Enteropathogenic Escherichia coli (EPEC), is an important pediatric diarrheal pathogen. It is a typical attaching and effacing (AE) enteric pathogen, which resides in the challenging niche of the host intestine throughout the course of infection. EPEC colonizes this niche in a process that is dependent on a type III secretion system (TTSS), through which protein effectors are translocated into the host. In this niche, EPEC competes for nutrients with both the intestinal epithelial cells (IEC) and the vast enteric microbiota. We therefore investigated whether the attached pathogen can overcome nutrient limitation by a putative mechanism that facilitates extraction of nutrients from the IEC cytoplasm. Our results show that starved EPEC, attached to the host cell, are capable of acquiring amino acids and synthesizing proteins, while non-attached EPEC fail to do so. Furthermore, we found that the non-pathogenic E. coli can extract nutrients from host cell only when the genes of TTSS are supplied in trans, indicating that the TTSS machinery is utilized for nutrient acquisition. Next, we tested for involvement of TTSS components in nutrient acquisition from host by EPEC. Mutational analysis revealed that this phenomenon requires TTSS proteins but the injection activity is dispensable. Strikingly, for nutrient acquisition only a subset of components is required. These proteins form the inner-membrane core-ring of the TTSS, encoded by escRSTUV genes. Hence, we hypothesize that the EPEC EscRSTUV proteins, possibly with additional yet to be defined components form an alternative surface apparatus. We further suggest that this putative apparatus operates to extract nutrients from the infected host cells.