TOPOLOGICAL RESTRICTION ON THE DISTRI- BUTION OF DEFECTS IN SURFACE CRYSTALS AND POSSIBLE BIOPHYSICAL APPLICATION W. F. Harris Department of Chemical Engineering Institute of Technology University of Minnesota Minneapolis, Minnesota 55455 Many thin biological structures such as some plasma membranes and virus capsids appear to be made up of units packed in two-dimensional lat 's. Such structures are termed serface crystals. Dislocations and disclinations are observable in some of these crystals. The perfect surface crystal is described by a pair of basis vectors and the conventional crystal by a triplet of basis vectors: both are regarded as embedded in three-dimensional space. This difference allows the existence of defects which have no counterpart in conventional crystals. The various defects are Classified as local or global, intrinsic or extrinsic. Surface crystals that form closed surfaces are considered and it is shown that the sum of the rotations of intrinsic (screw) disclinations in them must equal 27y where x is the Euler-Poincaré characteristic of the surface. The biophysical con- sequences are discussed briefly. Key words: Dislocations in biophysics: protein structure; surface crystals; surface dislocations. I. Introduction In the biological literature, particularly of recent years, there are many examples of thin structures that exhibit periodicity in two dimensions. Such structures include bacterial cell walls [24], bacterial flagella [17], cell membranes [4, 22, 23] and protein coats of viruses [3, 5, 8. 9]. After disruption many of them are able to reassemble or crystallize spontane- ously under suitable conditions [2, 12, 17, 21]. It is possible to identify dislocations in one of Watson and Remsen’s [24] micrographs of a cell wall and disclinations in models (Caspar and Klug [7]; Hull, Hills, and Markham [14]; Kellenberger [15, 16), if not in actual micrographs, of some viruses. se Wits and RL. Wullonate, 1970}, 579In the simpler viruses the protein coat is usually either a spherical or cylindrical shell around a nucleic acid or nucleoprotein core but toroidal shells have been observed (Dmochowski et al. [10]). Membranes of cyto- plasmic organelles can be highly convoluted and many appear to be shells of high connectivity. Caspar et al. [6] refer to viral protein coats as surface crystals. It is useful to generalize this term to include all structures exhibiting periodicity twe dimensions. Harris and Scriven [13] have discussed the passage of dislocations through cylindrical surface crystals and have suggested that dislocations may be involved in the contraction of certain viruses and in other biophysical processes. In this paper the importance of disclinations in biology is brought out. IL. The Perfect Surface Crystal A perfect surface lattice is an infinite set of points invariant under translation by all vectors of the form T=n.aa qd) and only those vectors; any two points can be connected by a vector of the same form. Summation is understood over repeated indices, the basis vectors of the lattice. T is a lattice translation vector or transla- tional symmetry operation, A perfect surface crystal is obtained by adding a unit cell to each lattice point in such a way that T is still a symmetry ‘operation. In this paper only perfect dislocations and disclinations are considered. Dislocations, therefore, must have Burgers vectors b of the form given by eq (1) and disclinations must have rotation vectors @ which are rota- tional symmetry operations of the perfect surface crystal (Nabarro [19, p. 123). The perfect surface lattice is contained, of course, in a planar surface. This surface is regarded as being embedded in the surface crystal and as deforming with the latter, when defects are introduced. It can be termed conveniently the surface of the surface crystal. It is the geometry of this surface that is referred to when the surface crystal is said to have some particular shape. The surface erystal is defined with reference to a pair of basis vectors whereas the conventional erystal is referred to a triplet of basis vectors, Both are regarded as being embedded in three-dimensional space (3-space)., This difference between the two types of crystal allows defects in surface crystals which have no counterpart in conventional crystals. The symmetry operations T and @, where w is normal to the surface of the perfect surface crystal, imply displacements in the plane of thesurface. Such displacements would be readily understood by the inhabi- tants of Abbott’s Flatland {1]; they result in intrinsic defects. All other displacements carry material out of the 2-space (the surface); they lead to extrinsic defects. Since no displacement carries material out of 3-space all defects in conventional crystals must be intrinsic defects. Extrinsic defects in 3-space paralleling those in surface crystals may arise from general relativity (Marder [18]; Nabarro [19, p. 590). Below the term defect is restricted to the class of defects of the Weingarten-Volterra type. ie.. defects resulting from rigid-body-type relative displacement of cut faces (Nabarro [19, p. 16)). (e) (er Ficul The surface erystal S embedded in a daubly-connected body B. In (a) the hole penetrates S, in (b) it does not. The right-hand end view of (b) is shown in (c) to illustrate the introduction of a global defect by rotation through 27 and translation through b: the defect results in a cylindrical surface crystal.Hi. The Imperfect Surface Crystal The various types of defects in surface crystals can be enumerated by considering a surface crystal embedded in an imaginary doubly- connected body B, The embedding (see fig. 1) can he such that the hole {a) intersects the surface crystal S or (b) does not intersect S$. A defect n be introduced by the usual method of making a eut to render B simply connected and displacing one surface relative to the other by a rigid- hody-type displacement, The cut must intersect $ and the relative dis- placement must be a symmetry operation of S. The defect line threads the hole, Where the latter penetrates S is a point or local defect in the surface crystal. If the latter does not penetrate S then the surface crystal contains a global defect. Local defects may be intrinsic or extrinsic, Intrinsic displacements in figure 1b are certainly possible but they leave the surface crystal unstrained. Insisting that strains in a defective surface crystal must not be zero everywhere one coneludes that global defects are always extrinsic. The hierarehy of defects is shown in table 1. Tabie 1. Classification of defects in surface crystals. DISLOCATION —w Edge INTRINSIC “Ss oiscuination > screw Locat’ ie 1¢ > DISCLINATION———— Edge. sENERAL OISLOCAT ION ————* Ege ‘GLOBAL ——* EXTRINSIC Edge OESCL IMATION, Screw IV. Global Defects The only symmetry properties that imply rigid-body-type displacements out of the plane of S are axes of rotation not normal to S, Perfect surface crystals may have 2-fold axes in their midplanes and all. of course, have an infinity of l-fold axes everywhere. Rotation by w about 2-fold axes which spring flat when applied stresses leads to folded or twisted she no defect results, Rotation by 27 about any L-fold axis are released; similarly result leads to a defect. If the retation by 27 is made about the axis of the hole in figure 1b and mpanied by translation in accordance with the translational in no defect. Therefore none of these operations alone it is acesymmetry eq (1) (see fig. 1c) then a cylindrical surface erystal results. If S is inextensible then the circumference of the cylinder, measured in S, is the magnitude of the translation, The global defect thus produced may be thought of as having two components, disclination with #=27 and dislocation with b equal to the circumference of the cylinder formed by S if § is inextensible. The disclination has screw character and the dislocation edge character, This global defect can also be regarded as a pair of screw disclinations whose combined angle of rotation is 27 and whose axes of rotation are parallel but not coincident. However, since the Burgers vector of the dislocation is related directly to the circumference of the eylinder the first description would appear preferable. A cylindrical erystal is shown in figure 2. Harris and Scriven [13] discuss cylindrical erystals in detail. The Burgers vector of the dislocation component corresponds to the character- istic vector G in their paper and the rotation vector of the diselination component is parallel to their vector z. A eylindrieal crystal can, of course, be obtained simply by identifying opposite sides x of a reetangular portion of a perfect surface crystal where Figure 2. A cylindrical surface crystal: global defect with (screw) disclination and (edge) -ation components.the other two sides ean be represented by b (fig. 3a). (A rectangle is chosen only for convenience.) If, in addition. the sides y are identified as in figure 3b then the result is a toroidal crystal. This corresponds to the introduc- tion of a second global defect, of screw-disclination and edge-dislocation character. at right angles to the first. In figure 3c the one side is rotated through an angle 7 about a 2-fold axis at right angles to the imaginary de- fect line and then rotated through 277 and translated by b as before. This is in fact the intraduction of an edge-disclination component o», into the global defect. S assumes the shape of a Mobius strip and is nonorientable or one-sided (in 3-space), An example is shown in figure 4. If interpenetra- tion is allowed then the addition of a second global defect, with screw- disclination (@:,) and edge-dislocation (b:) components, to the Mobius crystal results in a crystal of the shape of a Klein bottle (fig. 3d). db — ts, a7 # he (a) (by | e (od (a) Ficure 3. [dentification of sides as shown leads to wlobal defects with Burgers and rotation vectors as shown: (a) cylinder, (b) torus, (c) Mabius strip, td) Klein bottle.4. Global defe clination (w=7), screw (Mobius strip) with c¢ onents edge di 27) and edge dislocation, dise Ficure, Extrinsic local defect (Mibius strip). It is purely edge disclination withVY. Local Defects Local defects result from Weingarten-Volterra dislocations introduced inte figure la. Rotation about axes normal to S leads to intrinsic defects and rotation about other axes (1-fold and possibly 2-fold in the midplane of the perfect surface crystal) to extrinsic defects. Dislocations are intrinsic defects and are clearly edge in character. Figure 5 shows aw extrinsi¢ local defect made by rotation through # about a 2-fold axis in the midplane of the perfect crystal: the surface is a Mobius strip. The difference between figures 4 and 5 should be noted. Rotation by 27 ahout the same axis leads to a Mébius strip of two half- twists. This last axis could, of course. be a one-fold axis. Rotation by 27 about other one-fold axes leads to Mobius strips of two half-twists or interpenetrating surfaces if they are allowed. Extrinsic local defects may be regarded as edge in character, Intrinsic defects are of two basic types: (edge) dislocation and (screw) disclination. Two of the latter are shown in figures 6 and 7, The axes of rotation for intrinsic disclinations are normal to 8 and may be s-fold where s=1.2.3, 4, or 6. The rotation angle is of the form (Nabarro [19, p. 124) ti w= 2nn/s (2) where n is any integer. The vector b and the angle w describing any defect depend only on the translational and rotational symmetry of the perfect surface crystal. A network of regular hexagons has the same appropriate symmetry prop- erties as any perfect hexagonal surface crystal and therefore can be used to represent the latter. Similarly a network of squares can represent a surface crystal with 4-fold rotation axes. By introducing defects into such networks and using the simple yet powerful Euler’s formula it is shown below that the number and strength of intrinsic disclinations pos- sible in surface crystals depends on the Euler-Poinearé characteristic x of the surface. Results for crystals of lower symmetry can be obtained by simple argument as special cases of the above. No similar restrictions are found for intrinsic dislocations. The nomenclature used in the graph theory below is that of Ore [20]. The number of end points of edges coinciding at a vertex is the valence p of that vertex. The number of boundary edges of a face in the graph is the dual valence p* of that face: an edge which is on the boundary of one face, only, is counted twice. A graph is regular if every v: the same vale It is dually regular if every face has the same dual valence. It is completely regular if it is both regular and dually regular. The hexagonal lattice of figure 8a has 6-fold rotation axes at face centers (A) and 3-fold axes at vertices (B). A disclination with o=7/3 produces a ex hasFicure 6. Local positive screw disclination with a= 7/3. Ficure 7. Local negative serew disclination with w=— 7/2.ted Ficure 8. fa) Perfect hexa; (ey Serew diselination (o nal lattice. tb) Screw disclination (w= 7/3} at a face center. m/3) at a vertex. (l) Edge disloe of diselinations of oppasite sign, n appearing as a pair pentagon surrounded by hexagons (fig. 8b), The graph is regular with p=3. In general a disclination with w= 27/6 results in a regular graph (p= 3) with a (6-n)-gon surrounded by 6-gons. The integer n is restricted to values less than 6, A disclination with rotation @ = 27/3 about B results in a dually regular graph (p* =6) with one vertex valence 2 and the rest valence 3 (fig. 8¢). In general a disclination at B with w= 27n*/3 leads to a dually regular graph (p*=6) with one vertex valence (3—n*) and the rest valence 3; n* is restricted to less than 3. In a similar manner disclinations can be introduced into a square lattice (fig. 9). The two lattices can be dealt with together. A disclination with angle w,=2nn/s (n (s—n)vn. (5) 7 If v2 =0 for all n* then each vertex is shared by p faces and the number of vertices is > (s—nyn. 6)Tf v,2=1 for n*=nf and py, =0 for n* # n} then one vertex has valence (p—n}) and (p—n}) polygons share that vertex. Equation (6) must be corrected by adding {1— (e—n#*)/p} or af/p. Generally =D omits Drtvne. (7) Pre Substitution of eqs (4), (5), and (7) in (3) gives (5 p-1) Smet Se" vat {s (1-30) +0} Se= We For both s=4 and 6 )+p=0. (8) & (3e “1) Samet En Vix = PX ne and s p-l > Py tdu + p = Pylon ¢ = 2X. From eq (8) > Paty +S) Yutone = 2rrX. This can be written simply SY wi=20y. (9) where «; is the rotation of disclination i. The dislocations of figures 8d and 9e can be regarded as pairs of disc! nations the sum of whose rota! rly dislocations w larger Burgers vectors may be regarded as groups of disclinations of zero total retation. Clearly, therefore, the above argument leads to no restric- tion on the number or Burgers vectors of dislocations in surfac By restricting rotations in a hexagonal lattice to 277n/3 one s crystal with 3-fold axes is a special case of the hexagonal lattice and eq (9) must hold for the crystal. Similarly crystals with 2 and 1-fold axes normal to the surface are special cases of the square lattice. Equation (9), therefore, holds for all surface crystals on closed surfaces at least for intrinsic disclinations of rotation less than 27. ns is zero, Simi hV Conclusion The smallest possible intrinsic disclination has rotation 7/3: it can occur only in a surface crystal with 6-fold symmetry. For a sphere y=2. There- fore, from eq (9), 12 such disclinations are necessary in a sphere. A spheri- eal surface crystal containing 12 disclinations is shown in figure 10: it is in fact a model of a small spherical virus (Caspar and Klug [7]; Kellenberger [15, 16)). The only closed surfaces that need not contain intrinsic disclinations are those with y=0; i.e. the torus and the Klein bottle (Eves [11]). These surfaces, of course, contain global defects with disclination components as discussed in section IV. Any closed, noninterpenetrating surface is topologically equivalent to a sphere with p handles. The Euler-Poincaré characteristic for such a surface is (Eves [11]) —2p. (10) x From eqs (9) and (10) one sees that, except for spherical and toroidal surface crystals (0 and 1-handled spheres), any closed, noninterpenetrating surface crystal must contain at least one negative intrinsic disclination, Figure 10. Spherical surface crystal containing 12 intrinsic disclinations of rotation 7/3. It is model of a spherical virus.Without change in the topology of its surface the shape of a surface crystal may be altered by rearranging its local defects or, perhaps, even by changing their number. Change in the topology of the surface generally involves change in both local and global defects. The writer is at present studying the details of these processes. The ability to undergo these types of changes is nothing less than a very characteristic of living systems. VII. Acknowledgements The writer wishes to express his gratitude to L. E. Scriven for his con- tinuing advice and encouragement. 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