Streptococcus pneumoniae Proteins AmiA, AliA, and AliB Bind Peptides Found in Ribosomal Proteins of Other Bacterial Species

Abstract

The nasopharynx is frequently colonized by both commensal and pathogenic bacteria including Streptococcus pneumoniae (pneumococcus). Pneumococcus is an important pathogen responsible for bacterial meningitis and community acquired pneumonia but is also commonly an asymptomatic colonizer of the nasopharynx. Understanding interactions between microbes may provide insights into pathogenesis. Here, we investigated the ability of the three oligopeptide-binding proteins AmiA, AliA, and AliB of an ATP-binding cassette transporter of pneumococcus to detect short peptides found in other bacterial species. We found three possible peptide ligands for AmiA and four each for AliA and AliB of which two for each protein matched ribosomal proteins of other bacterial species. Using synthetic peptides we confirmed the following binding: AmiA binds peptide AKTIKITQTR, matching 50S ribosomal subunit protein L30, AliA binds peptide FNEMQPIVDRQ, matching 30S ribosomal protein S20, and AliB binds peptide AIQSEKARKHN, matching 30S ribosomal protein S20, without excluding the possibility of binding of the other peptides. These Ami–AliA/AliB peptide ligands are found in multiple species in the class of Gammaproteobacteria which includes common colonizers of the nostrils and nasopharynx. Binding such peptides may enable pneumococcus to detect and respond to neighboring species in its environment and is a potential mechanism for interspecies communication and environmental surveillance.

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

“…Less suppression of growth was seen by AmiA peptide in the ΔAmiA mutant supporting the idea that this is the specific receptor for the peptide (Figure 1E). In contrast, AliA peptide affects the ΔAliA mutant in the same way as it affects the D39 wild type as expected since AliA peptide is known to bind to AmiA receptor (Figure 1F; Nasher et al, 2018b). Unlike the wild type D39 strain, growth of the D39 ΔAliB mutant was reduced by the AliB peptide (Figure 1G).…”

“…We propose that there is interspecies communication between bacteria that live in the human nasopharynx and that detecting other bacterial species allows S. pneumoniae to adapt to its environment. Previously, we reported that S. pneumoniae AmiA, AliA, and AliB lipoproteins of an ABC transporter are able to bind peptides matching ribosomal proteins of other bacteria species including common nasopharynx colonisers (Nasher et al, 2018b). These proteins are encoded by genes of the core pneumococcal genome (Obert et al, 2006) and so are of relevance across the pneumococcal population.…”

“…For the three substrate binding proteins of the Ami-AliA/AliB permease, we have shown recently that AmiA binds peptide AKTIKITQTR, matching an amino acid sequence found in 50S ribosomal subunit protein L30; AliA binds peptide FNEMQPIVDRQ, matching an amino acid sequence found in 30S ribosomal protein S20 and AliB binds peptide AIQSEKARKHN, matching an amino acid sequence found in 30S ribosomal protein S20 (Nasher et al, 2018b). These Ami-AliA/AliB peptide ligands are found in multiple bacterial species in the class of Gammaproteobacteria which includes common colonisers of the nostrils and nasopharynx (Pettigrew et al, 2012; Biesbroek et al, 2014; Mika et al, 2015; Teo et al, 2015).…”

Exploring metal availability in the natural niche of Streptococcus pneumoniae to discover potential vaccine antigens

“…Interestingly, AliA has been shown to be important for survival in vivo and is thought to play a role in bacterial communication by binding oligopeptides derived from other common colonizers. Peptide uptake by pneumococci via AliA has shown to influence the behavior of the bacterium in vitro, including reduced growth, reduced capsule thickness, and increased biofilm formation [11,57,58,77]. It is, therefore, tempting to speculate that in vivo anti-AliA antibodies could hamper the uptake of oligopeptides by AliA and consequently affect pneumococcal persistence in the host.…”

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).…”