Abstract
ABSTRACTExpression of a capsular polysaccharide is considered a hallmark of most invasive species of bacteria, including Streptococcus pneumoniae, in which the capsule is among the principal virulence factors and is the basis for successful vaccines. Consequently, it was previously assumed that capsule production distinguishes S. pneumoniae from closely related commensals of the mitis group streptococci. Based on antigenic and genetic analyses of 187 mitis group streptococci, including 90 recognized serotypes of S. pneumoniae, we demonstrated capsule production by the Wzy/Wzx pathway in 74% of 66 S. mitis strains and in virtually all tested strains of S. oralis (subspecies oralis, dentisani, and tigurinus) and S. infantis. Additional analyses of genomes of S. cristatus, S. parasanguinis, S. australis, S. sanguinis, S. gordonii, S. anginosus, S. intermedius, and S. constellatus revealed complete capsular biosynthesis (cps) loci in all strains tested. Truncated cps loci were detected in three strains of S. pseudopneumoniae, in 26% of S. mitis strains, and in a single S. oralis strain. The level of sequence identities of cps locus genes confirmed that the structural polymorphism of capsular polysaccharides in S. pneumoniae evolved by import of cps fragments from commensal Streptococcus species, resulting in a mosaic of genes of different origins. The demonstrated antigenic identity of at least eight of the numerous capsular polysaccharide structures expressed by commensal streptococci with recognized serotypes of S. pneumoniae raises concerns about potential misidentifications in addition to important questions concerning the consequences for vaccination and host-parasite relationships both for the commensals and for the pathogen.
Highlights
Expression of a capsular polysaccharide is considered a hallmark of most invasive species of bacteria, including Streptococcus pneumoniae, in which the capsule is among the principal virulence factors and is the basis for successful vaccines
None of the antisera reacted with group O antigen, i.e., the common cell wall polysaccharide antigen shared by S. mitis and S. pneumoniae [16], which is known as C-polysaccharide
In invasive strains of S. pneumoniae, the capsule is among the principal virulence factors, as demonstrated by results of in vitro experiments, experimental infections, and the success of the current conjugate vaccines based on selected serotypes of capsular polysaccharides
Summary
Expression of a capsular polysaccharide is considered a hallmark of most invasive species of bacteria, including Streptococcus pneumoniae, in which the capsule is among the principal virulence factors and is the basis for successful vaccines. The demonstrated antigenic identity of at least eight of the numerous capsular polysaccharide structures expressed by commensal streptococci with recognized serotypes of S. pneumoniae raises concerns about potential misidentifications in addition to important questions concerning the consequences for vaccination and host-parasite relationships both for the commensals and for the pathogen. Other mitis group streptococci, including Streptococcus oralis, Streptococcus sanguinis, Streptococcus gordonii, and Streptococcus mitis, may produce several extracellular polysaccharides, including simple glucans that serve as nutritional storage and matrix in biofilms and more structurally complex polysaccharides [13,14,15,16,17] Some of the latter were shown to function as ligands in pilus-mediated interspecies interactions during oral biofilm formation and have been referred to as coaggregation receptor polysaccharides (CRPs) [17, 18]. Systematic studies of other mitis group species have not been performed [10, 18, 27]
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