Streptococcus pneumoniaedetects and responds to foreign bacterial peptide fragments in its environment

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.

Capsular Polysaccharide Expression in CommensalStreptococcusSpecies: Genetic and Antigenic Similarities to Streptococcus pneumoniae

“…S1) but not in S. anginosus , S. intermedius , S. constellatus , S. cristatus , S. parasanguinis , S. australis , S. sanguinis , and S. gordonii . Orthologous genes at the start of the cps locus were previously demonstrated in nonencapsulated strains of S. pneumoniae (40, 42, 44). Remarkably, the cps locus of none of the encapsulated pneumococci includes functional aliB -like genes although there are traces of their prior existence in the form of small fragments in most serotypes and almost full-length pseudogenes in strains of serotypes 25A, 25F, and 38 (10, 43) and in S. pseudopneumoniae (Fig.…”

“…This gene is similar to aliA immediately downstream of the cps locus. It has been suggested that this group of proteins are involved in substrate recognition (44, 45) and may not participate directly in the polysaccharide synthesis. Seven other genes of the SK137 cps locus are common to the Wzy-dependent capsular polysaccharide biosynthesis pathway.…”

“…The pressure that eliminated the genes in encapsulated pneumococci but not in their noninvasive counterparts (i.e., nonencapsulated pneumococci and the most closely related species S. mitis , S. oralis , and S. infantis ) is unknown, but might be related to their parallel adaptation to either pathogenic or mutualistic lifestyles (26). Claverys et al (45) and Hathaway et al (44) reported that AliA and AliB-like proteins are involved in sensing environmental conditions by their ability to detect and respond to foreign bacterial peptide fragments in their environment. In this context, their proximity to capsular biosynthesis genes and their potential regulatory effects in commensal streptococci are of obvious interest.…”

Streptococcus pneumoniae Colonization Disrupts the Microbial Community within the Upper Respiratory Tract of Aging Mice

“…Inter-and intraspecies competition between S. pneumoniae and members of the upper respiratory tract microbiome contribute to the ability of S. pneumoniae to establish colonization, the ability of the host to mount a robust antibacterial response, and the expression of virulence factors required to establish disease (47)(48)(49)(50)(51). For example, by sensing peptides released by neighboring bacterial species, S. pneumoniae stops replication, initiates a stress response (including the induction of competence), and becomes more adept at maintaining pneumococcal colonization in mouse models (52). Many clinical studies in children demonstrate that pneumococcal carriage is positively associated with Haemophilus influenzae carriage but negatively associated with the carriage of Staphylococcus aureus (17,23).…”

Composition and immunological significance of the upper respiratory tract microbiota

“…In vitro studies have also suggested different bacteria can support or hinder S. pneumoniae growth. S. pneumoniae has the ability to respond to peptides from nasopharyngeal bacteria, including Prevotella species, which activate transcription of important colonization factors . In contrast, Corynebacterium species seem to impair the persistence of S. pneumoniae .…”