponential-phase cells. In contrast to the effects of pH on XIP, competence induction and responses to CSP in complex medium were not affected by pH, although a decreased response to CSP in cells that had exited early-exponential phase was observed. Collectively, these results indicate that competence development may be highly sensitive to microenvironments within oral biofilms and that XIP and CSP signaling in biofilms could be spatially and temporally heterogeneous.

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

Growth Phase and pH Influence Peptide Signaling for Competence Development in Streptococcus mutans

Guo

Ahn

Kaspar

et al. 2013

Journal of Bacteriology

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“…While a number of operons have been identified in M. catarrhalis, little is known about how environmental factors influence transcriptional regulation (13,27,(44)(45)(46)(47)(48)(49)(50). In the present study, we show that the entire opp gene cluster is transcribed as a single transcript and is thus an operon (Fig.…”

Section: Discussionmentioning

confidence: 54%

Expression of the Oligopeptide Permease Operon of Moraxella catarrhalis Is Regulated by Temperature and Nutrient Availability

Jones

Murphy

2015

Infect Immun

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Moraxella catarrhalis causes otitis media in children and exacerbations of chronic obstructive pulmonary disease in adults. Together, these two conditions contribute to enormous morbidity and mortality worldwide. The oligopeptide permease (opp) ABC transport system is a nutritional virulence factor important for the utilization of peptides. The substrate binding protein OppA, which binds peptides for uptake, is a potential vaccine antigen, but little was known about the regulation of gene expression. The five opp genes oppB, oppC, oppD, oppF, and oppA are in the same open reading frame. Sequence analysis predicted two promoters, one located upstream of oppB and one within the intergenic region between oppF and oppA. We have characterized the gene cluster as an operon with two functional promoters and show that cold shock at 26°C for <0.5 h and the presence of a peptide substrate increase gene transcript levels. Additionally, the putative promoter upstream of oppA contributes to the transcription of oppA but is not influenced by the same environmental cues as the promoter upstream of oppB. We conclude that temperature and nutrient availability contribute to the regulation of the Opp system, which is an important nutritional virulence factor in M. catarrhalis. Moraxella catarrhalis is an increasingly important human-specific pathogen contributing to worldwide morbidity and mortality that has transitioned from an emerging to an established pathogen (1-3). Otitis media in children is the primary cause of new antibiotic prescriptions and pediatric office visits, with M. catarrhalis accounting for 10% to 20% of acute otitis media episodes (2, 4-6). Chronic obstructive pulmonary disease (COPD) is the third leading cause of death in the United States, with M. catarrhalis contributing to at least 10% of exacerbations (7-11). The socioeconomic burden of otitis media and COPD is significant, with an estimated $50 billion dollars annually in health care expenses globally (5, 9, 12). In view of the morbidity and health care cost associated with M. catarrhalis, it is important to understand the mechanisms of pathogenesis in order to guide development of novel approaches to treatment and prevention (2,13,14). In previous work, we identified OppA as a promising vaccine antigen and a nutritional virulence factor for M. catarrhalis (15,16).We previously characterized the oligopeptide permease (opp) gene cluster as an ABC transport system vital for the utilization of peptide substrates. The gene cluster encodes two permeases, OppB and OppC; two ATPases, OppD and OppF; and a substrate binding protein, OppA (16). We hypothesized that this gene cluster was transcribed as an operon and that environmental factors, temperature and essential nutrients available as peptides, would alter the rate of transcription.The lower respiratory tract has a normal body temperature of 37°C, while the upper airways, specifically the nasopharynx, where M. catarrhalis first colonizes, ranges from 34°C at room temperature (25°C) down to 26°C after a short...

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“…Binding of S. mutans cells to a saliva‐coated surface was determined in 96‐well flat‐bottom microtitre plates (Nalge Nunc International, Rochester, NY) as previously described, but with minor modifications (Nepomuceno et al. , 2007).…”

Section: Methodsmentioning

confidence: 99%

The Pst system of Streptococcus mutans is important for phosphate transport and adhesion to abiotic surfaces

Luz

Nepomuceno

Spira

et al. 2012

Molecular Oral Microbiology

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The Pst system is a high-affinity inorganic phosphate transporter found in many bacterial species. Streptococcus mutans, the etiological agent of tooth decay, carries a single copy of the pst operon composed of six cistrons (pstS, pstC1, pstC, pstB, smu.1134 and phoU). Here, we show that deletion of pstS, encoding the phosphate-binding protein, reduces phosphate uptake and impairs cell growth, which can be restored upon enrichment of the medium with high concentrations of inorganic phosphate. The relevance of Pst for growth was also demonstrated in the wild-type strain treated with an anti-PstS antibody. Nevertheless, a reduced ability to bind to saliva-coated surfaces was observed, along with the reduction of extracellular polysaccharide production, although no difference on pH acidification was observed between mutant and wild-type strains. Taken together, the present data indicate that the S. mutans Pst system participates in phosphate uptake, cell growth and expression of virulence-associated traits.

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The oligopeptide (opp) gene cluster of Streptococcus mutans: identification, prevalence, and characterization

Abstract: Collectively, these results indicate that, in contrast to other Streptococcus species, the S. mutans Opp system, and particularly the OppA protein, does not represent an important trait required for growth and colonization.

Cited by 15 publications

References 44 publications

Growth Phase and pH Influence Peptide Signaling for Competence Development in Streptococcus mutans

Growth Phase and pH Influence Peptide Signaling for Competence Development in Streptococcus mutans

Expression of the Oligopeptide Permease Operon of Moraxella catarrhalis Is Regulated by Temperature and Nutrient Availability

The Pst system of Streptococcus mutans is important for phosphate transport and adhesion to abiotic surfaces

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