pH-Independent Charge Resonance Mechanism for UV Protective Functions of Shinorine and Related Mycosporine-like Amino Acids

Abstract

The UV-protective ability of mycosporine-like amino acids (MAAs) has been well documented and is believed to serve as a protecting agent for marine organisms from solar radiation. However, the effective UV absorption by MAAs has not been well correlated to MAA (neutral) structures. In this study, the origin of UV-protecting ability of MAAs was elucidated by experimental and theoretical spectroscopic investigations. The absorption maxima of mycosporine-glycine and shinorine in the UVA region were practically unaffected over a wide range of pH 4-10 and only slightly blue-shifted at pH 1-2. It was revealed that the zwitterionic nature of the amino acid residue facilitates the protonation to the chromophoric 3-aminocyclohexenone and 1-amino-3-iminocyclohexene moieties and the operation of the charge resonance in the protonated species well accounts for their allowed low-energy transitions in the UVA region. The RI-CC2/TZVP calculations on model systems in their protonated forms well reproduced the observed transition energies and oscillator strengths of MAAs, only with insignificant systematic overestimations of the both values. The slight hypsochromic shifts at pH 1-2 were explained by (partial) protonation to a carboxylate anion in the amino acid residue, as confirmed by theory. Fluorescence spectral investigations of shinorine were also performed for the first time in water to confirm the effective nonradiative deactivation. Consequently, this study unequivocally demonstrated that the 3-aminocyclohexenone as well as 1-amino-3-iminocyclohexene moieties, which are readily protonated at a wide range of pH, are responsible for the UV-protective ability of aqueous solution of MAAs.

Unravelling the Photoprotective Mechanisms of Nature-Inspired Ultraviolet Filters Using Ultrafast Spectroscopy

“…To conclude the mycosporine discussion, it is noted that additional studies on the mycosporines, mycosporine-glycine (see Figure 13 for structure) and mycosporine-glutaminol-glucoside, have also demonstrated high photostability, as only small decreases in their absorption spectra were observed after continuous UV irradiation [ 81 , 123 ]. Furthermore, a computational study on a model of mycosporine-glycine (glycine substituent at carbon three is exchanged for a NHCH 3 group) by Matsuyama et al [ 129 ] determined the species responsible for its UV absorption profileto be protonated on the oxygen at carbon one. In the same work, Matsuyama et al [ 129 ] studied the effect of pH on mycosporine-glycine.…”

“…Furthermore, a computational study on a model of mycosporine-glycine (glycine substituent at carbon three is exchanged for a NHCH 3 group) by Matsuyama et al [ 129 ] determined the species responsible for its UV absorption profileto be protonated on the oxygen at carbon one. In the same work, Matsuyama et al [ 129 ] studied the effect of pH on mycosporine-glycine. The findings were that a small hypsochromic shift was observed for the absorption maximum at low pH (1–2) in comparison to pH 4 to 10 which remained unchanged.…”

“…From these findings, the authors concluded that the charge resonance through the chromophore, which is a result of the amino acid residue facilitating a zwitterionic structure (see Figure 13 ), is the reason for the low energy allowed transition observed in mycosporines, and is also responsible for their UV protective function. Matsuyama et al [ 129 ] suggest that after photoexcitation, non-radiative decay of mycosporines likely occurs via the triplet state. However, Matsuyama et al’s study does not map the MEPs or identify CIs to elucidate the photoprotection mechanism [ 129 ].…”

“…Matsuyama et al [ 129 ] suggest that after photoexcitation, non-radiative decay of mycosporines likely occurs via the triplet state. However, Matsuyama et al’s study does not map the MEPs or identify CIs to elucidate the photoprotection mechanism [ 129 ].…”

“…Whilst Sampedro [ 86 ] determined that protonated palythine is responsible for the UV-absorbing properties compared to its neutral form, and Hatakeyama et al [ 90 ] determined that the zwitterionic form of porphyra-334 was responsible for the UV-absorbing properties, neither study performed a comparison between the protonated form and the zwitterionic form. A study on shinorine by Matsuyama et al [ 129 ] performed such calculations, and took experimental data over a broad pH range (1–10). The findings were the same as those discussed in Section 2.2.1 for mycosporine-glycine; over the pH range 4–10, the maximum absorbance did not change, but, at pH 1 to 2, a small hypsochromic shift was observed.…”