Foreign peptide triggers boost in pneumococcal metabolism and growth
Abstract Background Nonencapsulated Streptococcus pneumoniae bacteria are successful colonizers of the human nasopharynx and often possess genes aliB-like ORF 1 and 2 in place of capsule genes. AliB-like ORF 2 binds peptide FPPQSV, found in Prevotella species, resulting in enhanced colonization. How...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2018-03-01
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| Series: | BMC Microbiology |
| Subjects: | |
| Online Access: | http://link.springer.com/article/10.1186/s12866-018-1167-y |
| _version_ | 1828323451706802176 |
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| author | Fauzy Nasher Sunniva Förster Efe C. Yildirim Denis Grandgirard Stephen L. Leib Manfred Heller Lucy J. Hathaway |
| author_facet | Fauzy Nasher Sunniva Förster Efe C. Yildirim Denis Grandgirard Stephen L. Leib Manfred Heller Lucy J. Hathaway |
| author_sort | Fauzy Nasher |
| collection | DOAJ |
| description | Abstract Background Nonencapsulated Streptococcus pneumoniae bacteria are successful colonizers of the human nasopharynx and often possess genes aliB-like ORF 1 and 2 in place of capsule genes. AliB-like ORF 2 binds peptide FPPQSV, found in Prevotella species, resulting in enhanced colonization. How this response is mediated is so far unknown. Results Here we show that the peptide increases expression of genes involved in release of host carbohydrates, carbohydrate uptake and carbohydrate metabolism. In particular, the peptide increased expression of 1,5-anhydro-D-fructose reductase, a metabolic enzyme of an alternative starch and glycogen degrading pathway found in many organisms, in both transcriptomic and proteomic data. The peptide enhanced pneumococcal growth giving a competitive advantage to a strain with aliB-like ORF 2, over its mutant lacking the gene. Possession of aliB-like ORF 2 did not affect release of inflammatory cytokine CXCL8 from epithelial cells in culture and the nonencapsulated wild type strain was not able to establish disease or inflammation in an infant rat model of meningitis. Conclusions We propose that AliB-like ORF 2 confers an advantage in colonization by enhancing carbohydrate metabolism resulting in a boost in growth. This may explain the widespread presence of aliB-like ORF 2 in the nonencapsulated pneumococcal population in the human nasopharynx. |
| first_indexed | 2024-04-13T18:52:35Z |
| format | Article |
| id | doaj.art-45908a4c815c4e60800c4e3a9ef84caf |
| institution | Directory Open Access Journal |
| issn | 1471-2180 |
| language | English |
| last_indexed | 2024-04-13T18:52:35Z |
| publishDate | 2018-03-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Microbiology |
| spelling | doaj.art-45908a4c815c4e60800c4e3a9ef84caf2022-12-22T02:34:22ZengBMCBMC Microbiology1471-21802018-03-0118111110.1186/s12866-018-1167-yForeign peptide triggers boost in pneumococcal metabolism and growthFauzy Nasher0Sunniva Förster1Efe C. Yildirim2Denis Grandgirard3Stephen L. Leib4Manfred Heller5Lucy J. Hathaway6Institute for Infectious Diseases, Faculty of Medicine, University of BernInstitute for Infectious Diseases, Faculty of Medicine, University of BernInstitute for Infectious Diseases, Faculty of Medicine, University of BernInstitute for Infectious Diseases, Faculty of Medicine, University of BernInstitute for Infectious Diseases, Faculty of Medicine, University of BernProteomics and Mass Spectrometry Core Facility, Department for BioMedical Research, University of BernInstitute for Infectious Diseases, Faculty of Medicine, University of BernAbstract Background Nonencapsulated Streptococcus pneumoniae bacteria are successful colonizers of the human nasopharynx and often possess genes aliB-like ORF 1 and 2 in place of capsule genes. AliB-like ORF 2 binds peptide FPPQSV, found in Prevotella species, resulting in enhanced colonization. How this response is mediated is so far unknown. Results Here we show that the peptide increases expression of genes involved in release of host carbohydrates, carbohydrate uptake and carbohydrate metabolism. In particular, the peptide increased expression of 1,5-anhydro-D-fructose reductase, a metabolic enzyme of an alternative starch and glycogen degrading pathway found in many organisms, in both transcriptomic and proteomic data. The peptide enhanced pneumococcal growth giving a competitive advantage to a strain with aliB-like ORF 2, over its mutant lacking the gene. Possession of aliB-like ORF 2 did not affect release of inflammatory cytokine CXCL8 from epithelial cells in culture and the nonencapsulated wild type strain was not able to establish disease or inflammation in an infant rat model of meningitis. Conclusions We propose that AliB-like ORF 2 confers an advantage in colonization by enhancing carbohydrate metabolism resulting in a boost in growth. This may explain the widespread presence of aliB-like ORF 2 in the nonencapsulated pneumococcal population in the human nasopharynx.http://link.springer.com/article/10.1186/s12866-018-1167-yStreptococcus pneumoniaePeptideNonencapsulatedaliB-like ORF 2TranscriptomeProteome |
| spellingShingle | Fauzy Nasher Sunniva Förster Efe C. Yildirim Denis Grandgirard Stephen L. Leib Manfred Heller Lucy J. Hathaway Foreign peptide triggers boost in pneumococcal metabolism and growth BMC Microbiology Streptococcus pneumoniae Peptide Nonencapsulated aliB-like ORF 2 Transcriptome Proteome |
| title | Foreign peptide triggers boost in pneumococcal metabolism and growth |
| title_full | Foreign peptide triggers boost in pneumococcal metabolism and growth |
| title_fullStr | Foreign peptide triggers boost in pneumococcal metabolism and growth |
| title_full_unstemmed | Foreign peptide triggers boost in pneumococcal metabolism and growth |
| title_short | Foreign peptide triggers boost in pneumococcal metabolism and growth |
| title_sort | foreign peptide triggers boost in pneumococcal metabolism and growth |
| topic | Streptococcus pneumoniae Peptide Nonencapsulated aliB-like ORF 2 Transcriptome Proteome |
| url | http://link.springer.com/article/10.1186/s12866-018-1167-y |
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