<p>Attaching and effacing pathogens overcome colonisation resistance by competing with metabolically similar organisms for limited resources. Enterohaemorrhagic <i>E. coli</i> (EHEC) utilises the pathogenicity island-encoded Accessory ʟ-arabinose Uptake (Aau) transporter to effectively colonise the mouse gut, hypothesised to be achieved via an enhanced capacity to scavenge ʟ-arabinose. Aau is regulated exclusively in response to ʟ-arabinose, but it is unclear how this system specifically benefits EHEC in vivo. Here, we show that Aau displays a &gt; 200-fold higher affinity for the monosaccharide <span>D</span>-ribulose, over ʟ-arabinose. EHEC cannot grow on <span>D</span>-ribulose as a sole carbon source and this sugar does not trigger <i>aau</i> transcription. However, Aau effectively transports <span>D</span>-ribulose into the cell only in the presence of ʟ-arabinose, where it feeds into the pentose phosphate pathway, after phosphorylation by the ʟ-ribulokinase AraB, thus providing EHEC a significant fitness advantage. EHEC has therefore evolved a mechanism of hijacking the canonical ʟ-arabinose utilisation machinery to promote <span>D</span>-ribulose utilisation in vivo. Furthermore, <i>Citrobacter rodentium</i> encodes an analogous system that exclusively transports <span>D</span>-ribulose and metabolises it via a dedicated <span>D</span>-ribulokinase. These unique mechanisms of <span>D</span>-ribulose utilisation suggest that convergent evolution has driven the ability of distinct pathogenic species to exploit this nutrient during invasion of the gut niche.</p>