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.2013 Apr 23;8(4):e61675.
doi: 10.1371/journal.pone.0061675. Print 2013.

Characterization and localization of insoluble organic matrices associated with diatom cell walls: insight into their roles during cell wall formation

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Characterization and localization of insoluble organic matrices associated with diatom cell walls: insight into their roles during cell wall formation

Benoit Tesson et al. PLoS One..

Abstract

Organic components associated with diatom cell wall silica are important for the formation, integrity, and function of the cell wall. Polysaccharides are associated with the silica, however their localization, structure, and function remain poorly understood. We used imaging and biochemical approaches to describe in detail characteristics of insoluble organic components associated with the cell wall in 5 different diatom species. Results show that an insoluble organic matrix enriched in mannose, likely the diatotepum, is localized on the proximal surface of the silica cell wall. We did not identify any organic matrix embedded within the silica. We also identified a distinct material consisting of glucose polymer with variable localization depending on the species. In some species this component was directly involved in the morphogenesis of silica structure while in others it appeared to be only a structural component of the cell wall. A novel glucose-rich structure located between daughter cells during division was also identified. This work for the first time correlates the structure, composition, and localization of insoluble organic matrices associated with diatom cell walls. Additionally we identified a novel glucose polymer and characterized its role during silica structure formation.

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Conflict of interest statement

Competing Interests:The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1.C. radiatus silica structure and organic matrix.
a; SEM micrograph of the valve matrix deposited on a filter (scale bar 5 µm). b; SEM micrograph of the proximal surface of the valve (scale bar 1 µm). c–e; AFM micrographs of the organic matrix associated with the valves, c) shows the organization of material corresponding to the foramen, d) shows a high resolution image of material corresponding to a single foramen, e) shows the fibrous nature of the material between foramen, and f) shows a height profile of the line in e. g and h; organic material associated with the girdle bands. The arrow in g points at the higher edge and in h shows nodules filling the pores in the silica structure (scan size for AFM images: 9.3x8.1, 2, 1.2, 10 and 2 µm respectively).
Figure 2
Figure 2.S. turris silica structure and organic matrix.
a and d; AFM micrographs of the organic matrix associated with the valves and the girdle bands respectively. b and c; SEM micrographs of the proximal and distal surface of the valve respectively (scale bar 1 µm). e; AFM micrograph of a silicified girdle band. AFM scan sizes are 3.6, 10, and 10.6 µm for a, d, and e respectively).
Figure 3
Figure 3.N. curvilineata silica structure and organic matrix.
a; SEM micrograph of the proximal side of the valve (scale bar 1 µm). b–h; AFM micrographs and height profiles. Arrows in a and b show the fibulae (black) and the location of the raphe slit (white). b and d; Organic matrix associated with the valves. c; organic matrix associated with the valve and girdle bands (GB). e; organic matrix associated with the GB and corresponding height profile (F). g; Silicified GB and corresponding profile (h). AFM scan sizes are 5, 20×9, 2, 3.1 and 2.7 µm for b–e and g, respectively).
Figure 4
Figure 4.T. dubium silica structure and organic matrix.
a–d; SEM micrographs of the valve structure. b; ocellus, c; proximal surface. d; distal surface. e and f; organic matrix associated with the valves and girdle bands. e inset; zoom on the ocellus opening, the arrow show the opening in the ocellus. AFM scan sizes, 24, 3.5 and 2 µm for e, inset e, and f, respectively, scale bars a, b and d = 2 µm, c = 1 µm.
Figure 5
Figure 5.A. salina silica structure and organic matrix.
a and c; SEM micrographs of the valve and girdle bands respectively (scale bar 2 µm). b and d; AFM micrographs of the organic matrix associated with the valves and the girdle bands respectively (scan size: 15 and 5 µm respectively).
Figure 6
Figure 6. Localization of the organic matrix inN. curvilineta (a, c and d),A. salina (b and e) andC. radiatus (f).
a, b, d and e: SEM of SDS-cleaned valves. a and b: SEM of valve proximal surface showing the organic matrix. d and e: SEM of distal surface showing naked silica. c: SEM of acid cleaned valve proximal surface (compare with a). Scale bar: a, c = 1 µm, d, e = 2 µm, a inset, b = 500 nm. f and inset; AFM and fluorescent micrographs of DAPI-stained SDS-cleanedC. radiatus valve showing the area where the organic layer peeled off (arrow in f).
Figure 7
Figure 7. a–c; SDS cleaned cell wall ofA. salina.
a; DIC and calcofluor (green fluorescence), b and c; DAPI (blue fluorescence) and corresponding DIC micrographs. Arrows show silica valve structures. d;A. salina in DIC and stained with calcofluor, arrow shows the fibrillar structure released into the medium. e;A. salina stained with calcofluor (green) and HCK123 (pink). f and g;N. cryptocephala stained with calcofluor and HCK123. h–j; AFM micrographs of the calcofluor stainable organic structure. h; height profile of single fibril from j. AFM scan sizes, 16.4×10.2, 1.7 and 2.8 µm for h–I, respectively, scale bars; a–d = 20 µm, e–f = 5 µm.
Figure 8
Figure 8. a–g; Fluorescent micrographs of whole cells stained with calcofluor (green) and HCK123 (pink).
a–d; Two different optical sections (a, b and c, d) of dividingN. curvilineata in longitudinal section (scale bars 2 µm). e; sketch ofN. curvilineata valve in transversal section showing the orientation of the section (double arrow) and the view (arrow head at top) of a–d. White arrows in a-d show a fibulae surrounded by calcofluor stained material, and correspond to the dark single-headed arrow in e. f and g; Longitudinal section of dividingC. cryptica (scale bars 2 µm). h–k;T. dubium stained with calcofluor (scale bars 5 µm). h; reconstructed 3D image of whole cell. i; Zoom on the matrix associated with the valve showing the absence of matrix in the area corresponding to the ocelli (white arrow) and the spine (red arrow). j and k; optical section through a dividing cell, calcofluor (j) and corresponding DIC (k). l;A. salina stained with calcofluor (scale bar 5 µm).
Figure 9
Figure 9. Peak Force Quantitative Nanomechanical (PF QMN) mapping.
The elasticity of the organic matrix associated withN. curvilineata (a),S. turris (b),A. salina (c), and calcofluor-stained material fromA. salina (d) are shown.PF QNM generates an elasticity map over the entire scanned region, variations in intensity relate to differences in elasticity. Mean elasticity value and scans size are respectively; 7.1, 11.6, 6.8 and 10.7 GPa and 5, 3.6, 5×3 and 5 µm.
Figure 10
Figure 10. The effect of mycafungin (a specific β-1-3-glucan synthase inhibitor) treatment on valve formation.
a–c, b–g; SEM micrographs of acid cleaned frustules ofC. cryptica andN. curvilineata. a and e; controls. b, c and f, g; Treated with mycafungin. d; Fluorescent micrograph of HCK123 (pink)-stainedC. cryptica treated with mycafungin (red = chlorophyll autofluorescence). Scale bar: a–d and f, g = 2 µm, e = 1 µm.
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This work was supported by AFOSR MURI grant FA9550-10-1-0555. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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