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Protistology Choanoflagellate Evolution: the Morphological

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Protistology Choanoflagellate Evolution: the Morphological Protistology Protistology 5 (4), 256–267 (2008) Choanoflagellate evolution: the morphological perspective 1 Barry S.C. Leadbeater School of Biological Sciences, University of Birmingham, Birmingham B15 2TT, UK Summary Choanoflagellates are a ubiquitous group of heterotrophic nanoflagellates found in aquatic en- vironments everywhere. Recent molecular phylogeny has confirmed them as being the sister group to the Metazoa. They are easily recognised by their spherical to ovoid cell with a single anterior flagellum surrounded by a collar of microvilli. Choanoflagellates are filter feeders, the flagellum creating a flow of water from which food particles, mostly bacteria, are trapped on the outside of the collar. To enhance the flow of water over the collar, the cell needs to be stationary and this is achieved by the production of an organic theca with a stalk. Thecate choanoflagel- lates are common in both freshwater and marine environments but require a substratum for settlement. A group of exclusively marine choanoflagellates, Acanthoecidae, has developed a siliceous basket-like covering, the lorica, that encloses the cell and serves not only to resist the locomotory forces created by the flagellum but also to direct and enhance water flow over the collar. Variations in the morphology of the lorica, the amount of silicification and the posi- tioning of the inner organic investment have allowed loricate species to diversify and thereby inhabit many different microniches within the water column. Key words: Choanoflagellate, glycocalyx, theca, lorica, siliceous costae, water flows, ecology, planktonic species, phylogeny Introduction subtle structural variations have facilitated ecologi- cal diversity on a global scale. This communication The very word ‘morphology’ conjures up thoughts will explore the relationship between choanoflagel- of the past and even in its modern guise as ultra- late morphology and ecology and will summarise structure, it still seems strangely outdated and only aspects that are now considered to be of evolutionary of ‘natural history’ interest. And yet, as recorded importance. here, a relatively little known but important group of heterotrophic nanoflagellates seems to contradict Cell Morphology this current view of biology. For the choanoflagel- lates, the study of morphology demonstrates par ex- Choanoflagellates are one of the most important cellence the integration of ultrastructure with ecol- and ubiquitous groups of heterotrophic nanoflagel- ogy and evolution. The justification for this claim lates in aquatic ecosystems. Their morphology is un- rests on the contrast between the living cell, which mistakeable on account of the remarkable constancy in terms of morphology and ultrastructure is so con- of the protoplast that is spherical to ellipsoidal in servative, and its external structures, which by many shape and bears a single flagellum surrounded by a 1 Materials presented on the V European Congress of Protistology (July 23–27, 2007, St. Petersburg, Russia). © 2008 by Russia, Protistology Protistology • 257 funnel-shaped collar made up of actin-supported mi- es and by inference the animal kingdom. William crovilli (Fig. 1) (Karpov and Leadbeater, 1997, 1998). Saville-Kent (1880-82), who for ten years dedicated The function of the flagellum is to create a current his life to the development of seawater aquaria, of water from which potential food particles, mostly named many new species which were ultimately pub- bacteria, become entrapped on the outer surface of lished in the Manual of the Infusoria. He erected a the collar (Pettitt et al., 2002). Pseudopodia arising new order, Choanoflagellata, within the Protozoa for from the base of the collar ingest trapped particles uniflagellate monads with a hyaline collar and delin- and create food vacuoles that are subsequently trans- eated two families based on the nature of the cell cov- ported to the rear of the cell where digestion takes ering. Members of the Codonosigidae were ‘naked’ place (Leadbeater, 1983). This mechanism of feeding and divided laterally (Fig. 3) whereas members of the has obviously suited choanoflagellates well and vari- Salpingoecidae possessed a thicker organic cover- ations on the basic pattern are relatively minor. A ing, the theca, and because of this physical limita- similar conservativeness also applies to the structure tion, division could only be accomplished by the cell and distribution of organelles within the cell (Fig. 2) becoming amoeboid and emerging from the anterior (Karpov and Leadbeater, 1997). end of the theca (Fig. 5). Kent (1880-82) was an en- The requirement for an external covering stems thusiastic advocate of the choanoflagellate/sponge from the functional behaviour of the cell. Movement relationship and when he observed a colonial cho- of the flagellum creates a locomotory force which, if anoflagellate in samples from a freshwater pond he not resisted in some way, propels the cell through the named it Proterospongia (first sponge). However, as water. In the swimming mode, local flows of water will be demonstrated later, motile colonial stages are extend less than a wavelength from the flagellum and common in the life-cycles of many sedentary species. the velocity of water movement reduces exponential- Much later a third family, the Acanthoecidae Norris ly with distance (Lighthill, 1976). Thus the capacity (1965), was added to accommodate species with sili- to bring fresh particle-laden water to the surface of ceous basket-like loricae (Figs. 10-22). Although cho- the cell is limited. However, if the cell is attached to anoflagellates with siliceous loricae were illustrated a surface then local flows of water extend for between unknowingly by Kent (1880) and later in detail by 10-20 body diameters around the organism thereby Ellis (1929), the full significance of the lorica was not ensuring extensive renewal of water over the cell sur- appreciated until Norris’s 1965 study. face (Lapage, 1925; Sleigh, 1964; Higdon, 1979). For The last thirty years have seen a resurgence of the cell to be an efficient feeder the locomotory force interest in the choanoflagellates, firstly because they must be resisted and in many species this is achieved are the sister group to the Metazoa (Carr et al., 2008), by attachment of the cell to a surface either directly and secondly because they are a major group of het- or by means of a peduncle (stalk) (Lighthill, 1976; erotrophic nanoflagellates particularly in marine en- Sleigh, 1991). At its simplest, the posterior end of the vironments (Thomsen et al., 1997 for refs). With the cell attaches to a surface but in many species attach- application of electron microscopy to nanoplankton- ment is the first step in the production of an organic ic studies a considerable literature has accumulated, coat or theca which partly surrounds the posterior particularly with respect to loricate species which are portion of the cell. To enhance the efficiency of feed- exclusively marine. Species lists are now available for ing, the coat or theca must not interfere with the lo- many regions around the world. cal water flows around the collar. To enclose a cell above the base of the collar a rigid framework with Cell Coverings apertures is necessary and one group of choanofla- gellates, the Acanthoecidae, has achieved this by de- The glycocalyx velopment of a siliceous basket-like lorica. Thistermisusedinageneralandunspecificman- Systematics of the Choanoflagellida ner to refer to the layer of fine fibrils on the outer sur- face of the plasma membrane. This feature is prob- The first unequivocal description of choanoflagel- ably universal for all choanoflagellate cells, although lates was by Henry James Clark (1866) when he sam- in those enclosed within a theca or lorica it may be pled marine and freshwater localities and described obscured. It is seen to greatest advantage in cells de- four species. He also astutely observed the similar- scribed as being ‘naked’, which includes motile cells ity between choanoflagellates and the choanocytes of resulting from division, some species of Monosiga, sponges and so initiated the idea that the choanofla- Codosiga and some colonial species (Leadbeater and gellates were the protozoan ancestors of the spong- Morton, 1974a; Karpov and Leadbeater, 1997). In 258 • Barry S.C. Leadbeater Fig. 1. Monosiga ovata. Cell with single flagellum (f) surrounded by a collar of tentacles (c). Two posterior tentacles for attachment to substratum. Fig. 2. M. ovata. Section of cell showing general disposition of organelles. Abbreviations: c - collar, f - flagellum, fb2 - second flagellar base; G - Golgi apparatus, n - nucleus, m - mitochondrion, fv - food vacuole. Fig. 3. Codosiga gracilis. Two daughter cells immediately following division. Fig. 4. C. gracilis. Whole mount of a stalk (s) and remaining glycocalyx (g) follow- ing extraction of cell with detergent. Fig. 5. Choanoeca perplexa. Cell division, showing amoeboid form of cell emerging from neck of flask-shaped theca. Fig. 6. Salpingoeca urceolata. Shadowcast empty flask-shaped theca showing inner flange at bottom of collar (arrow). Fig. 7. Proterospongia sp. (ATCC 50818). ”Proterospongia” colony of six cells with long flagella and collars of tentacles. Scale bars: 1– 2 µm; 2 – 0,5 µm; 3 – 2 µm; 4 – 0,5 µm; 5 – 2 µm; 6 – 1 µm; 7 – 4 µm. Protistology • 259 Codosiga gracilis the thin outer covering is sufficient- end and in this case the organic covering provides ly robust to hold the top of the stalk to the base of the both an inner lining to the lorica and a direct attach- cell and it survives extraction after the cell has been ment to the cell (Leadbeater, 1972). However, in some removed with dilute detergent (Fig. 4). of the larger tectiform species, such as Diaphanoeca grandis¸ the cell is located centrally (Fig. 11) and is Organic coverings attached to a ring at the anterior end of the lorica. In this case it is the collar tentacles that secure the cell to In addition to the glycocalyx, the majority of the lorica. In many species a second organic invest- choanoflagellates possess a continuous organic cov- ment is present which comprises a thinner and more ering of some description.
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