Proteins harboring intrinsically disordered regions (IDRs) that lack regular secondary or tertiary structure are abundant across three domains of life. Here, using a deep neural network (DNN)-based method we predict IDRs in the extracytoplasmic proteome of Streptococcus mutans , Streptococcus pyogenes and Streptococcus pneumoniae . We identify a subset of the serine/threonine-rich IDRs and demonstrate that they are O -glycosylated with glucose by a GtrB-like glucosyltransferase in S. pyogenes and S. pneumoniae , and N-acetylgalactosamine by a Pgf-dependent mechanism in S. mutans . Loss of glycosylation leads to a defect in biofilm formation under ethanol-stressed conditions in S. mutans . We link this phenotype to a C-terminal IDR of peptidyl-prolyl isomerase PrsA which is protected from proteolytic degradation by O -glycosylation. The IDR length attenuates the efficiency of glycosylation and expression of PrsA. Taken together, our data support a model in which extracytoplasmic IDRs function as dynamic switches of protein homeostasis in streptococci.