Disorder–Order Interplay of a Barnacle Cement Protein Triggered by Interactions with Calcium and Carbonate Ions: A Molecular Dynamics Study

Barnacles strongly adhere to immersed solid substrates using a mixture of cement proteins (CP) that self-assembles into a permanently bonded layer and binds the barnacles’ shells to foreign surfaces. MrCP20 from Megabalanus rosa has been identified as a putative interfacial CP; however, its functional role remains uncertain. Since the barnacle shell is primarily composed of calcite, we carry out molecular dynamics simulations to investigate the molecular interactions between MrCP20 and calcium carbonate (in free ionic form and as calcite surface). We find that MrCP20 sequesters free Ca2+ and CO32– ions on its highly charged surface through disorder–order interplay of the protein and ions. A similar ordering is seen in the protein conformational landscape upon interactions with the calcite surface. Structural examinations indicate that the energetically favorable interactions with calcium carbonate are mediated by charged functional groups that flank the structured regions of MrCP20 and networks of water molecules. In vitro biomineralization experiments and X-ray diffraction indicate that MrCP20 favors the precipitation of the less stable vaterite polymorph of CaCO3. Our study suggests that the barnacles exploit the semi-(dis)ordered nature of acidic MrCP20 to adhere to surfaces like calcite, thereby regulating nucleation, growth, or morphology of the mineral, while simultaneously interacting with other biomolecules in cement.