The human gut microbiota is composed of more than 50% of Bacteroides species whose membranes are enriched in sphingolipids. In particular, Bacteroides fragilis produced glycosphingolipids termed as α-Galactosylceramides (α-GalCerBf) have the ability to activate both mouse and human type I Natural Killer T (NKT) cells. While they share key chemical similarities with the type I NKT cell marker antigen, α-Galactosylceramide (KRN7000), they possess distinctive structural features including short branched acyl chains with the variations in their hydroxyl group positions. Here, using X-ray crystallography, we have determined the crystal structures of four type I NKT TCR-mouse CD1d-lipid ternary complexes revealing a parallel docking mode of the TCR atop the F’-pocket of the antigen presenting molecule CD1d in recognising the presented bacterial sphingolipids. The measured binding affinities between the mouse CD1d presented sphingolipids and NKT TCR were observed to be in nanomolar range. As translation of results from benchside to bedside with KRN7000 has proven challenging, the study of these physiologically relevant α-GalCerBf lipids may open new avenues in designing novel immunomodulatory agents to achieve desired immune outcomes in various clinical conditions. Further, this study sheds light on the better understanding of the existing symbiotic relationship between the microbes producing these endogenous lipids and the host. This manuscript is currently under review in Cell journal.