We carried out a first-principles quantum-mechanical study of a set of full-turn A-form DNA oligonucleotides using density functional approximations. The structural features of the fully relaxed model DNA molecules and more importantly, the energetic and structural changes of these molecules under stretching conditions are examined in detail. Special attention is paid to the dependence of the structural properties on the stacking sequences of the constituent DNA base pairs. It appears that DNA oligonucleotides are extremely flexible, and structural properties such as the diameter and the widths of the minor and major grooves change regularly as a function of the stretching rate (stretching length in percentage). Additionally, we found that the length of the hydrogen bonds in the DNA base pairs varies with the DNA stacking sequence. This work indicates that rich information and insights can be gained from first principles studies of model DNA molecules of only atoms.
REFERENCES
1.
J. D.
Watson
and F. H. C.
Crick
, “Molecular structure of nucleic acids: A structure for deoxyribose nucleic acid
,” Nature
171
, 737
–738
(1953
).2.
A.
Ghosh
and M.
Bansal
, “A glossary of DNA structures from A to Z
,” Acta Crystallogr. Sect. D: Struct. Biol.
59
, 620
–626
(2003
).3.
R. E.
Franklin
and R. G.
Gosling
, “Molecular configuration in sodium thymonucleate
,” Nature
171
, 740
–741
(1953
).4.
M. D.
Wang
, H.
Yin
, R.
Landick
, J.
Gelles
, and S. M.
Block
, “Stretching DNA with optical tweezers
,” Biophys. J.
72
, 1335
–1346
(1997
).5.
L. H.
Pope
, M. L.
Bennink
, K. A.
van Leijenhorst-Groener
, D.
Nikova
, J.
Greve
, and J. F.
Marko
, “Single chromatin fiber stretching reveals physically distinct populations of disassembly events
,” Biophys. J.
88
, 3572
–3583
(2005
).6.
S. B.
Smith
, L.
Finzi
, and C.
Bustamante
, “Direct mechanical measurements of the elasticity of single DNA-molecules by using magnetic beads
,” Science
258
, 1122
–1126
(1992
).7.
C.
Gosse
and V.
Croquette
, “Magnetic tweezers: Micromanipulation and force measurement at the molecular level
,” Biophys. J.
82
, 3314
–3329
(2002
).8.
C.
Danilowicz
, C.
Limouse
, K.
Hatch
, A.
Conover
, V. W.
Coljee
, N.
Kleckner
, and M.
Prentiss
, “The structure of DNA overstretched from the 5′5′ ends differs from the structure of DNA overstretched from the 3′3′ ends
,” Proc. Natl. Acad. Sci. U. S. A.
106
, 13196
–13201
(2009
).9.
H.-X.
Fu
, H.
Chen
, J. F.
Marko
, and J.
Yan
, “Two distinct overstretched DNA states
,” Nucleic Acids Res.
38
, 5594
–5600
(2010
).10.
P. A.
Wiggins
, T.
van der Heijden
, F.
Moreno-Herrero
, A.
Spakowitz
, R.
Phillips
, J.
Widom
, C.
Dekker
, and P. C.
Nelson
, “High flexibility of DNA on short length scales probed by atomic force microscopy
,” Nat. Nanotechnol.
1
, 137
–141
(2006
).11.
T. E.
Cheatham
III and D. A.
Case
, “Twenty-five years of nucleic acid simulations
,” Biopolymers
99
, 969
–977
(2013
).12.
M.
Pasi
and R.
Lavery
, “Structure and dynamics of DNA loops on nucleosomes studied with atomistic, microsecond-scale molecular dynamics
,” Nucleic Acids Res.
44
, 5450
–5456
(2016
).13.
E. G.
Marklund
, A.
Mahmutovic
, O. G.
Berg
, P.
Hammar
, D.
van der Spoel
, D.
Fange
, and J.
Elf
, “Transcription-factor binding and sliding on DNA studied using micro- and macroscopic models
,” Proc. Natl. Acad. Sci. U. S. A.
110
, 19796
–19801
(2013
).14.
P. J.
Flory
, Statistical Mechanics of Chain Molecules
(Hanser Publishers
, Munich, Vienna, New York
, 1989
).15.
H.-J.
Zhou
, Y.
Zhang
, and Z.-C.
Ou-Yang
, “Elastic property of single double-stranded DNA molecules: Theoretical study and comparison with experiments
,” Phys. Rev. E
62
, 1045
–1058
(2000
).16.
P. J.
de Pablo
, F.
Moreno-Herrero
, J.
Colchero
, J.
Gómez Herrero
, P.
Herrero
, A. M.
Baró
, P.
Ordejón
, J. M.
Soler
, and E.
Artacho
, “Absence of DC-conductivity in λ-DNA
,” Phys. Rev. Lett.
85
, 4992
(2000
).17.
E.
Artacho
, M.
Machado
, D.
Sánchez-Portal
, P.
Ordejón
, and J. M.
Soler
, “Electrons in dry DNA from density functional calculations
,” Mol. Phys.
101
, 1587
(2003
).18.
J. B.
MacNaughton
, A.
Moewes
, J. S.
Lee
, S. D.
Wettig
, H.-B.
Kraatz
, L. Z.
Ouyang
, W. Y.
Ching
, and E. Z.
Kurmaev
, “Dependence of DNA electronic structure on environmental and structural variations
,” J. Phys. Chem. B
110
, 15742
(2006
).19.
X.
Chen
, “Theoretical electrical conductivity of hydrogen-bonded benzamide-derived molecules and single DNA bases
,” J. Biol. Phys.
39
, 607
–624
(2013
).20.
M. H.
Lee
and O. F.
Sankey
, “Theory of tunneling across hydrogen-bonded base pairs for DNA recognition and sequencing
,” Phys. Rev. E
79
, 051911
(2009
).21.
R. N.
Barnett
, C. L.
Cleveland
, U.
Landman
, E.
Boone
, S.
Kanvah
, and G. B.
Schuster
, “Effect of base sequence and hydration on the electronic and hole transport properties of duplex DNA: Theory and experiment
,” J. Phys. Chem. A
107
, 3525
–3537
(2003
).22.
T. A.
Zubatiuk
, O. V.
Shishkin
, L.
Gorb
, D. M.
Hovorun
, and J.
Leszczynski
, “B-DNA characteristics are preserved in double stranded d(A)3·d(T)3 and d(G)·d(C)3 mini-helixes: Conclusions from DFT/M06-2X study
,” Phys. Chem. Chem. Phys.
15
, 18155
(2013
).23.
C. S.
Sarap
, P.
Partovi-Azar
, and M.
Fyta
, “Optoelectronic properties of diamondoid-DNA complexes
,” ACS Appl. Bio Mater.
1
, 59
(2018
).24.
M.
Tassi
, A.
Morphis
, K.
Lambropoulos
, and C.
Simserides
, “RT-TDDFT study of hole oscillations in B-DNA monomers and dimers
,” Cogent Phys.
4
, 1361077
(2017
).25.
A. A.
Voityuk
, “Electronic couplings and on-site energies for hole transfer in DNA: Systematic quantum mechanical/molecular dynamic study
,” J. Chem. Phys.
128
, 115101
(2008
).26.
S. T.
Mutter
, N.
Margiotta
, P.
Papadia
, and J. A.
Platts
, “Computational evidence for structural consequences of kiteplatin damage on DNA
,” J. Biol. Inorg. Chem.
20
, 35
(2015
).27.
M. C. R.
Melo
, R. C.
Bernardi
, T.
Rudack
, M.
Scheurer
, C.
Riplinger
, J. C.
Phillips
, J. D. C.
Maia
, G. B.
Rocha
, J. V.
Ribeiro
, J. E.
Stone
, F.
Neese
, K.
Schulten
, and Z.
Luthey-Schulten
, “NAMD goes quantum: An integrative suite for hybrid simulations
,” Nat. Methods
15
, 351
(2018
).28.
E.
Benson
, A.
Mohammed
, J.
Gardell
, S.
Masich
, E.
Czeizler
, P.
Orponen
, and B.
Högberg
, “DNA rendering of polyhedral meshes at the nanoscale
,” Nature
523
, 441
(2015
).29.
A.
Samanta
and I. L.
Medintz
, “Nanoparticles and DNA: A powerful and growing functional combination in bionanotechnology
,” Nanoscale
8
, 9037
–9095
(2016
).30.
S.
Roche
, D.
Bicout
, E.
Maciá
, and E.
Kats
, “Long range correlations in DNA: Scaling properties and charge transfer efficiency
,” Phys. Rev. Lett.
91
, 228101
(2003
).31.
H.
Yamada
, “Localization of electronic states in chain models based on real DNA sequence
,” Phys. Lett. A
332
, 65
(2004
).32.
E. L.
Albuquerque
, U. L.
Fulco
, V. N.
Freire
, E. W. S.
Caetano
, M. L.
Lyra
, and F. A. B. F.
de Moura
, “DNA-based nanobiostructured devices: The role of quasiperiodicity and correlation effects
,” Phys. Rep.
535
, 139
(2014
).33.
H.
Mehrez
and M. P.
Anantram
, “Interbase electronic coupling for transport through DNA
,” Phys. Rev. B
71
, 115405
(2005
).34.
X. F.
Wang
and T.
Chakraborty
, “Charge transfer via a two-strand superexchange bridge in DNA
,” Phys. Rev. Lett.
97
, 106602
(2006
).35.
R. E.
Franklin
and R. G.
Gosling
, “The structure of sodium thymonucleate fibres. I. The influence of water content
,” Acta Crystallogr.
6
, 673
–677
(1953
).36.
A.
Tkatchenko
, M.
Rossi
, V.
Blum
, J.
Ireta
, and M.
Scheffler
, “Unraveling the stability of polypeptide helices: Critical role of van der Waals interactions
,” Phys. Rev. Lett.
106
, 118102
(2011
).37.
K.
Wang
, “DNA-based single-molecule electronics: From concept to function
,” J. Funct. Biomater.
9
, 8
(2018
).38.
M.-H.
Chen
, G.-C.
Guo
, and L.-X.
He
, “Systematically improvable optimized atomic basis sets for ab initio calculations
,” J. Phys.: Condens. Matter
22
, 445501
(2010
).39.
P.-F.
Li
, X.-H.
Liu
, M.-H.
Chen
, P.-Z.
Lin
, X.-G.
Ren
, L.
Lin
, C.
Yang
, and L.-X.
He
, “Large-scale ab initio simulations based on systematically improvable atomic basis
,” Comput. Mater. Sci.
112
, 503
(2016
).40.
See http://abacus.ustc.edu.cn for the ABACUS software webpage.
41.
D. R.
Hamann
, M.
Schlüter
, and C.
Chiang
, “Norm-conserving pseudopotentials
,” Phys. Rev. Lett.
43
, 1494
–1497
(1979
).42.
L.
Kleinman
and D. M.
Bylander
, “Efficacious form for model pseudopotentials
,” Phys. Rev. Lett.
48
, 1425
(1982
).43.
J. P.
Perdew
, K.
Burke
, and M.
Ernzerhof
, “Generalized gradient approximation made simple
,” Phys. Rev. Lett.
77
, 3865
(1996
).44.
W.
Kohn
and L. J.
Sham
, “Self-consistent equations including exchange and correlation effects
,” Phys. Rev.
140
, A1133
(1965
).45.
S.
Grimme
, “Semiempirical GGA-type density functional constructed with a long-range dispersion correction
,” J. Comput. Chem.
27
, 1787
(2006
).46.
P.
Jurečka
, J.
Šponer
, J.
Černý
, and P.
Hobza
, “Benchmark database of accurate (MP2 and CCSD(T) complete basis set limit) interaction energies of small model complexes, DNA base pairs, and amino acid pairs
,” Phys. Chem. Chem. Phys.
8
, 1985
(2006
).47.
K.
Lejaeghere
, G.
Bihlmayer
, T.
Bjoerkman
, P.
Blaha
, S.
Bluegel
, V.
Blum
, D.
Caliste
, I. E.
Castelli
, S. J.
Clark
, A.
Dal Corso
, S.
de Gironcoli
, T.
Deutsch
, J. K.
Dewhurst
, I.
Di Marco
, C.
Draxl
, M.
Dulak
, O.
Eriksson
, J. A.
Flores-Livas
, K. F.
Garrity
, L.
Genovese
, P.
Giannozzi
, M.
Giantomassi
, S.
Goedecker
, X.
Gonze
, O.
Granaes
, E. K. U.
Gross
, A.
Gulans
, F.
Gygi
, D. R.
Hamann
, P. J.
Hasnip
, N. A. W.
Holzwarth
, D.
Iusan
, D. B.
Jochym
, F.
Jollet
, D.
Jones
, G.
Kresse
, K.
Koepernik
, E.
Kuecuekbenli
, Y. O.
Kvashnin
, I. L. M.
Locht
, S.
Lubeck
, M.
Marsman
, N.
Marzari
, U.
Nitzsche
, L.
Nordstrom
, T.
Ozaki
, L.
Paulatto
, C. J.
Pickard
, W.
Poelmans
, M. I. J.
Probert
, K.
Refson
, M.
Richter
, G.-M.
Rignanese
, S.
Saha
, M.
Scheffler
, M.
Schlipf
, K.
Schwarz
, S.
Sharma
, F.
Tavazza
, P.
Thunstroem
, A.
Tkatchenko
, M.
Torrent
, D.
Vanderbilt
, M. J.
van Setten
, V.
Van Speybroeck
, J. M.
Wills
, J. R.
Yates
, G.-X.
Zhang
, and S.
Cottenier
, “Reproducibility in density functional theory calculations of solids
,” Science
351
, 1411
(2016
).48.
W.
Zhang
, P.
Lin
, X.
Ren
, and L.
He
, “Numerical atomic basis sets for ab initio calculations: The generating procedure and benchmark tests
” (unpublished).49.
See http://www.scfbio-iitd.res.in/software/drugdesign/bdna.jsp for DNA Sequence to Structure online tool webpage.
50.
S.
Arnott
, P. J.
Campbell-Smith
, and R.
Chandrasekaran
, Handbook of Biochemistry and Molecular Biology
, 3rd ed., Nucleic Acids (CRC Press
, Cleveland
, 1976
), pp. 411
–422
.51.
S.
Bag
, S.
Mogurampelly
, W. A.
Goddard
III, and P. K.
Maiti
, “Dramatic changes in DNA conductance with stretching: Structural polymorphism at a critical extension
,” Nanoscale
8
, 16044
–16052
(2016
).52.
A.
Garai
, S.
Mogurampelly
, S.
Bag
, and P. K.
Maiti
, “Overstretching of B-DNA with various pulling protocols: Appearance of structural polymorphism and S-DNA
,” J. Chem. Phys.
147
, 225102
(2017
).53.
A.
Aggarwal
, S.
Bag
, and P. K.
Maiti
, “Remarkable similarity of force induced dsRNA conformational changes to stretched dsDNA and their detection using electrical measurements
,” Phys. Chem. Chem. Phys.
20
, 28920
–28928
(2018
).54.
A. M.
Naserian-Nik
, M.
Tahani
, and M.
Karttunen
, “Pulling of double-stranded DNA by atomic force microscopy: A simulation in atomistic details
,” RSC Adv.
3
, 10516
–10528
(2013
).55.
G.-H.
Zheng
, X.-J.
Lu
, and W. K.
Olson
, “Web 3DNA—A web server for the analysis, reconstruction, and visualization of three-dimensional nucleic-acid structures
,” Nucleic Acids Res.
37
, W240
(2009
).56.
D. W.
Ussery
, “DNA structure: A-, B- and Z-DNA helix families
,” in eLS
(American Cancer Society
, 2002
).57.
J. M.
Vargason
, K.
Henderson
, and P. S.
Ho
, “A crystallographic map of the transition from B-DNA to A-DNA
,” Proc. Natl. Acad. Sci. U. S. A.
98
, 7265
–7270
(2001
).58.
X.-J.
Lu
, Z.
Shakked
, and W. K.
Olson
, “A-form conformational motifs in ligand-bound DNA structures
,” J. Mol. Biol.
300
, 819
–840
(2000
).59.
R. E.
Dickerson
, “DNA structure from A to Z
,” in DNA Structures Part A: Synthesis and Physical Analysis of DNA
, Methods in Enzymology Vol. 211 (Academic Press
, 1992
), pp. 67
–111
.60.
T. E.
Cheatham
III and P. A.
Kollman
, “Molecular dynamics simulations highlight the structural differences among DNA:DNA, RNA:RNA, and DNA:RNA hybrid duplexes
,” J. Am. Chem. Soc.
119
, 4805
–4825
(1997
).61.
S.
Harteis
and S.
Schneider
, “Making the bend: DNA tertiary structure and protein-DNA interactions
,” Int. J. Mol. Sci.
15
, 12335
–12363
(2014
).62.
J.-F.
Xu
, L.-Y.
Zhao
, Y.-Y.
Xu
, W.-X.
Zhao
, P.
Sung
, and H.-W.
Wang
, “Cryo-EM structures of human RAD51 recombinase filaments during catalysis of DNA-strand exchange
,” Nat. Struct. Mol. Biol.
24
, 40
–46
(2017
).63.
A.
Garai
, S.
Saurabh
, Y.
Lansac
, and P. K.
Maiti
, “DNA elasticity from short DNA to nucleosomal DNA
,” J. Phys. Chem. B
119
, 11146
–11156
(2015
).64.
M.
Santosh
and P. K.
Maiti
, “Structural rigidity of paranemic crossover and juxtapose DNA nanostructures
,” Biophys. J.
101
, 1393
–1402
(2011
).65.
C. G.
Baumann
, S. B.
Smith
, V. A.
Bloomfield
, and C.
Bustamante
, “Ionic effects on the elasticity of single DNA molecules
,” Proc. Natl. Acad. Sci. U. S. A.
94
, 6185
–6190
(1997
).66.
D.
Watkins
, C.-J.
Gong
, P.
Kellish
, and D. P.
Arya
, “Probing a-form DNA: A fluorescent aminosugar probe and dual recognition by anthraquinone-neomycin conjugates
,” Bioorg. Med. Chem.
25
, 1309
–1319
(2017
).67.
A. E.
Maris
, M. R.
Sawaya
, M.
Kaczor-Grzeskowiak
, M. R.
Jarvis
, S. M. D.
Bearson
, M. L.
Kopka
, I.
Schröder
, R. P.
Gunsalus
, and R. E.
Dickerson
, “Dimerization allows DNA target site recognition by the NARL response regulator
,” Nat. Struct. Biol.
9
, 771
–778
(2002
).68.
L.
Dostál
, C.-Y.
Chen
, A. H.-J.
Wang
, and H.
Welfle
, “Partial B-to-A DNA transition upon minor groove binding of protein Sac7d monitored by Raman spectroscopy
,” Biochemistry
43
, 9600
–9609
(2004
).© 2019 Author(s).
2019
Author(s)
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