# Wigner crystal model of counterion induced bundle formation of rod-like polyelectrolytes

## Abstract

A simple electrostatic theory of condensation of rod-like polyelectrolytes under influence of polyvalent ions is proposed. It is based on the idea that Manning condensation of ions results in formation of the Wigner crystal on a background of a bundle of rods. It is shown that, depending on a single dimensionless parameter, this can be the densely packed three-dimensional Wigner crystal or the two-dimensional crystal on the rod surfaces. For DNA the location of charge on the spiral results in a model of the one-dimensional Wigner crystal. It is also argued that the Wigner crystal idea can be applied to self-assembly of other polyelectrolytes, for example, colloids and DNA-lipid complexes.

Many rod-like polyelectrolytes, such as double helix DNA , F-actin, microtubules, and tobacco mosaic virus  are known to self-assemble into bundles of parallel densely packed rods. All these macromolecules are negatively charged and their lateral association is induced by $`Z`$-valent cations where $`Z2`$. For DNA this phenomenon is called condensation and is studied in connection with the dense packing of viral DNA. According to the mean field Poisson-Boltzmann theory, two parallel rods should always repel each other. Two physical phenomena which are not included in this theory were suggested as possible reasons for the puzzling attraction . When distance between rods is large their attraction is related to the correlation of thermal fluctuations of screening atmospheres of two rods. At smaller distances one should take into account that the Manning condensation of ions on the surface of rods leads to strong spatial correlations of ions or even to their crystallization. In this situation, two crystals with proper phases attract each other. Below I calculate the binding energy of a dense bundle and therefore talk only about the second mechanism. I also resolve an important contradiction in the literature. Most of the publications deal with two rods and calculate a pairwise force acting between them . On the other hand, two recent publications  claim that bundles are formed by non-pairwise-additive interaction.

The first goal of this paper is to present a theory of attractive interactions of rod-like polyelectrolytes, based solely on electrostatic interactions. It considers formation of densely packed bundles in a very dilute solution of cylindrical rod-like molecules of the radius $`r`$ and length $`Lr`$. It assumes that the cylindrical surface of a rod is negatively charged with the charge density $`e/b`$ per unit length of the rod. Point-like positive ions with the charge $`Ze`$ are added to the solution.

The main idea of this paper is that a bundle of parallel rods can be considered as an uniform negative background at which condensed ions form the Wigner crystal. The cohesive energy of this crystal is the reason for the attraction and the bundle formation. (This idea is similar to the theory of matter in a superstrong magnetic field of a neutron star where electrons behave as negative rods and nuclei form the Wigner crystal on the background of electron bundles .) For the case in which ions can not penetrate the rods, the binding energy of the bundle per rod is calculated below as the function of the dimensionless parameter $`Zb/r`$. The result is that for $`Zb/r1`$, the three-dimensional densely-packed Wigner crystal is formed and interaction is not-pairwise-additive. In the opposite case, $`Zb/r1`$ the two-dimesional Wigner crystal appears on the surface of each rod and the interaction becomes short-range pairwise. My results in the first case qualitatively resemble Ref. , while in the second case this paper is close to Ref. , where idea of the surface Wigner crystal was originally suggested. None of these papers, however, produced simple analytical dependencies similar to those which I derive below using $`Zb/r`$ as a large or small parameter of the theory.

The second half of this paper concentrates on the specifics of DNA where surface charges form a spiral. I show that this leads to the appearence of the one-dimesional spiral-like Wigner crystal of ions on the surface of each rod. Interaction of such crystals determines the DNA condensation. It is also argued that the idea of a Wigner crystal can be applied not only to the rods, but also to the self-assembly of many other different polyelectrolytes. I apply this theory to colloids and complexes of DNA with cationic lipid membranes.

Returning to the main problem of rods and point-like counterions, I argue that for sufficiently large dimensionless parameter $`Z\xi `$, where $`\xi =e^2/b\kappa k_BT`$ and $`\kappa `$ is the effective dielectric constant of the water-polymer system, rods condense in the maximum density cylindrical bundles of $`N`$ parallel molecules. At large $`Z\xi `$ the charge of the bundle is almost completely compensated by the opposite charge of $`NL/b`$ of positive ions which experience the Manning condensation inside the bundle. To find a configuration of condensed ions, one can view the bundle as the uniformly charged cylindrical background. The potential energy of the Coulomb repulsion of ions in these conditions is much larger than their kinetic energy. Therefore, they form the Wigner crystal on the negative background. Assume first that $`N`$ is so large that the radius of the bundle $`rN^{1/2}`$ is much larger than the lattice constant of the Wigner crystal $`R`$. In this case ions form a densely packed three-dimensional crystal. One can easily calculate $`R`$ from the condition that the charge of the Wigner-Seitz cell, $`R^3/br^2`$, equals $`Z`$. This gives

$$R(Zbr^2)^{1/3}.$$
(1)   
Comparing $`R`$ with the bundle radius $`rN^{1/2}`$ one finds that the three-dimensional case takes place at $`NN_c=(Zb/r)^{2/3}`$. (In the opposite case $`NN_c`$ ions form one-dimensional crystal as shown below). I assume that ions can not penetrate rods. Then ions can fit in the free space between rods without strong deformation of the three-dimensional crystal only at $`Rr`$. According to Eq. (1) this inequality means that $`Zb/r1`$. Now we see how the important parameter $`Zb/r`$ appears in the theory. Assuming, for the beginning, that rods are narrow and weakly charged so that $`Zb/r1`$ one finds that $`N_c1`$ so that both situations $`NN_c`$ and $`NN_c`$ have to be considered.

The binding energy of a crystal per ion, $`\epsilon _i`$, can be estimated as the energy of interaction of an ion with its Wigner-Seitz cell

$$\epsilon _i\frac{Z^2e^2}{\kappa R}.$$
(2)   
Substituting $`R`$ from Eq. (1) one obtains

$$\epsilon _i\frac{Ze^2}{\kappa b}(Zb/r)^{2/3}(Zb/r1;NN_c).$$
(3)   
If $`NN_c`$, the bundle is narrow and the ions form a one-dimensional Wigner crystal, lattice constant of which, $`R`$, is equal to $`Zb/N`$. Then, the energy of interaction of an ion with its Wigner-Seitz cell is

$$\epsilon _i\frac{Ze^2N}{\kappa b}ln(N_c/N)(Zb/r1;NN_c).$$
(4)   
It is easy to verify that Eq. (2) matches Eq. (3) at $`NN_c`$. Thus, at $`Zb/r1`$, the energy per ion, $`\epsilon _i`$, grows linearly at small $`N`$ and reaches saturation at $`NN_c`$. This is a clear demonstration of a non-pairwise additive interaction. Of course, the surface correction to the energy of the bundle provides some growth even at $`NN_c`$ and leads to formation of macroscopic bundles.

In order to obtain the binding energy per molecule, Eq. (4) and Eq. (3) have to be multiplied by the number of ions per molecule, $`M=L/bZ`$. This transition does not change the dependence on $`N`$. Therefore below I will continue to present results in the form of $`\epsilon _i`$.

Before switching to the more complicated case $`Zb/r1`$, I discuss the condition on the temperature $`T`$ or, in other words, on the parameter $`Z\xi `$ at which the suggested above theory is valid. Consider a large bundle of three-dimensional densely packed Wigner crystal, which stays neutral even at quite a small concentration of ions. If $`k_BT\epsilon _i`$ the thermal motion can be neglected and my theory is valid. Using Eq. (3) one can rewrite inequality $`k_BT\epsilon _i`$ as

$$Z\xi (r/Zb)^{2/3}.$$
(5)   
At $`Zb/r1`$ this inequality is much weaker than the standard condition $`Z\xi 1`$ of the Manning condensation of ions with charge $`Z`$ at an isolated molecule (it follows from Eq. (4) at $`N=1`$), because of the simultaneous interaction of each ion with many rods. Even if one uses $`\kappa =81`$ of pure water, $`\xi 4`$ at room temperature and the condition of Eq. (5) is easily fulfilled.

It is obvious that wnen Eq. (5) is valid, the maximum density bundle is more strongly bounded than one with the smaller density. Indeed, the decreasing density results in the increase of the lattice constant $`R`$ and, according to Eq. (2), substantially diminishes $`\epsilon _i`$. At the same time the increase of the entropy term in free energy can not compensate for this loss in the binding energy.

As stated above, this theory works if $`k_BT\epsilon _i`$. Actually the Wigner crystal melts when $`k_BT`$ is yet numerically much smaller than $`\epsilon _i`$, so in some experimental conditions or for low dimensionalities (see below) one deals with strongly correlated liquid, not a crystal. This, however, does not change the estimate for its correlation energy and for $`\epsilon _i`$ and leaves unchanged the validity criterion of the theory. The fact that it is the short range order of ions which is responsible for the attraction of rods at a finite temperature was emphasized in Ref. . Below, I continue to use the Wigner crystal language because it creates a simpler image.

Consider now more strongly charged and thicker rods for which $`Zb/r1`$. In this case $`N_c1`$ and, therefore, one has to deal only with a three-dimensional problem. However, the rods are so thick that their radius is larger than the lattice constant of the optimal densely packed crystal. If, as we assumed, ions can not penetrate rods, the optimal densely packed crystal can not be formed. Under this restriction, ions condense at the surface of each rod forming the two-dimensional Wigner crystal  with the lattice constant

$$R(Zbr)^{1/2}.$$
(6)   
An insulated rod has a similar crystal at its surface. The binding energy of the bundle originates in narrow contact stripes where rods pairwise contact each other so that their Wigner crystals overlap. The width $`W`$ of this stripe will be calculated below. Inside the stripe, densities of both negative background and positive ions are doubled and the local lattice constant $`R_s`$ becomes smaller ($`R_s=R/\sqrt{2}`$). As a result, according to Eq. (2), the cohesive energy of the crystal per ion of the stripe becomes larger than for the case of the two separated rods. Combining Eq. (2) and Eq. (6) one finds that the binding energy of the bundle per one ion of the stripe equals $`Z^{3/2}e^2/(br)^{1/2}`$. To get $`\epsilon _i`$ one must multiply this energy by the fraction, $`pW/r`$, of all ions of the bundle which reside in the contact stripes. The width $`W`$ can be found from the condition that at the distance $`W`$, from the line of contact the surfaces of two contacting rods diverge from each other at the distance of the order of $`R`$. Indeed, the interaction between two-dimensional Wigner crystals is exponentially weak if the distance between parallel planes in which they are situated is larger than their lattice constant $`R`$. A simple geometrical estimate gives $`W(rR)^{1/2}`$. Finishing the calculation of $`\epsilon _i`$ one obtains

$$\epsilon _i\frac{Ze^2}{\kappa b}(Zb/r)^{3/4}(Zb/r1;N1).$$
(7)   
Together Eq. (7) and Eq. (3) give binding energy per ion of a three-dimensional crystal at all values $`Zb/r`$. At $`Zb/r=1`$ they obviously match each other. At $`Zb/r1`$ energy given by Eq. (7) is smaller than the one from Eq. (3). This is a natural result of the restriction that ions do not penetrate rods.

Consider now the validity of the main assumption, that an array of negative discrete charges on the rod surface can be effectively replaced by an uniform negative background. This idea works exactly only in the limit $`Z1`$. On the other hand, it fails at $`Z=1`$ because in low temperature limit all ions and discrete negative charges form neutral Bjerum pairs and nothing depends on the mutual positions of the rods. Thus, $`\epsilon _i=0`$ at $`Z=1`$. What happens at $`Z2`$ depends on the spatial distribution of the discreet negative charges. If they are distributed randomly, then at $`Z=2`$ Eqs. (3), (4) and (7) overestimate $`\epsilon _i`$ roughly by a factor of 2, while at $`Z3`$ they work well. On the other hand, when negative charges are clustered, $`\epsilon _i`$ can be much lower even at $`Z=3`$. Imagine, for example, that negative charges form compact triplets. Each one would be neutralized by an ion and $`\epsilon _i`$ would vanish. More interesting effect of concentration of negative charges in DNA is discussed below.

But first assume that the surface of DNA is uniformly negatively charged. For DNA $`b=0.17`$nm and $`r=1`$nm, so that $`Z=6`$ is the border between range of validity of Eq. (7) and Eq. (3). This means that for DNA in this model, attraction is due to the short range pairwise interaction of molecules induced by correlation between their surface Wigner crystals. This conclusion is in agreement with Ref. .

Recall now that in DNA, negative charges are located along two spirals which are separated by wide and narrow grooves. For simplicity, assume that the width of the narrow one is zero what leaves only one spiral of the negative charge with the double density. (This approximation, of course, overestimates the inhomogeniety of the negative charge distribution and can be easily avoided with minor change in the result.) Ions tend to concentrate on the same spiral and form the one-dimensional Wigner crystal along it. When two parallel DNA rods touch each other by these crystaline spirals (for this purpose one rod should be shifted along their direction by the half of the helical period) they create a spot with larger binding energy per ion. Thus, attraction is produced in a way very similar to the case of contacting two-dimensional crystals discussed above. Extending this analogy for two contacting DNA molecules, one can introduce the contact stripe where attraction is generated. The only difference is that the width of this stripe $`W`$ is smaller for DNA, because the Wigner crystal spirals of the two contacting DNA molecules diverge not only in the plain perpendicular to the rods but also along direction of the rods (spirals cross at a finite angle). One can find that $`WRr/nbR`$, where $`R=\pi r/n`$ is a period of the one-dimensional crystal and $`n=10`$ is the number of base pairs in the helix period. Thus, roughly speaking, only one ion per helix period adjusts its position due to the contact and contributes to the binding energy of the two contacting rods. Multiplying Eq. (2) by the fraction of such ions $`R/2\pi r`$ one obtains

$$\epsilon _i\frac{Ze^2}{\kappa b}\frac{Zb}{2\pi r}.$$
(8)   
At $`Zb/r1`$, Eq. (8) gives smaller energy than Eq. (7). This is an effect of concentration of negative charges on the spiral. Note that this effect is exactly opposite to the prediction of Ref. . The reason for this difference is that the authors of Ref.  assumed that charge of ions is uniformly distributed over DNA surface, so that negative and positive charges are strongly separated. Such a separation of charge costs a large electrostatic energy and can happen only if nonelectrostatic forces dominate. These forces are beyond the scope of my work.

One might wonder whether each contacting pair of DNA molecules in a bundle can gain the energy given by Eq. (8). This can be easily done in a square lattice of rods, with one square sublattice shifted along the rod direction by the half of the helical period. In a densely packed hexagonal lattice one can shift in the same way every second layer, so that each rod is attracted to 4 its neighbours. Thus in the approximation of one spiral both lattices have the same energy.

Note that literally speaking this theory is applicable only to molecules of DNA which are shorter than its persistent length. It is known that in a weak DNA solution of longer molecules, each molecule self-assembles into a toroidal particle, where locally strands of all turns are parallel to each other. Theory of this paper is applicable to toroidal particles as well. Even longer DNA molecules condense in more complex globules . If such a globula consists of condensed bundles this theory can still work.

Although three-dimensional densely packed Wigner crystal of ions is not realized in DNA bundles (for $`Z<6`$), many other rod-like polyelectrolytes are known. Some of them are narrower or more weakly charged so that $`Zb/r1`$ and three-dimensional crystal of ions should appear. PPP3 with $`b/r2`$ is a good example .

I would like to show now that the idea of Wigner crystal (or strongly correlated liquid) of ions for description of their Manning condensation can be applied not only to rods but to quite a variety of systems. Imagine, for example, a rigid plane polyelecrolyte in the presence of counterions with a large charge $`Z`$. Such a system self-assembles in a dense stack of parallel sheets which provides uniform background for the Wigner crystal of ions. Once more, depending on the thickness of the sheets and their surface charge density, one can talk about the three-dimensional Wigner crystal of ions or about two-dimensional crystals in gaps between sheets.

Counterions should not necessarily be small. The role of a counterion can be played by a strongly charged rodlike polymer while the uniform background is provided by the stack of positive parallel sheets. Complexes of DNA with cationic lipid membranes are good examples of such a system . All the rods orient themselves parallel to each other and to the sheets. Their ordering in a plane perpendicular to their long axis depends on the sheet thickness. At a small enough sheet thickness, the circular cross-sections of rods are arranged in the two-dimensional Wigner crystal similar to vortex lattice in superconductors, while at larger thicknesses they form parallel one dimensional crystals in the gaps between sheets.

Returning to small counterions, consider the self-assembly of rigid spherical polyelectrolytes. Thinking about colloids, assume that the surface of a sphere is charged negatively and positive ions can not penetrate it. If spheres are large enough, ions form the two-dimensional Wigner crystal at the surface of a sphere. This leads to contact attraction of spheres similar to the one calculated above for two contacting cylinders. The binding energy of two spheres with the radius $`r`$ and the charge $`Qe`$, originates in the contact disc (an analog of the contact stripe for two cylinders) of the radius $`(rR)^{1/2}`$, where $`r`$ is the sphere radius, $`R`$ is the lattice constant of the Wigner crystal (see computer simulation of these discs in Ref. ). The additional energy per ion of the disc is gained, because the disc has a denser background and a larger ion density than the rest of the surfaces of the spheres. Once more $`\epsilon _i`$ is given by Eq. (2). Multiplying this energy by the number of ions in such a disc, $`r/R`$, and substituting $`Rr(Z/Q)^{1/2}`$ one gets a surprisingly simple expression for the binding energy of two spheres

$$\epsilon \frac{ZQe^2}{\kappa r},$$
(9)   
which looks like a Coulomb attraction energy of the spherical colloid particle and a single ion at its surface. Eq. (9) fails with the decrease of the ion concentration in the solution, $`c`$, when each sphere acquires the net negative charge sufficient to overcome calculated attraction. This happens at $`k_BTln(1/c)Z^2e^2/\kappa R`$. At lower temperature Eq. (9) gives energy which is larger than proportional to $`T`$ depletion energy of Ref. .

In conclusion, this paper studies the attraction and self-assembly of rigid polyelectrolytes due to strong correlations in positions of polyvalent counterions. To describe these correlations, I adopt the notion of the Wigner crystal. For rods I find that, depending on the value of a single dimensionless combination, $`Zb/r`$, optimal cofiguration of ions on the background of a bundle is the three-dimensional densely packed Wigner crystal or the two-dimensional crystal on the surface of rods. When applying this theory to DNA condensation I introduce the notion of one-dimensional spiral Wigner crystal and estimate the binding energy of two DNA helixes due to the contact of these crystals. I also calculate the binding energy of two colloidal particles created by the contact of Wigner crystals of ions on their surfaces. Future developments of this work should include such factors as behaviour of the dielectric constant of water at small distances, the finite size of counterions, and more realistic distributions of polyelectrolyte charges.

###### Acknowledgements.

I am grateful to V. A. Bloomfield, A. M. Dykhne, M. D. Frank-Kamenetskii, A. Yu. Grosberg, R. Holyst, A. R. Khokhlov, and I. Rouzina for valuable discussions. This work was started in Aspen Center for Physics and was supported by NSF DMR-9616880.