CHAPTER I
INTRODUCTION: GREGARINES AMONG APICOMPLEXA
By
Joseph SCHRÉVEL and Isabelle DESPORTES With the technical collaboration of Doanh BACCAM
Contents. – The high morphological diversity of the vegetative stages of Gregarine trophozoites – Schizogony and taxonomy of Gregarines – Life cycles of Gregarines: A. Life cycle of a Eugre- garine: Lecudina tuzetae; B. Life cycle of an Archigregarine: Selenidium pendula the type-spe- cies; C. Life cycle of a Neogregarine: Mattesia oryzaephili – Bibliography
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Within the superkingdom eukaryota, the Alveolata Cavalier-Smith, 1991 are uni- cellular organisms characterized by the presence of cortical alveoli corresponding to flattened vesicles underlying the plasma membrane (Cavalier-Smith, 2004). The major phyla of Alveolata are: Ciliates (Ciliophora) protists with many cilia; Dinoflagellates (Dinophyceae), a large group of biflagellate protists; and Apicomplexa, parasite pro- tists including Coccidia, Hematozoa, well known for their involvement in human and veterinary diseases (malaria, toxoplasmosis, babesiosis etc.), and Gregarines, the early Apicomplexa (Fig. 1.1a) (see Aravind et al., 2003 and Adl et al., 2012 for reviews). The phylum Apicomplexa Levine, 1970 is characterized by the common basic stage, the so-called ‘zoite’. The zoite, the infective stage of all their life cycles, is involved in cell to cell dissemination inside the host and/or host to host transmission. The zoite, usually a fusiform, banana or pear-shaped cell, is a remarkable example of cell polar ity with specific apical organelles such as rhoptries, micronemes, and dense granules (Fig. 1.1b). In addition, a truncated cone formed by spirally arranged microtubules is observed in Conoidasida Levine, 1988 (Coccidia and Gregarines) and absent in Aconoidasida Mehlhorn, Peters & Haberkorn, 1980 (Hemosporidia and Piroplasma) (Perkins, 2000). This unique cell organization of the zoite apex was used to substitute the term Apicomplexa for the classic old term of Sporozoa (Levine, 1970).
7 chapter I introduction: gregarines among apicomplexa
In the Apicomplexa life cycles, ‘zoite’ refers to different cell types: sporozoite, mero- zoite, schizozoite. The sporozoite is the basic stage since it results from the sexual process starting with the gamogony, then fertilization followed by meiosis and finally the sporogony process that differentiates sporozoites. This sexual process is accompa- nied by genomic recombination during fertilization. Such a situation is quite different from the asexual multiplication that occurs during the vegetative phase and is termed schizogony or merogony and in which the genetic material derives from the mother cell. The term merogony is usual in Coccidia where several rounds of merozoites can be produced (1st, 2nd generations). Merogony is an efficient way to generalize par- asitic infections. In Gregarines, the term schizogony has been used preferentially to merogony. This led to the creation of the taxon Schizogregarines (Léger, 1900; Léger, 1907; Brasil & Fantham, 1907; Fantham, 1908 for review; Weiser, 1955), in consequence the zoites were called schizozoites. In fact the two terms merogony/schizogony are similar: for instance in malaria during the hepatic or erythrocytic schizogony zoites are termed merozoites.
In the gregarine life cycle, the vegetative phase starts with interactions between the zoite and the host cells, followed by a transition from the zoite to the trophozoite stage. The trophozoite assures the gregarine growth. In contrast to Coccidia and Hematozoa where the growth is inside a host cell, gregarine trophozoites are usually extracellular and their growth provides an exceptional diversity of sizes and cell shapes (Fig. 1.2). In addition, this extracellular localization correlates a unique sexual phase among Api- complexa. The clearer characteristic that differentiates Gregarines from other Apicomplexa is the sexual association, called syzygy, between two haploid gamonts: one female and the other male (Fig. 1.1c). The gamonts, usually of similar sizes, will form a cyst or ga- metocyst where the gamogony will start. The result is the production of large and equal numbers of male and female gametes able to assure fertilization inside the cyst. It can be noticed that some gregarine species, such as Diplauxis hatti (Fig. 1.2c), live more than two years in paired association, and the gamogony starts only in the last period of the life cycle after encystment and formation of the gametocyst (Prensier,
Figure 1.1 a. Simplified phylogenic tree of the superkingdom Eukaryota showing that the Alveolate clade emerges from a common ancestor and the Gregarine class belongs to the Apicomplexa. The phyla of the hosts are underlined in green for Gregarines and in red for Coccidia in the Craniata phylum; sar = Stramenopiles, Alveolata, Rhizaria. b. Schematic diagram of a zoite, the infectious stage of all Apicomplexa species. c. Syzygy corresponding to the association between one male and one female haploid gamont to produce a gametocyst which is a specific character of Gregarines among Apicomplexa. d. In Gregarines, but also in Coccidia, the sporozoites are inside a spore. [(a) adapted from Aravind et al., 2003 and Adl et al., 2012; (b) modified from Porchet-Henneré & Vivi- er, 1971; (c) light micrograph of a living Epicavus syzygy Schrével & Philippe, 1993; (d) DIC micrograph of living Gonospora mature spores Schrével & Gèze original data] ⇒
8 Treatise on Zoology – Anatomy, Taxonomy, Biology. The Gregarines Volume I