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Characterisation of bacterial cellulose from diverse Komagataeibacter strains and their application to construct plant cell wall analogues

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Abstract

This study investigated cellulose production and microstructure variation from six Komagataeibacter strains (ATCC 53524, ATCC 10245, ATCC 23769, ATCC 700178, NBRC 13693 and KTH 5655). Strain KTH 5655 produced the highest cellulose yields (10.39 g/l) after 9 days cultivation. Nuclear magnetic resonance spectroscopy and X-ray diffraction revealed that strain ATCC 23769 synthesised cellulose with the lowest crystallinity and decreased ratio of Iα/Iβ allomorph, whilst strain KTH 5655 produced a relatively ordered cellulose structure. However, the average widths of cellulose ribbons were similar (30–50 nm) for all types of cellulose. Phylogenetic analysis of the 16S rRNA gene indicated that these strains shared a high level of genetic similarity (ranging from 88 to 98%). All strains were used to produce cellulose in the presence of arabinoxylan or xyloglucan as simplified cell wall analogues. Our results provide guidance for the selection of cellulose-producing strains for specific biotechnological and research applications.

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References

  • Atalla RH, Vanderhart DL (1984) Native cellulose: a composite of two distinct crystalline forms. Science 223:283–285

    Article  CAS  Google Scholar 

  • Bailey IW (1938) Cell wall structure of higher plants. Ind Eng Chem Res 30:40–47

    Article  CAS  Google Scholar 

  • Blackwell J, Kolpak FJ (1975) The cellulose microfibril as an imperfect array of elementary fibrils. Macromolecules 8:322–326

    Article  CAS  Google Scholar 

  • Brown RM (1982) Cellulose and other natural polymer systems: biogenesis, structure and degradation. Plenum Press, New York

    Book  Google Scholar 

  • Castro C, Zuluaga R, Alvarez C, Putaux JL, Caro G, Rojas OJ, Mondragon I, Ganan P (2012) Bacterial cellulose produced by a new acid-resistant strain of Gluconacetobacter genus. Carbohydr Polym 89:1033–1037

    Article  CAS  Google Scholar 

  • Chanliaud E, Burrows K, Jeronimidis G, Gidley MJ (2002) Mechanical properties of primary plant cell wall analogues. Planta 215:989–996

    Article  CAS  Google Scholar 

  • Chanliaud E, De Silva J, Strongitharm B, Jeronimidis G, Gidley MJ (2004) Mechanical effects of plant cell wall enzymes on cellulose/xyloglucan composites. Plant J 38:27–37

    Article  CAS  Google Scholar 

  • Deng Y, Nagachar N, Fang L, Luan X, Catchmark JM, Tien M, Kao TH (2015) Isolation and characterization of two cellulose morphology mutants of Gluconacetobacter hansenii ATCC23769 producing cellulose with lower crystallinity. PLoS ONE 10:e0119504

    Article  Google Scholar 

  • Fang L, Catchmark JM (2014) Characterization of water-soluble exopolysaccharides from Gluconacetobacter xylinus and their impacts on bacterial cellulose crystallization and ribbon assembly. Cellulose 21:3965–3978

    Article  CAS  Google Scholar 

  • Fang L, Catchmark JM (2015) Characterization of cellulose and other exopolysaccharides produced from Gluconacetobacter strains. Carbohydr Polym 115:663–669

    Article  CAS  Google Scholar 

  • Fu L, Zhou P, Zhang S, Yang G (2013) Evaluation of bacterial nanocellulose-based uniform wound dressing for large area skin transplantation. Mater Sci Eng C Mater Biol Appl 33:2995–3000

    Article  CAS  Google Scholar 

  • Guhados G, Wan W, Hutter JL (2005) Measurement of the elastic modulus of single bacterial cellulose fibers using atomic force microscopy. Langmuir 21:6642–6646

    Article  CAS  Google Scholar 

  • Horii F, Hirai A, Kitamaru R (1987) CP/MAS carbon-13 NMR spectra of the crystalline components of native celluloses. Macromolecules 20:2117–2120

    Article  CAS  Google Scholar 

  • Hu Y, Zhu Y, Zhou X, Ruan C, Pan H, Catchmark JM (2016) Bioabsorbable cellulose composites prepared by an improved mineral-binding process for bone defect repair. J Mater Chem B 4:1235–1246

    Article  CAS  Google Scholar 

  • Huang HC, Chen LC, Lin SB, Hsu CP, Chen HH (2010) In situ modification of bacterial cellulose network structure by adding interfering substances during fermentation. Bioresour Technol 101:6084–6091

    Article  CAS  Google Scholar 

  • Ishida T, Sugano Y, Nakai T, Shoda M (2002) Effects of acetan on production of bacterial cellulose by Acetobacter xylinum. Biosci Biotechnol Biochem 66:1677–1681

    Article  CAS  Google Scholar 

  • Ishihara M, Matsunaga M, Hayashi N, TiÅ¡ler V (2002) Utilization of d-xylose as carbon source for production of bacterial cellulose. Enzyme Microb Technol 31:986–991

    Article  CAS  Google Scholar 

  • Ishikawa A, Matsuoka M, Tsuchida T, Yoshinaga F (2014) Increase in cellulose production by sulfaguanidine-resistant mutants serived from Acetobacter xylinum subsp.sucrofermentans. Biosci Biotechnol Biochem 59:2259–2262

    Article  Google Scholar 

  • Kanchanarach W, Theeragool G, Yakushi T, Toyama H, Adachi O, Matsushita K (2010) Characterization of thermotolerant Acetobacter pasteurianus strains and their quinoprotein alcohol dehydrogenases. Appl Microbiol Biotechnol 85:741–751

    Article  CAS  Google Scholar 

  • Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649

    Article  Google Scholar 

  • Kennedy JF, Phillips GO, Williams PA (1989) Cellulose: structural and functional aspects. Ellis Horwood, Chichester

    Google Scholar 

  • Kersters K, Lisdiyanti P, Komagata K, Swings J (2006) The family Acetobacteraceae: the genera Acetobacter, Acidomonas, Asaia, Gluconacetobacter, Gluconobacter, and Kozakia. Springer Science & Business Media, Berlin

    Google Scholar 

  • Klemm D, Heublein B, Fink HP, Bohn A (2005) Cellulose: fascinating biopolymer and sustainable raw material. Angew Chem Int Ed 44:3358–3393

    Article  CAS  Google Scholar 

  • Klemm D, Schumann D, Kramer F, Heßler N, Koth D, Sultanova B (2009) Nanocellulose materials—different cellulose, different functionality. Macromol Symp 280:60–71

    Article  CAS  Google Scholar 

  • Kurosumi A, Sasaki C, Yamashita Y, Nakamura Y (2009) Utilization of various fruit juices as carbon source for production of bacterial cellulose by Acetobacter xylinum NBRC 13693. Carbohydr Polym 76:333–335

    Article  CAS  Google Scholar 

  • Liang C, Marchessault R (1959) Infrared spectra of crystalline polysaccharides. I. Hydrogen bonds in native celluloses. J Polym Sci 37:385–395

    Article  CAS  Google Scholar 

  • Lin D, Lopez-Sanchez P, Li R, Li Z (2014) Production of bacterial cellulose by Gluconacetobacter hansenii CGMCC 3917 using only waste beer yeast as nutrient source. Bioresour Technol 151:113–119

    Article  CAS  Google Scholar 

  • Lisdiyanti P, Navarro RR, Uchimura T, Komagata K (2006) Reclassification of Gluconacetobacter hansenii strains and proposals of Gluconacetobacter saccharivorans sp. nov. and Gluconacetobacter nataicola sp. nov. Int J Syst Evol Microbiol 56:2101–2111

    Article  CAS  Google Scholar 

  • Lopez-Sanchez P, Rincon M, Wang D, Brulhart S, Stokes JR, Gidley MJ (2014) Micromechanics and poroelasticity of hydrated cellulose networks. Biomacromolecules 15:2274–2284

    Article  CAS  Google Scholar 

  • Lopez-Sanchez P, Cersosimo J, Wang D, Flanagan B, Stokes JR, Gidley MJ (2015) Poroelastic mechanical effects of hemicelluloses on cellulosic hydrogels under compression. PLoS ONE 10:e0122132

    Article  Google Scholar 

  • Maneerung T, Tokura S, Rujiravanit R (2008) Impregnation of silver nanoparticles into bacterial cellulose for antimicrobial wound dressing. Carbohydr Polym 72:43–51

    Article  CAS  Google Scholar 

  • Martinez-Sanz M, Lopez-Rubio A, Lagaron JM (2012) Optimization of the dispersion of unmodified bacterial cellulose nanowhiskers into polylactide via melt compounding to significantly enhance barrier and mechanical properties. Biomacromolecules 13:3887–3899

    Article  CAS  Google Scholar 

  • Martinez-Sanz M, Gidley MJ, Gilbert EP (2016) Hierarchical architecture of bacterial cellulose and composite plant cell wall polysaccharide hydrogels using small angle neutron scattering. Soft Matter 12:1534–1549

    Article  CAS  Google Scholar 

  • Martínez-Sanz M, Lopez-Sanchez P, Gidley MJ, Gilbert EP (2015) Evidence for differential interaction mechanism of plant cell wall matrix polysaccharides in hierarchically-structured bacterial cellulose. Cellulose 22:1541–1563

    Article  Google Scholar 

  • Martínez-Sanz M, Mikkelsen D, Flanagan B, Gidley MJ, Gilbert EP (2016) Multi-scale model for the hierarchical architecture of native cellulose hydrogels. Carbohydr Polym 147:542–555

    Article  Google Scholar 

  • Masaoka S, Ohe T, Sakota N (1993) Production of cellulose from glucose by Acetobacter xylinum. J Biosci Bioeng 75:18–22

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Mikkelsen D, Flanagan BM, Dykes GA, Gidley MJ (2009) Influence of different carbon sources on bacterial cellulose production by Gluconacetobacter xylinus strain ATCC 53524. J Appl Microbiol 107:576–583

    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) Interactions of arabinoxylan and (1,3)(1,4)-beta-glucan with cellulose networks. Biomacromolecules 16:1232–1239

    Article  CAS  Google Scholar 

  • Naritomi T, Kouda T, Yano H, Yoshinaga F (1998) Effect of ethanol on bacterial cellulose production from fructose in continuous culture. J Biosci Bioeng 85:598–603

    CAS  Google Scholar 

  • Oehme DP, Doblin MS, Wagner J, Bacic A, Downton MT, Gidley MJ (2015) Gaining insight into cell wall cellulose macrofibril organisation by simulating microfibril adsorption. Cellulose 22:3501–3520

    Article  CAS  Google Scholar 

  • Ojinnaka C, Jay AJ, Colquhoun IJ, Brownsey GJ, Morris ER, Morris VJ (1996) Structure and conformation of acetan polysaccharide. Int J Biol Macromol 19:149–156

    Article  CAS  Google Scholar 

  • Park S, Johnson DK, Ishizawa CI, Parilla PA, Davis MF (2009) Measuring the crystallinity index of cellulose by solid state 13C nuclear magnetic resonance. Cellulose 16:641–647

    Article  CAS  Google Scholar 

  • Pettolino FA, Walsh C, Fincher GB, Bacic A (2012) Determining the polysaccharide composition of plant cell walls. Nat Protoc 7:1590–1607

    Article  CAS  Google Scholar 

  • Ruka DR, Simon GP, Dean KM (2012) Altering the growth conditions of Gluconacetobacter xylinus to maximize the yield of bacterial cellulose. Carbohydr Polym 89:613–622

    Article  CAS  Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Meth 9:671–675

    Article  CAS  Google Scholar 

  • Schramm M, Hestrin S (1954) Factors affecting production of cellulose at the air/liquid interface of a culture of Acetobacter xylinum. Microbiology 11:123–129

    CAS  Google Scholar 

  • Sherif M (2005) Evaluation of different carbon sources for bacterial cellulose production. Afr J Biotechnol 4:478

    Google Scholar 

  • Shoda M, Sugano Y (2005) Recent advances in bacterial cellulose production. Biotechnol Bioprocess Eng 10:1–8

    Article  CAS  Google Scholar 

  • Son H-J, Heo M-S, Kim Y-G, Lee S-J (2001) Optimization of fermentation conditions for the production of bacterial cellulose by a newly isolated Acetobacter. Biotechnol Appl Biochem 33:1–5

    Article  CAS  Google Scholar 

  • Son H-J, Kim H-G, Kim K-K, Kim H-S, Kim Y-G, Lee S-J (2003) Increased production of bacterial cellulose by Acetobacter sp. V6 in synthetic media under shaking culture conditions. Bioresour Technol 86:215–219

    Article  Google Scholar 

  • Tokoh C, Takabe K, Fujita M (2002) 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, Okano T (2001) Localization of I α and I β phases in algal cellulose revealed by acid treatments. Cellulose 8:183–188

    Article  CAS  Google Scholar 

  • Watanabe K, Tabuchi M, Ishikawa A, Takemura H, Tsuchida T, Morinaga Y, Yoshinaga F (1998) Acetobacter xylinum mutant with high cellulose productivity and an ordered structure. Biosci Biotechnol Biochem 62:1290–1292

    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 

  • Yamamoto H, Horn F (1994) In Situ crystallization of bacterial cellulose I. Influences of polymeric additives, stirring and temperature on the formation celluloses I α and I β as revealed by cross polarization/magic angle spinning (CP/MAS) 13C NMR spectroscopy. Cellulose 1:57–66

    Article  CAS  Google Scholar 

  • Yang XY, Huang C, Guo HJ, Xiong L, Luo J, Wang B, Lin XQ, Chen XF, Chen XD (2016) Bacterial cellulose production from the litchi extract by Gluconacetobacter xylinus. Prep Biochem Biotechnol 46:39–43

    Article  CAS  Google Scholar 

  • Yu Z, Forster R (2005) Nucleic acid extraction, oligonucleotide probes and PCR methods. In: Makkar H, McSweeney C (eds) Methods in Gut Microbial Ecology for Ruminants. Springer, Netherlands, Dordrecht, pp 81–104

    Chapter  Google Scholar 

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Acknowledgments

The authors would like to thank Prof. Vincent Bulone for providing strain KTH 5655. This work was supported by the Australian Research Council Centre of Excellence in Plant Cell Walls (CE110010007) and a studentship to SC from the China Scholarship Council and The University of Queensland.

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  1. Dongjie Wang

    Present address: College of Food Science and Biotechnology, Tianjin University of Science and Technology, Tianjin Binhai New Area Thirteenth Avenue, No. 29, Tianjin, 300457, China

Authors and Affiliations

  1. ARC Centre of Excellence in Plant Cell Walls, Centre for Nutrition and Food Sciences, Queensland Alliance for Agriculture and Food Innovation, The University of Queensland, St. Lucia, Brisbane, QLD, 4072, Australia

    Si-Qian Chen, Deirdre Mikkelsen, Patricia Lopez-Sanchez, Dongjie Wang, Marta Martinez-Sanz, Bernadine M. Flanagan & Michael J. Gidley

  2. Australian Centre for Neutron Scattering, Australian Nuclear Science and Technology Organization (ANSTO), Locked Bag 2001, Kirrawee DC, NSW, 2232, Australia

    Marta Martinez-Sanz & Elliot P. Gilbert

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  1. Si-Qian Chen
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Correspondence to Michael J. Gidley.

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Chen, SQ., Mikkelsen, D., Lopez-Sanchez, P. et al. Characterisation of bacterial cellulose from diverse Komagataeibacter strains and their application to construct plant cell wall analogues. Cellulose 24, 1211–1226 (2017). https://doi.org/10.1007/s10570-017-1203-3

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