E uplotes (Dorsoventrally Flattened Ciliates)

Abstract

Euplotes spread into every aquatic habitat of our planet and diversified into dozens of species that can promptly be identified taxonomically on the basis of well‐established diagnostic traits related to their ciliary and cortical structures. In large numbers, they can be easily collected and cultivated in laboratory for years with no apparent sign of senescence and decline. They are a rich source of secondary metabolites of terpenoid nature, host symbiotic bacteria in their cytoplasm and manifest sex in the form of conjugation and, more exceptionally, autogamy. Owing to their capacity to synthesise families of diffusible protein pheromones in functional association with their high‐multiple mating systems, Euplotes species provide valuable experimental material to study the molecular basis of self/nonself recognition phenomena in early forms of the eukaryotic life.

Key Concepts

  • Euplotes is one of the most diversified and widely distributed ciliates in every aquatic habitat of our planet.
  • Intraclonal and intraspecific variations in relevant diagnostic traits are relatively common among Euplotes species and raise problems in their taxonomic diagnosis.
  • An outbreeding population structure is distinctive of most Euplotes species and determined by the pervasive evolution of high‐multiple (virtually open) mating systems.
  • The occasional appearance of autogamy (in concomitance with conjugation) in some Euplotes populations does not appear to be able to generate inbreeding depression, as this sexual event in Euplotes is exceptionally destined to maintain preexistent states of heterozygosity.
  • Euplotes houses Francisella endosymbionts and, therefore, is a potential vector of pathogenic bacteria.
  • Marine species of Euplotes produce large amounts of sesquiterpenoid compounds as secondary metabolites, and use these chemicals as devices against predators and ecological competitors.
  • Euplotes pheromones produce species‐specific families of water‐borne, globular and cysteine‐rich proteins which, owing to their structural homology (as determined by NMR and crystallographic analyses), can bind to cells in competition with one another.
  • A double activity characterises Euplotes pheromones: a self‐activity directed to promote the vegetative growth of the same cells from which they are secreted and to which they bind in autocrine manner, and a nonself, presumably secondarily acquired mating‐induction activity on cells to which they bind in heterologous manner.

Keywords: protozoan protists; cytoplasmic endosymbionts; mating systems; conjugation; autogamy; water‐borne proteins; pheromones; secondary metabolites; terpenes

Figure 1. Morphological traits of common use in Euplotes taxonomy illustrated taking E. petzi as an example. (a, b) Scanning electron microscopy of the cell dorsal surface carrying single bristle cilia, and of the ventral surface carrying cirri and adoral membranelles. (c, d) Silver‐stained specimens showing the dorsal argyrome of double‐patella type (with unequal rows of polygons between adjacent rows of the bristle cilia), and the patterned distribution of cirri and adoral membranelles on the cell ventral surface. (e, f) Diagrams of the cell dorsal and ventral surfaces of silver‐stained specimens. Abbreviations: DK, dorsal kineties; FVC, frontoventral cirri; TC, transverse cirri; CC, caudal cirri; MC, marginal cirri; AZM, adoral zone of ciliary membranelles; PM, paroral membrane; K1, lateroventral kinety (#1). Bar = 10 µm. Reproduced with permission from Di Giuseppe et al. (2014) © Elsevier.
Figure 2. Morphology of the nuclear apparatus of E. crassus. (a) Dapi‐stained specimen showing the hook‐shaped macronucleus (ma) and the spherical micronucleus (mi). (b, d) Freeze‐fracture replicas in transmission electron microscopy of the micro‐ and macronuclear envelopes showing the different distribution of the nuclear pores, uniform in the micronucleus and patched in the macronucleus (11 000×). (c, e) Thin‐section micrographs across the micro‐ and macronucleus showing the different organisation of chromatin, which forms a unique body well spaced from the nuclear membrane in the micronucleus and condensed in distinct bodies frequently adherent to the nuclear membrane in the macronucleus (9000×). Abbreviations: ch, chromatin bodies; nm, nuclear membrane; nl, nucleolus. Reproduced and modified from Dallai and Luporini (1982) © Elsevier.
Figure 3. Phylogenetic tree of Euplotes based on comparisons of SSU rRNA gene sequences available from the GenBank/EMBL databases for certified Euplotes species. Fully supported branches are marked with solid circles. The six fully supported clades are highlighted in grey boxes. The scale bar corresponds to two substitutions per 100 nucleotide positions. Certesia quadrinucleata and Aspidisca steini, which are species of a Euplotes sister clade, were used as outgroups. According to Di Giuseppe et al. (2014).
Figure 4. Ultrastructural aspects of the cell–cell union in mating pairs in E. crassus. (a) Scanning electron micrograph of a mating pair in an initial stage of union (magnification, 300×); the bar indicates the orientation of the cross‐section shown in the following picture. (b) Low‐magnification electron micrograph (6250×) of the just‐fused peristomial areas of the two mating partners. (c) The rotational symmetry distinctive of the Euplotes cell–cell union in mating pairs as represented by the ‘ying‐yang’ symbol. Abbreviations: cb, cytoplasmic bridge; c, cell cortex; pm, naked (new) plasma membrane; mn, microtubule network; cm, ciliary membranelles on the left edge of the perstomial field; ir, intermembranelle ridges; rpe, right peristomial edge; bc, bacteria; ma, macronucleus; mt, mitochondria. Reproduced with permission from Dallai and Luporini (1989) © Elsevier.
Figure 5. Scheme of the micronucleus and synkaryon divisions that take place in relation to conjugation and autogamy in E. crassus. Large and small circles refer to diploid and aploid products, respectively. Light circles with a dashed contour indicate products destined to be reabsorbed. The whole set of divisions is usually completed within 12 h, of which five are required by the first meiotic division. According to Dini et al. (1999).
Figure 6. NMR structures of Euplotes pheromones. (a) Ribbon presentations of the pheromones Er‐1 and En‐6 taken as representative of the E. raikovi and E. nobilii pheromone families, respectively. The disulfide bridges are represented as gold spheres and sticks; the three core α‐helices are indicated by h1, h2 and h3; the En‐6 pheromone‐specific 310 helical turn is indicated by 310; the molecule amino and carboxyl termini are labelled N and C, respectively. (b) Intra‐ and interspecific superposition of pheromone molecular backbones. From left to right: backbone superposition among the E. raikovi pheromones Er‐1, Er‐2, Er‐10, Er‐11 and Er‐22, among the E. nobilii pheromones En‐1, En‐2 and En‐6, and between the E. raikovi pheromone Er‐1 and the E. nobilii pheromone En‐6. The Protein Data Bank codes of the E. raikovi and E. nobilii pheromones represented in this figure are the following ones: Er‐1 (1erc and 1ERL for the NMR and crystal structures, respectively); Er‐2 (1erd); Er‐10 (1erp); Er‐11 (1ery); Er‐22 (1hd6); En‐1 (2nsv); En‐2 (2nsw); En‐6 (2jms). According to Alimenti et al. (2009).
Figure 7. Distinct classes of terpenoid metabolites that have been structurally characterised from five different marine species of Euplotes: E. crassus, E. vannus, E. raikovi, E. focardii and E. rariseta. According to Guella et al. (2010).
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Further Reading

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Hausmann K and Radek R (2014) Cilia and Flagella – Ciliates and Flagellates. Stuttgart: Schweizerbart Science Publisshers.

Lynn DH and Corliss JO (1991) Ciliophora. In: Harrison FW and Corliss JO (eds) Microscopic Anatomy of Invertebrates, vol. 1: Protozoa, pp. 333–467. New York: John Wiley & Sons.

Lynn DH (2007) The Ciliated Protozoa. New York: Springer.

Sleigh M (1989) Protozoa and Other Protists, 2nd edn. London: Arnold.

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Di Giuseppe, Graziano, Dini, Fernando, Vallesi, Adriana, and Luporini, Pierangelo(Dec 2015) E uplotes (Dorsoventrally Flattened Ciliates). In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001965.pub2]