Investigation of the micro- and nano-scale architecture of cellulose hydrogels with plant cell wall polysaccharides: A combined USANS/SANS study

Abstract The structure of protiated, deuterated and composite cellulose hydrogels with plant cell wall (PCW) polysaccharides has been investigated by combined USANS/SANS experiments, complemented with spectroscopy and microscopy. The broad size range covered by the USANS/SANS experiments enabled the identification of cellulose architectural features in the cross-sectional and longitudinal directions. In the cross-sectional direction, cellulose ribbons are modelled as core-shell structures. Xyloglucan and mixed linkage glucans interfere with the cellulose crystallisation process, reducing the crystallinity and establishing cross-bridges between ribbons. However, only xyloglucan is able to establish strong interactions with the cellulose microfibrils, affecting the properties of the ribbons’ core. Longitudinally, the ribbons are hypothesised to present a ca. 1.4–1.5 μm periodic twist with a crystallite length of ca. 140–180 nm for the individual microfibrils. These results highlight the potential of USANS/SANS techniques to investigate the multi-scale architecture of cellulose hydrogels as well as the interaction mechanism between cellulose and PCW polysaccharides.

[1]  G. Beaucage.  Small-Angle Scattering from Polymeric Mass Fractals of Arbitrary Mass-Fractal Dimension , 1996 .

[2]  A. Bacic,et al.  Effects of structural variation in xyloglucan polymers on interactions with bacterial cellulose. , 2006, American journal of botany.

[3]  M. Gidley,et al.  Interactions of pectins with cellulose during its synthesis in the absence of calcium , 2016 .

[4]  M. Khandelwal,et al.  Origin of chiral interactions in cellulose supra-molecular microfibrils. , 2014, Carbohydrate polymers.

[5]  M. Gidley,et al.  Poroelastic Mechanical Effects of Hemicelluloses on Cellulosic Hydrogels under Compression , 2015, PloS one.

[6]  Sadayoshi Watanabe,et al.  Biosynthesis of Cellulose by Acetobacter Xylinum. II. Morphological Observations on the Formation of Cellulose Microfibrils by Acetobacter Xylinum , 1975 .

[7]  D. Wang,et al.  Micromechanics and poroelasticity of hydrated cellulose networks. , 2014, Biomacromolecules.

[8]  R. Brown,et al.  Rotation of Cellulose Ribbons During Degradation with Fungal Cellulase , 2001 .

[9]  Wei Chen,et al.  Molecular modeling of cellulose in amorphous state. Part I: model building and plastic deformation study , 2004 .

[10]  M. Gidley,et al.  Diffusion of macromolecules in self-assembled cellulose/hemicellulose hydrogels. , 2015, Soft matter.

[11]  E. J. Foster,et al.  Comparison of the properties of cellulose nanocrystals and cellulose nanofibrils isolated from bacteria, tunicate, and wood processed using acid, enzymatic, mechanical, and oxidative methods. , 2014, ACS applied materials & interfaces.

[12]  Yue Zhang,et al.  Utilization of bacterial cellulose in food , 2014 .

[13]  Yong Bum Park,et al.  Effects of plant cell wall matrix polysaccharides on bacterial cellulose structure studied with vibrational sum frequency generation spectroscopy and X-ray diffraction. , 2014, Biomacromolecules.

[14]  A. Bacic,et al.  Interactions of arabinoxylan and (1,3)(1,4)-β-glucan with cellulose networks. , 2015, Biomacromolecules.

[15]  Michael D. Abràmoff,et al.  Image processing with ImageJ , 2004 .

[16]  M. Tsuji,et al.  Helical sense of ribbon assemblies and splayed microfibrils of bacterial cellulose , 1998 .

[17]  Paul Gatenholm,et al.  Role of (1,3)(1,4)-β-glucan in cell walls: interaction with cellulose. , 2014, Biomacromolecules.

[18]  Zhihong Wu,et al.  Investigation on artificial blood vessels prepared from bacterial cellulose. , 2015, Materials science & engineering. C, Materials for biological applications.

[19]  M. Gidley,et al.  Mechanical and structural properties of native and alkali-treated bacterial cellulose produced by Gluconacetobacter xylinus strain ATCC 53524 , 2009 .

[20]  Masaya Nogi,et al.  Transparent Nanocomposites Based on Cellulose Produced by Bacteria Offer Potential Innovation in the Electronics Device Industry , 2008 .

[21]  J. Catchmark,et al.  The impact of cellulose structure on binding interactions with hemicellulose and pectin , 2013, Cellulose.

[22]  B. Davison,et al.  Controlled incorporation of deuterium into bacterial cellulose , 2013, Cellulose.

[23]  M. Gidley,et al.  In vitro fermentation of bacterial cellulose composites as model dietary fibers. , 2011, Journal of agricultural and food chemistry.

[24]  Ralph Müller,et al.  Mechanical evaluation of bacterial nanocellulose as an implant material for ear cartilage replacement. , 2013, Journal of the mechanical behavior of biomedical materials.

[25]  Terry Noakes,et al.  ‘Quokka’—the small-angle neutron scattering instrument at OPAL , 2006 .

[26]  Elliot P. Gilbert,et al.  Evidence for differential interaction mechanism of plant cell wall matrix polysaccharides in hierarchically-structured bacterial cellulose , 2015, Cellulose.

[27]  Sergio Torres-Giner,et al.  Extraction of Microfibrils from Bacterial Cellulose Networks for Electrospinning of Anisotropic Biohybrid Fiber Yarns , 2010 .

[28]  M. Fujita,et al.  Cellulose synthesized by Acetobacter xylinum in the presence of plant cell wall polysaccharides , 2002 .

[29]  Marta Martínez-Sanz,et al.  Optimization of the dispersion of unmodified bacterial cellulose nanowhiskers into polylactide via melt compounding to significantly enhance barrier and mechanical properties. , 2012, Biomacromolecules.

[30]  Rajai H. Atalla,et al.  Influence of hemicelluloses on the aggregation patterns of bacterial cellulose , 1995 .

[31]  Gidley,et al.  In vitro synthesis and properties of pectin/Acetobacter xylinus cellulose composites , 1999, The Plant Journal.

[32]  Michael J Gidley,et al.  Formation of cellulose-based composites with hemicelluloses and pectins using Gluconacetobacter fermentation. , 2011, Methods in molecular biology.

[33]  Hiroyuki Yamamoto,et al.  In Situ Crystallization of Bacterial Cellulose III. Influences of Different Polymeric Additives on the Formation of Microfibrils as Revealed by Transmission Electron Microscopy , 1998 .

[34]  Steven R. Kline,et al.  Reduction and analysis of SANS and USANS data using IGOR Pro , 2006 .

[35]  S. Kuga,et al.  Effect of Trace Electrolyte on Liquid Crystal Type of Cellulose Microcrystals , 2001 .

[36]  Kai Zhang.  Illustration of the development of bacterial cellulose bundles/ribbons by Gluconacetobacter xylinus via atomic force microscopy , 2013, Applied Microbiology and Biotechnology.

[37]  Gregory Beaucage,et al.  Approximations Leading to a Unified Exponential/Power-Law Approach to Small-Angle Scattering , 1995 .

[38]  M. Himmel,et al.  Computer simulation studies of microcrystalline cellulose Iβ , 2006 .

[39]  M. Wolcott,et al.  Thermal and mechanical properties of poly(3-hydroxybutyrate-co-3-hydroxyvalerate)/cellulose nanowhiskers composites , 2010 .

[40]  A. Ragauskas,et al.  The effect of deuteration on the structure of bacterial cellulose. , 2013, Carbohydrate research.

[41]  Hugh O'Neill,et al.  Breakdown of cell wall nanostructure in dilute acid pretreated biomass. , 2010, Biomacromolecules.

[42]  Marcus B. Foston.  Advances in solid-state NMR of cellulose. , 2014, Current opinion in biotechnology.

[43]  M. Ioelovich,et al.  Study of cellulose paracrystallinity , 2010, BioResources.

[44]  A. Darke,et al.  In vitro assembly of cellulose/xyloglucan networks: ultrastructural and molecular aspects , 1995 .

[45]  Marta Martínez-Sanz,et al.  Multi-scale model for the hierarchical architecture of native cellulose hydrogels. , 2016, Carbohydrate polymers.

[46]  T. Kondo,et al.  Bacterium organizes hierarchical amorphous structure in microbial cellulose , 2008, The European physical journal. E, Soft matter.

[47]  J. Lagarón,et al.  Optimization of the nanofabrication by acid hydrolysis of bacterial cellulose nanowhiskers , 2011 .

[48]  Andreas K. Freund,et al.  Kookaburra: the ultra‐small‐angle neutron scattering instrument at OPAL , 2013 .

[49]  T. Darwish,et al.  Biopolymer deuteration for neutron scattering and other isotope-sensitive techniques. , 2015, Methods in enzymology.

[50]  M. Tsuji,et al.  Phase separation behavior in aqueous suspensions of bacterial cellulose nanocrystals prepared by sulfuric acid treatment. , 2009, Langmuir : the ACS journal of surfaces and colloids.

[51]  Masatoshi Iguchi,et al.  Bacterial cellulose—a masterpiece of nature's arts , 2000 .

[52]  Minoru Fujita,et al.  Cellulose Synthesized by Acetobacter Xylinum in the Presence of Acetyl Glucomannan , 1998 .

[53]  Marta Martínez-Sanz,et al.  Hierarchical architecture of bacterial cellulose and composite plant cell wall polysaccharide hydrogels using small angle neutron scattering. , 2016, Soft matter.

[54]  Marta Martínez-Sanz,et al.  Application of X-ray and neutron small angle scattering techniques to study the hierarchical structure of plant cell walls: a review. , 2015, Carbohydrate polymers.

[55]  Paul Gatenholm,et al.  In vivo biocompatibility of bacterial cellulose. , 2006, Journal of biomedical materials research. Part A.

[56]  M. Schramm,et al.  Synthesis of cellulose by Acetobacter xylinum. II. Preparation of freeze-dried cells capable of polymerizing glucose to cellulose. , 1954, The Biochemical journal.

[57]  K. Nishitani,et al.  Genomic basis for cell-wall diversity in plants. A comparative approach to gene families in rice and Arabidopsis. , 2004, Plant & cell physiology.

[58]  A. Darke,et al.  Structural aspects of the interaction of mannan-based polysaccharides with bacterial cellulose , 1998 .

[59]  Antony Bacic,et al.  Determining the polysaccharide composition of plant cell walls , 2012, Nature Protocols.

[60]  Yong Bum Park,et al.  Changes in Cell Wall Biomechanical Properties in the Xyloglucan-Deficient xxt1/xxt2 Mutant of Arabidopsis1[W][OA] , 2011, Plant Physiology.

[61]  E. Saino,et al.  Multifunctional bionanocomposite films of poly(lactic acid), cellulose nanocrystals and silver nanoparticles , 2012 .

[62]  O. Teleman,et al.  Interface between Monoclinic Crystalline Cellulose and Water: Breakdown of the Odd/Even Duplicity , 1997 .

[63]  R. Brown,et al.  Enzymatic hydrolysis of cellulose: Visual characterization of the process. , 1981, Proceedings of the National Academy of Sciences of the United States of America.