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Streptococcus pneumoniae detects and responds to foreign bacterial peptide fragments in its environment.

Hathaway LJ, Bättig P, Reber S, Rotzetter JU, Aebi S, Hauser C, Heller M, Kadioglu A, Mühlemann K - Open Biol (2014)

Bottom Line: AliB-like ORF 1 binds specifically peptide SETTFGRDFN, matching 50S ribosomal subunit protein L4 of Enterobacteriaceae, and facilitates upregulation of competence for genetic transformation.We found that AliB-like ORF 2 mediates the early phase of nasopharyngeal colonization in vivo.These findings reveal a completely new concept of pneumococcal interspecies communication which may have implications for communication between other bacterial species and for future interventional therapeutics.

View Article: PubMed Central - PubMed

Affiliation: Institute for Infectious Diseases, University of Bern, Bern, Switzerland.

ABSTRACT
Streptococcus pneumoniae is an important cause of bacterial meningitis and pneumonia but usually colonizes the human nasopharynx harmlessly. As this niche is simultaneously populated by other bacterial species, we looked for a role and pathway of communication between pneumococci and other species. This paper shows that two proteins of non-encapsulated S. pneumoniae, AliB-like ORF 1 and ORF 2, bind specifically to peptides matching other species resulting in changes in the pneumococci. AliB-like ORF 1 binds specifically peptide SETTFGRDFN, matching 50S ribosomal subunit protein L4 of Enterobacteriaceae, and facilitates upregulation of competence for genetic transformation. AliB-like ORF 2 binds specifically peptides containing sequence FPPQS, matching proteins of Prevotella species common in healthy human nasopharyngeal microbiota. We found that AliB-like ORF 2 mediates the early phase of nasopharyngeal colonization in vivo. The ability of S. pneumoniae to bind and respond to peptides of other bacterial species occupying the same host niche may play a key role in adaptation to its environment and in interspecies communication. These findings reveal a completely new concept of pneumococcal interspecies communication which may have implications for communication between other bacterial species and for future interventional therapeutics.

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Colonization of the nasopharynx of female MF1 mice. Quantification of bacterial load in the nasopharynx at different timepoints post-inoculation was determined by plating out dilutions of nasopharyngeal tissue homogenate and counting the number of colony-forming units for the wild-type strain 110.58 (solid lines with circles), its mutant lacking the aliB-like ORFs (ΔORF 1 ± 2) (dashed lines with squares), ΔORF 1 (solid line with triangles) and ΔORF 2 (dotted lines with inverted triangles). All data derive from five mice per timepoint per strain tested. Data are expressed as mean log10 cfu/ml nasopharyngeal tissue ± s.e.m.
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RSOB130224F6: Colonization of the nasopharynx of female MF1 mice. Quantification of bacterial load in the nasopharynx at different timepoints post-inoculation was determined by plating out dilutions of nasopharyngeal tissue homogenate and counting the number of colony-forming units for the wild-type strain 110.58 (solid lines with circles), its mutant lacking the aliB-like ORFs (ΔORF 1 ± 2) (dashed lines with squares), ΔORF 1 (solid line with triangles) and ΔORF 2 (dotted lines with inverted triangles). All data derive from five mice per timepoint per strain tested. Data are expressed as mean log10 cfu/ml nasopharyngeal tissue ± s.e.m.

Mentions: AliB-like ORF 2 protein bound ligands that matched peptides of the nasopharyngeal commensal species Prevotella, a frequent component of the human nasopharyngeal microbiota. When we compared adherence of wild-type strain 110.58 and mutant ΔORF 1 + 2 to Detroit 562 human nasopharyngeal epithelial cells we found a slightly (non-significant, p = 0.13) greater adherence for the wild-type strain (figure 5), and so we speculated that the phenotype related to ORF 2 may be enhanced colonization in vivo. We measured colonization of the mouse nasopharynx for wild-type strain 110.58 and its ORF 1 and ORF 2 mutants. At 20 min post-inoculation, there was no difference in nasopharyngeal colonization between any of the strains; however at 24 and 48 h, there was significantly (p < 0.05) less colonization by the ΔORF 1 + 2 and ΔORF 2 mutants than the wild-type strain 110.58 (figure 6). By day 7, the differences had disappeared. There was no significant difference in colonization between the wild-type strain and ΔORF 1.Figure 5.


Streptococcus pneumoniae detects and responds to foreign bacterial peptide fragments in its environment.

Hathaway LJ, Bättig P, Reber S, Rotzetter JU, Aebi S, Hauser C, Heller M, Kadioglu A, Mühlemann K - Open Biol (2014)

Colonization of the nasopharynx of female MF1 mice. Quantification of bacterial load in the nasopharynx at different timepoints post-inoculation was determined by plating out dilutions of nasopharyngeal tissue homogenate and counting the number of colony-forming units for the wild-type strain 110.58 (solid lines with circles), its mutant lacking the aliB-like ORFs (ΔORF 1 ± 2) (dashed lines with squares), ΔORF 1 (solid line with triangles) and ΔORF 2 (dotted lines with inverted triangles). All data derive from five mice per timepoint per strain tested. Data are expressed as mean log10 cfu/ml nasopharyngeal tissue ± s.e.m.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4043112&req=5

RSOB130224F6: Colonization of the nasopharynx of female MF1 mice. Quantification of bacterial load in the nasopharynx at different timepoints post-inoculation was determined by plating out dilutions of nasopharyngeal tissue homogenate and counting the number of colony-forming units for the wild-type strain 110.58 (solid lines with circles), its mutant lacking the aliB-like ORFs (ΔORF 1 ± 2) (dashed lines with squares), ΔORF 1 (solid line with triangles) and ΔORF 2 (dotted lines with inverted triangles). All data derive from five mice per timepoint per strain tested. Data are expressed as mean log10 cfu/ml nasopharyngeal tissue ± s.e.m.
Mentions: AliB-like ORF 2 protein bound ligands that matched peptides of the nasopharyngeal commensal species Prevotella, a frequent component of the human nasopharyngeal microbiota. When we compared adherence of wild-type strain 110.58 and mutant ΔORF 1 + 2 to Detroit 562 human nasopharyngeal epithelial cells we found a slightly (non-significant, p = 0.13) greater adherence for the wild-type strain (figure 5), and so we speculated that the phenotype related to ORF 2 may be enhanced colonization in vivo. We measured colonization of the mouse nasopharynx for wild-type strain 110.58 and its ORF 1 and ORF 2 mutants. At 20 min post-inoculation, there was no difference in nasopharyngeal colonization between any of the strains; however at 24 and 48 h, there was significantly (p < 0.05) less colonization by the ΔORF 1 + 2 and ΔORF 2 mutants than the wild-type strain 110.58 (figure 6). By day 7, the differences had disappeared. There was no significant difference in colonization between the wild-type strain and ΔORF 1.Figure 5.

Bottom Line: AliB-like ORF 1 binds specifically peptide SETTFGRDFN, matching 50S ribosomal subunit protein L4 of Enterobacteriaceae, and facilitates upregulation of competence for genetic transformation.We found that AliB-like ORF 2 mediates the early phase of nasopharyngeal colonization in vivo.These findings reveal a completely new concept of pneumococcal interspecies communication which may have implications for communication between other bacterial species and for future interventional therapeutics.

View Article: PubMed Central - PubMed

Affiliation: Institute for Infectious Diseases, University of Bern, Bern, Switzerland.

ABSTRACT
Streptococcus pneumoniae is an important cause of bacterial meningitis and pneumonia but usually colonizes the human nasopharynx harmlessly. As this niche is simultaneously populated by other bacterial species, we looked for a role and pathway of communication between pneumococci and other species. This paper shows that two proteins of non-encapsulated S. pneumoniae, AliB-like ORF 1 and ORF 2, bind specifically to peptides matching other species resulting in changes in the pneumococci. AliB-like ORF 1 binds specifically peptide SETTFGRDFN, matching 50S ribosomal subunit protein L4 of Enterobacteriaceae, and facilitates upregulation of competence for genetic transformation. AliB-like ORF 2 binds specifically peptides containing sequence FPPQS, matching proteins of Prevotella species common in healthy human nasopharyngeal microbiota. We found that AliB-like ORF 2 mediates the early phase of nasopharyngeal colonization in vivo. The ability of S. pneumoniae to bind and respond to peptides of other bacterial species occupying the same host niche may play a key role in adaptation to its environment and in interspecies communication. These findings reveal a completely new concept of pneumococcal interspecies communication which may have implications for communication between other bacterial species and for future interventional therapeutics.

Show MeSH
Related in: MedlinePlus