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Extrusomes in Ciliates: Diversification, Distribution, and Phylogenetic Implications
Exocytosis is, in all likelihood, an important communication method among microbes. Ciliates are highly differentiated and specialized micro-organisms for which versatile and/or sophisticated exocytotic organelles may represent important adaptive tools. Thus, in ciliates, we find a broad range of different extrusomes, i.e ejectable membrane-bound organelles. Structurally simple extrusomes, like mucocysts and cortical granules, are widespread in different taxa within the phylum. They play the roles in each case required for the ecological needs of the organisms. Then, we find a number of more elaborate extrusomes, whose distribution within the phylum is more limited, and in some way related to phylogenetic affinities. Herein we provide a survey of literature and our data on selected extrusomes in ciliates. Their morphology, distribution, and possible function are discussed. The possible phylogenetic implications of their diversity are considered
Micro-Game Hunting: Predatory Behavior and Defensive Strategies in Ciliates
Using various feeding strategies ciliates consume all sizes of autotrophic cells from bacteria to the larger dinoflagellates or diatoms. In addition they consume other heterotrophic protists. In this way every component of prokaryotic and eukaryotic nanoproducer biomass can be transferred to higher trophic levels. Predator ciliates provide an intermediate level in the microbial loop and to obtain adequate information on their biology is important from an ecological point of view. On the other hand, effort spent in attempting to deepen our understanding of predation among protozoa are completely justified by the basic importance of this process. Protozoa, indeed, were not only the first primary consumers in the primeval Oceans, but the first predators as well. Such a new trophic niche is quite important, due to the two consequences it leads to: 1) it creates new empty spaces for new organisms to settle in; 2) it triggers a sort of evolutionary competition between predators and prey as to their morpho-functional acquisitions. So predation in protozoa offers a wide range of examples of more or less species specific and more or less direct cell interactions leading the organism to specific morphological or behavioral responses. Indeed if predators developed a variety of hunting strategies, the potential prey evolved defensive responses. Nevertheless there are not models exhaustively examined to obtain an overall picture of this phenomenon considered from a more specific sinecological point of view. This chapter deals with predation in ciliates. After an introduction to the various feeding strategies of ciliates and a survey of the ciliate predator-prey systems already studied by other authors, the model Amphileptus preying on Euplotes, is presented in more detail as a prototype of ciliate raptorial feeding behavior. Our attention is successively focused on: a) the ultrastructure of predator toxicysts (the hunting devices); b) the electrophysiological and ultrastructural effects of toxicysts discharge by Amphileptus on Euplotes; c) the behavioral patterns of the predator (prey recognition from a distance; nearby recognition; engulfment process); d) the peculiar digestion process; e) the defensive strategies of the prey
Euplotes uncinatus (Ciliophora, Hypotrichia), a new species with zooxantellae
During the observations of a field collection of Maristentor dinoferus with fluorescence microscopy, we discovered a smaller ciliate with zooxanthellae. On the basis of morphological, morphometric and ultrastructural characters, this ciliate has been recognized as a new species of the genus Euplotes. To emphasize the peculiar shape and extension of the right buccal margin, the species has been named Euplotes uncinatus sp. n. The most distinctive traits of E. uncinatus are the presence of mucocyst-like vesicles, a kind of extrusome not previously found in Euplotes, and the presence of zooxanthellae. Evidence from ciliate behavior and zooxanthellae ultrastructure make it very likely that the zooxanthellae are symbiotic, even though some are evidently consumed by the host
Flagellated endosymbiotic bacteria in Frontonia sp. (Olygohymenophorea, Peniculida)
Frontonia sp. was repeatedly found in sea water samples collected from a shore near Leghorn
(Ligurian sea). Endosymbiotic rod shaped bacteria 5–6 μm long were found in the cytoplasm of
each Frontonia sp. specimen examined at the fluorescent microscope following DAPI staining
procedure. These bacteria, as revealed by electron microscopy, are contained in vacuoles (one
or two symbionts are present in each vacuole) and are covered by numerous flagella which are
in close contact with the vacuolar membrane. Flagellated symbiotic bacteria in ciliates have
been seldom described. All the cases referred in the literature concern Paramecium, a genus
that mainly consists of fresh-water species. This is the first record of flagellated bacteria living
in a marine ciliate species belonging to a different taxon. The fact that these symbionts have
been constantly observed in just collected Frontonia and are maintained in specimens grown in
the lab for at least one month, suggests that we are not dealing with an occasional relationship.
The abundance of cytoplasmic vesicles and glycogen particles, around and sometimes within
the vacuoles, suggests a movement of metabolites between the host cytoplasm and the symbionts.
The bacteria maintained their motility once outside the host cell
Epixenosomes, peculiar Epibionts of the hypotrich Ciliate Euplotidium itoi, defend their host against predators
Euplotidium itoi harbors on its dorsal surface peculiar episymbionts (referred to as epixenosomes) equipped with a
complex extrusive apparatus. In the laboratory, E. itoi stocks without epixenosomes behave and reproduce like symbiotized stocks. The
hypothesis that epixenosomes play a defensive role against predators was tested by comparing the behavior of Lironotus lamella when
preying upon Euplotes crassus, E. itoi without epixenosomes, and E. itoi with epixenosomes. Litonotus discharges its toxicysts upon
direct-cell-to cell contact, and paralyzes the three types of prey with the same efficiency. Nevertheless, Litonotus can ingest Euplotes,
Euplotidium without epixenosomes, and to a certain extent, Euplotidium with epixenosomes whose ejecting capability has been inhibited,
while it never eats Euplotidium with unaltered epixenosomes. In each prey-type, about 60% of the individuals attacked by Litonotus
toxicyst discharge are able to recover their normal behavior once transferred into pure sea water. This percentage for E. itoi with
epixenosomes that are never eaten by the predator corresponds to the probability of survival. This probability is lower for the other
two prey-types in which the prey engulfed by the predator do not have the chance to recover. These data support the hypothesis and
suggest the involvement of the epixenosome’s ejecting apparatus in a defensive function
Trichites of Strombidium (Ciliata Oligotrichita) are extrusomes
The trichites of Strombidium and related genera have been considered either as a cytoskeletal armature or as extrusomes.
To demonstrate their true nature, a study was undertaken on two marine Strombidium species by ultrastructural and cytochemical
analysis as well as in vivo experiments. Trichites, extending from the cortex into the cell, are rod-shaped, membrane-bounded, and have
a complex structure. The following elements of the trichites, are distinguishable: an electron-transparent lumen, a laminated layer, and
a compact layer. In trichites of one species, thin ‘‘rings’’ surround the lumen. Numerous short, curved tubules with a polysaccharide
wall are present in the cytoplasm surrounding the trichites. At the cortical end, each trichite is enveloped by a ‘‘cap’’ of electron-dense
proteinaceous material. In some cases, the cortical alveoli appear interrupted, forming a ‘‘hole’’ for trichite ejection. Ejection of rodshaped
structures, up to 5 times longer than resting trichites, was obtained by in vivo treatments with dextran and aminoethyldextran.
Negative staining indicated that these structures were transformed trichites. As no other possible extrusive structures were observed in
the cytoplasm of Strombidium, trichites were considered extrusomes
A multidisciplinary approach to descrive protists: a morphological, ultrastructural, and molecular study on Peritromus kahli Villeneve-Brachon, 1940 (Ciliophora, Heterotrichea)
This study represents the first extended report on a species of the ciliate genus Peritromus, widespread in marine biotopes,
characterized by a dorso-ventral differentiation peculiar among Heterotrichea. Morphological observations (live, stained, scanning, and
transmission electron microscope) were combined with behavioral and molecular data. On the basis of the whole body of observations,
the species was recognized as Peritromus kahli. Scanning and transmission electron microscopy have revealed a number of features
such as peculiar chalice-like structures external to the dorsal surface, two types of extrusomes, and differences between dorsal and
ventral somatic ciliature. The almost complete SSrDNA gene sequence was also determined. A molecular phylogenetic analysis indicated
that Peritromus diverged early from other members of the Class Heterotrichea. The dorso-ventral differentiation that certainly influences
the behavior of P. kahli (e.g. preference for crawling and thigmotaxis) may have been selected as an adaptation to the constraints of
the interstitial habitat
Morphological, ultrastructural, and molecular characterization of Euplotidium rosati n.sp. (Ciliophora, Euplotida) from Guam
We combined morphological (i.e. live, stained, scanning, and transmission electron
microscopy) with morphometric and molecular analysis to describe a ciliate
species collected from shallow reefs in Guam, grown, and maintained in our
laboratory. The species was recognized as a member of Euplotidium, and compared
with established species of the genus: Euplotidium itoi Ito 1958; Euplotidium
psammophilus (Vacelet 1961) Borror 1972; Euplotidium arenarium
Magagnini and Nobili 1964; Euplotidium helgae Hartwig 1980; Euplotidium prosaltans
Tuffrau 1985, and Euplotidium smalli Lei, Choi and Xu, 2002. To obtain
more elements to compare the species, new morphometric data and additional
SSU rRNA gene sequences of E. itoi and of E. arenarium are reported. On the
basis of this comparison, we established the new species Euplotidium rosati
that has a cirral pattern composed of 12 frontoventral and six transverse cirri,
and lacks the left marginal cirrus. Euplotidium rosati harbors on its dorsal surface
epixenosomes, the peculiar extrusive symbionts described in other Euplotidium
species. The whole body of our observations together with the analysis of
the data available in the literature leads us to propose a redefinition of the
genus. The results may also be useful to clarify the tangled relationship
between Euplotidium and Gastrocirrhus
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