Evolution of Cariogenic Character in Streptococcus mutans: Horizontal Transmission of Glycosyl Hydrolase Family 70 Genes

Hoshino, T.; Fujiwara, Taku; Kawabata, Shigetada

doi:10.1038/srep00518

Cited by 41 publications

(44 citation statements)

References 33 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…Hoshino et al [39] reported the evolution of the cariogenic characteristics of Streptococcus mutans using glucosyltransferase. In that study, a middle catalytic domain (residues 400-900) instead of the 1500-amino acid full-length sequence of glucosyltransferase was used for the alignment, because the rest of the sequence varied enormously among species.…”

Section: Discussionmentioning

confidence: 99%

Discrimination based on Gly and Arg/Ser at position 673 between dipeptidyl-peptidase (DPP) 7 and DPP11, widely distributed DPPs in pathogenic and environmental gram-negative bacteria

et al. 2013

Self Cite

View full text Add to dashboard Cite

Porphyromonas gingivalis, an asaccharolytic gram-negative rod-shaped bacterium, expresses the novel Asp/Glu-specific dipeptidyl-peptidase (DPP) 11 (Ohara-Nemoto, Y. et al., (2011) J. Biol. Chem. 286, 38115-38127), which has been categorized as a member of the S46/DPP7 family that is preferential for hydrophobic residues at the P1 position. From that finding, 129 gene products constituting five clusters from the phylum Bacteroidetes have been newly annotated to either DPP7 or DPP11, whereas the remaining 135 members, mainly from the largest phylum Proteobacteria, have yet to be assigned. In this study, the substrate specificities of the five clusters and an unassigned group were determined with recombinant DPPs from typical species, i.e., P. gingivalis, Capnocytophaga gingivalis, Flavobacterium psychrophilum, Bacteroides fragilis, Bacteroides vulgatus, and Shewanella putrefaciens.Consequently, clusters 1, 3, and 5 were found to be DPP7 with rather broad substrate specificity, and clusters 2 and 4 were DPP11. An unassigned S. putrefaciens DPP carrying Ser 673 exhibited Asp/Glu-specificity more preferable to Glu, in contrast to the Asp preference of DPP11 with Arg 673 from Bacteroidetes species. Mutagenesis experiments revealed that Arg 673 /Ser 673 were indispensable for the Asp/Glu-specificity of DPP11, and that the broad specificity of DPP7 was mediated by Gly 673 . Taken together with the distribution of the two genes, all 264 members of the S46 family could be attributed to either DPP7 or DPP11 by an amino acid at position 673. A more compelling phylogenic tree based on the conserved C-terminal region suggested two gene duplication events in the phylum Bacteroidetes, one causing the development of DPP7 and DPP11 with altered substrate specificities, and the other producing an additional DPP7 in the genus Bacteroides.

show abstract

Section: Discussionmentioning

confidence: 99%

Discrimination based on Gly and Arg/Ser at position 673 between dipeptidyl-peptidase (DPP) 7 and DPP11, widely distributed DPPs in pathogenic and environmental gram-negative bacteria

et al. 2013

Self Cite

View full text Add to dashboard Cite

show abstract

“…In contrast, the four S. criceti strains studied possessed dblA and dblB genes, suggesting that the dblA and dblB regions are conserved in S. criceti. Furthermore, tandemly arranged genes, such as gtfB and gtfC in S. mutans, are considered to have replicated by tandem duplication (Hoshino et al, 2012). Regarding the dblA and dblB genes, orthologous genes were found in S. sobrinus, S. downei and S. criceti (Kojima et al, 2012).…”

mentioning

confidence: 98%

Molecular characterization of the dextran-binding lectin B gene dblB of Streptococcus criceti in Streptococcus mutans strain GS-5 with mutations in both gbpC and spaP genes

2014

View full text Add to dashboard Cite

Streptococcus mutans, a cariogenic agent, has a glucan-binding protein gene, gbpC, and S. criceti possesses four gbpC homologs, including dblA and dblB, as does S. sobrinus. The S. criceti dblB gene encodes a 1,717-amino-acid protein having two repetitive alanine-rich and proline-rich regions and an LPXTG motif, which is recognized by the sortase SrtA, near the C terminus. Reverse transcription-PCR analysis indicated no cotranscription of the dblA and dblB genes of S. criceti. As we could not obtain a dblB mutant of S. criceti, the dblB gene was characterized in S. mutans strain GS-5, which has genetic mutations in both gbpC and spaP genes and shows an inability to agglutinate triggered by dextran. A dextran-induced agglutination assay showed that S. mutans cells carrying dblB agglutinated in the presence of dextran. A hydrophobicity assay showed that the cells containing dblB were hydrophobic. A biofilm formation assay showed that the dblB gene was associated with biofilm formation by cells cultivated in brain heart infusion broth supplemented with glucose and maltose, but not sucrose. Nucleotide sequence analysis of the S. criceti strains studied revealed a frameshift mutation in the srtA gene encoding sortase, but intact dblA and dblB genes were found in dextran-induced agglutination-negative strains, whereas intact dblA, dblB and srtA genes were found in dextran-induced agglutination-positive strains. These results suggest the cell-surface localization of dblA and dblB gene products by SrtA and the responsibility of dblB for dextran-induced agglutination, cellsurface hydrophobicity and biofilm formation in S. criceti.

show abstract

“…Likewise, evolutionary genomic analysis of over 50 sequenced isolates of S. mutans from around the globe led to the conclusion that there was a large expansion in the population and genetic complexity of this species some 5,000 to 10,000 years ago (17). Phylogenetic analyses have also pointed to a strong influence on the genomic composition of S. mutans associated with widespread consumption of refined sucrose during the industrial revolution (18). In particular, it has been suggested that many of the genes responsible for enhanced cariogenicity in S. mutans were introduced into this bacterium via horizontal gene transfer, including the three glucosyltransferase genes, which encode enzymes that produce biofilmpromoting, adhesive glucans (17)(18)(19).…”

mentioning

confidence: 99%

“…Phylogenetic analyses have also pointed to a strong influence on the genomic composition of S. mutans associated with widespread consumption of refined sucrose during the industrial revolution (18). In particular, it has been suggested that many of the genes responsible for enhanced cariogenicity in S. mutans were introduced into this bacterium via horizontal gene transfer, including the three glucosyltransferase genes, which encode enzymes that produce biofilmpromoting, adhesive glucans (17)(18)(19). Therefore, characterization of the effects of sucrose on gene expression and physiology of S. mutans is critical not only to gain a fuller appreciation of how this carbohydrate enhances the cariogenicity of the organism but also to gain insights into niche adaptations that occurred during coevolution with a human host, which can be highly specific to S. mutans and thus lead to new therapeutic or preventive strategies.…”

mentioning

confidence: 99%

Sucrose- and Fructose-Specific Effects on the Transcriptome of Streptococcus mutans, as Determined by RNA Sequencing

Zeng

Burne

2016

Appl Environ Microbiol

View full text Add to dashboard Cite

Recent genome-scale studies have begun to establish the scope and magnitude of the impacts of carbohydrate source and availability on the regulation of gene expression in bacteria. The effects of sugars on gene expression are particularly profound in a group of lactic acid bacteria that rely almost entirely on their saccharolytic activities for energy production and growth. For Streptococcus mutans, the major etiologic agent of human dental caries, sucrose is the carbohydrate that contributes in the most significant manner to establishment, persistence, and virulence of the organism. However, because this organism produces multiple extracellular sucrolytic enzymes that can release hexoses from sucrose, it has not been possible to study the specific effects of sucrose transport and metabolism on gene expression in the absence of carbohydrates that by themselves can elicit catabolite repression and induce expression of multiple genes. By employing RNA deep-sequencing (RNA-Seq) technology and mutants that lacked particular sucrose-metabolizing enzymes, we compared the transcriptomes of S. mutans bacteria growing on glucose, fructose, or sucrose as the sole carbohydrate source. The results provide a variety of new insights into the impact of sucrose transport and metabolism by S. mutans, including the likely expulsion of fructose after sucrose internalization and hydrolysis, and identify a set of genes that are differentially regulated by sucrose versus fructose. The findings significantly enhance our understanding of the genetics and physiology of this cariogenic pathogen.N early all isolates of the primary etiologic agent of human dental caries, Streptococcus mutans, encode at least five secreted enzymes that act on sucrose in the extracellular environment, including three glucosyltransferases (GtfB, GtfC, and GtfD) that incorporate the glucose moiety of sucrose into high-molecular-mass ␣1,3-and ␣1,6-linked homopolymers of glucose that promote biofilm formation (1, 2); a fructosyltransferase (Ftf) that catalyzes the incorporation of fructose into ␤2,1-and ␤2,6-linked homopolymers of fructose (fructans) that serve as extracellular stores of carbohydrate within the biofilm matrix (3, 4); and a fructan hydrolase (FruA) that releases fructose from fructans, sucrose, and other ␤-fructosides (4, 5). While these exoenzymes contribute significantly to the virulence of S. mutans, most of the sucrose presented to S. mutans is rapidly internalized by a highaffinity, high-capacity sugar-phosphotransferase system (PTS) (6,7). A single open reading frame (ORF), scrA, encodes the enzyme II permease of a sucrose-specific PTS, which internalizes and concomitantly phosphorylates sucrose. Transcribed divergently from scrA are two genes that encode a sucrose-6-PO 4 (S-6-P) hydrolase (scrB), which cleaves S-6-P into glucose-6-PO 4 (G-6-P) and fructose, and a transcriptional regulator (scrR) that represses the expression of both scrA and scrB (6,8,9). In addition, the multiplesugar metabolism (msm) ABC transporter and a trehalose-PTS e...

show abstract

Evolution of Cariogenic Character in Streptococcus mutans: Horizontal Transmission of Glycosyl Hydrolase Family 70 Genes

Cited by 41 publications

References 33 publications

Discrimination based on Gly and Arg/Ser at position 673 between dipeptidyl-peptidase (DPP) 7 and DPP11, widely distributed DPPs in pathogenic and environmental gram-negative bacteria

Discrimination based on Gly and Arg/Ser at position 673 between dipeptidyl-peptidase (DPP) 7 and DPP11, widely distributed DPPs in pathogenic and environmental gram-negative bacteria

Molecular characterization of the dextran-binding lectin B gene <i>dblB</i> of <i>Streptococcus criceti</i> in <i>Streptococcus mutans</i> strain GS-5 with mutations in both <i>gbpC</i> and <i>spaP</i> genes

Sucrose- and Fructose-Specific Effects on the Transcriptome of Streptococcus mutans, as Determined by RNA Sequencing

Contact Info

Product

Resources

About