Abstract
Quinones are known to perform diverse functions in a variety of biological and chemical processes as well as molecular electronics owing to their redox and protonation properties. Electrostatics chiefly governs intermolecular interaction behaviour of quinone states in such processes. The electronic distribution of a prototypical quinone, viz., p-benzoquinone, with its reduction and protonation states (BQS) is explored by molecular electrostatic potential (MESP) mapping using density functional theory. The reorganization of electronic distribution of BQS and their interaction with electrophiles are assessed for understanding the movement of ubiquinone in bacterial photosynthetic reaction centre, by calculating their binding energy with a model electrophile viz., lithium cation (\(\hbox {Li}^{+}\)) at B3LYP/6-311+G(d,p) level of theory. The changes in the values of the MESP minima of BQS states alter their interacting behaviour towards \(\hbox {Li}^{+}\). A good correlation is found between the value of MESP minimum of BQS and the \(\hbox {Li}^{+}\) binding strength at the respective site. To acquire more realistic picture of the proton transfer process to quinone with respect to its reduction state in the photosynthetic reaction center, interaction of BQS with model protonated motifs of serine, histidine as well as \(\hbox {NH}_{4}^{+}\) is explored. Further, the electronic conjugation of the reduced states of 9,10-anthraquinone is probed through MESP for understanding the switching nature of their electronic conductivity.
Graphical Abstract
Quinones perform important function of proton transfer in photosynthesis and also act as a switch in molecular electronics. This work explores the electronic distribution of reduction and protonation states of p-benzoquinone using molecular electrostatic potential, for understanding the mechanisms of quinone activity in the photosynthesis and its switching nature in electronic conductivity.
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References
Heffner J E, Raber J C, Moe O A and Wigal C T 1998 Using cyclic voltammetry and molecular modelling to determine substituent effects in the one-electron reduction of benzoquinones J. Chem. Educ. 75 365
Guin P S, Das S and Mandal P C 2011 Electrochemical reduction of quinones in different media: a review Int. J. Electrochem . 2011 1
Ernster L and Dallner G 1995 Biochemical physiological and medical aspects of ubiquinone function Biochim. Biophys. Acta 1271 195
Marreiros B C, Calisto F, Castro P J, Duarte A M, Sena F V, Silva A F, Sousa F M, Teixeira M, Refojo P N and Pereira M M 2016 Exploring membrane respiratory chains Biochim. Biophys. Acta 1857 1039
Kato Y, Nagao R and Noguchi T 2016 Redox potential of the terminal quinone electron acceptor \(\text{ Q }_{{\rm b}}\) in photosystem II reveals the mechanism of electron transfer regulation Proc. Natl. Acad. Sci. (U. S. A.) 113 620
Okamura M Y, Paddock M L, Graige M S and Feher G 2000 Proton and electron transfer in bacterial reaction centres Biochim. Biophys. Acta 1458 148
Feher G, Allen J C, Okamura M Y and Rees D C 1989 Structure and function of bacterial photosynthetic reaction centres Nature 339 111
Nabedryk E and Breton J 2008 Coupling of electron transfer to proton uptake at the \({}_{{\rm QB}}\) site of the bacterial reaction center: A perspective from FTIR difference spectroscopy Biochim. Biophys. Acta 1777 1229
Fyfe P K and Jones M R 2000 Re-emerging structures: continuing crystallography of the bacterial reaction centre Biochim. Biophys. Acta 1459 413
Stowell M H B, McPhillips T M, Rees D C, Soltis S M, Abresch E and Feher G 1997 Light-induced structural changes in photosynthetic reaction center: implications for mechanism of electron-proton transfer Science 276 812
Walden S E and Wheeler R A 2002 Protein conformational gate controlling binding site preference and migration for ubiquinone-b in the photosynthetic reaction center of Rhodobacter sphaeroides J. Phys. Chem. B 106 3001
Lancaster C R D and Michel H 1997 The coupling of light-induced electron transfer and proton uptake as derived from crystal structures of reaction centres from Rhodopseudomonas viridis modified at the binding site of the secondary quinone, \(\text{ Q }_{{\rm B}}\) Structure 5 1339
Zhu Z and Gunner M R 2005 Energetics of Quinone-Dependent Electron and Proton Transfers in Rhodobacter sphaeroides Photosynthetic Reaction Centers Biochemistry 44 82
Breton J, Boullais C, Mioskowski C, Sebban P, Baciou L and Nabedryk E 2002 Vibrational spectroscopy favors a unique \(\text{ Q }_{{\rm B}}\) binding site at the proximal position in wild-type reaction centers and in the Pro-L209 \(\rightarrow \text{ Tyr }\) Mutant from Rhodobacter sphaeroides Biochemistry 41 12921
Takahashi E and Wraight C A 1996 Potentiation of proton transfer function by electrostatic interactions in photosynthetic reaction centers from Rhodobacter sphaeroides : first results from site-directed mutation of the H subunit Proc. Natl. Acad. Sci. U. S. A. 93 2640
Manojkumar T K, Choi H S, Tarakeshwar P and Kim K S 2003 Ab initio studies of neutral and anionic \(p\)-benzoquinone-water clusters J. Chem. Phys. 118 8681
Nepal B and Scheiner S 2016 Enhancing the reduction potential of quinones via complex formation J. Org. Chem. 81 4316
Darwish N, Díez-Pérez I, Da Silva P, Tao N, Gooding J J and Paddon-Row M N 2012 Observation of electrochemically controlled quantum interference in a single anthraquinone-based norbornylogous bridge molecule Angew. Chem. Int. Edit. 51 3203
Baghernejad M, Zhao X, Ørnsø K B, Füeg M, Moreno-García P, Rudnev A V, Kaliginedi V, Vesztergom S, Huang C, Hong W, Broekmann P, Wandlowski T, Thygesen K S and Bryce M R 2014 Electrochemical control of single-molecule conductance by fermi level tuning and conjugation switching J. Am. Chem. Soc. 136 17922
van Dijk E H, Myles D J T, van der Veen M H and Hummelen J C 2006 Synthesis and properties of an anthraquinone-based redox switch for molecular electronics Org. Lett. 8 2333
Xiang D, Wang X, Jia C, Lee T and Guo X 2016 Molecular-scale electronics: from concept to function Chem. Rev. 116 4318
Markussen T, Schiötz J and Thygesen K S 2010 Electrochemical control of quantum interference in anthraquinone-based molecular switches J. Chem. Phys. 132 224104
Seidel N, Hahn T, Liebing S, Seichter W, Jens K and Weber E 2013 Synthesis and properties of new 9,10-anthraquinone derived compounds for molecular electronics New J. Chem. 37 601
Greene L E, Godin R and Cosa G 2016 Fluorogenic ubiquinone analogue for monitoring chemical and biological redox processes J. Am. Chem. Soc. 138 11327
Nonella M 1997 Structures and vibrational spectra of \(p\)-benzoquinone in different oxidation and protonation states: a density functional study J. Phys. Chem. B 101 1235
Boesch S E and Wheeler R A 1997 \(\uppi \)-Donor substituent effects on calculated structures spin properties and vibrations of radical anions of \(p\)-chloranil \(p\)-fluoranil and \(p\)-benzoquinone J. Phys. Chem. A 101 8351
Brandt U and Trumpower B L 1994 The protonmotive Q cycle in mitochondria and bacteria Crit. Rev. Biochem. 29 165
Trumpower B L and Gennis R B 1994 Energy transduction by cytochrome complexes in mitochondrial and bacterial respiration: the enzymology of coupling electron transfer reactions to transmembrane proton translocation Annu. Rev. Biochem. 63 675
O’Malley P J 1997 A density functional study of the effect of reduction on the geometry and electron affinity of hydrogen bonded 1,4-benzoquinone implications for quinone reduction and protonation in photosynthetic reaction centres Chem. Phys. Lett. 274 251
Nonella M, Mathias G and Tavan P 2003 Infrared spectrum of \(p\)-benzoquinone in water obtained from a QM/MM hybrid molecular dynamics simulation J. Phys. Chem. A 107 8638
Pou-Amérigo R, Merchán M and Ortí E 1999 Theoretical study of the electronic spectrum of \(p\)-benzoquinone J. Chem. Phys. 110 9536
Zhao X, Imahori H, Zhan C-G, Sakata Y, Iwata S and Kitagawa T 1997 Resonance Raman and FTIR spectra of isotope-labeled reduced 1,4-benzoquinone and its protonated forms in solutions J. Phys. Chem. A 101 622
Politzer P and Truhlar D G 1981 In Chemical applications of atomic and molecular electrostatic potentials (New York: Plenum)
Politzer P, Landry S J and Wärnhelm T J 1982 Proposed procedure for using electrostatic potentials to predict and interpret nucleophilic processes J. Phys. Chem. 86 4767
Sjöberg P and Politzer P 1990 Use of the electrostatic potential at the molecular surface to interpret and predict nucleophilic processes J. Phys. Chem. 94 3959
Tomasi J, Bonaccrosi R and Cammi R 1990 In: Theoretical methods of chemical bonding, Part 3 Maksic Z B (Ed.) (NewYork: Springer) and references therein
Gadre S R, Pundlik S S and Shrivastava I H 1994 A “Critical” appraisal of electrostatic charge models for molecules Proc. Ind. Acad. Sci. (J. Chem. Sci.) 106 303
(a) Orozco M and Luque J 1996 in Molecular electrostatic potentials concepts and applications Vol. 3. J S Murray and K D Sen (Eds.) (Amsterdam: Elsevier) and references therein; (b) Gadre S R, Bhadane P K, Pundlik S S and Pingale S S 1996 In Molecular electrostatic potentials concepts and applications Vol. 3. J S Murray and K D Sen (Eds.) (Amsterdam: Elsevier) and references therein; (c) Roy D K, Balanarayan P and Gadre S R 2009 Signatures of molecular recognition from the topography of electrostatic potential J. Chem. Sci. 121 815
Gejji S P, Suresh C H, Bartolotti L J and Gadre S R 1997 Electrostatic potential as a harbinger of cation coordination: \(\text{ CF }_{3}\text{ SO }^{3-}\) ion as a model example J. Phys. Chem. 101 5678
Pingale S S, Gadre S R and Bartolotti L J 1998 Electrostatic insights into the molecular hydration process: a case study of crown ethers J. Phys. Chem. A 102 9987
Gadre S R and Bhadane P K 1997 Patterns in hydrogen bonding via electrostatic potential topography J. Chem. Phys. 107 5625
Gadre S R and Pundlik S S 1997 Complementary electrostatics for the study of DNA base-pair interactions J. Phys. Chem. B 101 3298
Lancaster C R D 2003 The role of electrostatics in proton-conducting membrane protein complexes FEBS Lett . 545 52
Sharma B, Neela Y I and Sastry G N 2016 Structures and energetics of complexation of metal ions with ammonia water and benzene: a computational study J. Comp. Chem. 37 992
Bhattacharjee A K, Pundlik S S and Gadre S R 1997 Conformational and electrostatic properties of naphthazarin, juglone and naphthoquinone: an ab initio theoretical study Cancer. Invest. 15 531
Abroshan H, Dhumal N R, Shimb Y and Kim H J 2016 Theoretical study of interactions of a \(\text{ Li }^{+}(\text{ CF }_{3}\text{ S }\text{ O }_{2})_{2}\text{ N }^{-}\) ion pair with \(\text{ CR }_{3}(\text{ OCR }_{2}\text{ CR }_{2})\text{ nOCR }_{3}\) (\(\text{ R }=\text{ H }\) or F) Phys. Chem. Chem. Phys. 18 6754
Gadre S R and Bhadane P K 1998 Complexes of ammonia with propane and cyclopropane: electrostatic guidelines for ab initio treatment Theor. Chem. Acc. 100 300
Pingale S S 2011 Molecular electrostatic potential for exploring \(\uppi \)-conjugation: a density-functional investigation Phys. Chem. Chem. Phys. 13 15158
Gaussian 09 Revision A 02 Frisch M J, Trucks G W, Schlegel H B, Scuseria G E, Robb M A, Cheeseman J R, Scalmani G, Barone V, Petersson G A, Nakatsuji H, Li X, Caricato M, Marenich AV, Bloino J, Janesko B G, Gomperts R, Mennucci B, Hratchian H P, Ortiz J V, Izmaylov A F, Sonnenberg J L, Williams-Young D, Ding F, Lipparini F, Egidi F, Goings J, Peng B, Petrone A, Henderson T, Ranasinghe D, Zakrzewski V G, Gao J, Rega N, Zheng G, Liang W, Hada M, Ehara M, Toyota K, Fukuda R, Hasegawa J, Ishida M, Nakajima T, Honda Y, Kitao O, Nakai H, Vreven T, Throssell K, Montgomery J A Jr, Peralta J E, Ogliaro F, Bearpark M J, Heyd J J, Brothers E N, Kudin K N, Staroverov V N, Keith T A, Kobayashi R, Normand J, Raghavachari K, Rendell A P, Burant J C, Iyengar S S, Tomasi J, Cossi M, Millam J M, Klene M, Adamo C, Cammi R, Ochterski J W, Martin R L, Morokuma K, Farkas O, Foresman J B and Fox D J 2009 Gaussian Inc, Wallingford CT.
The topographical analysis is brought out in term of characterizing the critical points (CPs) where the first order partial derivatives of this field vanish. The CPs are represented by a notation (rank, signature) where rank is the number of nonzero eigenvalues of the Hessian matrix and signature is the algebraic sum of the signs of these eigenvalues. The non-degenerate CPs are further characterized viz., minimum (3, \(+3\)), maximum (3, \(-3\)) or saddles of types (3, \(+1\)) and (3, \(-1\)).
Shirsat R N, Bapat S V and Gadre S R 1992 Molecular electrostatics: a comprehensive topographical approach Chem. Phys. Lett. 200 373
Kulkarni S A 1996 Electron correlation effects on the topography of molecular electrostatic potentials Chem. Phys. Lett. 254 268
Gadre S R, Kulkarni S A, Suresh C H and Strivastava I H 1995 Basis set dependence of the molecular electrostatic potential topography a case study of substituted benzenes Chem. Phys. Lett. 239 273
Limaye A C and Gadre S R 2001 UNIVIS-2000: An indigenously developed comprehensive visualization package Curr. Sci. (India) 80 1296
Boys S F and Bernardi F 1970 The calculation of small molecular interactions by the differences of separate total energies. Some procedures with reduced errors Mol. Phys. 19 553
Zhao Y and Truhlar D G 2008 The M06 suite of density functionals for main group thermochemistry, thermochemical kinetics, noncovalent interactions, excited states, and transition elements: two new functionals and systematic testing of four M06-class functionals and 12 other functionals Theor. Chem. Acc. 120, 215
Pathak R K and Gadre S R 1990 Maximal and minimal characteristics of molecular electrostatic potentials J. Chem. Phys. 93 1770
Bijina P V, Suresh C H and Gadre S R 2018 Electrostatics for probing lone pairs and their interactions J. Comput. Chem. 39 488
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The APW and SSP gratefully acknowledge the Board of College and University Development (BCUD) and UPE Phase II budget, respectively, Savitribai Phule Pune University, Pune for financial support.
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Pingale, S.S., Ware, A.P. & Gadre, S.R. Unveiling electrostatic portraits of quinones in reduction and protonation states. J Chem Sci 130, 50 (2018). https://doi.org/10.1007/s12039-018-1450-3
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DOI: https://doi.org/10.1007/s12039-018-1450-3