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Review
. 2009 Jan 7;276(1654):3-11.
doi: 10.1098/rspb.2008.0844.

Three-dimensional images of choanoflagellate loricae

Affiliations
Review

Three-dimensional images of choanoflagellate loricae

Barry S C Leadbeater et al. Proc Biol Sci. .

Abstract

Choanoflagellates are unicellular filter-feeding protozoa distributed universally in aquatic habitats. Cells are ovoid in shape with a single anterior flagellum encircled by a funnel-shaped collar of microvilli. Movement of the flagellum creates water currents from which food particles are entrapped on the outer surface of the collar and ingested by pseudopodia. One group of marine choanoflagellates has evolved an elaborate basket-like exoskeleton, the lorica, comprising two layers of siliceous costae made up of costal strips. A computer graphic model has been developed for generating three-dimensional images of choanoflagellate loricae based on a universal set of 'rules' derived from electron microscopical observations. This model has proved seminal in understanding how complex costal patterns can be assembled in a single continuous movement. The lorica, which provides a rigid framework around the cell, is multifunctional. It resists the locomotory forces generated by flagellar movement, directs and enhances water flow over the collar and, for planktonic species, contributes towards maintaining cells in suspension. Since the functional morphology of choanoflagellate cells is so effective and has been highly conserved within the group, the ecological and evolutionary radiation of choanoflagellates is almost entirely dependent on the ability of the external coverings, particularly the lorica, to diversify.

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Figures

Figure 1
Figure 1
Monosiga ovata. Cell with single flagellum, f surrounded by collar of tentacles (c). Bar=2 μm.
Figure 2
Figure 2
Acanthoeca spectabilis. Bars, 2 μm. (a) Recently divided cell showing juvenile, j and sister cell both with a flagellum, f. (b) Juvenile cell with covering of vertical bundles of costal strips (arrows). Stephanoeca diplocostata. Bars, 2 μm. (c) Cell with substantial accumulation of costal strips at top of collar (arrow). (d) Recently divided cell showing inverted juvenile, j emerging from parent lorica with covering of costal strips. (e) Recently released juvenile with bundles of strips in vertical and transverse planes (arrows). (f) Juvenile with extended lorica forming tentacles, lft. Siliceous costae have been removed with hydrofluoric acid.
Figure 3
Figure 3
Computer-generated images of developing loricae from juveniles with vertical bundles of strips and actual loricae of nudiform choanoflagellates. Bars, 2 μm. (a(i)–(v)) Formation, during one complete rotation (360°), of an outer longitudinal and inner helical costa from two vertically aligned strips (figure 3a(i)). Arrows denote direction of movement; arrowheads denote angle of inclination of helical costa. (b) Helgoeca nana. (i)–(iii) Assembly of the lorica during one rotation (360°). (iv) Lorica of actual specimen. Arrowheads point to junctions between anterior ends of helical costae and respective longitudinal costae. (c) Savillea micropora. (i)–(iii) Assembly of the lorica during 1.5 rotations (540°). (iv) Lorica of actual specimen. (d) Acanthoeca spectabilis. (i) Juvenile with covering of vertical bundles of costal strips (asterisks). (ii) Juvenile undergoing lorica assembly. Note the left-handed rotation of costae. (iii) Computer-generated image of the lorica with one helical costa highlighted. (iv) Scanning electron microscopy (SEM) image of the lorica showing helical costae and anterior spines.
Figure 4
Figure 4
Computer-generated images of developing loricae from juveniles with vertical and transverse bundles of strips and actual loricae of tectiform choanoflagellates. Bars, 2 μm except figure 4e(v) whose bar is 10 μm. (a) Saepicula pulchra. (i)–(iii) Assembly of the lorica during one rotation (360°). (iv) Lorica of actual specimen. (b) Acanthocorbis unguiculata. (i)–(iii) Assembly of the lorica during one rotation (360°). (iv) Lorica of actual specimen. Arrowheads point to junctions between anterior ends of helical costae and respective longitudinal costae. (c) Stephanoeca diplocostata. (i)–(iii) Assembly of the lorica with 12 longitudinal costae during one rotation (360°). (iv) Lorica of actual specimen with eight longitudinal costae. (d) Parvicorbicula quadricostata. (i)–(iii) Assembly of the lorica. (iv) Lorica of actual specimen. (e) Bicosta spinifera. (i)–(iii) Assembly of lorica during half a rotation (180°). (iv),(v) Loricae of actual specimens.

References

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