Molecular mechanisms of the photostability of life
Abstract
Organic molecules are generally not stable under persistent irradiation with ultraviolet (UV) light. UV photons can break covalent bonds and thus can induce a great variety of chemical transformations, in particular fragmentations. In view of this well-known fact, it is amazing that life can thrive under full exposure to sunlight. Moreover, biogenesis took place long before the formation of the stratospheric ozone layer (which today filters out the most dangerous UV components of sunlight) and thus under conditions of very intense short-wavelength UV radiation. There must have been an extreme selection pressure for UV protection. These considerations suggest that photostability may have been the decisive selection criterion which has determined the molecular architecture of life at the beginning of the biological evolution.
The building blocks of life are, first of all, the four nucleic acid bases adenine, cytosine, guanine and thymine, which encode the genetic information of all organisms in deoxyribonucleic acid (DNA). The exceedingly manifold world of proteins is built from just 20 amino acids. Another widespread molecular motif are carbohydrates (e.g., sugars). Sugar molecules are part of the backbone of DNA and of structure-forming biopolymers such as cellulose.
In recent years, remarkable advances in the investigation of the structure, spectroscopy and photoinduced chemical dynamics of isolated building blocks of life, in particular the DNA bases, DNA base pairs, amino acids and peptides, have been achieved. With special laser evaporation techniques, even fragile biomolecules such as DNA base pairs or folded peptides can be brought into the gas phase and cooled to low temperatures in supersonic jets. Various spectroscopic techniques have provided detailed insight into the multiple molecular structures of biomolecules and their structure-specific photochemistry. This research has provided increasingly compelling evidence that the fundamental building blocks of life are endowed with particularly efficient mechanisms of excited-state deactivation after the absorption of UV photons. It seems that potentially dangerous photochemical reactions are efficiently quenched by ultrafast (femtosecond) nonradiative decay processes back to the electronic ground state, thus providing biological matter with a particularly high degree of photostability. Computational studies have revealed the essential role of ultrafast non-Born–Oppenheimer dynamics at conical intersections for the highly efficient deactivation of excited electronic states in the building blocks of life as well as in hydrogen-bonded supramolecular structures such as DNA and proteins.
The purpose of this themed issue is to provide a snapshot of this intellectually appealing research field. As the reader will notice, the interplay of advanced spectroscopy with high-level ab initio calculations and molecular dynamics simulations is an essential element of this research. There are five contributions which cover experimental and/or theoretical investigations of isolated DNA bases. Delchev et al. (DOI: 10.1039/b922505f) and Asturiol et al. (DOI: 10.1039/c001556c) report on the exploration of the nonradiative excited-state deactivation mechanisms in uracil and thymine with computational methods. Nachtigallova et al. (DOI: 10.1039/b925803p) and Lobsiger et al. (DOI: 10.1039/b924395j) have investigated these same mechanisms in modified thymine and uracil with spectroscopic as well as computational tools. The investigation of the photophysics of substituted or otherwise modified DNA bases can provide additional insight into the peculiar properties which distinguish the DNA bases from “ordinary” heterocycles. The work of Barbatti et al. (DOI: 10.1039/b924956g) describes the development a comprehensive first-principles computational simulation of the UV absorption spectra of all five nucleobases.
Four of the papers in the issue are concerned with the computational modelling of the effects of a condensed-phase environment on the photophysics of DNA bases or DNA oligomers. Together, they represent an informative snapshot of the state of the art in the computational simulation of solvation effects in the spectroscopy of organic chromophores. Marian (DOI: 10.1039/b925677f) considers the excited states of micro-solvated thymine and uracil with quantum mechanical (QM) methods, combined with a continuum modelling of long-range electrostatic solvation effects. Kistler and Matsika (DOI: 10.1039/b926125g) describe the combination of a multi-reference configuration-interaction description of the solute with a molecular-mechanics (MM) simulation of the environment. Santoro et al. (DOI: 10.1039/b925108a) investigate the effects of stacking of nucleobases and explore the relevance of intra-strand charge-transfer states. Conti et al. (DOI: 10.1039/b926608a) report first results of a simulation of the electronic structure of an adenine molecule in the MM force field of a DNA double strand.
There are three papers which focus on the spectroscopy and photochemistry of isolated aromatic amino acids or their chromophores. Schmitt and collaborators present an experimental (DOI: 10.1039/c001778g) and theoretical analysis (DOI: 10.1039/c001776k) of the notoriously difficult vibronic-coupling problem of the La and Lb states in indole. Siegert et al. (DOI: 10.1039/b926289j) demonstrate a novel approach towards the spectroscopic observation of neutral contact charge-transfer states in anionic hetero-clusters involving tryptophan. Tseng et al. (DOI: 10.1039/b925338f) report results on the size-dependence of the competition of photodissociation and nondissociative internal conversion in various phenylalanine chromophores. Oncák et al. (DOI: 10.1039/b925246k) performed a computational study of the photochemistry micro-solvated zwitterionic glycine. Deamination (loss of ammonia), hydrogen detachment as well as hydrogen back-transfer to the non-ionic form of glycine are predicted to be the main processes on the femtosecond time scale. Shemesh et al. (DOI: 10.1039/b927024h) report ab initio computational results for an aromatic dipeptide which confirm the important role of hydrogen bonds for the efficient excited-state deactivation of peptides, which may enhance their photostability.
In summary, we believe that this collection of research articles illustrates the enormous progress that has been achieved in the understanding of the peculiar photochemical processes in the building blocks of life. The reader may also realize that this is a wide open research area with numerous challenges, calling for innovative developments in molecular spectroscopy as well as in computational chemistry. We wish to thank our friends and colleagues who were so kind to contribute to this themed issue. We also thank the PCCP editorial team for their highly effective support in all stages of the editing.
Andrzej L. Sobolewski, Institute of Physics, Polish Academy of Sciences, Warsaw, Poland
Wolfgang Domcke, Institute of Physical and Theoretical Chemistry, Technical University of Munich, Germany
| This journal is © the Owner Societies 2010 |