Abstract

Background Streptococcus oralis, Streptococcus mitis, and Streptococcus sanguinis are members of the Mitis group of streptococci and agents of oral biofilm, dental plaque and infective endocarditis, disease processes that involve bacteria-bacteria and bacteria-host interactions. Their close relative, the human pathogen S. pneumoniae uses pilus-islet 2 (PI-2)-encoded pili to facilitate adhesion to eukaryotic cells.Methodology/Principal FindingsPI-2 pilus-encoding genetic islets were identified in S. oralis, S. mitis, and S. sanguinis, but were absent from other isolates of these species. The PI-2 islets resembled the genetic organization of the PI-2 islet of S. pneumoniae, but differed in the genes encoding the structural pilus proteins PitA and PitB. Two and three variants of pitA (a pseudogene in S. pneumoniae) and pitB, respectively, were identified that showed ≈20% difference in nucleotide as well as corresponding protein sequence. Species-independent combinations of pitA and pitB variants indicated prior intra- and interspecies horizontal gene transfer events. Polyclonal antisera developed against PitA and PitB of S. oralis type strain ATCC35037 revealed that PI-2 pili in oral streptococci were composed of PitA and PitB. Electronmicrographs showed pilus structures radiating >700 nm from the bacterial surface in the wild type strain, but not in an isogenic PI-2 deletion mutant. Anti-PitB-antiserum only reacted with pili containing the same PitB variant, whereas anti-PitA antiserum was cross-reactive with the other PitA variant. Electronic multilocus sequence analysis revealed that all PI-2-encoding oral streptococci were closely-related and cluster with non-PI-2-encoding S. oralis strains.Conclusions/SignificanceThis is the first identification of PI-2 pili in Mitis group oral streptococci. The findings provide a striking example of intra- and interspecies horizontal gene transfer. The PI-2 pilus diversity provides a possible key to link strain-specific bacterial interactions and/or tissue tropisms with pathogenic traits in the Mitis group streptococci.

Highlights

  • Oral streptococci of the Mitis group streptococci [1,2], such as Streptococcus mitis, Streptococcus oralis, and Streptococcus sanguinis are close relatives of the important human pathogen Streptococcus pneumoniae

  • pilus-islet 2 (PI-2) pilus islets were identified by PCR in S. oralis strain ATCC10557 and strain 34 (both formerly classified as S. sanguis [34,36] (Figure 1)

  • The overall similarity between the PI-2 nucleotide sequences of the seven strains ranged from 87% to 94% identity, and their GC-content was 37.8 to 38.4%, which is lower than the average GC-content of the available genomic sequences of the hosting S. oralis, S. mitis, S. sanguinis strains, and S. sp

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Summary

Introduction

Oral streptococci of the Mitis group streptococci [1,2], such as Streptococcus mitis, Streptococcus oralis, and Streptococcus sanguinis are close relatives of the important human pathogen Streptococcus pneumoniae. Fimbrial extensions on the surface of bacteria have recently been identified in many Gram-positive species, including streptococci [9,10,11,12,13], enterococci [14,15], bacilli [16], lactobacilli [17], and actinomyces [18,19], and they have diverse, and often unresolved roles in environmental interactions or pathogenesis [20] These pili are typically encoded by gene clusters, sometimes called pilus islets [21], that contain in addition the genes required for pilus biosynthesis [22]. Streptococcus oralis, Streptococcus mitis, and Streptococcus sanguinis are members of the Mitis group of streptococci and agents of oral biofilm, dental plaque and infective endocarditis, disease processes that involve bacteriabacteria and bacteria-host interactions Their close relative, the human pathogen S. pneumoniae uses pilus-islet 2 (PI-2)encoded pili to facilitate adhesion to eukaryotic cells

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