Why flavins are not competitors of chlorophyll in the evolution of biological converters of solar energy

Abstract

Excited flavin molecules can photocatalyze reactions, leading to the accumulation of free energy in the products, and the data accumulated through biochemical experiments and by modeling prebiological processes suggest that flavins were available in the earliest stages of evolution. Furthermore, model experiments have shown that abiogenic flavin conjugated with a polyamino acid matrix, a pigment that photocatalyzes the phosphorylation of ADP to form ATP, could have been present in the prebiotic environment. Indeed, excited flavin molecules play key roles in many photoenzymes and regulatory photoreceptors, and the substantial structural differences between photoreceptor families indicate that evolution has repeatedly used flavins as chromophores for photoreceptor proteins. Some of these photoreceptors are equipped with a light-harvesting antenna, which transfers excitation energy to chemically reactive flavins in the reaction center. The sum of the available data suggests that evolution could have led to the formation of a flavin-based biological converter to convert light energy into energy in the form of ATP.

Figure 1

Some coenzymes of “dark metabolism” act as chromophores in photoreceptor proteins. Flavin molecules, riboflavin-5′-phosphate (also known as flavin mononucleotide (FMN)) or flavin adenine dinucleotide (FAD) (anionic dihydroflavin H-FAD⁻_red in DNA photolyases) function in the photocatalytic (reaction) center. Coenzyme molecules also act as photon harvesters in some flavoprotein photoreceptors, including 5,10-methenyl-tetrahydrofolate (MTHF) or 8-hydroxy-7,8-didemehyl-5-deazariboflavin (8-HDF), which is present in different organisms. FMN and FAD also act as antennae for some organisms. The boxed formula represents the structure of reduced isoalloxazine, the basic ring of the flavin molecule in the anionic dihydro form of H-FAD⁻_red.