Biomimetic engineering ofcellulose-based materialsTuula T. Teeri1, Harry Brumer III1, Geoff Daniel2 and Paul Gatenholm3

1 Swedish Center for Biomimetic Fiber Engineering, KTH Biotechnology, AlbaNova, SE-10691 Stockholm, Sweden2 WURC, Department of Wood Sciences, Swedish University of Agricultural Sciences, Box 7008, SE-75007 Uppsala, Sweden3 Chalmers University of Technology, Department of Chemical and Biological Engineering, Biopolymer Technology,

SE-412 96 Gothenburg, Sweden

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Biomimetics is a field of science that investigatesbiological structures and processes for their use asmodels for the development of artificial systems. Biomi-metic approaches have considerable potential in the de-velopment of new high-performance materials with lowenvironmental impact. The cell walls of different plantspecies represent complex and highly sophisticated com-posite materials that can provide inspiration on how todesign and fabricate lightweight materials with uniqueproperties. Such materials can provide environmentallycompatible solutions in advanced packaging, electronicdevices, vehicles and sports equipment. This review givesan overview of the structures and interactions in naturalplant cell walls and describes the first attempts towardsmimicking them to develop novel biomaterials.

Trends in biological material scienceThe development of materials has shaped the fate andsuccess of mankind since the development of the first tools,made of wood and stone. Innovations in polymer chemistryafter the World War II launched a new, rapidly changingera of materials technology. Composite materials, featur-ing glass, carbon fiber or Kevlar (http://www2.dupont.com/)embedded in polymer matrices, are widespread through-out modern societies. However, declining oil resources andglobal requirements for sustainable development impose aneed to replace petrochemical-basedmaterials with renew-able ones. The synthesis of biological materials in natureoccurs by energy efficient processes at moderate tempera-tures and low pressure, using water as the solvent. The lowenergy input of these processes is compensated by theprecise molecular design of the constituent biopolymers,which drives efficient self-assembly of biomaterials [1].Owing to their smart design, natural materials outperformmost man-made composites. Classical examples of naturalhigh-performance composites in which matrix proteinscontrol the formation of the inorganic component includeabalone shells, bone and enamel [2,3]. Other natural com-posites with unique properties include cactus spines, withtheir high degree of stiffness contributed by an arabinan–cellulose composite [4], and the tunics of sea peaches,composed of cellulose, proteins and mucopolysaccharides[5]. Therefore, mimicry of biological structures and the

Corresponding author: Teeri, T.T. (tuula@biotech.kth.se).Available online 23 May 2007.

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processes controlling their synthesis and self-assemblyhas great technical and scientific potential.

Wood is perhaps one of the most complex naturalcomposite substances and it is widely used as a structuralmaterial. The properties of wood are governed by threelevels of organization [6]: (i) the chemical composition andnanostructure of the cell walls; (ii) the patterning of the cellwalls and the size and shape of the constituent wood cells;and (iii) the hierarchical organization of the different celltypes to form higher orders of the wood structure. Theexcellent mechanical properties of wood rely on the compo-site nature of the fiber cell walls, in which the cellulosemicrofibrils reinforce a matrix of hemicelluloses and lignin.Owing to their low density and excellent strength proper-ties, fibers extracted from hemp or linen have been used todevelop lightweight biocomposites, particularly for use inautomobile interiors.However, owing to thedifferent chemi-cal properties of natural fibers and synthetic matrices, poorinterfacial stability of such composites is a common problem[7,8]. Another problem is the high moisture absorption ofplant fibers, which leads to poor dimensional stability.Because living plants have reconciled these problems,the compatibility between phases can be improved bylearning from nature, to produce materials with increasedfunctionality.

The plant cell wall – a versatile biocompositeThe primary cell wall is a dynamic structure that undergoesmany changes during plant development, and it must beable to accommodate a variety of mechanical requirements[9]. The basic building blocks of primary cell walls arecellulose, hemicelluloses, pectin and structural proteins(Box 1). The strong crystalline cellulose microfibrils encap-sulate the cell in a mesh-like structure (Figure 1a), andhemicelluloses associate with the cellulose microfibrils tocombine strength with extensibility. For example, the xylo-glucans that associate intimately with cellulosemicrofibrils[10] also act as tethers between adjacent microfibrils,thereby contributing to the porosity and extensibility oftheprimary cellwalls of dicotyledons. Pectins [11] are joinedbycovalentand ionic cross-links to formstructural networksthat are independent but synergistic with the cellulose–hemicellulose networks [12]. The physical properties ofhemicelluloses and pectin are largely determined by thenature and abundance of side chains, and depend on thelocal concentrations of ionically and covalently bound salts

d. doi:10.1016/j.tibtech.2007.05.002

Box 1. Main components of plant cell walls

� Cellulose is a linear polymer of b-(1,4)-D-glucose units. During

cellulose biosynthesis the individual polymers stack onto each

other forming crystalline microfibrils that act as the main load-

bearing component of the cell wall (Figure Ia).

� Hemicelluloses are a heterogeneous group of branched polysac-

charides, including xyloglucan in the primary cell walls of

dicotyledons, glucuronoxylans in the secondary cell walls of

hardwoods, as well as glucomannan and arabinoxylan in the

secondary cell walls of softwoods. Arabinoxylan is also commonly

found in the cell walls of grasses (Figure Ib).

� Pectin constitutes another group of branched polysaccharides,

including homogalacturonans, rhamnogalacturonans, and substi-

tuted galacturonans [10]. Pectin is typically found in the middle

lamella, cementing together the primary walls of adjacent plant

cells (Figure Ic).

� Lignin is a complex phenolic polymer composed of three mono-

meric building blocks: coniferyl alcohol, sinapyl alcohol and

paracoumaryl alcohol. Lignin fills the spaces in the cell wall

between cellulose, hemicellulose and pectin, thereby conferring

mechanical strength to the cell walls. Lignin is typically present in

the secondary cell walls of trees (wood) (Figure Id).

� Structural proteins commonly found in plant cell walls include, for

example, extensins, arabinogalactan proteins (AGP) as well as

glycine-rich (GRPs), and proline-rich (PRPs) proteins [16] (Figure Ie).

Figure I. Main components of plant cell walls. (a) The repeating unit of a cellulose polymer; (b) the repeating unit of a xyloglucan polymer, one of the cell wall

hemicelluloses; (c) part of the structure of polygalacturonan, a cell wall pectic polysaccharide; (d) the building blocks of lignin; (e) the amino acid sequence of a typical

proline-rich protein (PRP) found in plant cell walls.

Figure 1. Organization of the cellulose structure in the primary (a) and secondary (S2) (b) cell wall layers of spruce wood tracheids, as observed using scanning electron

microscopy. The individual cellulose microfibrils are organized into larger aggregates that have multidirectional orientation in the primary wall but show distinct alignment

in the secondary wall layers. Bars = 1 mm.

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(e.g. calcium and boron) and potential cross-linking agents,such as ferulic and coumaric acids [11,13]. By varying thestructures or the chemical environment of these polymers,themechanical properties of cell walls can be altered duringdevelopmental stages and in different plant tissues [6]. Thediversity of mechanical properties observed in differentparts of thistle flower is an excellent example of such vari-ation [14].

A variety of cell wall-associated enzymes and otherproteins also influence cell wall properties and behavior[15]. For example, the extensibility of the cellulose–xyloglu-can network can be regulated by the action of expansins,

Figure 2. Varied structures of wood cell walls. (a, c and e) birch fibers (F) and vessels (V)

and intervessel pitting (IP). (b) Spruce latewood tracheids (T). (d) Douglas fir with typ

bordered pit (BP) with margo (M); (g) Devil tree (Alstonia scholaris) vessel with vestured

rich (CR) inner S2 wall layer. Bars: (a) = 100 mm; (b, d and f) = 50 mm; (c, e and h) = 20 m

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specific cell-wall proteins [16]. In addition, many differentstructural proteins (Box 1) are cross-linked to the cell walland might influence its mechanical behavior [17].

The basic structural elements of wood – the trachearyelements in softwood and fibers in hardwood – are hollowdeadcells surroundedbysecondary cellwalls (Figure2).Thesecondary walls contain different hemicelluloses to theprimary walls and are lignified (Box 1) in the latter stagesof wood formation. The cellulose microfibrils are depositedin the secondarywalls byahighlyorganizedprocess, leadingto a hierarchical structure with three layers (S1, S2 and S3).In the dominant, S2, layer the cellulose microfibrils are well

showing characteristic scalariform perforation plates (SP) that connect axial vessels

ical spiral thickening (SP) and bordered pits (BP) in earlywood tracheids. (f) Pine

intervessel pits (VIP). (h) Tension wood fibers from poplar wood with thick cellulose

m; (g) = 10 mm.

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aligned (Figure 1b), contributing to the general mechanicalstrength of wood [18]. Changes in the chemical compositionor the fine structure of wood cells by developmentally con-trolled or by externally induced stimuli lead to differentmechanical properties. For example, the secondary walls ofmany wood cells display a wide variation in pitting(Figure 2). The length and width of the cells also varybetween softwoods and hardwoods, and between differenttree species. Furthermore, deviations from the vertical pos-ition of the stem are compensated by the formation oftension wood with high cellulose content in hardwoods(Figure 2h), and compression wood with increased lignincontent in softwoods. The gelatinous, non-lignified cellwallsof tension wood and flax fibers feature thick S2 layers(Figure 2h) and a high proportion of galactose-containingpolymers [19]. Understanding the structure–propertyrelationships in different types of plant tissues paves theway for the rational development of novel materials.

Genetic approaches for studying and engineeringplant cell wallsThe isolation and characterization of the components ofdifferent plant organs and tissues are not trivial tasks. Forstructural analysis, the individual polymers must bechemically or physically separated from other cell wallcomponents. Because the different cell wall polymers areintimately entangled and cross-linked by many non-covalent and covalent interactions they are difficult toseparate without changing their chemical and/or physicalstructures. It has been difficult to correlate cell wall mech-anical properties with the structural characteristics of theconstituent polymers using traditional techniques.

Screening and characterizing cell wall mutants of thalecress (Arabidopsis thaliana), combined with mechanical,spectroscopic and enzymatic characterization of the affectedtissues, have recently provided powerful tools towards un-derstanding cell wall properties [20–24]. Furthermore,recent advances in genomic and proteomic approaches pro-vide rapid and convenient tools to identify previouslyunknown enzymes that synthesize plant cell walls [25]. Arecent and elegant example describes how xyloglucan sidechains influence the overall wall strength of Arabidopsishypocotyls [26]. By measuring the tensile parameters ofhypocotyls of a series of dark-grown Arabidopsis mutants,the loss of galactose-containing side chains of xyloglucanwas shown to impair the overall wall strength, whereas lossof xyloglucan fucosylation only caused a slight decrease oftensile strength. By contrast, loss of fucose in rhamnogala-curonan II (RGII) reduced the degree of boron-mediatedcross-linking of pectin and resulted in clearly reduced ten-sile strength [26].

Microbes provide rich sources of enzymes that degradeplant biomass [24], and several recent examples demon-strate their potential as tools to alter plant cell wall proper-ties. Expression of microbial cellulases or non-catalyticcellulose-bindingmodules [27] increasedtherateof cellulosebiosynthesis and altered the morphology of the celluloseproduced by transgenic plants [28]. Transgenic tobacco(Nicotiana tabacum) and rice (Oryza sativa), both expres-singmicrobial cellulases, exhibited swollen cell walls, whichimproved thedigestibility of this structure [29,30]. In Italian

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ryegrass (Lolium multiflorum) the arabinosyl residues inarabinoxylansare cross-linkedby ferulic acidesters, and theexpression of a fungal ferulic acid esterase gene in trans-genic ryegrass made the cell wall more susceptible to enzy-matic attack by endoxylanases [31]. These examples aimedto improve the digestibility of plant biomass by ruminants,but the expression of enzymes acting to increase cross-linking of the cell wall components could also be used toimprove cell wall mechanical properties.

Bacterial cellulose: towards novel biocompatiblematerialsBacteria of the Gluconacetobacter genus extrude purecellulose ribbons into their culturemedium[32]. Theproper-ties of the resulting cellulosic material can be modulated byusing different bacterial strains, by varying the parametersof the cultivation, and by adding chemicals and polymersinto the culture medium [33,34]. Access to such non-assembled building blocks opens opportunities towards anew generation of materials. Cellulose is fully biocompati-ble, and interesting potential applications have alreadyemerged in the health-care sector, including wound healingsystems and artificial-skin products [32]. Bacterial cellulosecan also be grown in defined shapes, such as hollow tubes,that can be used to replace blood vessels in surgical oper-ations [34]. Tubular implants made of bacterial cellulosewithhighwater contentareflexibleandelastic butmaintaina constant shape. They are stable against pressure and canbe easily sutured into biological tissues [34,35]. Nativebacterial cellulose has recently also been presented as apotential, biocompatible scaffold with good mechanicalproperties for the engineering of cartilage and blood vessels[36,37].

Understanding the composite nature of plantcell wallsGrowth of the bacterium Gluconacetobacter xylinus in thepresence of various plant cell wall polysaccharides providesa convenient model system to investigate the properties ofnatural cell walls. The addition of hemicelluloses to thebacterial fermentation of cellulose affected the size of themicrofibrils [38,39], which supports the hypothesis thathemicelluloses influence the aggregation pattern of cellu-lose [40]. The addition of xyloglucan reduced the crystal-linity of cellulose, possibly by intercalating into the cellulosecrystals [41]. The galactose side chains of xyloglucan con-stitute the major determinant of cellulose composite for-mation, whereas the fucose substitution seems to act as asecondary modulator [42]. Xyloglucan, glucomannans andsome galactomannans that cross-link cellulose microfibrilsin primary cell walls contributed considerably to the elasticproperties of bacterial cellulose-based composites [43,44].By contrast, the formation of cellulose and/or pectin net-works apparently does not occur by direct binding inter-actionsbetweencelluloseandpectin,but insteaddependsonthe presence of preformed pectin networks of moderatestrength [45]. Tensile deformation tests carried out withdifferent combinations of cellulose, xyloglucan and pectinrevealed that the best strength was achieved by celluloseonly, whereas composites including xyloglucan or pectinwere weaker but more extensible [46]. The properties of

Figure 3. Atomic force microscopy (AFM) images (2�2 mm) of (a) a film of pure bacterial cellulose; (b) a composite film containing 75% bacterial cellulose and 25% xylan,

and (c) a composite film containing 50% bacterial cellulose and 50% xylan [48].

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the composites could be further modulated by addinghydrolytic enzymes or expansin [47,48].

The structure of secondary cell walls has been mimickedbymixing bacterial cellulosewith glucuronoxylan extractedby alkali from aspen wood [49]. The mechanical properties,suchas tensile strength and stiffness, of thenanocompositesreached a maximum at the same cellulose:xylan ratio as inthe secondary cell wall, and their morphology resembledthat of native secondary cell walls (Figure 1, 3a–c). Evencloser similarity with secondary cell walls was achievedwhen the composites were prepared by using glucuronox-ylan extracted from delignified aspen wood chips usingDMSO to preserve the native acetyl groups. Moisture-induced softening due to the plasticization of glucuronox-ylan was observed with both the wood fibers and in themodel system. However, the softening behavior of the twomaterials was not identical, most probably owing to differ-ences in spatial organization of the components [50]. Inaddition to excellent mechanical properties, the cellulose–glucuronoxylan composites had a transparent appearancesimilar to plastic films or composites of cellulose nanocrys-tals mixed with polymer resins [51,52]. Furthermore, thecellulose–glucuronoxylan composites also exhibited rema-rkable oxygen barrier properties, which make them excel-lent candidates for future advanced packaging materials[53].

Biomimetic modification of cellulose surfacesMost cellulose-based materials used industrially arechemically treated at various points in the manufacturingprocess to alter their properties. When chemically modifiedby acetylation, cellulose loses its native structure andstrength [34]. In applications relying on the superb load-bearing properties of cellulose, coating rather than directchemical modification is therefore used to alter the surfaceand the bulk mechanical properties, but not the structure,of cellulose. For example, paperboard used as packagingmaterial for liquids and foodstuffs is often laminatedwith athermoplastic and aluminium to provide an impermeablebarrier to aqueous solutions.

Inbiocomposites, cellulose isblended inapolymermatrixin the presence of various compatibilizers, to achieve goodstrength properties [7]. With current technology, however,problemsareoftenencountered in the retentionof chemicals

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on the fiber surfaces and the interfacial stability of thematerial blends [8]. In plants, the combination of strengthand interfacial stability is achievedby coating cellulosewithmatrix polysaccharides that can interactwith other cellwallpolymers and proteins. One idea borrowed from nature is touse chemically or enzymatically modified xyloglucan toattach functional groups to cellulose surfaces [54]. Xyloglu-can can be isolated in bulk amounts from tamarind seedsand it binds to cellulose surfaces with high affinity. It can beeasily modified by a step-wise process (Figure 4), startingwith chemical modification of small xyloglucan oligosac-charides, which are not retained on cellulose surfaces butwhich can be joined to polymeric xyloglucan by usingthe enzyme xyloglucan endo-transglycosylase (XET, E.C.2.4.1.207).Adsorptionof themodifiedhighmolecularweightxyloglucan onto cellulosic materials results in surface-specific chemical functionalization. Using this approach, awide range of different chemical groups (Figure4) havebeenattached onto different types of cellulose surfaces, includingpulp fibers, regenerated cellulose films and filter paper[54,55]. Of particular interest is the attachment of initiatorsof polymerization reactions that permit the construction ofextended polymer architectures onto cellulose surfaces[56,57]. In this way, the cellulose fibers can be completelyencapsulated in a polymer sheath, which should consider-ably improve their compatibility with the polymer matricescommonly used to prepare biocomposites.

In addition to xyloglucan, the affinity of xylan to thesurfaces of cotton linters and bacterial cellulose has beenused to modify their surface properties [58], and modifi-cation of pulp fibers by controlled assembly of xylans hasbeen shown to improve the wettability of the pulp [59].Pullulan abietate, a compound mimicking the naturalhemicellulose- and lignin-containing interfaces in plantcell walls, has also been found to rapidly self-assemblein a desorption-resistant fashion onto cellulose surfaces[60]. Following enzymatic cross-linking or thermoplasticconsolidation, it might also prove useful for improving theinterfacial stability of cellulose-based composites.

Besides physical binding interactions and entanglement,plant cell walls are consolidated by covalent or non-covalentcross-linking of the matrix polysaccharides with each otheror with lignin. Enzymes have crucial roles in creatingthese interactions and thus provide interesting tools for

Figure 4. An overview of xyloglucan-mediated cellulose surface modification [50]. (a) Low molecular weight xylogluco-oligosaccharides (XGO) bearing chemical

functionality (R) are incorporated into high molecular weight xyloglucan (XG) by the enzymatic action of a xyloglucan endo-transglycosylase (XET). (b) The resulting

xyloglucan conjugate (XG-R) is adsorbed from aqueous solution at ambient temperature onto a cellulose surface, for example, cotton fiber, wood pulp fiber or regenerated

cellulose. (c) The installed functional group might produce a desired surface effect itself or might be transformed through further reactions on the cellulose surface.

Examples include fluorescent optical brightening agents (i); nucleophiles such as amino groups (ii); thiol groups for specific, reversible modification (iii); biomolecule

capture agents, including ligands and reactive groups (iv); and initiators for radical polymerization, for example, atom transfer radical polymerization (ATRP), to produce

highly hydrophobic surfaces (v). Xylogluco-oligosaccharides (XGO) are based on a b–(1–4) glucan backbone and have the general composition Glc4Xyl3Gal0–2. Native

tamarind xyloglucan (XG) comprises multimers of these oligosaccharides and has a molecular weight >200 000 Da. A xyloglucan chain of >5 XGO units is required for

quantitative binding to cellulose. Abbreviations: DTT, dithiothreitol (a disulfide bond reducing agent); FITC, fluorescein isothiocyanate; MTS, methanethiolsulfonate.

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fiber modification. The wood particles and fibers used tomanufacture boards are traditionally treatedwith syntheticformaldehyde-based resins or subjected to high pressuresand temperatures to improve strength properties. In wood,oxidative enzymes catalyze the formation of monolignolradicals, which undergo chemical coupling to form ligninpolymers. Oxidative enzymes have been used to activatesurface exposed lignin and lignin precursors on wood fibersurfaces, leading to enhanced bonding strength of mediumdensity fiber boards [61,62]. Pilot-scale testing of fiber-boardsmade of enzyme-activatedwood fibers demonstratedstrength properties comparable to boards bonded by syn-thetic resins [63,64].

Cross-linking proteins for interfacial stabilityNatural or engineered cross-linking proteins might alsobecomeuseful tools toenhancebinding interactionsbetweennatural polymers, thereby leading to improved strengthproperties of the resulting composites [65]. Extensins(Box 1) represent natural cross-linking proteins that prob-ably form covalent networks in plant cell walls by theirtyrosyl and lysyl residues cross-linked by extensin peroxi-dases [66]. Because complex natural cross-linking proteinsare difficult to produce in large quantities, biomimeticapproaches might provide a practical alternative. Forexample, the addition of engineered double-headed cellu-lose-bindingproteins improved themechanical properties ofpapers and increased thewater-repellence of paper surfaces[67]. Furthermore, bi-functional proteins consisting of cel-lulose- and starch-binding modules promoted interactionsbetween cellulose and granular starch and improved thebinding of soluble starch onto cellulose surfaces [65]. Bybuilding on the natural diversity of protein-binding inter-actions as well as protein engineering, a wide range ofmolecular architectures can be designed. Small proteindomains can also be engineered to bind metals, semi-con-ducting oxides and other inorganic compounds to fabricatedifferent types of functional nanostructures [68]. Whenlinked to cellulose-binding modules, such molecular assem-blies can be anchored to cellulose surfaces to give rise to awhole rangeofnew types of functions.Potential applicationsof such surfaces extend far beyond the traditional uses ofcellulose.

Conclusions and future perspectivesThe interest in entirely bio-based materials is steadilyincreasing in response to growing environmental awarenessand declining supplies of raw oil. Cellulose microfibrils arenatural reinforcing elements with excellent mechanicalproperties but, nevertheless, poor performance in technicalapplications. This is mainly due to insufficient dispersion ofthe microfibrils into commonly used polymeric matrices intraditional processing equipment, differences in polaritybetween cellulose and hydrophobic polymers that resultin poor interfacial adhesion, and poor dimensional stabilityof cellulose fibers when subjected to moisture. As summar-ized in this review, itmight bepossible to solve some of thesebottlenecks by learning how cellulose interacts with otherbiopolymers in plant tissues. In particular, the lack ofinterfacial interactions with other polymers can be over-come by coating cellulose with (bio)polymers that bind to

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cellulose surfaces and can, in turn, be chemically activated.This opens the whole range of composite manufacturingtechnologies relying on in situ polymerizing matrices.Natural cellulose fibers that exhibit a range of differentsizes and shapes are not suitable building blocks for nanos-tructured composites. However, recent technology to pre-pare cellulose nanocrystals of defined dimensions isovercoming this limitation [69], thus paving the way forthe development of cellulose-based nanomaterials for differ-ent types of coating applications and packaging materials.In addition, cellulose-based materials with an excellentcapacity to hold water have interesting applications asbiocompatible materials that can be used in contact withthe human body, including tissue scaffolds and implants,wound dressings, biocompatible coatings and drug-releaseformulations. The biomimetic approaches described in thisreview have great potential to tailor the functionality and toimprove the performance of these new materials.

AcknowledgementsWe thank the Knut and Alice Wallenberg Foundation (http://www.wallenberg.org) (G.D., P.G. and T.T.) and the Swedish ResearchCouncil (http://www.vr.se) (H.B.) for financial support.

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