Planarizing cytosine: The S1 state structure, vibrations, and nonradiative dynamics of jet-cooled 5,6-trimethylenecytosine

Abstract

We measure the S → S spectrum and time-resolved S state nonradiative dynamics of the "clamped" cytosine derivative 5,6-trimethylenecytosine (TMCyt) in a supersonic jet, using two-color resonant two-photon ionization (R2PI), UV/UV holeburning, and ns time-resolved pump/delayed ionization. The experiments are complemented with spin-component scaled second-order approximate coupled cluster (SCS-CC2), time-dependent density functional theory, and multi-state second-order perturbation-theory (MS-CASPT2) ab initio calculations. While the R2PI spectrum of cytosine breaks off ∼500 cm above its 0 band, that of TMCyt extends up to +4400 cm higher, with over a hundred resolved vibronic bands. Thus, clamping the cytosine C-C bond allows us to explore the S state vibrations and S → S geometry changes in detail. The TMCyt S state out-of-plane vibrations ν, ν, and ν lie below 420 cm, and the in-plane ν, ν, and ν vibrational fundamentals appear at 450, 470, and 944 cm. S → S vibronic simulations based on SCS-CC2 calculations agree well with experiment if the calculated ν, ν, and ν frequencies are reduced by a factor of 2-3. MS-CASPT2 calculations predict that the ethylene-type S ⇝ S conical intersection (CI) increases from +366 cm in cytosine to >6000 cm in TMCyt, explaining the long lifetime and extended S → S spectrum. The lowest-energy S ⇝ S CI of TMCyt is the "amino out-of-plane" (OP) intersection, calculated at +4190 cm. The experimental S ⇝ S internal conversion rate constant at the S(v=0) level is k=0.98-2.2⋅10 s, which is ∼10 times smaller than in 1-methylcytosine and cytosine. The S(v=0) level relaxes into the T(ππ*) state by intersystem crossing with k=0.41-1.6⋅10 s. The T state energy is measured to lie 24 580±560 cm above the S state. The S(v=0) lifetime is τ=2.9 ns, resulting in an estimated fluorescence quantum yield of Φ=24%. Intense two-color R2PI spectra of the TMCyt amino-enol tautomers appear above 36 000 cm. A sharp S ionization threshold is observed for amino-keto TMCyt, yielding an adiabatic ionization energy of 8.114±0.002 eV.

How nature covers its bases

“…It appears that the amino group at C2 tends to provide an efficient access to a conical intersection while oxygen substitution at C2 tends to have the opposite effect. This observation is consistent with computations by Szabla et al 104 By contrast, the isoG dynamics does resemble that of C with the C5-C6 bond immobilized, similar to the "planarized" cytosine structure of trimethylenecytosine, reported by Traschel et al 43 The reported pump−probe results for enol C were not obtained at the 0−0 transition but rather on the rising edge of its broad initial absorption region. (**) For Isoguanine we cannot be sure whether we observe KA1, KA2, or a mixture of both.…”

“…Leutwyler and coworkers have demonstrated similar trends for cytosine (C), where immobilizing the C5=C6 bond by a five membered ring leads to orders of magnitude longer excited state lifetime. 43 The bottom row compares a series of purines in which those with an unsubstituted C2adenine and hypoxanthinehave ultrashort lifetimes. Those with a substituent at C2 have much longer excited state lifetimes.…”

Photodynamics of alternative DNA base isoguanine

“…49 Similar excited-state dynamics and lifetimes of B1 ns were also reported for jet-cooled 5,6-trimethylenecytosine, which resembles isoG structurally. 74,75 The 5,6-trimethylenesubstituent was suggested to lock the planarity of the aromatic pyrimidine ring and hinder ring-puckering motions 74,75 which enable the formation of pp*/S 0 state crossings in canonical C. 45 Most importantly, the resulting low photostability of keto isoG is consistent with the prebiotic scenario assuming that intense UV irradiation was one of the crucial selection factors for RNA constituents on an early Earth. This observation, together with the population of multiple tautomeric forms in bulk water and potential wobble base pairing make isoG a much less reliable component of primordial informational polymers than its biological counterpart.…”

Ultrafast excited‐state dynamics of gas‐phase 5‐methylcytosine tautomers

“…[3][4][5][6] Among all nucleobases, cytosine (Cy) and its derivatives are probably the most studied system experimentally in the gas phase. [7][8][9][10][11][12][13][14][15][16][17][18][19][20][21][22][23][24][25][26] Ultrafast excited-state dynamics of Cy in the gas phase has been explored by several groups. [22][23][24][25][26] Our group has previously used femtosecond pump-probe photoionization spectroscopy to investigate the ultrafast excited-state dynamics of Cy and its microsolvated complexes.…”

“…[4,[33][34][35][36][37][38][39][40][41] The importance of this C5-C6-twisting ethylenic type CI has been supported by the observation of a dramatic lengthening of the 1 ππ* state lifetime in 5,6-trimethylenecytosine in which the C5-C6 bond of Cy ring is covalently clamped with a trimethylene bridge. [14,16,45] Thus, it is intriguing to explore how methylation at the C5 position influences the energetics of this CI and the associated relaxation dynamics. Ultrafast measurements of 5mCy and its derivatives in aqueous solutions have been reported, [46,47] but direct femtosecond pump-probe measurements in the gas phase are still lacking.…”