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Bordetella parapertussis  is a respiratory-disease pathogen producing symptomatology similar to that of pertussis but of underestimated incidence and with no specific vaccine existing. We recently designed a vaccine candidate from  B. parapertussis  outer-membrane vesicles (OMVs) that proved to be safe and protective in a murine-infection model. Based on protection recently reported for the  B. parapertussis  O antigen in aqueous solution, we assessed here whether the  B. parapertussis  O-antigen-containing lipopolysaccharide (BppLPS-O + ) embedded in the membranes, as present in  B. parapertussis -derived OMVs (OMVs(Bpp-LPS-O + )), was the component responsible for that previously observed protection by OMVs. By performing a comparative study with OMVs from a human strain with undetectable O antigen (OMVs(Bpp-LPS-O − )), we demonstrated that the OMVs(Bpp-LPS-O + ), but not the OMVs(Bpp-LPS-O − ), protected mice against sublethal  B. parapertussis  infections. Indeed, the  B. parapertussis  loads were significantly reduced in the lungs of OMVs(Bpp-LPS-O + ) -vaccinated animals, with the CFUs recovered being decreased by 4 log units below those detected in the non-immunized animals or in the animals treated with the OMVs(Bpp-LPS-O − ), ( p  < 0.001). We detected that the OMVs(Bpp-LPS-O + ) induced IgG antibodies against  B. parapertussis  whole-cell lysates, which immunocomponents recognized, among others, the O antigen and accordingly conferred protection against  B. parapertussis  infection, as observed in  in-vivo –passive-transfer experiments. Of interest was that the OMVs(Bpp-LPS-O + ) -generated sera had opsonophagocytic and bactericidal capabilities that were not detected with the OMVs(Bpp-LPS-O − )-induced sera, suggesting that those activities were involved in the clearance of  B. parapertussis . Though stimulation of cultured spleen cells from immunized mice with formulations containing the O antigen resulted in gamma interferon (IFN-γ) and interleukin-17 production, spleen cells from OMVs(Bpp-LPS-O + ) -immunized mice did not significantly contribute to the observed protection against  B. parapertussis  infection. The protective capability of the  B. parapertussis  O antigen was also detected in formulations containing both the OMVs derived from  B. pertussis  and purified BppLPS-O + . This combined formulation protected mice against  B. pertussis  along with  B. parapertussis .

Outer-Membrane-Vesicle–Associated O Antigen, a Crucial Component for Protecting Against Bordetella parapertussis Infection