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

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.

[1]  C. Haigler,et al.  Calcofluor white ST Alters the in vivo assembly of cellulose microfibrils. , 1980, Science.

[2]  D. Cosgrove Growth of the plant cell wall , 2005, Nature Reviews Molecular Cell Biology.

[3]  Anja Geitmann,et al.  Mechanical modeling and structural analysis of the primary plant cell wall. , 2010, Current opinion in plant biology.

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

[5]  C. Haigler,et al.  Alteration of in vivo cellulose ribbon assembly by carboxymethylcellulose and other cellulose derivatives , 1982, The Journal of cell biology.

[6]  J. Sugiyama,et al.  Cp/mas 13c nmr and Electron Diffraction Study of Bacterial Cellulose Structure Affected by Cell Wall Polysaccharides , 2002 .

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

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

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

[10]  C PEAUD-LENOEL,et al.  [Biosynthesis of cellulose]. , 1960, Bulletin de la Societe de chimie biologique.

[11]  L. Viikari,et al.  Changes in submicrometer structure of enzymatically hydrolyzed microcrystalline cellulose. , 2010, Biomacromolecules.

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

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

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

[15]  A. Donald,et al.  Structure of Acetobacter cellulose composites in the hydrated state. , 2001, International journal of biological macromolecules.

[16]  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.

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

[18]  Peter Lindner,et al.  Small-angle scattering study of structural changes in the microfibril network of nanocellulose during enzymatic hydrolysis , 2013, Cellulose.

[19]  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.

[20]  Kyung Min Park,et al.  Macro/Nano-gel composite as an injectable and bioactive bulking material for the treatment of urinary incontinence. , 2014, Biomacromolecules.

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

[22]  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 .

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

[24]  Michael J Gidley,et al.  Heterogeneity in the chemistry, structure and function of plant cell walls. , 2010, Nature chemical biology.

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

[26]  Hiroyuki Yamamoto,et al.  In situ crystallization of bacterial cellulose II. Influences of different polymeric additives on the formation of celluloses Iα and Iβ at the early stage of incubation , 1996 .

[27]  V. T. Forsyth,et al.  Nanostructure of cellulose microfibrils in spruce wood , 2011, Proceedings of the National Academy of Sciences.

[28]  P. Weimer,et al.  Fermentation of a bacterial cellulose/xylan composite by mixed ruminal microflora: implications for the role of polysaccharide matrix interactions in plant cell wall biodegradability. , 2000, Journal of agricultural and food chemistry.

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

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

[31]  T. Baskin Anisotropic expansion of the plant cell wall. , 2005, Annual review of cell and developmental biology.

[32]  A. Reiterer,et al.  Experimental evidence for a mechanical function of the cellulose microfibril angle in wood cell walls , 1999 .

[33]  J. Sugiyama,et al.  Native celluloses on the basis of two crystalline phase (Iα/Iβ) system , 1993 .

[34]  I. Burgert,et al.  The implication of chemical extraction treatments on the cell wall nanostructure of softwood , 2008 .

[35]  H. Fink,et al.  Some aspects of lateral chain order in cellulosics from X-ray scattering , 1995, Cellulose.

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

[37]  B. Simmons,et al.  Study of enzymatic digestion of cellulose by small angle neutron scattering. , 2010, Biomacromolecules.

[38]  R. Newman,et al.  WAXS and 13C NMR study of Gluconoacetobacter xylinus cellulose in composites with tamarind xyloglucan. , 2008, Carbohydrate research.

[39]  Robin Zuluaga,et al.  Structural characterization of bacterial cellulose produced by Gluconacetobacter swingsii sp. from Colombian agroindustrial wastes , 2011 .

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

[41]  V. T. Forsyth,et al.  Structure of Cellulose Microfibrils in Primary Cell Walls from Collenchyma1[C][W][OA] , 2012, Plant Physiology.

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

[43]  M. Gidley,et al.  Characterisation Techniques in Food Materials Science , 2012 .

[44]  E. Bonnin,et al.  Xyloglucan-cellulose nanocrystal multilayered films: effect of film architecture on enzymatic hydrolysis. , 2013, Biomacromolecules.

[45]  J. Gu,et al.  Roles of xyloglucan and pectin on the mechanical properties of bacterial cellulose composite films , 2014, Cellulose.

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

[47]  A. Donald,et al.  Tensile deformation of bacterial cellulose composites. , 2003, International journal of biological macromolecules.

[48]  Enyong Ding,et al.  Thermal degradation behaviors of spherical cellulose nanocrystals with sulfate groups , 2007 .

[49]  J. Ilavsky,et al.  The Absolute Calibration of a Small-Angle Scattering Instrument with a Laboratory X-ray Source , 2010 .

[50]  Jin Gu,et al.  Impact of hemicelluloses and pectin on sphere-like bacterial cellulose assembly , 2012 .

[51]  H. Fink,et al.  Investigation of the supramolecular structure of never dried bacterial cellulose , 1997 .

[52]  E. Gilbert,et al.  Application of small-angle X-ray and neutron scattering techniques to the characterisation of starch structure: A review , 2011 .

[53]  Yong Bum Park,et al.  A Revised Architecture of Primary Cell Walls Based on Biomechanical Changes Induced by Substrate-Specific Endoglucanases1[C][W][OA] , 2012, Plant Physiology.

[54]  A Darvill,et al.  Molecular domains of the cellulose/xyloglucan network in the cell walls of higher plants. , 1999, The Plant journal : for cell and molecular biology.

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

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

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

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

[59]  M. Sierakowski,et al.  Nanostructural reorganization of bacterial cellulose by ultrasonic treatment. , 2010, Biomacromolecules.

[60]  Jeremy C. Smith,et al.  Common processes drive the thermochemical pretreatment of lignocellulosic biomass , 2014 .

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

[62]  D I Svergun,et al.  Protein hydration in solution: experimental observation by x-ray and neutron scattering. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[63]  Elliot P. Gilbert,et al.  Neutron scattering: a natural tool for food science and technology research , 2009 .

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

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

[66]  Pete R. Jemian,et al.  Irena: tool suite for modeling and analysis of small‐angle scattering , 2009 .

[67]  C. Kennedy,et al.  Microfibril diameter in celery collenchyma cellulose: X-ray scattering and NMR evidence , 2007 .

[68]  Mudrika Khandelwal,et al.  Small angle X-ray study of cellulose macromolecules produced by tunicates and bacteria. , 2014, International journal of biological macromolecules.