The ability of microorganisms to use root-derived metabolites as growth substrates is a key trait for success in the rhizospheric niche. However, few studies describe which specific metabolites are consumed or to what degree microbial strains differ in their substrate consumption patterns. Here, we present a liquid chromatography-mass spectrometry (MS) exometabolomic study of three bacterial strains cultivated using either glucose or Arabidopsis thaliana root extract as the sole carbon source. Two of the strains were previously isolated from field-grown Arabidopsis roots, the other is Escherichia coli, included as a comparison. When cultivated on root extract, a set of 62 MS features were commonly taken up by all three strains, with m/z values matching components of central metabolism (including amino acids and purine or pyrimidine derivatives). Escherichia coli took up very few MS features outside this commonly consumed set, whereas the root-inhabiting strains took up a much larger number of MS features, many with m/z values matching plant-specific metabolites. These measurements define the metabolic niche that each strain potentially occupies in the rhizosphere. Furthermore, we document many MS features released by these strains that could play roles in cross-feeding, antibiosis, or signaling. We present our methodological approach as a foundation for future studies of rhizosphere exometabolomics.