A quantum biochemistry investigation of the protein–protein interactions for the description of allosteric modulation on biomass-degrading chimera

The worldwide dependence of population on fossil fuels continues to have several harmful implications for the environment. Bioethanol is an excellent option for renewable fuel to replace the current greenhouse gas emitters. In addition, its production by enzymatic route has gained space among the industrial processes because it replaces the traditional acid treatment. Due to its high versatility, the xylanase family is used in this process as an accessory enzyme for degrading the lignocellulosic substrate of biomass. A chimera built by a xylanolytic domain (Xyl) and a xylose-binding protein (XBP) showed an experimentally improved catalytic efficiency and interdomain allosteric modulation after xylose binding. In this context, we performed a quantum biochemistry characterization of the interactions between these domains and dynamic cross-correlation (DCC) analysis after performing molecular dynamics (DM) simulations of the systems in the presence and absence of xylose in the XBP active site. We used the density functional theory (DFT) within the molecular fractionation with the conjugated caps (MFCC) approach to describe the pair energies, and the corresponding energy difference between the chimera domains responsible for the allosteric effect and amino acid DCC to evaluate the interdomain coupling differences between the energy states. The detailed energetic investigation together with the related structural and dynamics counterparts revealed the molecular mechanisms of chimeric improvement of the xylanase activity observed experimentally. This mechanism was correlated with greater stability and high connectivity at the interdomain interface in the xylose bound relative to the free chimera. We identify the contributions of hydrogen bonds, hydrophobic interactions and water–mediated interactions in the interdomain region responsible for stability together with the structural and dynamical elements related to the allosteric effect. Taken together, these observations led to a comprehensive understanding of the chimera's modulatory action that occurs through the formation of a highly connected interface that makes the essential movements related to xylanolytic activity in xylanase correlated to those of the xylose-binding protein.