Type 1 fimbria, the short hair-like appendage assembled on the bacterial surface, plays a pivotal role in adhesion and invasion in . The type III secretion system (T3SS), another bacterial surface appendage, facilitates 's replication by delivering effectors into host cells. Our previous research demonstrated that T3SS protein EseJ inhibits adhesion and invasion of by suppressing type 1 fimbria. However, how EseJ suppresses type 1 fimbria remains elusive. In this study, a -like operator (nt -245 to -1 of ) upstream of type 1 fimbrial operon in was identified, and EseJ inhibits type 1 fimbria through the -like operator. Moreover, through DNA pull-down and electrophoretic mobility shift assay, an AraC-type T3SS regulator, EsrC, was screened and verified to bind to nt -145 to -126 and nt -50 to -1 of , suppressing type 1 fimbria. EseJ is almost abolished upon the depletion of EsrC. EsrC and EseJ impede type 1 fimbria expression. Intriguingly, nutrition and microbiota-derived indole activate type 1 fimbria through downregulating T3SS, alleviating EsrC or EseJ's inhibitory effect on -like operator of type 1 fimbrial operon. By this study, it is revealed that upon entering the gastrointestinal tract, rich nutrients and indole downregulate T3SS and thereof upregulate type 1 fimbria, stimulating efficient adhesion and invasion; upon being internalized into epithelium, the limit in indole and nutrition switches on T3SS and thereof switches off type 1 fimbria, facilitating effector delivery to guarantee 's survival/replication .IMPORTANCEIn this work, we identified the -like operator of type 1 fimbrial operon in , which was suppressed by the repressors-T3SS protein EseJ and EsrC. We unveiled that upregulates type 1 fimbria upon sensing rich nutrition and the microbiota-derived indole, thereof promoting the adhesion of . The increase of indole and nutrition promotes type 1 fimbria by downregulating T3SS. The decrease in EseJ and EsrC alleviates their suppression on type 1 fimbria, and .