Sequence, Structure and Energy Transfer in DNA†

Abstract

Excitation energy transfer in DNA has similarities to charge transfer, but the transport is of an excited state, not of mass or charge. Use of the fluorescent, modified adenine base 2-aminopurine (2AP) as an energy trap in short (3- to 20-base) single- and double-stranded DNA oligomers is reviewed. Variation of 2AP's neighboring sequence shows (1) relatively efficient transfer from adenine compared to that from cytosine and thymine, (2) efficient transfer from guanine, but only when 2AP is at the 3' end, (3) approximate equality of efficiencies for 3' to 5' and 5' to 3' directional transfer in adenine tracks. The overall, average transfer distance at room temperature is about four adenine bases or less before de-excitation. The transfer fluorescence excitation spectral shape is similar to that of the absorption spectrum of the neighboring normal bases, confirming that initial excitation of the normal bases, followed by emission from 2AP (i.e. energy transfer), is occurring. Transfer apparently may take place both along one strand and cross-strand, depending on the oligomer sequence. Efficiency increases when the temperature is decreased, rising above 50% (overall efficiency) in decamers of adenine below -60 degrees C (frozen media). Modeling of the efficiencies of transfer from the nearest several adenine neighbors of 2AP in these oligomers suggests that the nearest two neighbors transfer with near 100% efficiency. As bases in B DNA, as well as in single-stranded DNA, are separated by less than 5 A (less than the size of a base), standard Förster transfer theory should not apply. Indeed, while both theory and experiment show efficiency decreasing with donor-acceptor distance, the experimental dependence clearly disagrees with Förster 1/r6 dependence. It is not yet clear what the best theoretical approach is, but any calculation must deal accurately with the excited states of bases, including strong base-base interactions and structural fluctuations, and should reflect the increase of efficiency with temperature decrease and the relative insensitivity to strandedness (single, double). Attempts to use DNA as a molecular "fiber optic" face three primary challenges. First, reasonable efficiency over more than a base or two occurs only in adenine stretches at temperatures well below freezing. Second, transfer in these adenine tracks is efficient in both directions. Third, absorption of UV light occurs randomly, making excitation at a specific site on this "fiber optic" a challenge.

On the origin of life in the Zinc world: 1. Photosynthesizing, porous edifices built of hydrothermally precipitated zinc sulfide as cradles of life on Earth

“…DNA and RNA are capable of long-range energy transfer along stacked nucleobases, over tens of nucleotide pairs [330-333]. In the context of the primordial Zn world, this property could have been useful: if a UV quantum hit a nucleotide having no direct contact with an energy-absorbing template, then, owing to the coupling between the stacked and paired nucleobases, the excess energy would still have promptly sunk into the ZnS substratum.…”

“…It is necessary to emphasize that neither the high photostability of single nucleobases [159-165,288-293], nor the even higher stability of their Watson-Crick pairs [164,355,356], nor the aptitude for long-range energy transfer along stacked nucleotides [330,333,360] have anything to do with the current functioning of RNA and DNA in the transfer of genetic information. All these traits, however, support the suggested involvement of UV light as a selecting factor during the initial stages of evolution [105,112,133,159,164].…”

Human Telomeres Are Hypersensitive to UV-Induced DNA Damage and Refractory to Repair

“…First, the TT on the G-rich strand is repeated thousands of times in each chromosome. On the other strand, the 5′CCCTAA3′ would nominally generate low frequency CC and CT CPD, but two factors supervene: tracts of adjacent pyrimidines tend to generate multiple CPDs on the same molecule, due to cooperative denaturation of the helix by each successive CPD [10] and A:T tracts tend to transfer energy down the base stack until depositing it at a G:C pair [11], [12]. These potential CCCT dimer tracts are again repeated thousands of times in each chromosome.…”

Highly fluorescent guanosine mimics for folding and energy transfer studies

“…The ratio of these excitation peaks weighted by the absorbance properties of the DNA and quantum yields of the probe can be used to calculate energy transfer efficiencies ( η t ) (34,40,41). Here η t is defined as the number of photons transferred from active nucleobase energy donors to each energy acceptor, divided by the total number of photons absorbed by all nucleobases at 260 nm.…”

“…Energy transfer efficiencies and quantum yields were calculated as previously reported (34,40,41). Absorption and emission spectra were recorded using a Molecular Devices SpectraMax M5 instrument in a 1-cm path-length quartz cuvette.…”