Rational Design of Magnetic DNA Motifs with Diradical Character

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Rational Design of Magnetic DNA Motifs with Diradical Character: Nitroxide Functionalization of Nucleobases Peiwen Zhao, and Yuxiang Bu J. Phys. Chem. C, Just Accepted Manuscript • DOI: 10.1021/acs.jpcc.8b02517 • Publication Date (Web): 02 Jul 2018 Downloaded from http://pubs.acs.org on July 9, 2018

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The Journal of Physical Chemistry

Rational Design of Magnetic DNA Motifs with Diradical Character: Nitroxide Functionalization of Nucleobases Peiwen Zhao†, Yuxiang Bu*,†,‡ †

School of Chemistry and Chemical Engineering, Shandong University, Jinan, 250100, People’s Republic of China

‡

School of Chemistry and Chemical Engineering, Qufu Normal University, Qufu, 273165, People’s Republic of China

ABSTRACT: In the current work, the nitroxide radical groups are utilized to functionalize the nucleobases, obtaining the nucleobase diradical building blocks for magnetic DNA with significant ferromagnetic or antiferromagnetic coupling characteristics. The nitroxide functionalization strategies include introduction of nitroxide radical group to the carbon site and oxidization of the amino group in nucleobases, and the diradical-functionalized nucleobases are denoted by

2NO

X, where X=A, G, T, and C bases. The DFT calculations

reveal that these nitroxide diradicalized nucleobases are stable and have large magnetic spin coupling magnitudes.

Almost all of them possess antiferromagnetic-like spin coupling

characteristics with considerably large spin coupling constants (J = -671.7 (2NOA1), -463.3 (2NOA3), -370.5 (2NOG), -494.9 (2NOC1), -3265.5 (2NOT), and -2445.5 cm-1 (2NOC3) expect for 2NO

C2 and

2NO

A2 which have the ferromagnetic-like spin coupling characteristics (J = 149.1

and 440.7 cm-1), respectively.

The spin alternation rule works well for these

nitroxide-diradicalized nucleobases in interpreting the magnetic spin coupling characters although such heterocyclic nucleobases (purine and pyrimidine) are as the couplers, and the spin coupling constants present good linear relationships with the HOMO-LUMO energy gaps and the energy gaps between the closed-shell singlet and triplet state of these nucleobase diradicals.

Besides, their magnetic coupling properties are also analyzed by the shape of the

SOMOs and SOMO-SOMO energy splitting of the triplet state, the H-bonding with their complementary nucleobases and the nitroxide radical group orientations.

Clearly, this work

provides a novel strategy for the rational design of the magnetic DNA motifs with well-defined diradical characters and also provides insights into the spin coupling interactions in these

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nucleobase-based magnet building blocks of the magnetic DNA nanowires. 

INTRODUCTION It is well known that due to its unique internal structure, diradicals are considered as one

of the most promising magnetic molecules.1-8 In the past few decades, the study of organic magnetic material molecules has attracted great impetus. Organic diradicals as reaction intermediates and various promising applications (such as magnetic and spintronic properties, magneto-optic behavior, and superconductivity and their potential applications) make the molecular materials an interesting area to explore.9-12 lively.

However, in general, they are fairly

Short-lived species play a crucial role in molecular transformation and materials

science.

Scientists have pioneered many of the pioneering approaches to detecting and

characterizing these short-lived intermediates.13,14 In theory, the biocompatibility of magnetic materials may lead to some prospective therapeutic applications, such as in the field of magnetic imaging, high-temperature oncology and the like.

Stable organic radicals can be

separated and processed in pure state, the most suitable for the magnetic study of organic molecules.6,15-17 In recent years, research on organic molecular materials with special biological functions has gradually become one of the hot topics.

Due to its good ability of molecular recognition

and self-assembly, the design and modification of DNA molecules are particularly attractive.18-21 To date, investigations into the modification of biological nanomaterials, especially DNA molecules, have been mainly focused on the modification of metals and carbon skeletons.

When it comes to radicals, it's always about their DNA damage.

series of the modified nucleobases have been explored.

Last few years, a

Importantly, DNA can form

well-ordered and fully-controllable π-aromatics through hydrogen bonding of complementary bases between purine and pyrimidine bases. organic biomaterials.

This feature is not available from most other

Besides, the DNA-based materials are also useful for tuning

alignment/interactions of organic/inorganic functional groups.

Therefore, DNA may have

potential applications in charge transport and magnetic exchange of nanomaterials.22-26 Admittedly, DNA bases also have some limitations. paired by hydrogen bonds.

They have only four and can only be

However, this also provides more space and ideas for our design 2


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and transformation.27 Nowadays, the transformation of DNA molecules is realized mainly from three aspects. First, the development of new assembly structures include the incorporation of other nanoparticles, such as metal modification (M-DNA), hybridization, etc.. Second, DNA bases are modified by ring expansion or metal modification, such as changing their magnetic, electrical and optical properties.28-35 In the latter case, our team has designed a series of basic monomer and base pair combinations, and discussed in more detail and extensively.36-41 We have successfully introduced radicals into DNA bases, giving them new magnetic properties, while also greatly improving their electronic properties, redox activity and the like.39,42 However, slightly less than that, while giving radical properties, the size of radical bases is also widened, which to some extent weakens the magnetic coupling between the radicals. Therefore, the magnetic coupling properties of such novel DNA diradicals are not very prominent. The third is to consider the selective oxidation of DNA bases, that is, without changing the structure of the main molecular structure, we can access radicals on the molecule or oxidize their groups to radicals.

In view of this idea, we note that the carbon-based

diradicals such as phenalenyl-, verdazyl-, triphenylmethyl-, dithiazolyl- and nitroxide-based molecules or molecules have become the most popular research topic recently due to their special structures and favorable properties.43-47 Because the nitroxide-based molecules or molecular patches are distinguished by the advantages of high information storage density, non-conductivity, high plasticity, and high bioactivity, these diradicals are believed to be probably one of the most important functionalized diradical carbon materials. Inspired by this, we combine the nitroxide (>N-O•) radicals with DNA nucleobases to design and modify four intramolecular nitroxide diradical nucleobases to study their diradical or spin coupling properties and discuss in detail the influencing factors of their magnetic coupling characteristics.

As a potential building block of the self-assembled structures and

electronic nanodevices, we believe this is a promising conductive molecular line of building materials and will have broad application prospects in the fields of magneto-optical devices and magnetic recording materials.

In this work, we further explore the radical functionalization

scheme of nucleobases by considering the introduction of nitroxide radical groups and/or oxidizing the amino groups (-NH2) and design eight diradical nucleobases, and hope these 3



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novel nitroxide diradical nucleobases could have well-defined diradical characters and exhibit the expected ferromagnetic (FM) or antiferromagnetic (AFM) spin coupling characteristics. Using the density functional theory (DFT) method, we computationally examine the structures and electronic properties with an emphasis on the magnetic spin coupling characteristics of the designed nitroxide diradical nucleobases. As expected, these radical-functionalized nucleobases exhibit noticeable intramolecular magnetic spin coupling characteristics.

Except for one

adenine-based and one cytosine-based diradicals which have the FM-like spin coupling feature, all other nitroxide diradical nucleobases exhibit AFM-like spin coupling characteristics, particularly the pyrimidine-based diradicals with considerably large AFM-like spin coupling interactions.

We further find that the spin coupling constants (J) present good linear

relationships with the molecular orbital energy level of the nitroxide diradical bases (in their closed-shell state) and the energy difference of the closed-shell singlet and triplet state, and are also associated with the shape of SOMO and the SOMO-SOMO energy splittings.

In addition,

the hydrogen bonding by their complementary nucleobases and the nitroxide group orientation do not switch the magnetic spin coupling characters but considerably affect the sizes of the magnetic spin coupling constants.

Clearly, this work provides insights into the intriguing spin

coupling phenomena in the nucleobase-based molecular materials and also offers a promising strategy to design the nitroxide diradical nucleobases, paving the way for their application as the promising building blocks of the biomimetic magnetic nanomaterials (e.g. magnetic DNA) or nanodevices. 

DESIGN STRATEGY AND COMPUTATIONAL DETAILS Design Strategy. With the aim of designing stable diradicalized DNA bases, we modify

the purine and pyrimidine with two nitroxide radical groups.

Here, four nucleobases (G, A, C,

and T) are modified by introducing stable, extensively used radical group (e.g. nitroxide radical) to the nucleobases or oxidizing the amino group (-NH2) according to the following three ways: (1) oxidizing the amino groups (-NH2) of nucleobases to be the nitroxide (>N-O•) radical group; (2) Nitroxide (>N-O•) radical group is introduced at the carbon sites of the purine base (C8 for G and C8 or C2 for A); (3) Nitroxide (>N-O•) radical group is introduced to the C5 or C6 site of the pyrimidine base by replacing the existing methyl group (-CH3) if available. The schematic 4


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diagram is shown in Scheme 1 and it is hoped that these novel nitroxide diradical DNA bases will exhibit outstanding FM or AFM spin coupling characteristics.

Here, we mainly use the

density functional theory (DFT) method to test the magnetic spin coupling characteristics of the designed nitroxide diradical nucleobases. Their stable ground state structures, magnetic spin coupling properties, spin delocalization and spin polarization characteristics, and other influencing factors are determined by comparing their closed-shell (CS) singlet, broken-symmetry (BS) singlet and triplet (T) states.

In particular, we can further analyze the

relative orientation effect of the two nitroxide (>N-O•) radical groups in the nucleobase molecule and the effects of hydrogen bonding with the complementary nucleobase on the magnetic spin coupling characteristics and regulation.

As expected, the intramolecular

magnetic spin coupling characteristics of them are obvious. Computational Details.

Calculations were performed on the nitroxide diradical

nucleobases to obtain a comprehensive understanding of their structural, electronic, and magnetic spin coupling properties using the Gaussian 09 package.48 The molecular geometric optimizations, frequency analyses, and energy calculations of the closed-shell (CS) singlet, broken symmetry (BS) open-shell singlet, and triplet (T) state of them were performed at the unrestricted spin polarized theory level (M06-2X) with a 6-311++G (d,p) basis set.49 An expression of the magnetic exchange coupling constant is given as:50 EBS – ET J = – T BS where EBS and ET are the energies of unrestricted open-shell BS singlet and T states, while BS and T are the corresponding average spin square values, respectively.

The

‘‘guess=mix’’ keyword is used in the open-shell singlet state optimizations. In addition, within the spin projection theory, the diradical character is also estimated using the diradical index (yPUHF) from the spin-projected unrestricted Hartree–Fock theory (UHF) as:51 y = 1–2t/(1+t2).

In fact, this scheme can be also applied to the UDFT situation.

We use this formula in the description of diradical character. That is, y(DFT) = 1–2t/(1+t2), where t is defined as the orbital overlap and is calculated using the occupation number (n) of the UDFT natural orbitals.

The numbers of UDFT natural orbital occupations corresponding

to HOMO and LUMO (denoted by nHOMO and nLUMO) are 1+t and 1-t, respectively, and thus t = 5



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(nHOMO - nLUMO)/2. 

RESULTS AND DISCUSSION According to the above-mentioned design scheme and using nitroxide radical groups as

spin sources, we obtain 8 nitroxide-based diradical nucleobases (Scheme 1), and then explore their structural characters, stability and spintronics properties.

As shown in Figure 1, each of

the nucleobases, G and T, has two nitroxide group linking sites, and therefore they can form only one nitroxide diradical nucleobase, respectively.

While there are three modifying sites

for A and C, and thus they can form three types of nitroxide diradical structures, respectively. In the meantime, we notice two factors that may affect the magnetic coupling characteristics, namely, the orientation of the nitroxide radical and the hydrogen bond with its complementary nucleobase. Therefore, similar to previous DNA ring-expanding diradicals, we also examine the intermolecular nitroxide diradical base pairs for their magnetic couplings.

In order to further

understand the basic diradical of magnetic coupling interactions, we gradually consider their geometry, electrochemistry and magnetic spin coupling, and conduct a detailed analysis and discussion.

In particular, spin alternating rules, spin density distributions and SOMO

distributions are also used to characterize all nitroxide diradicals in their ground states. Detailed analyses and discussions are as follows: Geometric Characters, Energetics, and Electronic Factors. As we all know, we adopt three ways to transform the natural bases.

Schematic diagrams of nitroxide diradical bases are

The modification sites and representations of them are as follows:

2NO

(C8 and -NH2 group sites), 2NOA2 (C2 and -NH2 group sites), 2NOA3 (C2 and C8 sites),

2NO

shown in Figure 1.

A1 C1

(C5 and -NH2 group sites), 2NOC2 (C6 and -NH2 group sites), 2NOC3 (C5 and C6 sites), 2NOG (C2 and C8 sites) and

2NO

T (C5 and C6 sites).

nitroxide diradicals are meta-distributions, the ortho-distributions and the

2NO

A3 and

In details, the

2NO

C1,

2NO

C3 and

2NO

A1,

2NO

A2 and

2NO

C2

2NO

T nitroxide diradicals are

2NO

G nitroxide diradicals are located at both ends of the

bases. Through optimization and frequency calculations, we obtain similar structures to the natural nucleobases, all of which have stable, planar configurations.

The energies (a.u.),

values of diradical base’s BS singlet state and triplet state are shown in Table 1.

6


The two

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nitroxide radical groups currently under study all maintain good planarity.

The energies of the

individual states in Table 1 show that, except for the 2NOA2 and 2NOC2 nitroxide diradical bases, the singlet energies of the other nitroxide diradical bases are all lower than those of the triplet states, i.e., ECS > ET > EBS. While the ground state of

That is, they all possess an open-shell singlet ground state.

2NO

C2 base is the open-shell triplet.

contamination values of the BS states of

2NO

A1,2NOA3,

2NO

G,

We note that the spin

2NO

C1 and

2NO

C3 nitroxide

diradical bases range from 0.986 to 1.007, indicating that they have completely open-shell BS ground state and are the typical diradicals.

For 2NOT and 2NOC2 nitroxide diradical bases, their

spin contamination values are 0.470 and 0.618, respectively. Although the values are slightly small, they also indicate a sufficient degree of diradicalization of their BS states. For a comparison, we used the B3LYP method for optimizations and frequency analyses for each of the A/G/C/T diradical nucleobases.

The relevant data are available in Table S1 (the SI).

We

can find that the properties of the magnetic coupling constants obtained by the two methods are consistent.

Considering that the M06-2X method has certain advantages in dealing with weak

interactions, we chose it to investigate our systems.

In addition, the M06-2X results are also

confirmed by the single-point calculations on some representative systems at the MP2/6-311++G(d,p) level using the M06-2X/6-311++G(d,p) geometries. The HOMO-LUMO energy gaps of the natural and nitroxide diradical nucleobases and the SOMOα-LUMOα energy gaps are also determined to reveal the fact that the nitroxide diradical nucleobases are more stable than the natural bases, as shown in Figure 2.

The orbital energy

levels (CS state) of normal bases range from 6.85 to 7.86 eV, while the orbital energy levels (CS state) of nitroxide diradical bases are reduced below 5.2 eV, or even 2.53 eV.

And, the

SOMOα-LUMOα energy gaps of nitroxide diradical bases under the T state vary from 5.62-6.49 eV.

Taking

2NO

A1 base as an example, we can see that the HOMO-LUMO energy

gap of A is 7.38 eV, while that of gap of it is 6.07 eV.

A1 reduces to 3.57 eV and the SOMOα-LUMOα energy

2NO

This explains the fact that the ground states of natural and nitroxide

diradical bases are closed-shell and open-shell states, respectively.

Meanwhile, the HOMO,

LUMO and HOMO-LUMO energy gaps (eV) of 2NOX’s (X=A, G, C, T base) ground states, the SOMO-SOMO energy gaps of their triplet states and the energy gaps between CS singlet and triplet states are supplied in Table S2( the SI).

We find that their orbital level difference is also 7



larger than others.

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This result seems to indicate that when the orbital energy level difference

is within 4.0-5.0 eV and the spin pollution is nearly half, the magnetic spin coupling of the nitroxide diradical nucleobases are noticeable. Magnetic Spin Coupling Properties. Furthermore, the associated magnetic exchange coupling constants (J) calculated at the (U) M062X/6-311++G(d,p) level are also collected in Table 1.

Interestingly, their magnetic coupling constants are quite different.

The J values of

2NO

A1, 2NOA3, 2NOG, 2NOC1 are -671.66 cm-1, -463.26 cm-1, -370.52 cm-1 and -494.85 cm-1 while

those of

2NO

2NO

C2 and

T and

2NO

C3 are -3265.52 cm-1 and -2445.53 cm-1, respectively.

2NO

A2 are 149.09 cm-1 and 440.69 cm-1.

In other words, most of them have

obvious AFM-like spin coupling characteristics, and the J of prominent.

However,

characteristics.

2NO

C2 and

In addition, J of

2NO

T and

2NO

C3 are particularly

2NO

A2 are characterized by the FM-like spin coupling

Our calculations show that the magnetic coupling constants of

2NO

T and

2NO

C3 are noticeable and the spin contamination values are around 0.5. In order to further

express their relationship more intuitively, we make linear correlation diagrams between the magnetic coupling constants J and the HOMO-LUMO energy gaps and the energy gaps between the CS singlet and triplet state.

As shown in Figure 3, the HOMO-LUMO energy

level difference distribution region of nitroxide diradical nucleobases is 2.5-5.5 eV.

When the

gap is greater than 4.5 eV, the AFM-like spin coupling characteristic reaches -2000 cm-1 or more, showing good AFM spin coupling characteristics.

When the gap difference is less than

2.53 eV, the FM-like coupling characteristics is exhibited.

Considering further the

relationship between the energy gaps between the CS singlet and triplet state and magnetic coupling constants, we find that the AFM spin coupling properties of nitroxide diradical nucleobases are the strongest (2NOT and

2NO

C3) when the singlet-triplet level difference is less

than -5 kcal/mol. When their energy difference reaches more than 30 kcal/mol, the nitroxide diradical base shows a FM-like coupling character (2NOC2).

In order to more fully explain

their diradical features, we also calculate the orbital occupation numbers, overlap integral (T) and the percentage of diradicals. occupancies of HOMO in

2NO

Detailed information are shown in Table 2, the orbital

A1-3 , 2NOG,

2NO

C1-2 nitroxide diradical nucleobases are in a

range of 1.047-1.199 and the orbital occupancies of LUMO of them are 0.801-0.953, indicating that the electrons on HOMO are almost completely excited to LUMO, with a high degree of 8


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diradicalization.

The diradical percentages of them are 64.4%, 90.7%, 71.4%, 73.6%, 61.7%,

and 81.1%, respectively.

2NO

Furthermore, the occupancy numbers of LUMO of

nitroxide diradical nucleobases is 0.254 and 0.361.

2NO

T and

C3

Their diradical percentages are only

4.16% (2NOT) and 9.25% (2NOC3). To confirm the diradical characters of these nitroxide diradicals, we verify them using the CASSCF(8,8) method and the results are shown in Table S3 (the SI) which indicate the degree of diradical in nitroxide diradicals consistent with the magnetic coupling constants.

The diradical character indexes determined by the two

calculational methods are basically in agreement with each other, confirming the diradical characters of these designed diradical nucleobases.

Clearly, the magnetic coupling constant is

negatively correlated with the diradical percentage.

As a consequence, the result shows two

points: i)

2NO

2NO

T and

C3 nitroxide diradical bases are indeed diradicalized, and their ground

states are the BS states; ii) their degree of diradical character is not as ideal as other nitroxide diradical bases.

Clearly, the above analyses are in accordance with each other.

Spin Polarization and SOMO Analyses. To further elucidate the magnetic spin coupling properties, we analyze the rule and characteristics of spin-polarization and SOMOs.

At first,

the spin alternation rule is a reliable guideline for predicting the nature of the ground state.3,52-54 Following this spin alternation rule, it is reported that the sign of magnetic exchange coupling constants (J) is determined by the number of bonds in the spin interacting pathway through the coupler and in this work, the couplers are the nucleobases. 2NO

the

A1-3, 2NOG, 2NOT,

2NO

C1-3 nitroxide diradical nucleobases are displayed in Figure 4.

Here, we can clearly see the spin polarization paths. 2NO

The scheme of spin alteration for

A3, 2NOG, 2NOT, 2NOC1, and

Hence, according to this rule,

2NO

A2 and

A1,

2NO

C3 nitroxide diradical nucleobases have negative J values as

the number of bonds in their coupling pathways are odd through their coupler bases. the

2NO

While,

2NO

C2 result in positive J values due to the even spin-interacting pathways

through the couplers.

Simultaneously, we also notice that both purine nitroxide diradical

nucleobases have two spin-polarized paths, which are the intra-molecular path and extra-molecular path.

That is to say, their radicals can be polarized both within the base ring

and also along the outer ring of bases, and their two nitroxide radicals are almost separated by a long distance.

In contrast, pyrimidine radicals are only polarized outside the base circle.

Both of their nitroxide radicals are neighboring, with the exception of the 9


2NO

C2 bases.

It is


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noteworthy that we find that the modified thymine (T) nitroxide diradical nucleobase has a very similar configuration to the

2NO

C3 nitroxide diradical one. Combined with their magnetic

coupling constants, perhaps we can explain that the introduction of nitroxide radicals at the C-based sites is one of the important reasons for the diradical nucleobases to exhibit very strong AFM-like couplings.

In order to more vividly describe their characters of diradicals, As we all known, Hoffmann suggested that55 if the energy

SOMOs are provided in Figure 5.

difference between two consecutive SOMOs (ΔESS) is less than 1.5 eV, two non-bonded electrons would occupy different degenerate orbitals to minimize the electrostatic repulsion of their spin-parallel orientation, resulting in a triplet ground state.

At the same time,

Constantinides et al. regarded that molecules possess singlet ground states when ΔESS > 1.3 eV based on the calculations of a series of linear and angular polyheteroacenes. Based on these two points of view, we find that our nitroxide diradical nucleobases also follow this rule (Table S2, the SI). When the ΔESS > 1.2 eV, the 2NO

T (2.56 eV)

2NO

C1 (1.67 eV) and

2NO

A1 (1.22 eV), 2NOA2 (1.38 eV), 2NOG (1.80 eV),

2NO

C3 (1.78 eV) nitroxide diradical nucleobases all have

singlet ground states because when a large ΔESS appears, the electrostatic repulsion of two nonbonding electrons is strong and spin antiparallel orientation is favorable. 2NO

A1 (0.59 eV) and

While, for the

C3 (0.26 eV) ones, their ΔESS are small, which may indicate that the

2NO

electrostatic repulsion between two nonbonding electrons in an atomic orbital is weak, and a spin-parallel orientation thus occurs, exhibiting a triplet ground state.

In the meantime, the

shapes of SOMOs can also determine whether a diradical possesses AFM or FM spin coupling characteristic.

Borden and Davidson pointed out that when the two SOMOs non-disjoint, the

molecule shows a T ground state.55 However, when the BS state energy is lower than the corresponding T state, their SOMOs are disjoint. Just as shown in Figure 5, SOMOs of 2NOX (X=A1, A3, G, T, C1, C3 nitroxide diradical nucleobases) are disjoint, leading to a BS ground state with AFM coupling character.

While, for the

2NO

A1 and

2NO

C2 ones, the SOMO

combination remains non-disjoint (atoms are common) and thus their ground states are the T state, with a FM coupling character. Spin Density Distributions. To obtain a better understanding of the above-mentioned magnetic phenomena, we further analyze the electron spin-density distributions.

Similarly, in

the case of a favorable rotational or ground state, the spin density in the center of adjacent 10


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atoms in the π-conjugated diradical has a preference for opposite spins, i.e. alternating α and β spins. And for undesired spin state or excited states, the two spin-polarized atoms adjacent to the spin-polarized mismatch exhibit the same α or β spin.

From Figure 5, we can clearly see

the distribution of spin density in the entire nitroxide diradical nucleobases.

Also, in order to

do a quantitative analysis, we list the values of the electron spin density concentratedly distributing in the nitroxide diradical nucleobases and detailed data can be seen in Figure 6. At the same time, we also plot the spin-polarized path in Figure 6 to allow us to combine spin polarization and spin density for a more detailed analysis.

The purple ring and red ring

represent the positive and negative phase distributions of electron spin density, respectively. Obviously, the results show that the Mulliken atomic spin densities of these nitroxide diradical nucleobases are associated with the spin-polarized path. As shown,

2NO

2NO

A1-3 and

G have

two spin polarization paths and the spin densities are distributed throughout the whole purine molecule but with a large number of electrons in the nitroxide group. Taking the

2NO

A1 base

as an example, the electron spin density percentage on both the nitroxide radicals are 72.6% and 60.1%.

For the

2NO

C1 and

2NO

C2 nitroxide diradical nucleobases, one of their nitroxide

radical is located on the hydrogen bonding surface.

The electron spin density percentage on

the nitroxide groups of them are 73.8%, 74.8% and 80.2%, 81.4%, respectively. again at the

2NO

T and

Looking

2NO

C3 nitroxide diradical nucleobases, since the two nitroxide radical

groups are located opposite the hydrogen bonding surface, they do not participate in any bonding, so most of their spin densities are concentrated in the only spin-polarized path, which possess a strong coupling ability.

Perhaps this is one of the reasons why their magnetic spin

coupling is even larger, compared to the base-radical magnetic coupling interactions reported so far. In summary, we find that spin polarization, SOMOs, and spin density distribution are closely related to their magnetic spin coupling properties.

Through the spin polarization rule

and SOMO shapes we can directly determine whether the magnetic spin coupling characteristic is the AFM or FM spin coupling. Moreover, the spin density distribution can help check the strength of the magnetic spin couplings. Pairing H-Bond Effect.

In designing nitroxide diradical nucleobases, we retain the 11



Page 12 of 28

Watson-Crick hydrogen bonding surface, which preserves the normal pairing ability of nucleobases, given their normal biological function.

Therefore, for these nitroxide diradical

nucleobases, it is necessary to examine the magnetic coupling characteristics of the diradical base pairs.

At first, the H-bonding energies of

2NO

X-Y (X=A, G, T, C and Y is the

corresponding complementary base) are shown in Figure S1 (the SI).

The bonding energies of

normal A-T and G-C base pairs are -12.67, -25.72 kcal/mol. By comparison, we see that almost all nitroxide diradical base pairs have a lower binding energy than normal base pairs, except for the G-2NOC2 and G-2NOC3 base pairs. A-2NOT > 2NOA3-T> 2NOA2-T> 2NOA1-T,

The order of their binding stability is

2NO

G-C > G-2NOC1 > G-2NOC2 > G-2NOC3.

Then, in

Table S4 (the SI), we provide a schematic structure of intramolecular nitroxide diradical base pairs as well as their energies and spin contamination values in the BS and T states, and the magnetic coupling constants are also provided in the table. Interestingly, we find that the hydrogen bonding effect plays a major role in the G-2NOC2 nitroxide diradical base pair.

In

contrast to Table 1, we can see that the G-2NOC2 base pair has a magnetic coupling constant of -88.73 cm-1.

In other words, its magnetic coupling properties have changed from the FM to

AFM spin couplings. For other nitroxide diradical base pairs, we can see that the magnetic coupling constants of

2NO

A1-T,

2NO

A2-T,

2NO

A3-T, A-2NOT, 2NOG-C, G-2NOC1 and G-2NOC3 are

-719.80, 449.43, -454.18, -3216.34, -379.16, -501.87 and -2446.53 cm-1, respectively. Compared with the single nitroxide diradical nucleobases, their absolute values of magnetic coupling constants increase to some extent, expect for the

2NO

A3-T and A-2NOT base pairs.

Meanwhile, there is almost no obvious change in the magnetic spin coupling characteristics of the G-2NOC3 base pair.

These results indicate that when the nitroxide diradical nucleobases

are involved in the life function, their diradical characters can still exist, and the hydrogen bonds have the function of promoting magnetic coupling increase to some extent.

The

enhancement magnitudes of the diradical magnetic couplings in the nitroxide diradical nucleobase pairs are 2NOA1-T > 2NOG-C >2NOA2-T > G-2NOC1 > G-2NOC3.

As for the 2NOA3-T

and A-2NOT ones, their J values are reduced by 9.08 cm-1 and 49.18 cm-1, respectively. also provide their SOMOs and spin-density profiles in Figure S2 (the SI) as well.

We

Obviously,

the profile of their single occupation orbitals and spin density distributions have not changed much.

The SOMOs of the

2NO

A1-T,

2NO

A3-T, A-2NOT, 12


2NO

G-C, G-2NOC1 and G-2NOC3

Page 13 of 28 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


nitroxide diradical base pairs are still disjoint, and thus they all have a BS ground state. However, the SOMOs of the 2NOA1-T one are non-disjoint, leading to a T ground state.

If we

simply judge from the spin alternation rule, these nitroxide diradical base pairs should not change their FM or AFM spin couplings, but the magnetic coupling constants of G-2NOC2 show that its magnetic spin coupling characteristics has indeed changed.

This phenomenon can be

explained by Figure S2 (the SI). As shown, their single occupied orbitals are disjoint, indicating that their ground states are the BS states.

Examining its distribution of the spin

density, we find that the phases of the spin density on the C4 and C5 atom are same, resulting in a change in spin alternation that eventually changes its own magnetic coupling properties. In other words, the ground state of it cannot be judged by the spin alternation rule. Indeed, the magnetic spin coupling properties

Intermolecular Magnetic Spin Coupling.

of intermolecular nitroxide diradical base pairs cannot be ignored.

Therefore, we select a part

of diradical base pairs to illustrate the relevant features of them.

Table S5 (the SI) provides

the structures, energies, spin-pollution values of their open shell singlet state and triplet, and their magnetic coupling constants.

Their SOMOs and spin-density distributions are shown in

Figure S3 (the SI). Since each base molecule only has one nitroxide radical group, this leads to many different combinations. diradical combinations.

Here, we study a total of 10 kinds of intermolecular nitroxide

The results shown that all of the intermolecular nitroxide diradical

base pairs show weak magnetic spin couplings, which is in good agreement with the results obtained in our previous work.39,41,42 Diradical spin coupling between two nucleobases does not follow the spin-alternating rule, and thus we can only determine the magnetic coupling characteristics through the SOMOs and spin density distributions.

Since the two nitroxide

radicals are connected by weak interaction of hydrogen bonds, their magnetic spin coupling characteristics are not remarkable, and their spin coupling constants |J| are between 0-3 cm-1. Finally, we also used the MP2 method to further verify the effect of base pairing on the diradical spin coupling.

We selected four configurations (i.e.

and 1-NOA-2NOT) for calculations.

G-C, A-2NOT, 3-2NOG-2NO C,

2NO

The calculated results are given in Table S6 (the SI).

Their spin coupling constants (J) are -351.87, -3120.93, -0.09 and 2.30 cm-1, respectively. Clearly, these results indicate that the calculated results of both the M06-2X and MP2 methods 13



are basically consistent.

Page 14 of 28

We can conclude that the pairing hydrogen bond has a more

pronounced effect on the magnetic spin coupling characteristics of intramolecular nitroxide diradical base pairs, while it has little effect on the magnetic coupling properties of intermolecular nitroxide diradical base pairs.

In a word, intramolecular nitroxide diradical

base pairs may have more potential applications in nano-molecular materials and bio-functional materials. Orientation Effect of Nitroxide Group. As shown in Figure 1, another factor we must consider is the orientation effect caused by nitroxide radicals. Here we divide them by the direction of the oxygen atoms on the nitroxide radical groups.

Through careful calculations,

we find that not all of the nitroxide radicals have a stable configuration when changing the orientation of the nitroxide radical groups. discuss the nitroxide orientation effect.

Therefore, we choose some configurations to

The molecular structures modified by the nitroxide

orientation, their energies (a.u.) and values of their BS singlet and triplet states can be found in Table S7 (the SI). By optimizations, we get these diradical nucleobases with different nitroxide radical orientations.

The energies and spin coupling constants of each state are

obtained by energy calculations.

At the same time, their SOMOs and spin density

distributions are shown in Figure 4S (the SI). As a whole, their magnetic spin coupling characteristics almost have not changed.

In other words, the

2NO

A1',

2NO

A3',

2NO

G',

2NO

T',

2NO

C3' nitroxide diradical nucleobases all exhibit the AFM coupling properties, while the

2NO

A2' and

2NO

C2' ones behave the FM coupling properties.

Undoubtedly, this fully

demonstrates that the configuration of the nitroxide diradicals within the DNA bases is stable and that the nitroxide radicals may exist in different orientations. J values of the 2NOA1-3',

2NO

In detail, we notice that the

G' and 2NOC2' nitroxide diradical nucleobases are -778.70, 457.52,

-588.92, -488.13 and 150.72 cm-1, respectively, which are larger than those of 2NOX (X=A1-3, G, C2).

While, the J values of

respectively.

2NO

T' and

2NO

C3' reduce to -3178.03 and -2061.47 cm-1,

These observations, we think, are mainly due to the change of radical orientation

resulting in the degrees of spin density distribution and spin coupling between the two radicals greatly different. Taking a more observable example, such as the

2NO

T' base, the change of

nitroxide radical orientation increases the spatial distance between them, and the spin coupling magnitude is thus weakened.

Other base structures show a similar situation also. Notably, 14


Page 15 of 28 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


the spin alternation rule is still applicable when considering the orientation effect.

In short,

the change of their nitroxide radical orientation only changes the spin-electron position and spin-density values and does not affect their magnetic spin coupling properties, except that they are numerically altered. 

CONCLUSIONS In summary, in this work, the DNA nucleobases are radicalized mainly by nitroxide

radical groups.

By introducing the nitroxide radical group(s) on the C-sites or oxidizing an

amino group, eight different diradical nucleobases can be combined.

At first, we carry out a

systematic and theoretical analysis of them by geometrical, electronic and magnetic spin coupling properties.

The modified nitroxide diradical nucleobases not only have stable

structures but also have remarkable magnetic coupling magnitudes, and their magnetic coupling constants are considerably large.

As expected, the intramolecular magnetic spin coupling

characteristics of them are noticeable. Except for the

2NO

A2 (J =440.69 cm-1) and

2NO

C2 (J

=149.09 cm-1) diradical nucleobases with a FM spin coupling character, all other nitroxide diradical nucleobases exhibit the AFM spin coupling characteristics, especially the

2NO

T (J =

-3265.52 cm-1) and 2NOC3 (J = -2445.53 cm-1) nucleobases which have considerably large AFM spin coupling interaction. The J values of the

2NO

A1,

2NO

A3,

2NO

G and

2NO

C1 nitroxide

diradical nucleobases are -671.66, -463.26, -370.52, and -494.85 cm-1, respectively.

We

further perform detailed analyses of the nitroxide diradical nucleobases through their electronic, magnetic spin coupling characteristic and other properties, such as molecular configurations, energies,

HOMO-LUMO

energy

gaps,

spin

polarization,

SOMOs,

SOMO-SOMO/SOMOα-LUMOα energy differences of triplet state, spin density, magnetic coupling constants (J) and so on.

We find that there are good linear relationships between the

spin coupling constant (J) and molecular orbital energy levels of the nitroxide diradical nucleobases (in the CS state), and the energy differences of the CS and T states. Moreover, we can also determine the magnetic or AFM spin coupling properties of the nitroxide diradical nucleobases by the spin polarization rule, the shape of SOMOs, SOMO-SOMO energy splitting and spin density distribution.

Further, our examinations reveal that the intramolecular

nitroxide diradical nucleobases combined with their canonical pairing bases still have an 15



Page 16 of 28

open-shell BS singlet ground state and possess the AFM spin coupling characteristics. While, the intermolecular nitroxide diradical nucleobases do not have noticeable J values. Additionally, the calculated results also suggest that the nitroxide diradical nucleobases with different radical orientations could exist stably and demonstrate the diversity of its magnetic spin coupling characters. In addition, it should be noted that the magnetic coupling magnitudes in some organic or inorganic magnets (diradicals) are small with |J|=1-10 cm-1,56-60 and in some other magnets the |J| may reach to several hundred wave number (cm-1).59-65 Certainly, the coupling magnitude requirement depends on their practical applications.

In our nitroxide-modified base molecules,

their magnetic coupling interactions are significantly enhanced which become close to the organic diradicals with a large range of |J| from slightly larger than 0 cm-1 to several thousand wave number (cm-1), indicating a great improvement for these H-bonding pair systems and an ideal range for broad applications. We here only theoretically study the magnetic coupling properties of the nitroxide diradical building blocks in the nucleobases, and subsequent experiments and related work are certainly needed for further verification. This

work

provides

a

completely

new

perspective

on

our

research

on

nitroxide–base–nitroxide diradicals and helps us to better understand the hydrogen bonding effects and the magnetic coupling property changes caused by radical orientation.

We predict

that they are potentially promising conductive biological molecular wires, which will have broad application prospects in the field of magneto-optical devices and magnetic recording materials as self-assembled structures and electronic nanodevices.



ASSOCIATED CONTENT

(S) Supporting Information Computational detail and calculated data and figures including geometrical parameters, singlet-triplet gaps, HOMO-LUMO gaps, magnetic coupling constants, SOMOs and spin density maps, and others.

This material is available free of charge via the Internet at

http://pubs.acs.org.

16


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


AUTHOR INFORMATION

Corresponding Author *E-mail: [email protected] Notes The authors declare no competing financial interest.



ACKNOWLEDGMENTS

This work was supported by NSFC (21573128, 21773137, and 21373123) of Shandong Province. A part of the calculations were carried out at National Supercomputer Center in Jinan and High-Performance Supercomputer Center at SDU-Chem. 

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Scheme 1. Schematic Diagram of the DNA Bases Modified by Nitroxide Radicals (NO•). There are Three Nitroxide Radical Insertion Sites Which are the C8 Sites of Adenine and Guanine, C-H and -CH3 Sites in Cytosine and Thymine, The Oxidation of –NH2 group on the H-bonding Surface.

By These Means, The Nitroxide diradicals within the Nucleobases Are

Achieved.

Figure 1. Schematic Diagram of nitroxide diradical DNA bases (2NOA, 2NOG, 2NOT, and 2NOC).

23



Figure 2. The HOMO-LUMO gaps of the natural (CS) and nitroxide diradical bases (CS). The SOMOα-LUMOα gaps of nitroxide diradical bases (T). Molecular orbital energy levels of the natural and nitroxide diradical adenine base. The HOMO-LUMO gaps of the natural and closed-shell diradicals are labeled, and the frontier orbital contours are also represented here.

Figure 3. The linear correlation diagrams between the magnetic coupling constants J and the HOMO-LUMO energy gaps and the energy gaps between the CS singlet and triplet state of all nitroxide diradical nucleobases.

24


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Figure 4. Scheme of spin alteration for the 2NOA1-3, 2NOG, 2NOT, 2NOC1-3 nitroxide diradical nucleobases.

Figure 5. SOMOs (BS), HOMO/HOMO-1(T) (isovalue = 0.02) and spin density distributions (isovalue=0.004) of the representative BS or T ground states for the (X=A, G, T, C) nitroxide diradical nucleobases.

2NO

X

The pink and purple colors correspond to

α- and β-spins, respectively.

25



Figure 6. Mulliken atomic spin densities for the ground states of the representative ground states in the 2NOX (X=A, G, T, C) nitroxide diradical nucleobases. The solid rings represent the total spin density of the NO radicals (positive and negative orientation). The dotted curves represent the spin-polarized path. The orange one represents the common polarization path, the green one represents the intramolecular polarization path and the purple one represents the extrapolar polarization path and the green straight dashed line represents the spin-polarized path partition.

26


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Table 1. The energies (a.u.) and values of their BS singlet state and triplet state, intramolecular

spin

exchange

coupling

constants

(J/cm-1),

calculated

at

the

UM062X/6-311++G(d,p) level. Energies (a.u.) J (cm-1)

Molecules BS

T

-671.6835694 0.996

-671.6805282 2.015

-671.6957956 1.012 -727.0610408 1.005 -746.9147407 1.006 -674.593727 0.470 -599.314957 0.986

-671.6978481 1.012 -727.0589092 2.015 -746.9130362 2.015 -674.5708208 2.009 -599.3126206 2.023

2NO

-599.3225629 1.007

-599.3232561 2.027

149.09

2NO

-654.690934 0.618

-654.6754069 2.012

-2445.53

2NO

A1

2NO

A2

2NO

A3

2NO

G

2NO

T

2NO

C1 C2 C3

-671.66 440.69 -463.26 -370.52 -3265.52 -494.85

Table 2. The orbital occupancies of HOMO and LUMO, their overlap integral (T) and diradical percentages of the 2NOA, 2NOG, 2NOT, 2NOC1, 2NOC2 and 2NOC3 nitroxide diradical nucleobases in the BS state, calculated at the UM062X/6-311++G(d,p) level. Molecules 2NO

A1 A2 2NO A3 2NO G 2NO T 2NO C1 2NO C2 2NO C3 2NO

nHOMO

nLUMO

Overlap (T)

y

1.184 1.047

0.816 0.953

0.18382 0.04660

64.4% 90.7%

1.146

0.854

0.14620

71.4%

1.135

0.865

0.13462

73.6%

1.746

0.254

0.74553

4.2%

1.199

0.801

0.19913

61.7%

1.095

0.905

0.09538

81.1%

1.639

0.361

0.63903

9.3%

27



TOC Graphic

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Rational Design of Magnetic DNA Motifs with Diradical Character

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