Skip to main content
SpringerLink
Log in

Evidence for differential interaction mechanism of plant cell wall matrix polysaccharides in hierarchically-structured bacterial cellulose

  • Original Paper
  • Published:
Cellulose Aims and scope Submit manuscript

Abstract

The interaction mechanism of two plant cell wall polysaccharides, arabinoxylan and xyloglucan, with cellulose has been investigated by means of bacterial cellulose fermentation to mimic the cell wall biosynthesis process. The combination of small angle scattering techniques with XRD and SEM has enabled the identification of different structural features comprising hierarchically-assembled bacterial cellulose, i.e. cellulose microfibrils and ribbons. The SANS results have been described by a core–shell formalism, which accounts for the presence of regions with different solvent accessibility and supports the existence of microfibril sub-structure within the ribbons. Additionally, SAXS and XRD results suggest that the microfibril packing and crystalline structure are not affected by arabinoxylan, while xyloglucan interferes with the crystallization and assembly processes, resulting in less crystalline Iβ-rich microfibrils. This specific interaction mechanism is therefore crucial for the cellulose microfibril cross-linking effect of xyloglucan in plant cell walls. It is proposed that the distinct interaction mechanisms identified have their origin in the differential structural role of arabinoxylan and xyloglucan in plant cell walls.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Abràmoff MD, Magalhães PJ, Ram SJ (2004) Image processing with imageJ. Biophotonics Int 11:36–41

    Google Scholar 

  • Astley OM, Chanliaud E, Donald AM, Gidley MJ (2001) Structure of acetobacter cellulose composites in the hydrated state. Int J Biol Macromol 29:193–202

    Article  CAS  Google Scholar 

  • Astley OM, Chanliaud E, Donald AM, Gidley MJ (2003) Tensile deformation of bacterial cellulose composites. Int J Biol Macromol 32:28–35

    Article  CAS  Google Scholar 

  • Baskin TI (2005) Anisotropic expansion of the plant cell wall. Annu Rev Cell Dev Biol 21:203–222

    Article  CAS  Google Scholar 

  • Blazek J, Gilbert EP (2011) Application of small-angle X-ray and neutron scattering techniques to the characterisation of starch structure: a review. Carbohydr Polym 85:281–293

    Article  CAS  Google Scholar 

  • Bootten TJ, Harris PJ, Melton LD, Newman RH (2008) WAXS and C-13 NMR study of Gluconoacetobacter xylinus cellulose in composites with tamarind xyloglucan. Carbohydr Res 343:221–229

    Article  CAS  Google Scholar 

  • Brown RM Jr (1996) The biosynthesis of cellulose. J Macromol Sci Pure Appl Chem 33:1345–1373

    Article  Google Scholar 

  • Burton RA, Gidley MJ, Fincher GB (2010) Heterogeneity in the chemistry, structure and function of plant cell walls. Nat Chem Biol 6:724–732

    Article  CAS  Google Scholar 

  • Castro C, Zuluaga R, Putaux JL, Caro G, Mondragon I, Gañán P (2011) Structural characterization of bacterial cellulose produced by Gluconacetobacter swingsii sp. from Colombian agroindustrial wastes. Carbohydr Polym 84:96–102

    Article  CAS  Google Scholar 

  • Cerclier CV, Guyomard-Lack A, Cousin F, Jean B, Bonnin E, Cathala B, Moreau C (2013) Xyloglucan–cellulose nanocrystal multilayered films: effect of film architecture on enzymatic hydrolysis. Biomacromolecules 14:3599–3609

    Article  CAS  Google Scholar 

  • Chanliaud E, Gidley MJ (1999) In vitro synthesis and properties of pectin/Acetobacter xylinus cellulose composites. Plant J 20:25–35

    Article  CAS  Google Scholar 

  • Chen W, Lickfield GC, Yang CQ (2004) Molecular modeling of cellulose in amorphous state. Part I: model building and plastic deformation study. Polymer 45:1063–1071

    Article  CAS  Google Scholar 

  • Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861

    Article  CAS  Google Scholar 

  • Fan L, Degen M, Bendle S, Grupido N, Ilavsky J (2010) The absolute calibration of a small-angle scattering instrument with a laboratory X-ray source. J Phys Conf Ser. doi:10.1088/1742-6596/247/1/012005

  • Fernandes AN et al (2011) Nanostructure of cellulose microfibrils in spruce wood. Proc Natl Acad Sci USA 108:E1195–E1203

    Article  Google Scholar 

  • Fink HP, Hofmann D, Philipp B (1995) Some aspects of lateral chain order in cellulosics from X-ray scattering. Cellulose 2:51–70

    CAS  Google Scholar 

  • Fink HP, Purz HJ, Bohn A, Kunze J (1997) Investigation of the supramolecular structure of never dried bacterial cellulose. Macromol Symp 120:207–217

    Article  CAS  Google Scholar 

  • Geitmann A (2010) Mechanical modeling and structural analysis of the primary plant cell wall. Curr Opin Plant Biol 13:693–699

    Article  CAS  Google Scholar 

  • Gilbert EP, Schulz JC, Noakes TJ (2006) ‘Quokka’-the small-angle neutron scattering instrument at OPAL. Phys B 385–386:1180–1182

    Article  Google Scholar 

  • Gilbert EP, Lopez-Rubio A, Gidley MJ (2012) Characterisation techniques in food materials science. In: Bhesh B, Yrjo R (eds) Food materials science and engineering. Wiley-Blackwell, p 52–93

  • Gu J, Catchmark JM (2012) Impact of hemicelluloses and pectin on sphere-like bacterial cellulose assembly. Carbohydr Polym 88:547–557

    Article  CAS  Google Scholar 

  • Gu J, Catchmark JM (2013) The impact of cellulose structure on binding interactions with hemicellulose and pectin. Cellulose 20:1613–1627

    Article  CAS  Google Scholar 

  • Gu J, Catchmark JM (2014) Roles of xyloglucan and pectin on the mechanical properties of bacterial cellulose composite films. Cellulose 21:275–289

    Article  CAS  Google Scholar 

  • Haigler CH, Brown RM Jr, Benziman M (1980) Calcofluor white ST alters the in vivo assembly of cellulose microfibrils. Science 210:903–906

    Article  CAS  Google Scholar 

  • Haigler CH, White AR, Brown RM Jr, Cooper KM (1982) Alteration of in vivo cellulose ribbon assembly by carboxymethylcellulose and other cellulose derivatives. J Cell Biol 94:64–69

    Article  CAS  Google Scholar 

  • He J et al (2014) Controlled incorporation of deuterium into bacterial cellulose. Cellulose 21:927–936

    Article  CAS  Google Scholar 

  • Heiner AP, Teleman O (1997) Interface between monoclinic crystalline cellulose and water: breakdown of the odd/even duplicity. Langmuir 13:511–518

    Article  CAS  Google Scholar 

  • Hirai A, Tsuji M, Yamamoto H, Horii F (1998) In situ crystallization of bacterial cellulose—III. Influences of different polymeric additives on the formation of microfibrils as revealed by transmission electron microscopy. Cellulose 5:201–213

    Article  CAS  Google Scholar 

  • Iguchi M, Yamanaka S, Budhiono A (2000) Bacterial cellulose—a masterpiece of nature’s arts. J Mater Sci 35:261–270

    Article  CAS  Google Scholar 

  • Ilavsky J, Jemian PR (2009) Irena: tool suite for modeling and analysis of small-angle scattering. J Appl Crystallogr 42:347–353

    Article  CAS  Google Scholar 

  • Jungnikl K, Paris O, Fratzl P, Burgert I (2008) The implication of chemical extraction treatments on the cell wall nanostructure of softwood. Cellulose 15:407–418

    Article  CAS  Google Scholar 

  • Kennedy CJ, Cameron GJ, Sturcova A, Apperley DC, Altaner C, Wess TJ, Jarvis MC (2007) Microfibril diameter in celery collenchyma cellulose: X-ray scattering and NMR evidence. Cellulose 14:235–246

    Article  CAS  Google Scholar 

  • Kent MS et al (2010) Study of enzymatic digestion of cellulose by small angle neutron scattering. Biomacromolecules 11:357–368

    Article  CAS  Google Scholar 

  • Khandelwal M, Windle AH (2014) Small angle X-ray study of cellulose macromolecules produced by tunicates and bacteria. Int J Biol Macromol 68:215–217

    Article  CAS  Google Scholar 

  • Kline SR (2006) Reduction and analysis of SANS and USANS data using IGOR Pro. J Appl Crystallogr 39:895–900

    Article  CAS  Google Scholar 

  • Koizumi S, Yue Z, Tomita Y, Kondo T, Iwase H, Yamaguchi D, Hashimoto T (2008) Bacterium organizes hierarchical amorphous structure in microbial cellulose. Eur Phys J E 26:137–142

    Article  CAS  Google Scholar 

  • Koizumi S, Tomita Y, Kondo T, Hashimoto T (2009) What factors determine hierarchical structure of microbial cellulose—interplay among physics, chemistry and biology. Macromol Symp 279:110–118

    Article  CAS  Google Scholar 

  • Langan P et al (2014) Common processes drive the thermochemical pretreatment of lignocellulosic biomass. Green Chem 16:63–68

    Article  CAS  Google Scholar 

  • Lopez-Rubio A, Gilbert EP (2009) Neutron scattering: a natural tool for food science and technology research. Trends Food Sci Technol 20:576–586

    Article  CAS  Google Scholar 

  • Martínez-Sanz M, Lopez-Rubio A, Lagaron J (2011) Optimization of the nanofabrication by acid hydrolysis of bacterial cellulose nanowhiskers. Carbohydr Polym 85:228–236

    Article  Google Scholar 

  • Matthews JF et al (2006) Computer simulation studies of microcrystalline cellulose Iβ. Carbohydr Res 341:138–152

    Article  CAS  Google Scholar 

  • McKenna BA, Mikkelsen D, Wehr JB, Gidley MJ, Menzies NW (2009) Mechanical and structural properties of native and alkali-treated bacterial cellulose produced by Gluconacetobacter xylinus strain ATCC 53524. Cellulose 16:1047–1055

    Article  CAS  Google Scholar 

  • Mikkelsen D, Gidley MJ (2011) Formation of cellulose-based composites with hemicelluloses and pectins using Gluconacetobacter fermentation (Clifton, NJ). Methods Mol Biol 715:197–208

    Article  CAS  Google Scholar 

  • Mikkelsen D, Gidley MJ, Williams BA (2011) In vitro fermentation of bacterial cellulose composites as model dietary fibers. J Agric Food Chem 59:4025–4032

    Article  CAS  Google Scholar 

  • Mikkelsen D, Flanagan BM, Wilson SM, Bacic A, Gidley MJ (2015) Bacterial cellulose composites suggest arabinoxylans and (1 → 3)(1 → 4)-β-d-glucans are not functional equivalents of either xyloglucans or pectins in plant cell walls. Biomacromolecules (in press)

  • Olsson RT, Kraemer R, Lopez-Rubio A, Torres-Giner S, Ocio MJ, Lagaron JM (2010) Extraction of microfibrils from bacterial cellulose networks for electrospinning of anisotropic biohybrid fiber yarns. Macromolecules 43:4201–4209

    Article  CAS  Google Scholar 

  • Park YB, Cosgrove DJ (2012) A revised architecture of primary cell walls based on biomechanical changes induced by substrate-specific endoglucanases. Plant Physiol 158:1933–1943

    Article  CAS  Google Scholar 

  • Park YB, Lee CM, Kafle K, Park S, Cosgrove DJ, Kim SH (2014) Effects of plant cell wall matrix polysaccharides on bacterial cellulose structure studied with vibrational sum frequency generation spectroscopy and X-ray diffraction. Biomacromolecules 15:2718–2724

    Article  CAS  Google Scholar 

  • Pauly M, Albersheim P, Darvill A, York WS (1999) Molecular domains of the cellulose/xyloglucan network in the cell walls of higher plants. Plant J 20:629–639

    Article  CAS  Google Scholar 

  • Penttilä PA et al (2010) Changes in submicrometer structure of enzymatically hydrolyzed microcrystalline cellulose. Biomacromolecules 11:1111–1117

    Article  Google Scholar 

  • Penttilä PA et al (2013) Small-angle scattering study of structural changes in the microfibril network of nanocellulose during enzymatic hydrolysis. Cellulose 20:1031–1040

    Article  Google Scholar 

  • Pingali SV et al (2010) Breakdown of cell wall nanostructure in dilute acid pretreated biomass. Biomacromolecules 11:2329–2335

    Article  CAS  Google Scholar 

  • Reiterer A, Lichtenegger H, Tschegg S, Fratzl P (1999) Experimental evidence for a mechanical function of the cellulose microfibril angle in wood cell walls. Philos Mag A 79:2173–2184

    Article  CAS  Google Scholar 

  • Scheller HV, Ulvskov P (2010) Hemicelluloses. Annu Rev Plant Biol 61:263–289

    Article  CAS  Google Scholar 

  • Svergun DI, Richard S, Koch MHJ, Sayers Z, Kuprin S, Zaccai G (1998) Protein hydration in solution: experimental observation by X-ray and neutron scattering. Proc Natl Acad Sci 95:2267–2272

    Article  CAS  Google Scholar 

  • Thomas LH et al (2013) Structure of cellulose microfibrils in primary cell walls from collenchyma. Plant Physiol 161:465–476

    Article  CAS  Google Scholar 

  • Tischer PCSF, Sierakowski MR, Westfahl H, Tischer CA (2010) Nanostructural reorganization of bacterial cellulose by ultrasonic treatment. Biomacromolecules 11:1217–1224

    Article  CAS  Google Scholar 

  • Tokoh C, Takabe K, Fujita M, Saiki H (1998) Cellulose synthesized by Acetobacter xylinum in the presence of acetyl glucomannan. Cellulose 5:249–261

    Article  CAS  Google Scholar 

  • Tokoh C, Takabe K, Sugiyama J, Fujita M (2002a) CP/MAS 13C NMR and electron diffraction study of bacterial cellulose structure affected by cell wall polysaccharides. Cellulose 9:351–360

    Article  CAS  Google Scholar 

  • Tokoh C, Takabe KJ, Fujita M (2002b) Cellulose synthesized by Acetobacter xylinum in the presence of plant cell wall polysaccharides. Cellulose 9:65–74

    Article  CAS  Google Scholar 

  • Uhlin KI, Atalla RH, Thompson NS (1995) Influence of hemicelluloses on the aggregation patterns of bacterial cellulose. Cellulose 2:129–144

    Article  CAS  Google Scholar 

  • Wada M, Sugiyama J, Okano T (1993) Native celluloses on the basis of two crystalline phase (I-alpha/I-beta) system. J Appl Polym Sci 49:1491–1496

    Article  CAS  Google Scholar 

  • Wang N, Ding E, Cheng R (2007) Thermal degradation behaviors of spherical cellulose nanocrystals with sulfate groups. Polymer 48:3486–3493

    Article  CAS  Google Scholar 

  • Weimer PJ, Hackney JM, Jung H-JG, Hatfield RD (2000) Fermentation of a bacterial cellulose/xylan composite by mixed ruminal microflora: implications for the role of polysaccharide matrix interactions in plant cell wall biodegradability. J Agric Food Chem 48:1727–1733

    Article  CAS  Google Scholar 

  • White AR, Brown RM Jr (1981) Enzymatic hydrolysis of cellulose: visual characterization of the process. Proc Natl Acad Sci USA 78:1047–1051

    Article  CAS  Google Scholar 

  • Whitney SE, Brigham JE, Darke AH, Reid JS, Gidley MJ (1995) In vitro assembly of cellulose/xyloglucan networks: ultrastructural and molecular aspects. Plant J 8:491–504

    Article  CAS  Google Scholar 

  • Whitney SEC, Brigham JE, Darke AH, Reid JSG, Gidley MJ (1998) Structural aspects of the interaction of mannan-based polysaccharides with bacterial cellulose. Carbohydr Res 307:299–309

    Article  CAS  Google Scholar 

  • Whitney SEC, Wilson E, Webster J, Bacic A, Reid JSG, Gidley MJ (2006) Effects of structural variation in xyloglucan polymers on interactions with bacterial cellulose. Am J Bot 93:1402–1414

    Article  CAS  Google Scholar 

  • Yamamoto H, Horii F, Hirai A (1996) In situ crystallization of bacterial cellulose. 2. Influences of different polymeric additives on the formation of celluloses I-alpha and I-beta at the early stage of incubation. Cellulose 3:229–242

    Article  CAS  Google Scholar 

  • Zhang K (2013) Illustration of the development of bacterial cellulose bundles/ribbons by Gluconacetobacter xylinus via atomic force microscopy. Appl Microbiol Biotechnol 97:4353–4359

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Dr. Joel Davis (ANSTO, Institute of Materials Engineering) for performing the SEM imaging and Dr. Tracey Hanley (ANSTO, Institute of Materials Engineering) for her valuable assistance with the XRD experiments. Dongjie Wang is acknowledged for composites production and SEM of fresh samples. M.M.S. would like to acknowledge a postdoctoral fellowship jointly funded by ANSTO and the ARC Centre of Excellence in Plant Cell Walls.

Author information

Authors and Affiliations

  1. Bragg Institute, Australian Nuclear Science and Technology Organisation, Locked Bag 2001, Kirrawee DC, NSW, 2232, Australia

    Marta Martínez-Sanz & Elliot P. Gilbert

  2. ARC Centre of Excellence in Plant Cell Walls, Centre for Nutrition and Food Sciences, University of Queensland, St. Lucia, Brisbane, QLD, 4072, Australia

    Marta Martínez-Sanz, Patricia Lopez-Sanchez & Michael J. Gidley

Authors
  1. Marta Martínez-Sanz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Patricia Lopez-Sanchez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michael J. Gidley
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Elliot P. Gilbert
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Elliot P. Gilbert.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 197 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Martínez-Sanz, M., Lopez-Sanchez, P., Gidley, M.J. et al. Evidence for differential interaction mechanism of plant cell wall matrix polysaccharides in hierarchically-structured bacterial cellulose. Cellulose 22, 1541–1563 (2015). https://doi.org/10.1007/s10570-015-0614-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10570-015-0614-2

Keywords

Search

Navigation