Maternal antibodies against the immunoglobulin M-degrading enzyme of Streptococcus suis, IdeSsuis, play an important role in bactericidal immunity in young piglets in the field

Streptococcus suis (S. suis) expresses a specific immunoglobulin M (IgM) protease, designated Ide_Ssuis. Vaccination with recombinant Ide_Ssuis elicits protection against S. suis serotype 2. This study was initiated by the finding that the isogenic deletion mutant Δide_Ssuis shows a hypervirulent phenotype in 4-week-old piglets, presumably in association with maternally derived antibodies against Ide_Ssuis. This prompted us to conduct a field study to test the working hypothesis that maternal αIde_Ssuis IgG antibodies are biologically relevant. Investigations in one herd with autogenous S. suis vaccination pre-farrowing showed a significant correlation of IgG levels against Ide_Ssuis in serum of 2-week-old-piglets and levels in colostrum. These antibody levels declined over the subsequent weeks of life. Levels of IgM binding to S. suis in sera of 2-week-old piglets did not correlate with respective levels in colostrum but with the amount of colostrum taken up. Bactericidal assays with wild type (wt) and ide_Ssuis mutants demonstrated that expression of functional or nonfunctional full-length Ide_Ssuis results in increased killing of S. suis serotype 2 in the blood of 2-week-old piglets. This phenotype disappeared as piglets aged. Linear mixed-effects models confirmed that serum IgG against Ide_Ssuis exerts a significant, time-independent effect on survival of S. suis wt and ∇ide_Ssuis_C195S, expressing a nonfunctional variant of Ide_Ssuis, but not Δide_Ssuis. Furthermore, IgM binding to S. suis wt influenced survival of wt and ∇ide_Ssuis_C195S in a time-dependent manner. This is in line with the concept that αIde_Ssuis IgG are protective through induction of fragment crystallizable (Fc)-mediated opsonophagocytosis rather than neutralization of the IgM protease, at least in suckling piglets.