Three-dimensional images of choanoflagellate loricae

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.

Biosilicification of loricate choanoflagellate: organic composition of the nanotubular siliceous costal strips of Stephanoeca diplocostata

“…The unicellular S. diplocostata are free-living flagellates that are common in coastal water. They take up free silica from the environment and use it as a building block for the synthesis of the lorica; their culture conditions are well defined, especially with respect to the formation of the lorica (Leadbeater, 1979a;Leadbeater, 1979b;Leadbeater and Davies, 1984;Leadbeater and Jones, 1984;Leadbeater, 1985;Leadbeater, 1989;Leadbeater et al, 2009). In the present study, we outline the ultrastructure of the siliceous strips and demonstrate the existence of organic components within the strips.…”

“…Those strip-containing vesicles are always associated with the membranes of the Golgi apparatus (Arndt et al, 2000). Once the strips are developed, they are released from the cells, stored at first in the top of the collar, from where they are taken for the assembly of the lorica; this organelle comprises a twolayer arrangement and is pieced together within a few minutes while the cells undergo a rotational movement (Buck and Garrison, 1988;Leadbeater, 1979a;Leadbeater, 1979b;Leadbeater et al, 2008;Leadbeater et al, 2009). Initial observations suggest that a connection between the strips exists that might contain some kind of organic connective material (Mann and Williams, 1983).…”

A family of diatom-like silicon transporters in the siliceous loricate choanoflagellates

“…Each costal strip is a hollow tube of silica, formed individually within an SDV before being exocytosed from the cell [19]. Costal strip size and shape varies within individual loricae, and the overall lorica morphology varies between species [20].…”

Competition between Silicifiers and Non-silicifiers in the Past and Present Ocean and Its Evolutionary Impacts

“…The siliceous lorica of choanoflagellates show a range of morphologies (Leadbeater et al, 2009), differing in size and density of siliceous components. This has been connected to niche partitioning, from large open structures that are required to maintain a planktonic lifestyle through the water column, to densely packed lorica of biofilm-inhabiting species (Leadbeater, 2015).…”

“…Examples include loricate choanoflagellates (Leadbeater et al, 2009), thaumatomonads (Scoble and Cavalier-Smith, 2014), chrysophytes (van Tol et al, 2012), and ascidians (Monniot et al, 1992). Repeatedly we can observe the evolution of similar morphologies in distantly related taxa, such as micropores in the siliceous components of choanoflagellates (Leadbeater, 2015), chrysophytes (Sandgren et al, 1996), diatoms (Finkel and Kotrc, 2010), and haptophytes (Yoshida et al, 2006); spines and spicules in radiolarians (Kunitomo et al, 2006), dictyochophytes (Preisig, 1994), centrohelids (Zlatogursky, 2016), and sponges (Weaver et al, 2007); or tablets and scales in haptophytes (Yoshida et al, 2006), rhizarians (Nomura and Ishida, 2016), synurophytes (Sandgren et al, 1996), amoebozoans (Lahr et al, 2013), and brachiopods (Williams et al, 2001).…”