Biomolecular structures of naturally occurring carbohydrate polymers

Biomolecular structures of naturally occurring carbohydrate

polymers

Edward Atkins H.H. Wills Physics Laboratory, University of Bristol, Tyndall Avenue, Bristol BS8 ITL, UK

(Received 29 September 1986)

The bonding mechanism in proteins and polysaccharides is compared and contrasted. Some of the structures for polyglucose are shown to mimic the classic fl-sheet, ~t-helix and collagen helices found in proteins. The effect of glycosidic linkage geometry on polysaccharide shape and structure is discussed together with the effect of changes in the geometry of the monomer units. Multistranded ropes and the effect of non-carbohydrate groups are mentioned briefly.

Keywords: Carbohydrate polymers; bonding mechanism; helices; fl-sheets

Introduction

Unlike their protein counterparts in the world of macromolecules the carbohydrate polymers utilize a wide variety of condensation linkage geometries. Figure 1 illustrates the basic types of linkages available in the proteins and those polysaccharides based on hexoses. The torsional angle pairs, 0, ~, of each swivel joint are influenced by interactions between atoms in the vicinity of the linkage. The proteins, with one type of condensation linkage (neglecting disulphide bridges and the like), are influenced and even obsequious in part to the amino acid sequence or R group appendage. Only a few regular structures are found naturally in the proteins: the fl-chain, stabilized by interchain hydrogen bonding and often occurring in sheets or stacks of sheets, the or-helix, stabilized by intrachain hydrogen bonding and forming a reasonably sturdy structure on its own, and finally the triple-strand rope of collagen where three helical chains (with threefold symmetry) drape around a common axis to create a robust structure, but one which demands glycine (R group being hydrogen) on every third residue. A large gap exists between these few regular structures and the complex folded globular protein structures, usually with a non-repeating amino acid sequence. Although the fl-chain and ~-helix can accommodate a variety of R groups, because both conformations dispose the R groups away from the backbone there is the inherent tendency for protein chains to be driven towards complex three-dimensional folded structures as the information content is increased, i.e. as the amino acid sequence becomes more diverse. Also there is little post- polymerization modification in proteins.

This short review is about carbohydrate structures and I now wish to highlight just some of the many features of polysaccharide conformation against the backcloth of the proteins, which after all are their most conspicuous rivals in the world of naturally occurring macro-

Presented in part at Biologically Engineered Polymers Conference, Churchill College, Cambridge, 21-23 July 1986.

molecules. The variety of condensation linkages imparts an extra dimension to understanding the shapes and interactions of carbohydrate molecules. When this extra dimension of glycosidic linkage geometry is coupled with a variable chemical sequence of saccharides, chosen from a reservoir of some 30-40 different saccharide monomers, a wonderful world of shapes and architectures is generated. If the shape of the puckered six-membered ring is changed--by alteration in the chemistry of side groups for example--the spatial arrangement of glycosidic linkage bonds will change and the polymer conformation

R I

~ C ~o

o , "/N / c N \

a

(.~t0

CH2

b Figure I Schematic diagram of bonding. (a) Amino acids in proteins, with only one type of condensation linkage (R represents side group) and (b) saccharide units in standard 4C~ chair with various types and combinations of linkage geometry. Bonds directed approximately parallel to ring are called equatorial (e) and bonds directed approximately perpendicular to ring are called axial (a)

0141-8130/86/0603234)7503.00 © 1986 Butterworth & Co. (Publishers) Ltd Int. J. Biol. Macromol., 1986, Vol 8, December 323

Structures of carbohydrate polymers: E. Atkins

will undergo a transformation with subsequent consequences on macromolecular interactions, properties and behaviour. Thus, a liaison exists between the chemistry, chemical modification and structure and interactions and an almost continuous spectrum of complexity in structure can exist from the simple to the exceedingly complex, the full appreciation of which is still over the horizon.

Three conformations of polyglucose

Let us consider three examples (and of course there are more!) of the chemically straightforward homopolymers of glucose which we can call the polyglucoses.

The commonly occurring cellulose has glucose units linked diequatorially (see Figure 1) through carbon atoms at ring positions 1 and 4 (i.e. le-4e). This glycosidic linkage geometry generates a rather extended, gently undulating ribbon-like chain with twofold helical symmetry which usually interacts with adjacent parallel chains to form hydrogen-bonded sheets. Such sheets stack to form three-dimensional crystallites I (Figure 2a) and exhibit features closely similar to the classic fl- structures found in particular in the protein fibrous silks. Bundles of cellulose chains in this stacked sheet arrangement form microfibrils of about 20nm in size which are the morphological units in plant cell wall surrounded by a less organized matrix of cellulose, xyloglucans or mixtures of other carbohydrate polymers to create a composite material with desirable, physical,

biological and biochemical properties. The second example is amylose, a constituent of starch.

In this case the linkage is la-4e. Although the glycosidic linkage occurs again through carbon atoms in ring positions 1 and 4 the axial disposition of the bond from C(1) affects the local stereochemistry and has a dramatic effect on the polymer conformation. Figure 2b illustrates the geometry of a particular polymorph of amylose 2. The polysaccharide chain traces out a hollow helical tube-like structure which is stabilized by intrachain hydrogen bonds between successive turns of the helix. This structure mimics the commonly occurring s-helix found in proteins. These self-stabilizing amylose tubes do not favour such strong interchain associations as are evident in cellulose and entirely different textures and properties are observed.

The third and final example in this theme is provided by an extracellular microbial polysaccharide which is used as a gelling polymer and is known as curdlan. The glucose units are linked through ring atom positions 1 and 3 diequatorially, i.e. le-3e. The molecule consists of three chains with the same polarity twisting in unison, and 120 ° out of phase respectively, around a common axis. Thus the molecule is a three-strand, solid rope-like molecule 3 with individual chains fitting neatly together as illustrated in Figure 2c. A triad of interchain hydrogen bonds occurs along the core of the molecule at approximately 0.3 nm intervals yielding a very stable structure. The structure of curdlan bears a striking architectural resemblance to collagen.

,i

a b c

Figere 2 Three structures for polyglucose. (a) Cellulose, le--4e linked polyglucose is a gentle undulating ribbon-like polymer. The conformation is similar to the/%conformation in proteins. (b) Amylose, 1 a--4e linked polyglucose in the V form is a hollow helical tube. The conformation is stabilized by intrachain hydrogen bonds and resembles the ~t-helix in proteins. (c) Curdlan, le-3e linked polyglucose forms a triple-strand rope stabilized by buried hydrogen bonds in the core. The conformation bears a striking resemblance to the protein collagen

324 Int. J. Biol. Macromol., 1986, Vol 8, December

Glycosidic linkage geometry versus chemistry In the three examples outlined in the previous section the

chemistry remains constant while the glycosidic linkage geometry changes. What happens in situations where the chemistry of the saccharide units is changed while the glycosidic linkage is maintained? Consider the le-4e linkage geometry first (i.e. similar to cellulose). Poly-N- acetylglucosamine (chitin), mannan, polymannuronic acid, yield similar twofold extended conformations and patterns of behaviour ~-6. Curdlan has a le-3e linked xylan counterpart, which occurs in siphoneous green algae, and which also exists as an almost identical triple- strand rope. In fact the elucidation of the model was first undertaken on xylan ~'s and it was interesting to find that the change in chemistry, from xylose to glucose, did not change the glycosidic linkage geometry or the desirability to form a rope-like macromolecule. Scleroglucan, which is a polysaccharide similar to curdlan but decorated with a glucose side branch on every third residue in the backbone also exists as a three-strand rope. It is useful to

2.54 nm

Figure 3 Projections of the 52 helix (five units in two turns) of cellulose nitrate. Note the azimuthal rotation from the cellulosic two-fold helix is only 35 °


note that xylan in algae and curdlan from bacteria are biosynthesized in entirely different biological systems, yet both develop the same ingenious hierarchical structure. A similar control of polymer conformation by glycosidic linkage geometry is evident in comparisons between the connective tissue polydisaccharides hyaluronic acid, the chondroitin sulphates and the microbial extracellular polysaccharides from pneumococcus type III and Klebsiella K25, all of which exhibit threefold helical structures 9. These polymers have backbones linked le-3e and le-4e in an alternating manner although the chemistry of the saccharide units changes considerably and Klebsiella K25 has an additional disaccharide side appendage ~ o.

Although glycosidic linkage geometry has a strong influence and places constraints on polymer conformation it does not have complete authority. The polyelectrolytic nature of the connective tissue polysaccharides, for example, means that the conformation is sensitive and responsive to the environment these molecules find themselves in and many polymorphs have been observed ~1. Modifications to cellulose, either chemically induced by forming cellulose nitrate or hydroxypropylcellulose, or biosynthetically by the addition of a hefty trisaccharide side appendage on alternate glucose units (formula I) as in xanthan affects the conformation. Cellulose nitrate forms a 52 helix 12 as illustrated in Figure 3 and hydroxypropylcellulose becomes a threefold helix ~ 3 shown in Figure 4. The X-ray fibre diffraction pattern of xanthan gum (Figure 5) indicates a fivefold symmetry for the molecule. This perturbation from the twofold helical cellulosic backbone has important consequences for chain--chain interactions and a number of these polymers exhibit liquid-crystalline properties and behaviour t3.

Change in shape of saccharide unit It has been pointed out in the introduction how changes

in the disposition of the bonds to the saccharide ring dramatically alter polymer conformation. Of course the ring itself is not a rigid body although in general for a particular chemistry (of side groups and their dispositions) the hexoses usually prefer a standard geometry. For glucose this is the 4C 1 chair 14 as illustrated in Figure 6. If the chemistry of the saccharide unit is changed the energetics of the puckered ring have to be reconsidered and the ring might flip into a different puckered arrangement, for example into the alternative

--~ 4)-fl-D-Glcp-(1 ~ 4)-fl-D-Glcp-(1 --, ± 3 T 1

I //-D-Manp-(1 --~ 4)-~-D-GlcAp-(1 --~ 2)<t-D-Manp-6-OAc / \

4 6 \ /

C / \

CH a COOH

formula I

Int. J. Biol. Macromol., 1986, Vol 8, December 325


T

1.51 n m

_L

Figure 4 Threefold model of hydroxypropylcellulose. The irregular substitution of side groups suppresses side-to-side crystallization and imparts liquid-crystalline properties to the molecule (courtesy of Dr W. S. Fulton)

Figure 5 X-ray fibre diffraction pattern of xanthan gum showing a meridional signal at spacing 0.95 nm on the fifth layer line indicating the fivefold symmetry of the molecule (courtesy of Dr K. Veluraja)

~C4 chair (see Figure 6) or various other shapes ~4. This occurs in a number of polysaccharides, but the obvious example to choose to illustrate the effect and subsequent consequences is alginate.

Alginate is a polyuronide found in brown algae and certain bacteria 15 and is extensively used industrially utilizing its characteristic gelling behaviour in the presence of divalent ions, particularly calcium. It was established by H~iug and coworkers 16 that alginic acid consists of blocks of fl-D-mannuronic acid (M) and C~-L- guluronic acid (G), diagrams of which are shown in Figure 7. The polymer is biosynthesized as polymannuronate and then sections of the polymer are epimerized with an enzyme which results in mannuronate being converted to guluronate such that runs of ( -G-) , occur in (-M-), . This is also an example where post- polymerization modification occurs in polysaccharides, other examples being in chondroitin sulphate, carrageenan and heparin. X-ray diffraction was used to establish the conformations of both polymannuronic acid 17 and polyguluronic acid is which enabled the gelation mechanism to be understood at atomic resolution. The mannuronate unit has one group, the hydroxyl group in the 2 position, axially disposed when in the normal 4C 1 chair (Figure 7a). The shape of the polymannuronic acid chain is similar to that expected for a le-4e linked homopolymer: a gentle rippling twofold helical ribbon (see Figure 8a) as mentioned previously. The epimerase moves the carboxylate group in the 5 position from an equatorial disposition to an axial disposition. The saccharide ring now has two groups axially placed: the carboxylate and the hydroxyl group at position 2. X-ray results ~8 show that the ring flips from the 4C~ chair to ~C4 chair so that both these groups become equatorially placed (Figure 7b). However the linking bonds at positions 1 and 4 change from diequatorial to diaxial with resultant change in the polymer shape, giving rise to a pronounced zig-zag appearance (Figure 8b) and a reduction of the chain periodicity of about 17 ~o. The X-ray structure refinement of polyguluronic acid 18 provides evidence for the incorporation of a water molecule into the largely

4 0 5 1

I 4

4C 1 lC 4

Figure 6 The normal 4C~ and alternative ~C 4 conformations of the pyranoid ring. The reference planes are indicated by dots and the carbon atoms numbered sequentially

OH OH

,coo o:,

OH

a b

Figure 7 Repeating monosaccharides in alginate (a) fl-D- mannuronic acid in normal 4C 1 chair. Glycosidic linkages are diequatorial via 1 and 4 positions. (b) a-L-guluronic acid in alternative 1C 4 chair. Glycosidic linkages are diaxial via 1 and 4 positions


t im

t im

a b

Figure 8 Projections of the chain conformations of alginate in directions perpendicular (top) and parallel (bottom) to chain axis. (a) Twofold helix for polymannuronic acid. (b) Twofold helix for polyguluronic acid. Note the pronounced zig-za'g shape compared with that of (a), and the contraction of the molecular dimensions from 1.04 to 0.87 nm

hydrophobic pocket created between juxtapositioned zig- zag chains. This feature of the structure has been used to speculatively propose 2° the so-called 'egg-box' model for incorporating divalent counterions such as calcium into the guluronate rich parts of alginate and creating junction zones in the gel as illustrated schematically in Figure 9.

Intertwining double helices

Multistranded ropes in polysaccharides were discovered 21, their proper characters established 7'a and their details analysed using good quality X-ray fibre diffraction patterns in the 1960s. Double-strand ropes were proposed for carrageenan based on X-ray fibre diffraction patterns 22'23 and although the measurement of the vital intensity data essential to confirm a model is irritated by reported statistical disorder 2 a in the patterns used for the analyses, which therefore adds an extra degree of uncertainty, a double helix with two similar chains axially displaced by half the pitch is favoured on X- ray diffraction grounds, at least for iota-carrageenan. The untwining, or more to the point, the retwining of chains as a function of temperature to form junction zones in gelation 24 is difficuB to visualize from a topological point of view. Although the original rather naive model for gelation has been replaced with aggregation* of double- helix molecules 25 as the basic mechanism for gelation, the single chain to double helix transition is still an

* Junc t ion zones based on aggrega t ion is an old concept and is ak in to the 'fringed micel le ' mode l found in m a n y texts on synthet ic polymers .


ingredient of the gelation mechanism and used to account for the change in optical rotation. An alternative model based on side-by-side association of two carrageenan chains has been proposed 26 to overcome the topological concern although such a model is not supported by X-ray diffraction studies on oriented fibres.

Gellan gum is a recently discovered extracellular polysaccharide. The native material contains approximately 6 wt % of O-acetyl groups. It forms weak gels whilst the deacetylated polysaccharide forms stiff, brittle gels. The primary structure 27'28 has a linear tetrasaccharide repeat (formula II). The X-ray diffraction patterns of oriented native and deacetylated samples show the same general features 29 although the latter is much more crystalline.

3)-fl-D-Glcp-(l ---* 4)-fl-D-GlcpA -(1 ---, 4)-fl-D-Glcp-(1 ---* 4)-Ct-L-Rhap-(l ---,

formula II

The first meridional diffraction signal occurs at a spacing of 0.94 nm which is less than half the expected value for a fully extended tetrasaccharide repeat. Although the model still needs to be refined to obtain a better fit with the intensity data a threefold double-helix, with the chains displaced by half the pitch relative to each other is the model preferred 29, a projection of which to illustrate the general features, is shown in Figure 10.

A double-helix model has also been proposed for the native polymorphs of amylose 3° which can be converted into a single helix 2 in such reagents as DMSO; however this is apparently a non-reversible process.

Clearly multistrand ropes exist in polysaccharides and I suspect more will be found, especially amongst the new microbial polysaccharides now being investigated. It would appear that Nature biosynthesizes multistrand ropes in an attempt to create more robust, less flexible molecules. Certainly we know on general grounds that the stiffer the macromolecule--the more rigid the rod in solution--the lower is the concentration for the transition from isotropic liquid to the liquid-crystalline phase. Since

Figure 9 Schematic representation of a guluronate junction zone in alginate, the egg-box model. The filled circles represent calcium ions

Int. J. Biol. Macromol., 1986, Vol 8, December 327


interaction between the chains increases locking the molecule into a stiff double-strand rod which will (at that concentration) interact and aggregate to form gels. It is interesting to note, for example in the case ofcarrageenan, that single chains have never been captured (with regular conformations) in the solid state and therefore a mechanism of loosely bound to tightly bound double- strand ropes might offer a solution.

i~ ~ .... i~i

///I Figure 10 Trial model structure of the double-helix model for geilan gum. The chains are displaced relative to each other by half the pitch (5.64 nm) in order to cancel completely odd-order layer lines of this spacing resulting in layer lines which are orders of 2.82 nm

for long-chain molecules liquid-crystalline formation and gelation can be different facets of the same phenomenon (gels being created due to chains connecting through from one mesophase domain to others), stiffer molecular ropes will interact at lower concentrations giving rise to gelation with lower levels of polymer present. On general, perhaps speculative, grounds a loosely coupled double- strand rope could be flexible in solution, yet when conditions change, say by lowering the temperature, the

Effect of acetylation

Two polysaccharides, the capsular polysaccharide produced by Klebsiella aerogenes serotype K54 and Enterobacter (NC1B 11870), known also as XM6, have similar chemical structures 31'32. The structure for K54 is given by formula III and consists of an octasaccharide repeat. K54 is similar except it does not have the O-acetyl group attached to every other fucose unit and so the formal chemical repeat reduces to a tetrasaccharide repeat. The X-ray fibre diffraction patterns are shown in Figure 11. As can be seen a considerable difference exists: the deacetylated K54 (similar to XM6) pattern is highly crystalline while the K54 pattern exhibits rather less crystallinity. In collaboration with Drs V. J. Morris and M.J . Miles at the Food Research Institute, Norwich my research student Philip Attwool and I have established 33 that deacetylation of K54 in the solid state converts the K54 X-ray pattern into a highly crystalline pattern similar to XM6. It is known that XM6 will disperse in water to form a viscous solution. Addition of inorganic salts to raise the ionic strength leads to thermoreversible gelation. K54 will also disperse in water to form a viscous solution but raising the ionic strength does not lead to gelation. Thus the presence of O-acetyl groups in K54 inhibits gelation. When K54 is deacetylated it will gel on the addition of ions. X-ray diffraction results suggest that the gelation of XM6 results from aggregation (crystallization) of segments of helices.

In the previous section I illustrated the effect of acetylation on gellan gum. These examples illustrate the importance of non-carbohydrate substituents on polysaccharide interactions. X-ray diffraction is a useful method to monitor the changes, both in terms of conformation and interactions, created by removing these decorating appendages.

--~ 4)-~t-D-GlcpA-(1 --* 3)-~-L-Fucp-(I --~ 3)-fl-D-Glcp-(1 --* 4 T 1

fl-o-Glcp

4)-~t-D-GlcpA-(1 --* 3)-~t-L-Fucp-(1 --~ 3)-fl-D-Glcp(1 --~ 4 4

(2 or 4) T T 1

OAc fl-D-Glcp

K54 and XM6 have identical glycosyl sequences. The only difference is that K54 contains one O-acetyl group attached to a fucosyl residue on every alternate tetrasaccharide.

formula III


i ~ %~i!~!i~ii~iii%i~iiii!i~ii~ii~i~iiiiiii~iii~iii®!!~iiiii~iiiiii~iii~iiiiii!~iii~i~iii~i!ii!iii~i!~iiiii~i~iiii~iiiii!~!~ii~ ~iiiii I~ ?!~ ~ii!ii ~ /

Structures o f carbohydrate polymers: E. Atkins

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

a b

Figure 11 (a) X-ray fibre diffraction pattern of native K54 polysaccharide. (b) X-ray pattern of deacetylated K54 (in the solid state) which bears a close resemblance to the pattern obtained for XM633 (courtesy of Mr P. T. Attwooi)

Summary

In such a short review it has been possible to touch on only a few of the features and problems still unsolved which involve the molecular biology of carbohydra te polymers. It is hoped however that just those glimpses of conformat ion and architecture will be sufficient to highlight the potent ia l advantages to be gained from a fuller unders tand ing of the relat ionship between structure, interact ion, funct ion and properties of these macromolecules.

Acknowledgements

I wish to thank Phil ip Attwool for al lowing me to show some results, in press bu t as yet unpubl ished, on XM6 and K54 and Drs M. J. Miles and V. J. Morris for useful discussions. I t hank the A F R C and SERC for suppor t ing this work.

References

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Biomolecular structures of naturally occurring carbohydrate polymers

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