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Does cellulose II exist in native alga cell walls? Cellulose structure of Derbesia cell walls studied with SFG, IR and XRD

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Abstract

In nature, algae produce cellulose I where all glucan chains are aligned parallel. However, the presence of cellulose II with anti-parallel glucan chains has been reported for certain Derbesia (Chlorophyceae algae) cell walls; if this is true, it would mean a new biological process for synthesizing cellulose that has not yet been recognized. To answer this question, we examined cellulose structure in Derbesia cell walls, intact as well as treated with cellulose isolation procedures, using sum-frequency-generation spectroscopy, infrared (IR) spectroscopy and X-ray diffraction (XRD). Derbesia walls contain large amounts of mannan and small amounts of crystalline cellulose. Evidence for cellulose II in the intact cell walls was not found, whereas cellulose II in the trifluoroacetic acid (TFA) treated cell wall samples were detected by IR and XRD. A control experiment conducted with ball-milled Avicel cellulose samples showed that cellulose II structure could be formed as a result of TFA treatment and drying of amorphous cellulose. These data suggest that the cellulose II structure detected in the TFA-treated Derbesia gametophyte wall samples is most likely due to reorganization of amorphous cellulose during the sample preparation. Our results contradict the previous report of cellulose II in native alga cell walls. Even if the crystalline cellulose II exists in intact Derbesia gametophyte cell walls, its amount would be very small (below the detection limit) and thus biologically insignificant.

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References

  • Abdul Khalil HPS, Bhat AH, Ireana Yusra AF (2012) Green composites from sustainable cellulose nanofibrils: a review. Carbohydr Polym 87(2):863–879

    Article  Google Scholar 

  • Atalla RH, Vanderhart DL (1984) Native cellulose: a composite of two distinct crystalline forms. Science 223(4633):283–285

    Article  CAS  Google Scholar 

  • Atalla RH, Vanderhart DL (1999) The role of solid state 13C NMR spectroscopy in studies of the nature of native celluloses. Solid State Nucl Magn Reson 15(1):1–19

    Article  CAS  Google Scholar 

  • Bahaji A, Li J, Ovecka M, Ezquer I, Munoz FJ, Baroja-Fernandez E, Romero JM, Almagro G, Montero M, Hidalgo M, Sesma MT, Pozueta-Romero J (2011) Arabidopsis thaliana mutants lacking ADP-glucose pyrophosphorylase accumulate starch and wild-type ADP-glucose content: further evidence for the occurrence of important sources, other than ADP-glucose pyrophosphorylase, of ADP-glucose linked to leaf starch biosynthesis. Plant Cell Physiol 52(7):1162–1176

    Article  CAS  Google Scholar 

  • Barnette AL, Bradley LC, Veres BD, Schreiner EP, Park YB, Park J, Park S, Kim SH (2011) Selective detection of crystalline cellulose in plant cell walls with sum-frequency-generation (SFG) vibration spectroscopy. Biomacromolecules 12:2434–2439

    Article  CAS  Google Scholar 

  • Barnette AL, Lee CM, Bradley LC, Schreiner EP, Park YB, Shin H, Cosgrove DJ, Park S, Kim SH (2012) Quantification of crystalline cellulose in lignocellulosic biomass using sum frequency generation (SFG) vibration spectroscopy and comparison with other analytical methods. Carbohydr Polym 89(3):802–809

    Article  CAS  Google Scholar 

  • Bowman JL, Floyd SK, Sakakibara K (2007) Green genes-comparative genomics of the green branch of life. Cell 129(2):229–234

    Article  CAS  Google Scholar 

  • Cho SH, Du J, Sines I, Poosarla VG, Vepachedu V, Kafle K, Park YB, Kim SH, Kumar M, Nixon BT (2015) In vitro synthesis of cellulose microfibrils by a membrane protein from protoplasts of the non-vascular plant Physcomitrella patens. Biochem J 470(2):195–205

    Article  Google Scholar 

  • Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6(11):850–861

    Article  CAS  Google Scholar 

  • Cosgrove DJ (2014) Re-constructing our models of cellulose and primary cell wall assembly. Curr Opin Plant Biol 22:122–131

    Article  CAS  Google Scholar 

  • De Ruiter GA, Schols HA, Voragen AG, Rombouts FM (1992) Carbohydrate analysis of water-soluble uronic acid-containing polysaccharides with high-performance anion-exchange chromatography using methanolysis combined with TFA hydrolysis is superior to four other methods. Anal Biochem 207(1):176–185

    Article  Google Scholar 

  • Dunn EK, Shoue DA, Huang X, Kline RE, MacKay AL, Carpita NC, Taylor IE, Mandoli DF (2007) Spectroscopic and biochemical analysis of regions of the cell wall of the unicellular ‘mannan weed’, Acetabularia acetabulum. Plant Cell Physiol 48(1):122–133

    Article  CAS  Google Scholar 

  • Fernandes AN, Thomas LH, Altaner CM, Callow P, Forsyth VT, Apperley DC, Kennedy CJ, Jarvis MC (2011) Nanostructure of cellulose microfibrils in spruce wood. Proc Natl Acad Sci USA 108(47):E1195–E1203

    Article  Google Scholar 

  • French AD (2014) Idealized powder diffraction patterns for cellulose polymorphs. Cellulose 21:885–896

    Article  CAS  Google Scholar 

  • Guerriero G, Fugelstad J, Bulone V (2010) What do we really know about cellulose biosynthesis in higher plants? J Integr Plant Biol 52(2):161–175

    Article  CAS  Google Scholar 

  • Hill JL Jr, Hammudi MB, Tien M (2014) The Arabidopsis cellulose synthase complex: a proposed hexamer of CESA trimers in an equimolar stoichiometry. Plant Cell 26(12):4834–4842

    Article  CAS  Google Scholar 

  • Horikawa Y, Sugiyama J (2009) Localization of crystalline allomorphs in cellulose microfibril. Biomacromolecules 10(8):2235–2239

    Article  CAS  Google Scholar 

  • Imai T, Sugiyama J (1998) Nanodomains of Iα and Iβ cellulose in algal microfibrils. Macromolecules 31:6275–6279

    Article  CAS  Google Scholar 

  • Jarvis M (2003) Chemistry: cellulose stacks up. Nature 426(6967):611–612

    Article  CAS  Google Scholar 

  • Jia X, Chen Y, Shi C, Ye Y, Wang P, Zeng X, Wu T (2013) Preparation and characterization of cellulose regenerated from phosphoric acid. J Agric Food Chem 61(50):12405–12414

    Article  CAS  Google Scholar 

  • Kafle K, Greeson K, Lee CM, Kim SH (2014a) Cellulose polymorphs and physical properties of cotton fabrics processed with commercial textile mills for mercerization and liquid ammonia treatments. Text Res J 84(16):1692–1699

    Article  Google Scholar 

  • Kafle K, Shi R, Lee CM, Mittal A, Park YB, Sun Y-H, Park S, Chiang V, Kim SH (2014b) Vibrational sum-frequency-generation (SFG) spectroscopy study of the structural assembly of cellulose microfibrils in reaction woods. Cellulose 21(4):2219–2231

    Article  CAS  Google Scholar 

  • Kafle K, Xi X, Lee C, Tittmann BR, Cosgrove DJ, Park YB, Kim SH (2014c) Cellulose microfibril orientation in onion (Allium cepa L.) epidermis studied by atomic force microscopy (AFM) and vibrational sum frequency generation (SFG) spectroscopy. Cellulose 21(2):1075–1086

    Article  Google Scholar 

  • Kim NH, Imai T, Wada M, Sugiyama J (2006) Molecular directionality in cellulose polymorphs. Biomacromolecules 7(1):274–280

    Article  CAS  Google Scholar 

  • Kim SH, Lee CM, Kafle K (2013a) Characterization of crystalline cellulose in biomass: basic principles, applications, and limitations of XRD, NMR, IR, Raman, and SFG. Korean J Chem Eng 30(12):2127–2141

    Article  CAS  Google Scholar 

  • Kim SH, Lee CM, Kafle K, Park YB, Xi X (2013b) Vibrational sum frequency generation (SFG) spectroscopic study of crystalline cellulose in biomass. In: Proceedings of SPIE, vol 8845, pp 884501–884508

  • Kong L, Lee CM, Kim SH, Ziegler GR (2014) Characterization of starch polymorphic structures using vibrational sum frequency generation spectroscopy. J Phys Chem B 118(7):1775–1783

    Article  CAS  Google Scholar 

  • Koyama M, Helbert W, Imai T, Sugiyama J, Henrissat B (1997) Parallel-up structure evidences the molecular directionality during biosynthesis of bacterial cellulose. Proc Natl Acad Sci USA 94(17):9091–9095

    Article  CAS  Google Scholar 

  • Kroon-Batenberg L, Bouma B, Kroon J (1996) Stability of cellulose structures studied by MD simulations. Could mercirized cellulose II be parallel? Macromolecules 29(17):5695–5699

    Article  Google Scholar 

  • Langan P, Nishiyama Y, Chanzy H (2001) X-ray structure of mercerized cellulose II at 1 Å resolution. Biomacromolecules 2(2):410–416

    Article  CAS  Google Scholar 

  • Lee CM, Mittal A, Barnette AL, Kafle K, Park YB, Shin H, Johhnson DK, Park S, Kim SH (2013) Cellulose polymorphism study with sum-frequency-generation (SFG) vibration spectroscopy: identification of exocyclic CH2OH conformation and chain orientation. Cellulose 20(3):991–1000

    Article  CAS  Google Scholar 

  • Lee CM, Kafle K, Park YB, Kim SH (2014) Probing crystal structure and mesoscale assembly of cellulose microfibrils in plant cell walls, tunicate tests, and bacterial films using vibrational sum frequency generation (SFG) spectroscopy. Phys Chem Chem Phys 16(22):10844–10853

    Article  CAS  Google Scholar 

  • Lee CM, Kafle K, Belias DW, Park YB, Glick RE, Haigler CH, Kim SH (2015) Comprehensive analysis of cellulose content, crystallinity, and lateral packing in Gossypium hirsutum and Gossypium barbadense cotton fibers using sum frequency generation, infrared and Raman spectroscopy, and X-ray diffraction. Cellulose 22(2):972–989

    Article  Google Scholar 

  • Magnusson M, Mata L, de Nys R, Paul NA (2014) Biomass, lipid and fatty acid production in large-scale cultures of the marine macroalga Derbesia tenuissima (Chlorophyta). Mar Biotechnol (NY) 16(4):456–464

    Article  CAS  Google Scholar 

  • Marubashi Y, Higashi T, Hirakawa S, Tani S, Erata T, Takai M, Kawamata J (2004) Second harmonic generation measurements for biomacromolecules: celluloses. Opt Rev 11(6):385–387

    Article  CAS  Google Scholar 

  • McNamara JT, Morgan JL, Zimmer J (2015) A molecular description of cellulose biosynthesis. Annu Rev Biochem 84:895–921

    Article  CAS  Google Scholar 

  • Newman RH, Hill SJ, Harris PJ (2013) Wide-angle X-ray scattering and solid-state nuclear magnetic resonance data combined to test models for cellulose microfibrils in mung bean cell walls. Plant Physiol 163(4):1558–1567

    Article  CAS  Google Scholar 

  • Nishiyama Y, Langan P, Chanzy H (2002) Crystal structure and hydrogen-bonding system in cellulose Ibeta from synchrotron X-ray and neutron fiber diffraction. J Am Chem Soc 124(31):9074–9082

    Article  CAS  Google Scholar 

  • Nishiyama Y, Sugiyama J, Chanzy H, Langan P (2003) Crystal structure and hydrogen bonding system in cellulose I(alpha) from synchrotron X-ray and neutron fiber diffraction. J Am Chem Soc 125(47):14300–14306

    Article  CAS  Google Scholar 

  • Page JZ, Kingsbury JM (1968) Culture studies on the marine green alga Halicystis parvula-Derbesia tenuissima. II. Synchrony and periodicity in gamete formation and release. Am J Bot 55(1):1–11

    Article  Google Scholar 

  • Park S, Baker JO, Himmel ME, Parilla PA, Johnson DK (2010) Cellulose crystallinity index: measurement techniques and their impact on interpreting cellulase performance. Biotechnol Biofuels 3:10

    Article  Google Scholar 

  • Park YB, Lee CM, Koo BW, Park S, Cosgrove DJ, Kim SH (2013) Monitoring meso-scale ordering of cellulose in intact plant cell walls using sum frequency generation (SFG) spectroscopy. Plant Physiol 163(2):907–913

    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(7):2718–2724

    Article  CAS  Google Scholar 

  • Pauly M, Keegstra K (2008) Cell-wall carbohydrates and their modification as a resource for biofuels. Plant J 54(4):559–568

    Article  CAS  Google Scholar 

  • Roelofsen PA, Dalitz VC, Wijnman CF (1953) Constitution, submicroscopic structure and degree of crystallinity of the cell wall of Halicystis osterhoutii. Biochim Biophys Acta 11(3):344–352

    Article  CAS  Google Scholar 

  • Ruan D, Zhang L, Zhou J, Jin H, Chen H (2004) Structure and properties of novel fibers spun from cellulose in NaOH/thiourea aqueous solution. Macromol Biosci 4(12):1105–1112

    Article  CAS  Google Scholar 

  • Rubin EM (2008) Genomics of cellulosic biofuels. Nature 454(7206):841–845

    Article  CAS  Google Scholar 

  • Sebe G, Ham-Pichavant F, Ibarboure E, Koffi AL, Tingaut P (2012) Supramolecular structure characterization of cellulose II nanowhiskers produced by acid hydrolysis of cellulose I substrates. Biomacromolecules 13(2):570–578

    Article  CAS  Google Scholar 

  • Sethaphong L, Haigler CH, Kubicki JD, Zimmer J, Bonetta D, DeBolt S, Yingling YG (2013) Tertiary model of a plant cellulose synthase. Proc Natl Acad Sci USA 110(18):7512–7517

    Article  CAS  Google Scholar 

  • Sisson WA (1938) The Existence of mercerized cellulose and its orientation in Halicystis as indicated by X-ray diffraction analysis. Science 87(2259):350

    Article  CAS  Google Scholar 

  • Somerville C (2006) Cellulose synthesis in higher plants. Annu Rev Cell Dev Biol 22:53–78

    Article  CAS  Google Scholar 

  • Sugiyama J, Persson J, Chanzy H (1991) Combined infrared and electron diffraction study of the polymorphism of native celluloses. Macromolecules 24:2461–2466

    Article  CAS  Google Scholar 

  • Thomas LH, Forsyth VT, Sturcova A, Kennedy CJ, May RP, Altaner CM, Apperley DC, Wess TJ, Jarvis MC (2013) Structure of cellulose microfibrils in primary cell walls from collenchyma. Plant Physiol 161(1):465–476

    Article  CAS  Google Scholar 

  • Wang T, Park YB, Caporini MA, Rosay M, Zhong L, Cosgrove DJ, Hong M (2013) Sensitivity-enhanced solid-state NMR detection of expansin’s target in plant cell walls. Proc Natl Acad Sci USA 110(41):16444–16449

    Article  CAS  Google Scholar 

  • White PB, Wang T, Park YB, Cosgrove DJ, Hong M (2014) Water-polysaccharide interactions in the primary cell wall of Arabidopsis thaliana from polarization transfer solid-state NMR. J Am Chem Soc 136(29):10399–10409

    Article  CAS  Google Scholar 

  • Wutz M, Zetsche K (1976) Biochemistry and regulation of the heteromorphic life cycle of the green alga Derbesia-Halicystis. Planta 129(3):211–216

    Article  CAS  Google Scholar 

  • Zugenmaier P (2008) Crystalline cellulose and derivatives: characterization and structures. In: Timell TE, Wimmer R (eds) Springer series in wood science. Springer, Berlin, pp 7–51

    Google Scholar 

Download references

Acknowledgments

This work was supported by The Center for LignoCellulose Structure and Formation, an Energy Frontier Research Center funded by the U.S. Department of Energy, Office of Science, and Office of Basic Energy Sciences under Award Number DE-SC0001090.

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Authors and Affiliations

  1. 208 Mueller Laboratory, Department of Biology, The Pennsylvania State University, University Park, PA, 16802, USA

    Yong Bum Park & Daniel J. Cosgrove

  2. Department of Chemical Engineering and Materials Research Institute, The Pennsylvania State University, University Park, PA, 16802, USA

    Kabindra Kafle, Christopher M. Lee & Seong H. Kim

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  1. Yong Bum Park
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  2. Kabindra Kafle
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Correspondence to Yong Bum Park or Seong H. Kim.

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Park, Y.B., Kafle, K., Lee, C.M. et al. Does cellulose II exist in native alga cell walls? Cellulose structure of Derbesia cell walls studied with SFG, IR and XRD. Cellulose 22, 3531–3540 (2015). https://doi.org/10.1007/s10570-015-0750-8

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