# Twist and writhe dynamics of stiff filaments

## Abstract

This letter considers the dynamics of a stiff filament, in particular the coupling of twist and bend via writhe. The time dependence of the writhe of a filament is $`W_r^2Lt^{1/4}`$ for a linear filament and $`W_r^2t^{1/2}/L`$ for a curved filament. Simulations are used to study the relative importance of crankshaft motion and tube like motion in twist dynamics. Fuller’s theorem, and its relation with the Berry phase, is reconsidered for open filaments.   

DNA and other stiff polymer systems such as actin filaments are of interest both for their intrinsic biological importance, but also due to the fact that micro-manipulation techniques give a very detailed vision of their properties, allowing one to study fundamental processes in polymer statics and dynamics. Recent theoretical and experimental work on DNA force-extension curves has shown the importance of the static coupling between bend and twist in stiff polymers . Non-trivial twist-writhe correlations in flexible polymers have been recently found in a simple dynamic lattice model in which linking number is conserved . Here I examine the dynamics of twist and writhe fluctuations in order to clarify the driving forces and dissipative processes important in the motion of filaments. I use a combination of scaling arguments and simulations; the numerical studies are complementary to recent work  which considers the zero temperature motion of stiff filaments via integration of the continuum differential equations. Here I study Brownian dynamics of stiff filaments and introduce a generalized bead-spring model suitable for studying twist and writhe dynamics of polymers.

There are two physical processes which can lead to the rotation of the end of a filament about its local tangent. The two mechanisms of spinning are twist and writhe. Twist corresponds to excitation of internal torsional degrees of freedom of the filament. Writhing is due to the three dimensional geometry of bending of the filament in space. We shall reserve the word “spinning” for this process of end rotation and denote the spinning angle by $`\mathrm{\Psi }`$. The two contributions are additive so that we can write $`\mathrm{\Psi }=\varphi +W_r`$, with $`\varphi `$ the contribution from internal twisting and $`W_r`$ the contribution from the geometry of the path in space.

Excitations of internal twist degrees of freedom are well understood  and have been observed in DNA and actin via depolarized light scattering experiments. The writhing of a filament is best expressed with the help of Fuller’s theorem, . Consider a filament (with boundary conditions such that the two end tangents are maintained parallel) which is bent into a non planar curve. The tangent to the filament t(s) sweeps out a curve on the unit sphere, $`𝒮_2`$ as a function of the internal coordinate $`s`$. It can be shown, , that the contribution to the spinning due to the writhe is just the area, $`A_\mathrm{\Omega }`$, enclosed by $`𝐭(s)`$ on $`𝒮_2`$.

Let us assume that we are working with uniform filaments with circular cross sections then the two process are controlled by two independent elastic constants, the torsional stiffness, $`K`$ and the bending stiffness $`\kappa `$. If we work in units such that $`k_BT=1`$ these two elastic constants have the dimensions of lengths, and are indeed the persistence lengths for static torsional and bending correlations of the filament. The dynamics obeyed by the torsional and bending modes are, however, different which leads to distinct contributions to $`\mathrm{\Psi }`$ as we shall now demonstrate.

The torsional motion of a straight filament obeys a Langevin equation

$$a^2\frac{\varphi }{t}=K\frac{^2\varphi }{s^2}+\xi (t,s)$$
(1)   
where the angle $`\varphi (s,t)`$ is the local rotation of the filament in the laboratory frame, $`\xi `$ is the thermal noise, $`a`$ is comparable to the radius of the filament, (we neglect all pre-factors of order unity and use units in which $`\eta =k_BT=1`$, in this system of units time has the dimensions of a volume, so that $`1s4\mu m^3`$). The solution of eq. (1) is well known: It is characterized by dynamic correlations of the angle which diffuse along the filament according to the law $`l_{tw}^2tK/a^2`$. A monomer on the filament rotates by an angle $`\varphi ^2\sqrt{t/Ka^2}`$, if $`l_{tw}<L`$. When $`l_{tw}>L`$ the twisting motion is sensitive to the boundary conditions on the filament; for free boundary conditions the filament rotates freely and $`\varphi _{free}^2t/La^2`$. If one end is held at a fixed angle the other has an amplitude of rotation which saturates to $`\varphi _{hold}^2L/K`$.

Let us now calculate the writhing contributions to the spinning. For a short filament $`(L/\kappa <1)`$ oriented along the z-axis the area enclosed by the curve $`𝐭(s)`$ is given by $`A_\mathrm{\Omega }=1/2e_z.(\dot{𝐭}𝐭)ds.`$ The writhe of a filament is signed and averages to zero for a polymer at thermal equilibrium. We shall consider the statistics and dynamics of $`A_\mathrm{\Omega }(t)A_\mathrm{\Omega }(t^{}).`$ The linearized bending modes of the filament obey a Langevin equation

$$\frac{𝐫_{}}{t}=\kappa \frac{^4𝐫_{}}{s^4}+𝐟_{}(t,s)$$
(2)   
with $`𝐫_{}`$ the transverse fluctuations of the filaments and $`𝐟_{}`$ the Brownian noise. Using eq. (2) we find that $`𝐭_i,(q,0)𝐭_j(q,t)=\delta _{i,j}\mathrm{exp}(\kappa q^4t)/\kappa q^2`$ with $`\{i,j\}=\{x,y\}`$. The fourth order correlation function in $`A_\mathrm{\Omega }(t)A_\mathrm{\Omega }(t^{})`$ can be expanded using Wick’s theorem: A short calculation shows that

$$A_\mathrm{\Omega }^2=W_r^2L^2/\kappa ^2.$$
(3)   
and that

$$(W_r(t)W_r(0))^2l_1(t)L/\kappa ^2t^{1/4}.$$
(4)   
with $`l_1(t)(\kappa t)^{1/4}`$ the characteristic length scale in solutions of eq.(2). We note that the same result can be found in a scaling approach using the following argument: The path $`𝐭(s)`$ on $`𝒮_2`$ is a Gaussian random walk ; On a time scale $`t`$ each section of length $`l_1`$ of the filament re-equilibrates a random walk with radius of gyration on $`𝒮_2`$ of $`r_\mathrm{\Omega }^2l_1/\kappa `$ and area $`A_1\pm l_1/\kappa `$. There are $`N_1=L/l_1`$ dynamically independent contributions to the writhe variation giving $`\mathrm{\Delta }W_r^2N_1A_1^2=l_1(t)L/\kappa ^2`$ as found above. This argument shows in addition that the scaling law eq. (4) is valid at short times even for filaments for which $`L>\kappa `$.

What influence does this writhe fluctuation have on the global motion of a filament. To answer this question consider two extreme, non-physical, cases before coming back to the typical experimental situation. Consider, firstly, the case $`K/\kappa 1`$; spinning of the end of a polymer can only occur via writhe, the twist degrees of freedom are frozen out. The derivation of eq. (4) has neglected rotational friction: It has been derived using a description of only the transverse motions of the polymer. It can only be valid when the rotational friction of a filament is so small that spinning driven by the writhe is able to relax without build up of torsional stress. Similar remarks have recently been made in the propagation of tensional stress in stiff polymers . In this case simple arguments allow one to deduce the validity of the approximation made by balancing the driven motion due to the transverse fluctuations against any additional sources of friction. We shall now apply the same argument to the torsional motion, before checking the results numerically. For the rotational friction to be negligible the free rotational diffusion of a section of filament of length $`L`$ must be faster faster than the driven writhing motion, implying $`\varphi _{free}^2>\mathrm{\Delta }W_r^2`$ or $`t/La^2>l_1(t)L/\kappa ^2`$. For filaments which do not satisfy this criterion, i.e. when $`L>l_{W_r}(t)=\sqrt{l_1^3\kappa /a^2}`$, the torsional stress has not had time to propagate between the two ends of the filament  and the law (4) does not apply. If we observe now the end of a filament for times shorter than the torsional equilibration time the spinning is due to an end section of length $`l_{W_r}`$ and we should substitute this effective length in eq. (4) to calculate the end motion $`\mathrm{\Delta }W_r^2l_1^{5/2}/a\kappa ^{3/2}t^{5/8}.`$ It is only after the propagation of the torsional fluctuations over the whole length of the filament that (4) becomes true. We thus hypothesize a scaling behavior for the spinning of a filament with $`K/\kappa 1`$

$$\mathrm{\Psi }^2=\frac{Lt^{1/4}}{\kappa ^{7/4}}𝒬\left(\frac{t\kappa ^{7/3}}{a^{8/3}L^{8/3}}\right),$$
(5)   
with $`𝒬(x)x^{3/8}`$ for $`x`$ small and $`𝒬(x)1`$ for $`x`$ large.

A second extreme case is $`K=0`$, as is for instance the case for many simple numerical bead-models of worm-like chains. In this case there is no need for the beads to rotate to follow writhe, the writhe fluctuations are absorbed by the internal twist degree of freedom without cost. The writhe does not lead to spinning; we do expect however that there are strong dynamic (anti)correlations between twist and writhe over the length of the filament. We conclude that the law (4) is valid for all times, it has no consequence however on the rotational dynamics of a monomer on the chain that could be detected, for instance, in a scattering experiment.

Let us now turn to the physical case, $`K/\kappa 1`$. From the expressions for $`l_{W_r}`$ and $`l_{tw}`$ we find that $`l_{tw}/l_{W_r}=\sqrt{l_1/\kappa }1`$ at short times. On the length scale $`l_{tw}`$ the twist field and the writhe of the filament are in equilibrium and we can add the fluctuations of the twist and writhe degrees of freedom. Beyond $`l_{tw}`$ the successive section of the polymer are dynamically decoupled: a writhe fluctuation can not be transmitted faster than the signal transmitted by $`l_{tw}`$ and the second scenario becomes valid with $`l_{tw}`$ playing the role of a bead size. Beyond $`l_{tw}`$ the filament can writhe freely without any local consequence on the dynamics of the chain. Thus the experimental consequences of the writhe fluctuations are probably negligible for times such that $`l_{tw}<L`$. When $`l_{tw}`$ reaches $`L`$ the amplitude of twist fluctuations saturates, while the dynamics of the slower bending modes continues to evolve with $`\mathrm{\Psi }`$ varying as eq. (4) until $`l_1(t)=L`$. These additional fluctuations could be observed experimentally.

These arguments have been checked by simulations on a discretized bead-spring model: Take $`N+1`$ spherical beads of diameter $`a`$ connected by stiff harmonic springs. Each bead is characterized by its position $`𝐫`$ and a triad of orthonormal vectors. $`𝐌=\{𝐛,𝐧,𝐭\}`$. The vector $`𝐭`$ is an approximation to the local tangent to the filament at $`𝐫`$. $`\{𝐧,𝐛\}`$ span the normal space of the filament; $`𝐧`$ could describe the position of some feature, such as the large groove in DNA on the surface of the molecule. The springs are not connected to the centers of the beads rather a bead $`i`$ is linked to its neighbors by connections situated on its surface at $`\{𝐫_ia𝐭_i/2,𝐫_i+a𝐭_i/2\}`$. The energy is

$`E`$ $`=`$ $`B/2{\displaystyle \underset{i}{}}(𝐫_i𝐫_{i+1}a𝐭_i/2+a𝐭_{i+1}/2)^2`$ (6)   
$`+`$ $`\kappa /2a{\displaystyle \underset{i}{}}(1𝐭_i𝐭_{i+1})`$ (7)   
$`+`$ $`K/4a{\displaystyle \underset{i}{}}(1𝐧_i𝐧_{i+1}𝐛_i𝐛_{i+1}+𝐭_i𝐭_{i+1})`$ (8)   
The first term imposes the linear topology of the filament; when $`B`$ is large the curvilinear length of the filament is $`L=Na`$. In the simulations we are only interested in the limit of large $`B`$. The second term is a bending energy. The third term is the torsional energy. I integrate the equations of motion for the position and orientation adding friction and thermal noise coupled to the translational and angular velocities, effectively leading to Brownian dynamics. Since we are particularly interested in the writhe dynamics I use boundary conditions where the positions of the ends of the filament are free to move but the end tangents are constrained via external torques, so that the writhe can be calculated via Fuller’s result.

A first series of simulations were performed to study the internal twisting dynamics of very long filaments. This simulation was performed to confirm the intuition  that twist modes can transport torsional stress even in the presence of large bends in the filament. This stress is carried by rapid spinning of the filament in a slowly evolving tube, rather than the rotation of the whole filament collectively moving against solvent friction, (like the rotation of a rigid crankshaft). Simulations are performed for filaments of varying length with two possible boundary conditions. The first boundary condition is that both ends are free to spin and we look for a crossover from the dynamics of internal modes described by eq. (1) to free rotation. In the second case we block the rotation of one end and check that this leads to a saturation of rotation angle. The scaling displayed by Fig. (1) shows that torsion propagates perfectly well over many persistence lengths without hindrance from the tortuosity of the path in space. Eq. (1) is valid for thermally bent filaments as well as for torsional fluctuations around a linear configuration.

A second family of simulations were performed to study the writhe and twist fluctuations of filaments both with very high torsional constants to verify the predictions made for the writhe dynamics. Fig(2) shows the the scaling proposed above, eq (5), is indeed seen in the case of high torsional stiffnesses.

In order to calculate the writhe of a curve via Fuller’s theorem we have until now considered paths $`𝐭(s)`$ which are closed on $`𝒮_2`$. In general this is most inconvenient: there are many experimental situations where one would like to compare the spinning of filaments oriented in an arbitrary direction. We now consider how one might generalize the idea of writhe and spinning to filaments with arbitrary open boundary conditions. In general it is impossible to compare the two rotation frames $`𝐌(L)`$ and $`𝐌(0)`$. The main ambiguity comes from the fact that rotations are non-commutative. However for filaments for which $`L/\kappa 1`$ the non-commutative nature of the rotations is a higher order correction and we can consider that in going along the filament oriented along $`z`$ we have a rotation which can be unambiguously decomposed into its three Cartesian coordinates $`(\mathrm{\Omega }_x,\mathrm{\Omega }_y,\mathrm{\Omega }_z)`$. We shall proceed by studying equations $`𝐌(s)/s=𝐎(s)𝐌(s)`$ where $`𝐎_{i,j}=ϵ_{ijk}\omega ^k`$ with $`\omega ^k=dt_k/ds`$ for $`k=\{x,y\}`$. The angular velocities $`\omega ^x`$ and $`\omega ^y`$ correspond to bending the filament, $`\omega ^z=0`$ in the absence of twist. We iteratively integrate this equation. The lowest order contribution to rotations about the z-axis comes in second order.

$$\mathrm{\Omega }_z=\frac{1}{2}_0^L𝑑s𝑑s^{}\theta (ss^{})(\omega _s^x\omega _s^{}^y\omega _s^{}^x\omega _s^y).$$
(9)   
Integrating by parts to transform the $`\theta `$-function into a $`\delta `$-function gives

$$\mathrm{\Omega }_z=\frac{1}{2}e_z.\left(_0^L(\dot{𝐭}𝐭)𝑑s+𝐭(0)𝐭(L)\right)$$
(10)   
For a closed curve on $`𝒮_2`$ the first term is the area enclosed by the curve $`𝐭(s)`$ on a patch of a sphere in agreement with Fuller’s theorem. The second, boundary, term present when the curve is open corresponds to closing the path by a geodesic from $`𝐭(L)`$ to $`𝐭(0)`$. Thus we have a simple generalization for Fuller’s theorem valid for short chains allowing one to calculate the writhe state of a polymer with fluctuating boundary conditions.

We remark that Fuller’s theorem is closely related to Berry’s phase in experiments on polarized light transmission along bent optical fibers . The vector $`𝐭(s)`$ corresponds to the local tangent to the fiber, while the vectors, $`\{𝐧,𝐛\}`$ transform in exactly the same manner as the plane of polarization, via parallel transport on $`𝒮_2`$. The problem of closing paths in $`𝒮_2`$ has close analogies in the treatment of Berry’s phase in non cyclic Hamiltonians. In quantum and optical systems interference phenomena allow one to define the relative phase of a system even if the evolution has not been cyclic  via the Pancharatnam connection. This convention also closes an open trajectory again via a geodesic; in wave physics this convention is even generally applicable and is not limited to small paths in the appropriate projective Hilbert space.

All the above discussion has been for a filament for which the round state is linear. Let us repeat the arguments leading to (4) for short bent filaments to study the writhe fluctuations of short curved DNA sections. The pre-existing bend considerably modifies the arguments. Consider a section of filament which bends an angle $`\mathrm{\Phi }`$ at zero temperature due to intrinsic curvature. At zero temperature the bent loop has a tangent map which maps to the equator of $`𝒮_2`$. Under the map to $`𝒮_2`$ a distance of $`s`$ in real space becomes $`\mathrm{\Phi }s/L`$. At finite temperature there is competition between this constant drift and the thermal agitation which leads to a Gaussian random walk on $`𝒮_2`$. Let us now consider the dynamics in a scaling picture: For the very shortest times only small scale structure is changing:- the writhe dynamics reduces to the case discussed above. At longer times the stretched path moves collectively:- each section of length $`\delta _1=\mathrm{\Phi }l_1/L`$ on $`𝒮_2`$ moves up or down by $`r_\mathrm{\Omega }=\sqrt{l_1/\kappa }`$. Counting $`N_1=L/l_1`$ dynamically independent sections

$$\mathrm{\Delta }W_r^2N_1(\delta _1r_\mathrm{\Omega })^2=\mathrm{\Phi }^2l_1^2/\kappa Lt^{1/2}.$$
(11)   
The exponent for the writhe fluctuations has changed from 1/4 to 1/2 due to the stretching of the configuration in $`𝒮_2`$. This prediction is tested in fig. (2), where we have added a spontaneous bending energy, in $`\alpha \mathrm{\Sigma }_i𝐧_𝐢.𝐭_{𝐢+\mathrm{𝟏}}`$ to curve the filament. We now see two distinct regimes in $`\mathrm{\Psi }^2t^{1/2}`$ due to the intrinsic twist dynamics and then the writhe dynamics, the writhing contribution is also much enhanced over its value for linear filaments. It would also be interesting to study the case of closed loops, but the simple scaling argument used here becomes considerably more complicated due to the non-local integral constraint $`𝐭(s)𝑑s=0`$ coming from closure.

This paper has studied the short time regime dominated by the bend and twist rigidities, rather than the very long time dynamics where crossovers to Zimm or Rouse dynamics occur. Our arguments have been for the simplest model of a stiff polymer, of uniform cross section and without disorder. The Marko-Siggia energy function  already has rich static behavior and one would anticipate that the cross terms in this Hamiltonian could increase the importance of the dynamically effects discussed here. Similarly disorder in the ground state is expected to dramatically modify the dynamics, by giving a preformed writhe on $`𝒮_2`$ and by modifying the picture of simple spinning of the polymer in its tube due to new dissipative processes; It has recently been argued that a mixture of crankshaft and tube spinning should co-exist even in the case of weak disorder coming from sequence fluctuations in DNA .

I would like to thank A. Ajdari, R. Everaers, F.Julicher, P. Olmstead, C. Wiggins and T.A. Witten for discussions.e