Foreign peptide triggers boost in pneumococcal metabolism and growth

Abstract

BackgroundNonencapsulated 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.ResultsHere 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.ConclusionsWe 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.Electronic supplementary materialThe online version of this article (10.1186/s12866-018-1167-y) contains supplementary material, which is available to authorized users.

In vivo proteomics identifies the competence regulon and AliB oligopeptide transporter as pathogenic factors in pneumococcal meningitis

“…These strains are associated with colonization and non-invasive diseases including non-bacteremic pneumonia [45, 46]. Consistent with these findings mutants with loss of function of AliC or AliD did not cause pneumococcal meningitis [47].…”

“…AmiA binds peptide AKTIKITQTR, AliA peptide FNEMQPIVDRQ and AliB peptide AIQSEKARKHN. Interestingly these peptides are part of 50S or 30S ribosomal proteins found in species of γ-proteobacteria, which are commensals of the upper respiratory tract [47].…”

Peptide Occurring in Enterobacteriaceae Triggers Streptococcus pneumoniae Cell Death

“…Streptococcus pneumoniae (S. pneumoniae) (pneumococcus) is a common asymptomatic colonizer of the human nasopharynx. The human nasopharynx is an ecosystem that hosts a diverse microbial community and we have previously proposed that pneumococcus senses bacteria in the environment through short peptide fragments derived from these other bacterial species sharing the same niche (Hathaway et al, 2014; Nasher et al, 2018a,b).…”

“…In the presence of competence stimulating peptide (CSP), binding of AliB-like ORF 1 to its ligand increases competence for genetic transformation. In contrast, AliB-like ORF 2 peptide ligand, FPPQSV, is found in proteins of Prevotella species (Hathaway et al, 2014) and binding of AliB-like ORF 2 to its peptide ligand leads to increased carbohydrate metabolism and increased growth (Nasher et al, 2018a).…”

Peptide Ligands of AmiA, AliA, and AliB Proteins Determine Pneumococcal Phenotype

“…One of these permease’s oligopeptide binding proteins, AliB, has also been shown to aid in colonisation of the nasopharynx in a mouse model (Kerr et al, 2004). Previously, it has been shown that peptides found in other bacterial species are recognised by homologs of AliB: AliB-like ORF1 and ORF2 in non-encapsulated S. pneumoniae and that binding of the proteins to their peptide ligands affected pneumococcal phenotype and gene expression (Hathaway et al, 2014; Nasher et al, 2018a).…”