Theoretical Study Of Nanoscale Water Film On Carboxyl-terminated Self-assembled Monolayers

As early in the 16 th century, it was recognized that water is essential to the life. The concept of “biological water” was formally proposed in literature in 1997, and the water molecules enclosed within the solvation shell present in the immediate vicinity of the biomolecule was termed as "biological water". Exploring the role of biological water at a molecular level in biological process can be traced back to the 1950 s when Watson and Crick stated that hydration is crucially important for the conformation of nucleic acids. Over the past 60 years, there is increasing experimental and theoretical evidence that solvation water is not a passive spectator in biomolecular processes, but plays an active role in the structural formation, stability and function of proteins, nucleic acids and membranes. Gradually, since it is found that the dynamics of the protein and solvent are mutually coupled, the molecular properties of water and their manifestation in unique physical and chemical characteristics are thought to occupy central roles. Hence, the conceptual boundary of what we view as “functional water” has expanded dramatically, and at the same time the physical boundaries we perceive between water and its biomolecular partners are dissolving. The concept of biological water is gradually evolving into a distinct species which itself is able to carry the biological functionalities. However, in July 2015, Pavel Jungwirth pointed out that “cellular ‘vicinal water’ carrying biological function” might be a hypothetical state for the biological water item, till now, there is no direct evidence that biological water is decisive for protein functions. He thus proposed that the term biological water should be dropped in the studying of water in biology. Whether water on surface of biomolecules carries biological functions is considered to be one of the key fundamental problems in biophysics, and is worthy of further study.Due to the complexity of biological systems, biomimetic structures such as self-assembled monolayers(SAMs) are preferred in the understanding of biological and biochemical processes as well as the behavior and property of water on biomolecules. However, even after 26 years of study, the two-dimensional monolayer with biomimetic structural properties formed by the self-assembly of carboxyl-terminated alkyl chains(hereinafter referred to as COOH-SAMs) continue to present puzzling observations. Experimental values of contact angles of water droplets on COOH-SAMs collected from forty literatures have ranged from 0° to 50°. Although COOH-SAMs were found to have higher water desorption energy than hydroxyl-terminated SAMs(OH-SAMs) and amide-terminated SAMs(CONH2-SAMs) at very low coverage of water in temperature-programmed desorption experiments, Raman spectral data revealed even less stability of the nanoscale interfacial water on COOH-SAM than that on OH-SAM. Moreover, COOH-SAM was found to present abnormal coverage-dependent kinetics of water desorption. Recently, James et al. reported the presence of nanoscale water droplets on top of a continuous few-angstrom-thin water layer on COOH-SAM by using X-ray, neutron reflectometry, and atomic force microscopy(AFM) methods. The physical nature behind these seemingly contradictory observations of the behavior of water on COOH-SAM is still an unsolved mystery.By combining molecular dynamics simulations and quantum mechanics calculations, we have studied the behavior of water on COOH-SAM. We have found that water molecules can be embedded into the COOH matrix on COOH-SAMs with appropriate packing densities to form embedded-water-COOH composite structures. The embedded water together with COOH groups maintain an integrated H-bond network within the composite structure, resulting in reduced H-bond formation between the composite structure and water molecules above the composite structure, which enhances the surface hydrophobicity of COOH-SAM. Our quantum mechanics calculations show that “water is active” to participate in the arrangement of the composite structure, meanwhile, the stable anhydrous COOH matrix falls into different conformations. Our finding provides a molecular-level understanding of how water becomes an active participant in the formation of the fine structure of COOH-SAM, and stabilizes the COOH structure to form the embedded-water–COOH composite structure, which affected the various possible processes related to the COOH-SAMs. Considering the fact that the COOH groups are the main functional groups of amino acids and are pervasive in nature, our study has implication for the understanding of the functionality of water on surface of biomolecules. In fact, the coexistence of water droplets and thin water films has been observed on a membrane formed with a BSA-Na2CO3(BSA, bovine serum albumin) mixture, we think that the ultrathin water layer they observed corresponds to the embedded water in the composite structure. This indicates that the composite structures may also exist on many other surfaces with hydrophilic groups, including surfaces on biomolecules.Our finding of the embedded water and the composite structure with an integrated hydrogen bonding network inside provides a molecular-level understanding of underlying physics of the behavior of water on COOH-SAM, and gives an explanation for all the above puzzling experimental observations. The formation of the embedded-water–COOH composite structure in which water molecules are embedded into the COOH matrix on COOH-SAMs explains both the abnormal increase of water desorption energy on COOH-SAM when water coverage decreasing even down to 4% and the decreased stabilization of interfacial water on top of the composite structure on COOH-SAM as compared to that on OH-SAM. The relevant contact angles, along with the related stability of the composite structure, were found to exhibit two states, at either ~0° or ~35° in our simulations. This outcome compares favorably to the experimental measurements of contact angles collected from forty literatures. Meanwhile, the formation of the composite structures together with water droplets above the composite structures we observed is also consistent with the experimental observation of “nanoscale water droplets on top of a continuous few-angstrom-thin water layer on COOH-SAM”. We think that the thin water layer they observed corresponds to the embedded water in the composite structure. Our findings provide a molecular-level understanding of water on surfaces(including surfaces on biomolecules) with hydrophilic functional groups, offering a guide for various relevant applications and may provide new insights into understanding the behavior of water on biological macromolecules.