Structural and thermodynamic analyses of a novel β‐1,2‐glucan binding mode in the <scp>ABC</scp> transporter solute‐binding protein Chy400_4166 from <i>Chloroflexus aurantiacus</i>

β-1,2-Glucans are glucose polymers widely distributed in nature and play various physiological roles in the interactions between organisms such as pathogenicity and symbiosis. While various β-1,2-glucan-degrading enzymes have been identified recently, transporters incorporating β-1,2-glucans are still poorly characterized. In this study, we have found a β-1,2-glucan binding protein of ABC transporter from Chloroflexus aurantiacus Y-400-fl, a filamentous anoxygenic phototrophic bacterium. The protein showed a clear affinity for linear β-1,2-glucan in the gel shift assay. Isothermal titration calorimetric analysis revealed high binding affinities for both linear and cyclic β-1,2-glucans, unlike for the barley β-glucan. The recorded binding constants were high for the binding of the ABC transporter to β-1,2-glucans. The observed unfavorable negative entropy change may have resulted from conformational restraints upon complex formation. Complex structures with linear β-1,2-glucan and cyclic β-1,2-glucans with degrees of polymerization of 17-20 were obtained using X-ray crystallography. Ten glucose units, designated A-J from the nonreducing end, were shared among the substrates in the complexes. Unit G is recognized by W74, W308, and D336, which are highly conserved residues within the phylogenetic group Chy400_4166. The substrate-binding mode of Chy400_4166 is completely different from that of the β-1,2-glucooligosaccharide-binding protein from Listeria innocua. The discovery of a new type of β-1,2-glucan-related binding protein has expanded our understanding of the metabolism of β-1,2-glucans.