The Hidden Biodiversity of Ciliate-Endosymbionts Systems
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Central JSM Microbiology Mini Review Corresponding author Sergei I. Fokin, Department of Invertebrate Zoology, St. Petersburg State University, Universitetskaya emb. 7/9, The Hidden Biodiversity of 199034 St. Petersburg, Russia, Email: Submitted: 24 November 2014 Ciliate-Endosymbionts Systems Accepted: 24 December 2014 Published: 26 December 2014 1,2 1 Sergei I. Fokin * and Valentina Sera Copyright 1Department of Biology, University of Pisa, Italy © 2014 Fokin et al. 2Department of Invertebrate Zoology, St. Petersburg State University, Russia OPEN ACCESS Abstract Keywords Many bacterial endosymbionts have been recorded in natural populations • Bacteria of different ciliates. However, it is possible to keep only some of them as infected • Ciliates stockcultures under laboratory conditions and then investigate these bacteria more • Exotic habitats precisely. However, large part of morphological descriptions for ciliate endosymbionts • Endosymbionts was made in the last quarter of XX c. Thus, these data cannot be compared with more • Rickettsia modern discoveries as reliable molecular methods have been introduced in order to study uncultivable bacteria quite recently. The novelty of new bacterial endosymbiont descriptions in ciliates is that among of the recently found species several bacteria closely related to the Rickettsia were reported. Mean time, many territories are still either insufficiently sampled or have never been investigated by professional ciliate taxonomists, and we can expect to find many more still hidden ciliate bacterial endosymbionts Diversity of Ciliates and Their Bacterial Surveys of bacterial endosymbiosis show this phenomenon Endocymbionts to be widespread in majority of ciliated protist groups. However, for the host cell this relationship is usually facultative [15,16- Ciliated protozoa (Phylum Ciliophora) are found in all 19]. Thus, the variety of ecological niches occupied by ciliates moist habitats [1-3]. They are generally cosmopolitan in their as well as their trophic strategies and preferences suggest distribution, but some endemics as well as climate depended that endosymbiosis with bacteria may originate in different systematic (especially in different ecological) groups but with unicellular dikaryotic organisms carrying cilia at some stages in unequal probability. At present, bacterial endosymbionts are species are present [4]. About 9 000 species of ciliates, defined as their life cycle, have been described by present [3,5]. Rich, but still recorded in the cells of about 300 ciliate species [11,15,20-22], poorly studied fauna of soil ciliates and numerous descriptions of new ciliate taxa from exotic habitats and scantily investigated Apparently, heterotrichs and oligohymenophoreans are the regions [6] provide grounds to believe that a total species mostwhich promising is definitely Ciliophora an infinitesimal groups for part such of investigations their total number. as they number about 20 000 – 25 000 for all Ciliophora is not far from manifest quite high level of bacterial endosymbionts biodiversity. reality. They may be ecto- and endocommensals and parasites of For instance, only in the Paramecium genus representatives both unicellular and multicellular animals and, at the same time, (class Oligohymenophorea) were already found more than 60 serve as hosts for bacterial ecto- and endosymbionts, fungi, algae different bacterial symbionts [11,12,22]. and other protists. Ecological and trophic preferences of ciliates seem to predetermine the possibility of their endosymbiosis It should be stressed that up to now there have been with bacteria and the diversity of symbiotic relationships. There almost no special diversity-oriented investigations of ciliate- is a broad literature about ciliate-endosymbionts systems and endosymbionts systems, especially in nature [11,22]. So relations between ciliates and its bacterial endosymbionts [7- far, there have been practically no comparative studies of 15], Apparently, the ability to maintain symbionts is different in the diversity of bacterial endosymbionts in several isolated various ciliate classes as well as in different groups of protists populations of the same host species, within a species or within in general. Among the detected prokaryotic endosymbionts, the same genus of ciliates. Only Paramecium, Euplotes and the main part belongs to Alphaproterobacteria. Hundreds of nowadays Spirostomum make an exception [11,15,19,21,23-25]. prokaryotic endosymbionts can occupy almost all cellular However, even for these genera the endosymbiotic studies are compartments of ciliated protists [11,12]. In most cases, these far from being accomplished [11,15,22,26,27]. One of the most intracellular bacteria show some kind of dependence upon striking features of these ciliate-endosymbionts relationships their host, and don’t grow on standard culture media outside of is their variability (also from evolutionary point of view). their natural habitat in the eukaryotic cell [9]. This is one of big Recently, it was shown, for example, that the obligate Euplotes endosymbiont Polynucleobacter necessarius has closely related difficulties to study the symbiosis under laboratory condition. Cite this article: Fokin SI, Sera V (2014) The Hidden Biodiversity of Ciliate-Endosymbionts Systems. JSM Microbiology 2(2): 1015. Fokin et al. (2014) Email: Central free-living relatives. This association, previously thought as cell, and the stages with phage capsides were detected both into going back to the very ancestor of freshwater Euplotes species the macronucleus and the cytoplasm (Figure 1A) the symbiont of [23], is nowadays regarded as the evolutionary youngest obligate S. minus presents an elongate cell shape and an unusual big size endosymbiosis so far discovered [27]. This recent result suggests that endosymbiosis in ciliates should be regarded as open and the ability to move quickly within the nucleoplasm and/or the dynamic system, in which different kind of associations can be cytoplasm(up to 20 μm). of the Surprisingly host which enough, is well visibleboth the in novelthe living species cell have[34] established in relatively short time. Therefore, it can support a (Figure 1C). view that some bacterial endosymbionts in ciliates and protists in generally are not necessarily derived from long co-evolutions sampled or have never been investigated by professional ciliate with certain host taxa. taxonomists.Mean time, Generally, many territories it is more arelikely still to eitherdetect insufficientlya number of Potentially Pathogenic Endosymbionts and new ciliate species in remote and therefore rarely investigated Geographical Areas promised for Investigations areas such as South America, Africa, and tropical Asia or in A new, intriguing topic emerged, in the last ten years, is about the contrary – Arctic and Antarctic regions. But as our current the possible role of ciliates as reservoir for potentially pathogenic knowledge suggest even in Europe the abundance of ciliate endosymbionts. Some of the bacteria are assigned to the group species seems to be higher than it was believed previously, and can be further increased [37]. In this context, exotic habitats and of Rickettsia-like organisms, closely related to the family Rickettsiaceae (Alphaproteobacteria) [10,28-34] (Figures 1A, 1B, 1C], which includes the etiologic agents of diseases produced ciliate biodiversity and thus of their bacterial endosymbionts as tropical countries, are yet poorly studied under the profile of by R. prowazekii, R. rickettsii and Orientia tsutsugamushi; some well. For instance, such studies of India ciliates and their bacterial – to eukaryotic parasites: kinetoplastida and microsporidia endosymbionts, which (for the last point of investigations) just [35,36]. The novelty of some recent reports arises from the fact started, already revealed three novel species of endosymbiotic that, despite the belonging of new bacterial endobiont species bacteria: “Candidatus Nebulobacter yamunensis” [32], to the genus Rickettsia, they seem to present unusual features “Candidatus Cyrtobacter zanobii” [33], and “Candidatus with respect to the other rickettsiae. In detail, the symbiont of P. Trichorickettsia mobilis” [34] found in an E. aediculatus strain, multimicronucleatum is localised in the macronucleus of the host sampled in the region of Yamuna river, in the surrounding of Figure 1 cytoplasm (form with viral capsids - b) of Paramecium multimicronucleatum B) TransmissionA) Transmission electron micrograph electron micrograph of “Candidatus of “Candidatus Cryptoprodotis Trichorickettsia polytropus ”mobilis” inside the inside cytoplasm the macronucleus of Pseudomicrothorax (flagellated dubius. form - a) and in the C) Part of the cytoplasm of Spirostomum minus . Bar = 0.5 μm. D) Double FISH reaction (eubacterial + Holospora BarParamecium = 0.5 μm. caudatum with Holospora obtusa (long bright particles).(living cell, H. DIC obtusa contrast) inside with the a macronucleus number of “Candidatus (MA) stained Gigarickettsia yellow; food flagellata” bacteria bacteria. inside food Bar =vacuoles 10 μm. -specific probes) performed after experimental infection of the macronucleum of (FV) in the cytoplasm stained green as well as some small introduced bacteria inside the MA (arrowheards). Fluorescence microscopy. Bar = 15 μm. JSM Microbiology 2(2): 1015 (2014) 2/4 Fokin et al. (2014) Email: Central Delhi. It means that we have great perspectives in looking for 5. hidden ciliate-symbionts systems. Guide to the Literature.