Theoretical Study of Chlorophyll a Hydrates Formation in Aqueous Organic Solvents

Abstract

A theoretical analysis of chlorophyll a (Chla) hydration processes in aqueous organic solvents has been carried out by means of quantum chemistry calculations. A detailed knowledge of the thermodynamics of these processes is fundamental in order to better understand the organization of chlorophyll molecules in vivo, specifically the structure of chlorophyll pairs in photosystems I and II. In the present work, we assumed a Chla model in which the phytyl chain is replaced by a methyl group. Calculations were performed at the B3LYP/6-31G(d) level corrected for basis set superposition errors and dispersion interaction energy. This computational scheme was previously shown to provide data close to MP2/6-311++(2d,2p) results. Solvents effects were taken into account using either continuum (for nonpolar solvents) or discrete-continuum (for polar coordinating solvents) methods. In the latter case, we first examined the structure of Chla in rigorously dry solutions. Two types of solvents were characterized according to Mg-atom coordination: In type I solvents (acetone, acetonitrile, DMSO), Mg exhibits five-coordination, whereas in type II solvents (THF, pyridine), Mg exhibits six-coordination. Hydration processes are quite dependent on solvent nature. In nonpolar or low-polarity solvents such as cyclohexane or chloroform, hydration is always exothermic and exergonic, despite a large entropy term that strongly opposes hydration. In polar solvents of type II, hydration is quite unfavorable, and essentially no hydrates are expected in these media, except perhaps at very large water concentrations (although, in such a case, the medium cannot be simply described as an organic solvent). In polar solvents of type I, the situation is intermediate, and dihydration is favorable in some cases (acetone, acetonitrile) and unfavorable in others (DMSO). It is interesting to note that first hydration processes in coordinating solvents (of either type I or type II), where a water molecule must displace a solvent molecule coordinated to Mg, exhibit values of DeltaH > 0 and DeltaS > 0, in sharp contrast to first hydration processes in nonpolar media. The present results represent the first theoretical attempt to rationalize the large amount of experimental data on hydration and aggregation of Chla in aqueous organic media that have been accumulated over the past four decades. The data stress, in particular, the key role of Chla dihydrates, a point that has been the object of intense debate in the literature. Clearly, dihydrates are found to be more stable than monohydrates owing to a particular structure in which cooperative interactions occur between the water molecules and Chla. The calculations also explain the irregular behavior observed for Chla in aqueous THF or pyridine: In these media, Chla remains basically unhydrated because the Chla-solvent adducts are stabilized by strong dispersion interactions.

Free energies for the coordination of ligands to the magnesium of chlorophyll-a in solvents

“…Ben Fredj and co-workers [7,8], have previously shown that BSSE contributions to ligation energies are significant. For large basis sets, the wisdom of this approach for hydrogen-bond and ligation interactions has been questioned as often the increase in the correlation energy with increasing basis exceeds the BSSE [41,42].…”

“…Following the basic methodology of Ben Fredj and RuizLópez [8], the ligation free energies in solution of Chl-a with explicit solvent molecules were calculated using a composite approach. Geometries for Chl-a complexed in the gas phase with various ligands in axial and diaxial coordination were optimised using Gaussian 09 Revision D.01 [31].…”

“…Single-point energies were then obtained at the 6-31+G(d) geometries using the 6-311++ G(2d,2p) basis sets and corrected for basis-set superposition error (BSSE) using the counterpoise correction method [36]. Its application here is slightly different to that employed by Ben Fredj and co-workers [7,8], however, defining the energy of the second adducts using a simple complexation reaction for the first adduct. Thermodynamic effects were estimated by vibrational frequency calculations at the 6-31G(d) level using the various density functionals.…”

“…Hence, as Ben Fredj and Ruiz-López [8] concluded, this term does not appear of great significance in terms of relative chemical property analysis. However, when the solvent dispersion correction [38] is added, the average correction increases to 12.4 kcal mol −1 with a spread of 9 kcal mol −1 .…”

“…For gas-phase reactions, Ben Fredj et al [7] have demonstrated the importance of dispersion to the binding, as well as the role of entropy effects. They also considered binding in various solvents focusing on water complexation, but did not include the dispersive contributions to solvation [8]. The results obtained showed qualitative trends that allowed many observed chlorophyll solvation processes to be rationalised, but in absolute magnitude the calculated ligation free energies G were too negative by ca.…”