Development of competence in <i>Streptococcus pneumoniae</i>: pheromone autoinduction and control of quorum sensing by the oligopeptide permease

Alloing, Geneviève; Martin, Bernard; Granadel, Chantal; Claverys, Jean‐Pierre

doi:10.1046/j.1365-2958.1998.00904.x

Cited by 147 publications

(158 citation statements)

References 24 publications

(54 reference statements)

Supporting

Mentioning

141

Contrasting

Unclassified

Order By: Relevance

“…This might support a hypothesis that the SsuDAT1I system is an exogenous element and that S. suis acquired the SsuDAT1I genes via a transformation event. However, the competence of some bacteria is coordinately expressed in response to the growth phase and culture conditions (2,27). Further studies may be needed to determine whether S. suis has the potential to be competent for genetic transformation.…”

Section: Discussionmentioning

confidence: 99%

Evidence for Horizontal Transfer of Ssu DAT1I Restriction-Modification Genes to the Streptococcus suis Genome

et al. 2001

View full text Add to dashboard Cite

Different strains of Streptococcus suis serotypes 1 and 2 isolated from pigs either contained a restrictionmodification (R-M) system or lacked it. The R-M system was an isoschizomer of Streptococcus pneumoniae DpnII, which recognizes nucleotide sequence 5-GATC-3. The nucleotide sequencing of the genes encoding the R-M system in S. suis DAT1, designated SsuDAT1I, showed that the SsuDAT1I gene region contained two methyltransferase genes, designated ssuMA and ssuMB, as does the DpnII system. The deduced amino acid sequences of M.SsuMA and M.SsuMB showed 70 and 90% identity to M.DpnII and M.DpnA, respectively. However, the SsuDAT1I system contained two isoschizomeric restriction endonuclease genes, designated ssuRA and ssuRB. The deduced amino acid sequence of R.SsuRA was 49% identical to that of R.DpnII, and R.SsuRB was 72% identical to R.LlaDCHI of Lactococcus lactis subsp. cremoris DCH-4. The four SsuDAT1I genes overlapped and were bounded by purine biosynthetic gene clusters in the following gene order: purF-purMpurN-purH-ssuMA-ssuMB-ssuRA-ssuRB-purD-purE. The G؉C content of the SsuDAT1I gene region (34.1%) was lower than that of the pur region (48.9%), suggesting horizontal transfer of the SsuDAT1I system. No transposable element or long-repeat sequence was found in the flanking regions. The SsuDAT1I genes were functional by themselves, as they were individually expressed in Escherichia coli. Comparison of the sequences between strains with and without the R-M system showed that only the region from 53 bp upstream of ssuMA to 5 bp downstream of ssuRB was inserted in the intergenic sequence between purH and purD and that the insertion target site was not the recognition site of SsuDAT1I. No notable substitutions or insertions could be found, and the structures were conserved among all the strains. These results suggest that the SsuDAT1I system could have been integrated into the S. suis chromosome by an illegitimate recombination mechanism.More than 3,000 restriction-modification (R-M) systems have been identified in a wide variety of microorganisms, where they are thought to protect the host from invasion by foreign DNA. Only a minority of R-M systems have been sequenced (6,37,56). Among them, some type II R-M systems, which recognize 4-bp palindromic sequence 5Ј-GATC-3Ј, involve a variety of isoschizomers. Three classes can be distinguished by their manners of DNA cleavage and susceptibilities to DNA methylation. The first class of isoschizomers, represented by Sau3AI, which was described for Staphylococcus aureus, is prevented from digesting host DNA by a cognate 5-methylcytosine methyltransferase and is not influenced by the modification of N 6 -methyladenine (48, 56). The second class, represented by DpnI, which was described for Streptococcus pneumoniae, is unique among restriction endonucleases in that it cleaves only at methylated DNA sequence 5Ј-GmeATC-3Ј, and thus the cells producing DpnI do not carry the corresponding methyltransferase gene (22,23). The third class, including MboI, DpnII, and LlaDCHI...

show abstract

Section: Discussionmentioning

confidence: 99%

Evidence for Horizontal Transfer of Ssu DAT1I Restriction-Modification Genes to the Streptococcus suis Genome

et al. 2001

View full text Add to dashboard Cite

show abstract

“…This is an extravagantly wasteful approach to sex-conjugation might have produced the same result without sacrificing cells. It is especially puzzling that competence for DNA transformation is a transient property of late-log-phase cells that precedes the massive autolysis occurring at stationary state (2). It seems that this massive suicide per se could actually be the main function of spontaneous autolysis.…”

Section: Pcd and Opportunistic Mutantsmentioning

confidence: 99%

Programmed Death in Bacteria

Lewis

2000

Microbiol Mol Biol Rev

539

411

View full text Add to dashboard Cite

SUMMARY Programmed cell death (PCD) in bacteria plays an important role in developmental processes, such as lysis of the mother cell during sporulation of Bacillus subtilis and lysis of vegetative cells in fruiting body formation of Myxococcus xanthus. The signal transduction pathway leading to autolysis of the mother cell includes the terminal sporulation sigma factor EςK, which induces the synthesis of autolysins CwlC and CwlH. An activator of autolysin in this and other PCD processes is yet to be identified. Autolysis plays a role in genetic exchange in Streptococcus pneumoniae, and the gene for the major autolysin, lytA, is located in the same operon with recA. DNA from lysed cells is picked up by their neighbors and recombined into the chromosome by RecA. LytA requires an unknown activator controlled by a sensory kinase, VncS. Deletion of vncS inhibits autolysis and also decreases killing by unrelated antibiotics. This observation suggests that PCD in bacteria serves to eliminate damaged cells, similar to apoptosis of defective cells in metazoa. The presence of genes affecting survival without changing growth sensitivity to antibiotics (vncS, lytA, hipAB, sulA, and mar) indicates that bacteria are able to control their fate. Elimination of defective cells could limit the spread of a viral infection and donate nutrients to healthy kin cells. An altruistic suicide would be challenged by the appearance of asocial mutants without PCD and by the possibility of maladaptive total suicide in response to a uniformly present lethal factor or nutrient depletion. It is proposed that a low rate of mutation serves to decrease the probability that asocial mutants without PCD will take over the population. It is suggested that PCD is disabled in persistors, rare cells that are resistant to killing, to ensure population survival. It is suggested that lack of nutrients leads to the stringent response that suppresses PCD, producing a state of tolerance to antibiotics, allowing cells to discriminate between nutrient deprivation and unrepairable damage. High levels of persistors are apparently responsible for the extraordinary survival properties of bacterial biofilms, and genes affecting persistence appear to be promising targets for development of drugs aimed at eradicating recalcitrant infections. PCD in unicellular eukaryotes is also considered, including aging in Saccharomyces cerevisiae. Apoptosis-like elimination of defective cells in S. cerevisiae and protozoa suggests that all unicellular life forms evolved altruistic programmed death that serves a variety of useful functions.

show abstract

“…The following pneumococcal strains were used in the study: CP1200 (24); CP1500, a novobiocin-resistant CP1200 derivative (29); and CP1415, an erythromycin-resistant comA knockout mutant of CP1200 unable to secrete CSP-1 (4). A CP1415 derivative with no endogenous ␤-galactosidase activity (ebg mutant) was constructed previously by transforming strain CP1415 with genomic DNA isolated from the pneumococcal strain R262 (disrupted in ebg by a spectinomycin cassette) (1,2,30) to make the mutant EK100 (Ery r Sp r comA ebg). Liquid cultures of S. pneumoniae were routinely grown in casein hydrolysate (CAT) broth (19) at 37°C in the presence of chloramphenicol (CHL) (2.5 g ml Ϫ1 ), erythromycin (2 g ml Ϫ1 ), novobiocin (10 g ml Ϫ1 ), streptomycin (100 g ml Ϫ1 ), spectinomycin (200 g ml Ϫ1 ), and kanamycin (KAN) (100 g ml Ϫ1 ) when appropriate.…”

Section: Methodsmentioning

confidence: 99%

“…Two separate, but related, peptide-controlled quorum-sensing pathways have been discovered in Streptococcus pneumoniae (6). One of them, the ComABCDE pathway, regulates development of natural competence and has been relatively well characterized (2,4,9,10,21,34). The other, more recently discovered pathway BlpABCSRH, regulates production of several class II bacteriocins and their immunity proteins (7,25).…”

mentioning

confidence: 99%

Two Separate Quorum-Sensing Systems Upregulate Transcription of the Same ABC Transporter inStreptococcus pneumoniae

Knutsen¹,

Ween²,

Håvarstein³

2004

J Bacteriol

View full text Add to dashboard Cite

Streptococcus pneumoniae secretes two different peptide pheromones used for intercellular communication. These peptides, which have completely unrelated primary structures, activate two separate signal transduction pathways, ComABCDE and BlpABCSRH, which regulate natural genetic transformation and bacteriocin production, respectively. Each signal transduction pathway contains a response regulator (ComE and BlpR, respectively) that activates transcription of target genes by binding to similar, but not identical, imperfect direct repeat motifs. In general the direct repeat binding sites are specific for one or the other of the two response regulators, ensuring that competence development and bacteriocin production are regulated separately. However, in the present study we show that the rate of transcription of an operon, encoding an ABC transporter of unknown function, can be stimulated by both peptide pheromones. We also show that this cross-induction is due to a hybrid direct repeat motif that can respond to both ComE and BlpR. To our knowledge this kind of convergent gene regulation by two separate two-component regulatory systems has not been described before in bacteria.Quorum-sensing systems control several different important biological processes in bacteria, such as natural genetic transformation, virulence, bioluminescence, and sporulation. In gram-positive bacteria quorum-sensing is predominantly mediated by peptide pheromones instead of the N-acyl homoserine lactones used by the gram-negatives (8,12,13,18). Two separate, but related, peptide-controlled quorum-sensing pathways have been discovered in Streptococcus pneumoniae (6). One of them, the ComABCDE pathway, regulates development of natural competence and has been relatively well characterized (2, 4, 9, 10, 21, 34). The other, more recently discovered pathway BlpABCSRH, regulates production of several class II bacteriocins and their immunity proteins (7,25). Each pathway consists of a peptide pheromone, encoded by comC and blpC, their dedicated secretion apparatuses ComAB and BlpAB, and the two-component regulatory systems ComDE and BlpSRH. The peptide pheromones are both ribosomally synthesized as precursor peptides containing a double-glycine leader peptide at their N-terminal ends. Concomitant with export the double-glycine leaders of ComC and BlpC are removed by proteolytic domains in their respective ABC transporters ComA and BlpA. The mature pheromones, hereafter called the competence stimulating peptide (CSP) and bacteriocin inducing peptide (BIP), are both strain specific. Allelic variation of the comC and blpC genes exists within the species S. pneumoniae, giving rise to at least two different CSPs and four different BIPs (7,11,23,36). The S. pneumoniae strain Rx used in the present study, which is closely related to strain R6 (33), produces CSP-1 consisting of 17 amino acids (NH 2 -EMRLSKFFRDFILQRKK-COOH) and BIP-1 consisting of 27 amino acids (NH 2 -GWWEELLHETILSKFKITKALELPI QL-COOH).Activation of the competent state takes place when the...

show abstract

Development of competence in Streptococcus pneumoniae: pheromone autoinduction and control of quorum sensing by the oligopeptide permease

Cited by 147 publications

References 24 publications

Evidence for Horizontal Transfer of Ssu DAT1I Restriction-Modification Genes to the Streptococcus suis Genome

Evidence for Horizontal Transfer of Ssu DAT1I Restriction-Modification Genes to the Streptococcus suis Genome

Programmed Death in Bacteria

Two Separate Quorum-Sensing Systems Upregulate Transcription of the Same ABC Transporter inStreptococcus pneumoniae

Contact Info

Product

Resources

About