Understanding the effects of ultraviolet radiation on nucleotides in solution is an important step towards a comprehensive description of the photochemistry of nucleic acids and their constituents. Apart from having implications for mutagenesis and DNA photoprotection mechanisms, the photochemistry of cytidines is a central element in UV-assisted syntheses of pyrimidine nucleotides under prebiotically plausible conditions. In this contribution, we present UV-irradiation experiments of β-2'-deoxycytidine in aqueous solution involving H-D exchange followed by NMR spectroscopic analysis of the photoproducts. We further elucidate the outcome of these experiments by means of high-level quantum chemical calculations. In particular, we show that prolonged UV-irradiation of cytidine may lead to H-C1' hydrogen atom abstraction by the carbonyl oxygen atom of cytosine. This process may enable photoanomerisation and nucleobase loss, two previously unexplained photoreactions observed in pyrimidine nucleotides.

Institute of Biophysics Academy of Sciences of the Czech Republic Královopolská 135 61265 Brno Czech Republic

Institute of Biophysics Academy of Sciences of the Czech Republic Královopolská 135 61265 Brno Czech Republic CEITEC Central European Institute of Technology Masaryk University Campus Bohunice Kamenice 5 CZ 62500 Brno Czech Republic

MRC Laboratory of Molecular Biology Hills Road Cambridge CB2 0QH UK

School of Chemistry The University of Manchester Oxford Road Manchester M13 9PL UK; Inorganic Chemistry Laboratory Department of Chemistry University of Oxford South Parks Road Oxford OX1 3QR UK

Theoretical Chemistry Group Institute of Physical and Theoretical Chemistry Wroclaw University of Technology Wybrzeże Wyspiańskiego 27 50 370 Wroclaw Poland

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Schreier W. J., Schrader T. E., Koller F. O., Gilch P., Crespo-Hernández C. E., Swaminathan V. N., Carell T., Zinth W., Kohler B. Science. 2007;315:625–629. PubMed PMC

Yuan S., Zhang W., Liu L., Dou Y., Fang W., Lo G. V. J. Phys. Chem. A. 2011;115:13291–13297. PubMed

Cuquerella M. C., Lhiaubet-Vallet V., Bosca F., Miranda M. A. Chem. Sci. 2011;2:1219–1232.

Haiser K., Fingerhut B. P., Heil K., Glas A., Herzog T. T., Pilles B. M., Schreier W. J., Zinth W., de Vivie-Riedle R., Carell T. Angew. Chem., Int. Ed. 2012;51:408–411. PubMed

Barks H. L., Buckley R., Grieves G. A., Di Mauro E., Hud N. V., Orlando T. M. ChemBioChem. 2010;11:1240–1243. PubMed

Szabla R., Tuna D., Góra R. W., Šponer J., Sobolewski A. L., Domcke W. J. Phys. Chem. Lett. 2013;4:2785–2788.

Boulanger E., Anoop A., Nachtigallova D., Thiel W., Barbatti M. Angew. Chem., Int. Ed. 2013;125:8158–8161. PubMed

Szabla R., Góra R. W., Šponer J., Šponer J. E. Chem.–Eur. J. 2014;20:2515–2521. PubMed

Powner M. W., Anastasi C., Crowe M. A., Parkes A. L., Raftery J., Sutherland J. D. ChemBioChem. 2007;8:1170–1179. PubMed

Powner M. W., Sutherland J. D. ChemBioChem. 2008;9:2386–2387. PubMed

Sobolewski A. L., Domcke W. Europhys. News. 2006;37:20–23.

Barbatti M., Aquino A. J. A., Szymczak J. J., Nachtigallová D., Hobza P., Lischka H. Proc. Natl. Acad. Sci. U. S. A. 2010:21453–21458. PubMed PMC

Kleinermanns K., Nachtigallová D., de Vries M. S. Int. Rev. Phys. Chem. 2013;32:308–342.

Canuel C., Mons M., Piuzzi F., Tardivel B., Dimicoli I., Elhanine M. J. Chem. Phys. 2005;122:074316. PubMed

de Vries M. S., Hobza P. Annu. Rev. Phys. Chem. 2007;58:585–612. PubMed

Crespo-Hernández C. E., Cohen B., Hare P. M., Kohler B. Chem. Rev. 2004;104:1977–2020. PubMed

Saigusa H. J. Photochem. Photobiol., C. 2006;7:197–210.

Weinkauf R., Schermann J.-P., Vries M. S. d., Kleinermanns K. Eur. Phys. J. D. 2002;20:309–316.

Crespo-Hernández C. E., Kohler B. J. Phys. Chem. B. 2004;108:11182–11188.

Crespo-Hernández C. E., Cohen B., Kohler B. Nature. 2005;436:1141–1144. PubMed

Nir E., de Vries M. S. Int. J. Mass Spectrom. 2002;219:133–138.

Asami H., Yagi K., Ohba M., Urashima S.-H., Saigusa H. Chem. Phys. 2013;419:84–89.

Tuna D., Sobolewski A. L., Domcke W. J. Phys. Chem. A. 2014;118:122–127. PubMed

Powner M. W., Gerland B., Sutherland J. D. Nature. 2009;459:239–242. PubMed

Powner M., Sutherland J., Szostak J. Synlett. 2011:1956–1964.

Sanchez R. A., Orgel L. E. J. Mol. Biol. 1970;47:531–543. PubMed

Deboer G., Klinghoffer O., Johns H. E. Biochim. Biophys. Acta. 1970;213:253–268. PubMed

Liu F.-T., Yang N. C. Biochemistry. 1978;17:4877–4885. PubMed

Johns H. E., LeBlanc J. C., Freeman K. B. J. Mol. Biol. 1965;13:849–861.

Bach T., Hehn J. Angew. Chem., Int. Ed. 2011;50:1000–1045. PubMed

Makino B., Kawai M., Kito K., Yamamura H., Butsugan Y. Tetrahedron. 1995;51:12529–12538.

De Mayo P., Suau R. J. Am. Chem. Soc. 1974;96:6807–6809.

Zgierski M. Z., Alavi S. Chem. Phys. Lett. 2006;426:398–404.

Keane P. M., Wojdyla M., Doorley G. W., Watson G. W., Clark I. P., Greetham G. M., Parker A. W., Towrie M., Kelly J. M., Quinn S. J. J. Am. Chem. Soc. 2011;133:4212–4215. PubMed

Quinn S., Doorley G. W., Watson G. W., Cowan A. J., George M. W., Parker A. W., Ronayne K. L., Towrie M., Kelly J. M. Chem. Commun. 2007:2130–2132. PubMed

Keane P. M., Wojdyla M., Doorley G. W., Kelly J. M., Clark I. P., Parker A. W., Greetham G. M., Towrie M., Magno L. M., Quinn S. J. Phys. Chem. Chem. Phys. 2012;14:6307–6311. PubMed

Chatterley A. S., West C. W., Stavros V. G., Verlet J. R. R. Chem. Sci. 2014;5:3963–3975. PubMed

Hocquet A., Leulliot N., Ghomi M. J. Phys. Chem. B. 2000;104:4560–4568.

Shishkin O. V., Pelmenschikov A., Hovorun D. M., Leszczynski J. J. Mol. Struct. 2000;526:329–341.

Foloppe N., Nilsson L. J. Phys. Chem. B. 2005;109:9119–9131. PubMed

Plavec J., Thibaudeau C., Chattopadhyaya J. Pure Appl. Chem. 1996;68:2137–2144.

Hocquet A., Ghomi M. Phys. Chem. Chem. Phys. 2000;2:5351–5353.

Hocquet A. Phys. Chem. Chem. Phys. 2001;3:3192–3199.

Plavec J., Tong W., Chattopadhyaya J. J. Am. Chem. Soc. 1993;115:9734–9746.

Barbatti M., Aquino A. J. A., Szymczak J. J., Nachtigallová D., Lischka H. Phys. Chem. Chem. Phys. 2011;13:6145–6155. PubMed

González-Vázquez J., González L. ChemPhysChem. 2010;11:3617–3624. PubMed

Mai S., Marquetand P., Richter M., González-Vázquez J., González L. ChemPhysChem. 2013;14:2920–2931. PubMed

Yarkony D. R. Rev. Mod. Phys. 1996;68:985–1013.

Yarkony D. R. Acc. Chem. Res. 1998;31:511–518.

Henne A., Fischer H. Angew. Chem., Int. Ed. Engl. 1976;15:435.

Rabi J. A., Fox J. J. J. Am. Chem. Soc. 1973;95:1628–1632. PubMed

Zhao Y., Truhlar D. G. Theor. Chem. Acc. 2008;120:215–241.

Goerigk L., Grimme S. Phys. Chem. Chem. Phys. 2011;13:6670–6688. PubMed

Barone V., Cossi M. J. Phys. Chem. A. 1998;102:1995–2001.

Scalmani G., Frisch M. J. J. Chem. Phys. 2010;132:114110. PubMed

Tomasi J., Mennucci B., Cammi R. Chem. Rev. 2005;105:2999–3094. PubMed

Hättig C., Weigend F. J. Chem. Phys. 2000;113:5154–5161.

TURBOMOLE v6.3 2011, a development of University of Karlsruhe and Forschungszentrum Karlsruhe GmbH, 1989–2007, TURBOMOLE GmbH, since 2007, 2011, http://www.turbomole.com.

Karlström G., Lindh R., Malmqvist P.-A., Roos B. O., Ryde U., Veryazov V., Widmark P.-O., Cossi M., Schimmelpfennig B., Neogrady P., Seijo L. Comput. Mater. Sci. 2003;28:222–239.

Aquilante F., De Vico L., Ferre N., Ghigo G., Malmqvist P.-A., Neogrady P., Pedersen T. B., Pitonak M., Reiher M., Roos B. O., Serrano-Andres L., Urban M., Veryazov V., Lindh R. J. Comput. Chem. 2010;31:224–247. PubMed

Lischka H., Müller T., Szalay P. G., Shavitt I., Pitzer R. M., Shepard R. Wiley Interdiscip. Rev.: Comput. Mol. Sci. 2011;1:191–199.

Lischka H., Shepard R., Shavitt I., Pitzer R. M., Dallos M., Müller T., Szalay P. G., Brown F. B., Ahlrichs R., Böhm H. J., Chang A., Comeau D. C., Gdanitz R., Dachsel H., Ehrhardt C., Ernzerhof M., Höchtl P., Irle S., Kedziora G., Kovar T., Parasuk V., Pepper M. J. M., Scharf P., Schiffer H., Schindler M., Schüler M., Seth M., Stahlberg E. A., Zhao J.-G., Yabushita S., Zhang Z., Barbatti M., Matsika S., Schuurmann M., Yarkony D. R., Brozell S. R., Beck E. V., Blaudeau J.-P., Ruckenbauer M., Sellner B., Plasser F. and Szymczak J. J., COLUMBUS, release 7.0 2012, an ab initio electronic structure program, 2012, http://www.univie.ac.at/columbus.

Frisch M. J., Trucks G. W., Schlegel H. B., Scuseria G. E., Robb M. A., Cheeseman J. R., Scalmani G., Barone V., Mennucci B., Petersson G. A., Nakatsuji H., Caricato M., Li X., Hratchian H. P., Izmaylov A. F., Bloino J., Zheng G., Sonnenberg J. L., Hada M., Ehara M., Toyota K., Fukuda R., Hasegawa J., Ishida M., Nakajima T., Honda Y., Kitao O., Nakai H., Vreven T., Montgomery J., Peralta J. E., Ogliaro F., Bearpark M., Heyd J. J., Brothers E., Kudin K. N., Staroverov V. N., Kobayashi R., Normand J., Raghavachari K., Rendell A., Burant J. C., Iyengar S. S., Tomasi J., Cossi M., Rega N., Millam J. M., Klene M., Knox J. E., Cross J. B., Bakken V., Adamo C., Jaramillo J., Gomperts R., Stratmann R. E., Yazyev O., Austin A. J., Cammi R., Pomelli C., Ochterski J. W., Martin R. L., Morokuma K., Zakrzewski V. G., Voth G. A., Salvador P., Dannenberg J. J., Dapprich S., Daniels A. D., Farkas O., Foresman J. B., Ortiz J. V., Cioslowski J. and Fox D. J., Gaussian 09, revision C.01, Gaussian Inc., Wallingford CT, 2009.

A prebiotically plausible synthesis of pyrimidine β-ribonucleosides and their phosphate derivatives involving photoanomerization