Alveolates Secondary article Michael A Sleigh, University of Southampton, Southampton, UK Article Contents . Outline Description and Characterization Three groups of Protozoa, the ciliates, dinoflagellates and sporozoans have been grouped . Phylogeny and Place in Overall Taxonomic Scheme together as ‘alveolates’ because typical cells in all three groups have a pair of subsurface . Major Subtaxa and Well-known Species membranes, forming inflated or flattened alveoli (fluid-filled cushions), beneath the surface membrane. The close relationship between the groups has been confirmed by molecular sequence analysis. Outline Description and any space between (Figure 1c). In all three groups the triple Characterization membrane structure tends to be underlain by a layer of granular cytoplasm containing microtubules, so that The name alveolates has been given to a cluster of three comparison of pellicular structure led to the suggestion large groups of protozoa, the ciliates (Ciliophora), that the membrane sandwich of the sporozoans probably Dinozoa (dinoflagellates) plus a few species with atypical arose from flattened internal alveoli beneath the surface features) and Sporozoa (more or less equivalent to membrane. Apicomplexa), which in many ways are very different All three groups that comprise the alveolates have had from one another. In former schemes of classification these an extensive evolutionary radiation, in each case depen- three groups were placed far apart, but the distinctive dent upon the development of a distinctive pattern of feature which they share appears to be a true ancestral organization which is unique in the living world. It is character, since phylogenetic analysis by ribosomal estimated that there are about 7500 species of ciliates, 2000 ribonucleic acid (rRNA) sequencing has shown that the living species of dinoflagellates (as well as a similar number three groups are more closely related to one another than any one of them is to any other protist group (Gajadhar et al., 1991). All three groups have an unusual arrangement of membranes at the cell surface in most members and at C C some stage in their life cycle. These membranes form a E system of alveoli over much of the surface in many ciliates and dinoflagellates, forming part of the pellicles which characterize these two groups, but are pressed together as a sandwich of three membranes in the Sporozoa. Ciliates like Paramecium and Tetrahymena were among the first cells whose fine structure was studied with the (a) electron microscope. Sections of these cells showed that over much of the body the surface membrane was underlain by two inner membranes separated by a fluid- filled space. It was soon discovered that the inner membranes actually belonged to cushion-shaped alveoli, regularly arranged between the rows of cilia of the cell surface, so that cilia and trichocysts could emerge in bands (b) between the alveoli where only a single membrane was present (Figure 1a). These alveoli occasionally contain M plates of glycoprotein which may be calcified. Comparable examination of the cells of dinoflagellates like Ceratium and Peridinium showed that the thecal plates which cover (c) these cells are actually situated internally, within alveoli Figure 1 Diagrams of sections through the surface of members of the which lie under the surface membrane (Figure 1b). The fine three alveolate groups to show the arrangement of membranes. In ciliates structure of sporozoan cells varies with the stage of the life (a), rows of cilia (C) and extrusive organelles (trichocysts or mucocysts) (E) cycle, and tends to be simplified in intracellular stages of emerge between the alveoli which underlie the surface membrane. In dinoflagellates (b), thecal plates may occupy the pellicular alveoli. In these parasites. In the extracellular stages of most species sporozoa (c), the two inner membranes are pressed tightly together the surface membrane of much of the cell is underlain by without any fluid space between, though these inner layers are interrupted two further membranes, tightly pressed together without at pits called ‘micropores’ (M). ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net 1 Alveolates of fossil species, due to the traces left by the hard theca in in corals and clams, and some species have unusual internal some forms) and 5000 species of sporozoans. organelles. Where sexual reproduction occurs, fertilization involves the fusion of two small biflagellate gametes. Characteristics of the three main groups Sporozoans Ciliates The sporozoans are haploid parasitic protozoa, mostly The ciliates are diploid cells, typically with two types of with complex life cycles usually involving at least one stage nuclei, one or more polyploid macronuclei as well as one or when the parasite grows within a host cell. Although the more diploid micronuclei, and with only the latter traditional name of Sporozoa has remained widely used participating in the exchange of genetic material during and understood, the principal subgroup was given the new the sexual process of conjugation. They also have a cortical name Apicomplexa a few years ago, in recognition of the structure in the pellicle, including the highly specific arrays fact that there is a distinctive group of organelles at the of cilia and their associated specific patterns of rootlet apical end of specific stages (those capable of penetrating fibres (the infraciliature) as well as the system of alveoli, host cells) in the life cycle of most species. This apical which is passed on to daughter cells through a mechanism complex of polar organelles consists of the conoid, a of nongenetic, somatic inheritance. The majority of ciliates truncated cone of short spiral microtubules, through which are free-living cells, actively swimming with their cilia and pass the stalks of secretory organelles called rhoptries, and feeding on other microorganisms filtered from the water or around which there are two rings, one circling the distal end picked up from surfaces. Food particles are ingested and the other circling the proximal end of the conoid. The through a special area of the body surface, the cytostome, apical complex is a site of attachment of the sporozoan to a and digested in food vacuoles. Contractile vacuoles for salt host cell, and the rhoptries are believed to release products and water balance are best developed in ciliates. The that stimulate the host cell to invaginate and draw in the parasitic forms typically live in the gut of their host, and parasite. In many cases hosts are infected with sporozoans usually retain distinctive ciliate features. by ingesting spores; these spores develop in the gut of the host to release spindle-shaped infective cells called sporozoites, which enter cells of the host. Similar sporo- Dinoflagellates zoites are injected into certain hosts by vector organisms, Most dinoflagellates are haploid cells whose nucleus like the mosquito when it transmits the malarial parasite. contains obvious condensed chromosomes throughout Parasite growth and (usually repeated cycles of) reproduc- the cell cycle. This is because the chromatin of dino- tion take place before a process of fertilization between two flagellates contains little histone protein, a feature that led parasite cells occurs, their nuclei fuse, and subsequent to the suggestion that dinoflagellates were ‘mesokaryotic’ meiosis is followed by spore and/or sporozoite formation. organisms that belonged part way between the prokaryotic In some cases the gamete cells which fuse are similar bacteria with no histones and the eukaryotes with many amoeboid cells, and in other cases a flagellate microgamete histones. However, dinoflagellates are true eukaryotes in swims to fuse with a stationary macrogamete. other respects, with mitotic and meiotic nuclear divisions and fertilization. They are typically biflagellate cells, generally with one longitudinal, backwardly-directed flagellum and one transverse flagellum which executes a Phylogeny and Place in Overall helical beat, often within an equatorial groove. The pellicle Taxonomic Scheme generally has a pattern of alveoli (called amphiesmal vesicles by workers on this group) which appear empty or Until recently the three groups that comprise the alveolates contain thin plates in the ‘naked’ or ‘unarmoured’ species were classified separately, and rather far apart. The ciliates but contain thick thecal plates in the thecate or ‘armoured’ were generally regarded as the most advanced of the species. The plates are principally composed of poly- protozoa, largely because many of them are among the saccharide material and impose specific shapes upon most complex cells known. Although Haeckel in 1866 thecate forms. About half of the species contain brown included ciliates (as Infusoria) in the Animal Kingdom, plastids and are photosynthetic. Most colourless species, as they were regarded as a separate class in the phylum well as some which contain plastids, engulf other micro- Protozoa in Bu¨ tschli’s 1880 classification and as a separate organisms at a naked area near the flagellar bases; some phylum in the kingdom Protozoa by Levine et al. in 1980. species produce, from the naked area, pseudopodia which The Sporozoa were likewise a separate class of the extend to form a thin protoplasmic veil around diatoms Protozoa in 1880 and a separate phylum (Levine’s larger than themselves and digest them within a food Apicomplexa) in 1980. With their haploid and rather vacuole outside the main body.