Cell walls of pathogenic and acidophilic bacteria, such as Mycobacterium tuberculosis and Mycobacterium leprae, comprise lipoarabinomannan and arabinogalactan, which are composed of D-arabinose, the enantiomer of the typical l-arabinose found in plants. Their unusual glycan structures serve to immune-evasive of pathogenic mycobacteria. In this study, we identified four enzymes (two GHxxx endo-d-arabinanases, GH172 exo-α-D-arabinofuranosidase, and GH116 exo-β-D-arabinofuranosidase) from Microbacterium arabinogalactanolyticum that degrade the D-arabinan core structure of lipoarabinomannan and arabinogalactan. These enzymes completely degraded the complex glycans in a concerted manner. Furthermore, based on biochemical characterization using synthetic substrates and X-ray crystallography, we revealed the substrate recognition and anomer-retaining hydrolytic reaction mechanisms of the α- and β-D-arabinofuranosidic bonds in endo- and exo-mode reactions.