Abstract
Most isolates of Streptococcus pneumoniae are mixed populations of transparent (T) and opaque (O) colony phenotypes. Differences in the production of capsular polysaccharide (CPS) between O and T variants were accentuated by changes in the environmental concentration of oxygen. O variants demonstrated a 5.2- to 10.6-fold increase in amounts of CPS under anaerobic compared to atmospheric growth conditions, while CPS production remained low under all conditions for T variants. Increased amounts of CPS in O compared to T pneumococci were associated with increased expression of cps-encoded proteins. The inhibitory effect of oxygen on expression of CPS in O variants correlated with decreased tyrosine phosphorylation of CpsD, a tyrosine kinase and regulator of CPS synthesis. Modulation of CpsD expression and its activity by tyrosine phosphorylation may allow the pneumococcus to adapt to the requirements of both colonization, where decreased CPS allows for adherence, and bacteremia, where increased CPS may be required to escape from opsonic clearance. In patients with invasive infection, paired isolates from the same patient were shown to have predominantly a T colony phenotype without phosphotyrosine on CpsD when cultured from the nasopharynx, and an O phenotype that phosphorylates CpsD in response to oxygen when cultured from the blood. Differences in the availability of oxygen, therefore, may be a key factor in allowing for the selection of distinct phenotypes in these two host environments.
Highlights
Streptococcus pneumoniae colonizes the mucosal surface of the human nasopharynx
Pathogens, including Haemophilus influenzae, Neisseria meningitidis, and Streptococcus pyogenes and Streptococcus agalactiae, have led to an appreciation that the amounts of capsular polysaccharide (CPS) must be varied at different stages in the pathogenesis of invasive infection to allow both for adhesive interactions with host cells and for resistance to humoral clearance mechanisms [7, 10, 15, 28, 29, 31]
These observations suggest that the pneumococcus varies between a form with cell surface characteristics optimized for adherence and carriage (T pneumococci) and a form that adheres poorly but is better adapted for survival during inflammation or invasive infection, when the amounts of antibody, complement, and phagocytic cells might otherwise limit the viability of the organism (O pneumococci)
Summary
Streptococcus pneumoniae (the pneumococcus) colonizes the mucosal surface of the human nasopharynx. During carriage in an infant rat model, there is a selection for variants of the T phenotype, which expresses increased amounts of these adhesins and diminished quantities of adherence-inhibiting CPS [38] Taken together, these observations suggest that the pneumococcus varies between a form with cell surface characteristics optimized for adherence and carriage (T pneumococci) and a form that adheres poorly but is better adapted for survival during inflammation or invasive infection, when the amounts of antibody, complement, and phagocytic cells might otherwise limit the viability of the organism (O pneumococci). Phenotypic differences in clinical isolates, support the concept that different host environments select for distinct subpopulations of pneumococci in natural infection
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