The impact of oxo functionalization in the photophysics and photochemistry of nucleobases: implications in prebiotic chemistry and the current composition of nucleic acids

Abstract

DNA is probably the most relevant biomolecule for life. Its capacity for storing the genetic information is completely essential to the performance of the living organisms. For this reason, important efforts from scientists of different areas have been focusing on the investigation of the origin of this biomolecule. From the protoRNA forms at the primordial era, a complex chemical evolution took place which has concluded in the structural and functional specialization of DNA. Understanding the selection processes have resulted in our current genetic alphabet can help discerning not only its composition but also its survival in time. Light is indeed considered a determinant factor for the selection of the five canonical nucleobases against other possible building blocks. In fact, far from being casual, all DNA nucleobases exposed to continuous UV-light irradiation are able to efficiently dissipate the absorbed energy. With out any doubt, this photostability must have contributed to the preservation of these systems. Thus, determining the electronic and structural characteristics that promote these properties would allow establishing a general pattern and understand the nature’s decision. This work is focused on the study of the response of oxo modified pyrimidine and purine nucleobases to light, employing a dual static and dynamic approach based on sophisticated multiconfigurational theoretical methods and the surface hopping algorithm which allows the description of the time evolution of the system. Our results show the photophysical importance of substituting the pyrimidine and purine rings with exocyclic oxo groups at the C4 position in pyrimidine and the C6 position in purine core to activate direct and barrierless relaxation routes which allow a fast deactivation of the modified nucleobases. Instead, the oxo monosubstitution at the C2 position in pyrimidine contributes to the generation of long-lived triplet excited states, being a doorway to secondary reactions. Interestingly the oxo monosubstution promote a photodegradation reactions which lead to the opening of the pyrimidine or purine rings. These competitive pathways, that conclude on the formation of diverse photoproducts, corroborated by time resolved experiments, jeopardize the integrity of the nucleobases. Therefore, although mono substitution with a carbonyl group opens up new accessible deactivation paths, its presence also provokes the photolability of specific bods of the heterocycles. Instead, the double carbonyl substitution in pyrimidine nucleobases, as uracil, seems essential to guarantee the photostability and photointegrity of the genetic material