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Diversity
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Biodiversity of Ciliates and their Symbionts
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Biodiversity of Ciliates and their Symbionts

A special issue of Diversity (ISSN 1424-2818). This special issue belongs to the section "Marine Diversity".

Deadline for manuscript submissions: closed (30 April 2020) | Viewed by 43567

Printed Edition Available!
A printed edition of this Special Issue is available here.

Special Issue Editor

Dr. Martina Schrallhammer

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Guest Editor
Department of Biology, Albert-Ludwigs Universität Freiburg, Freiburg im Breisgau, Germany
Interests: prokaryotic and eukaryotic symbionts of ciliates; microbial ecology; adaptation; evolution; intracellular bacteria; Paramecium; Rickettsia; Holospora; Caedibacter; Megaira
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Ciliates occur worldwide in a multitude of diverse habitats: not only in freshwater, brackish, and marine environments, but also in soil or associated with animals or plants. Basically, they exist wherever there is sufficient humidity for them to survive. They are predators of microorganisms such as other protists, fungi, bacteria, and archaea. As mixotrophs, they contribute to primary production and, as prey, they serve as a link to higher trophic levels. Another important, but still frequently overlooked, role is their function as habitat—or host—for other microorganisms including bacteria, archaea, and even other eukaryotes.

The study of Ciliates and their symbionts has a century-old tradition dating back to observations by Hafkine and Buetschli in the late 19th century. Recent technological innovations in the fields of microscopy and sequencing are enabling a new and more detailed perspective on their diversity, resulting in the molecular characterization of many new and “old” symbionts. Furthermore, methodological improvements are facilitating a closer view into the different interactions and the symbionts’ role and contribution, which are still unknown for the vast majority of systems.

This Special Issue on “Biodiversity of Ciliates and their Symbionts” provides a platform to highlight new research and significant advances in the description of Ciliates and their symbionts. A better picture of the diversity of Ciliates’ symbionts will help to improve our understanding of the different kinds of symbiotic relationships between these partners as well as their co-evolution.

Dr. Martina Schrallhammer
Guest Editor

Manuscript Submission Information

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Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2100 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • algae
  • biogeography
  • Ciliophora
  • diversity
  • infection
  • phylogeny
  • methanogen
  • symbiont
  • taxonomy

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Published Papers (8 papers)

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Editorial

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3 pages, 197 KiB  
Editorial
Biodiversity of Ciliates and Their Symbionts: A Special Issue
by Martina Schrallhammer
Diversity 2020, 12(11), 441; https://doi.org/10.3390/d12110441 - 23 Nov 2020
Cited by 1 | Viewed by 2008
Abstract
Interests to estimate and assess the diversity of ciliates have a centuries-long history [...] Full article
(This article belongs to the Special Issue Biodiversity of Ciliates and their Symbionts)

Research

Jump to: Editorial

17 pages, 7583 KiB  
Article
Algal Diversity in Paramecium bursaria: Species Identification, Detection of Choricystis parasitica, and Assessment of the Interaction Specificity
by Felicitas E. Flemming, Alexey Potekhin, Thomas Pröschold and Martina Schrallhammer
Diversity 2020, 12(8), 287; https://doi.org/10.3390/d12080287 - 23 Jul 2020
Cited by 8 | Viewed by 6899
Abstract
The ‘green’ ciliate Paramecium bursaria lives in mutualistic symbiosis with green algae belonging to the species Chlorella variabilis or Micractinium conductrix. We analysed the diversity of algal endosymbionts and their P. bursaria hosts in nine strains from geographically diverse origins. Therefore, their [...] Read more.
The ‘green’ ciliate Paramecium bursaria lives in mutualistic symbiosis with green algae belonging to the species Chlorella variabilis or Micractinium conductrix. We analysed the diversity of algal endosymbionts and their P. bursaria hosts in nine strains from geographically diverse origins. Therefore, their phylogenies using different molecular markers were inferred. The green paramecia belong to different syngens of P. bursaria. The intracellular algae were assigned to Chl. variabilis, M. conductrix or, surprisingly, Choricystis parasitica. This usually free-living alga co-occurs with M. conductrix in the host’s cytoplasm. Addressing the potential status of Chor. parasitica as second additional endosymbiont, we determined if it is capable of symbiosis establishment and replication within a host cell. Symbiont-free P. bursaria were generated by cycloheximid treatment. Those aposymbiotic P. bursaria were used for experimental infections to investigate the symbiosis specificity not only between P. bursaria and Chor. parasitica but including also Chl. variabilis and M. conductrix. For each algae we observed the uptake and incorporation in individual perialgal vacuoles. These host-symbiont associations are stable since more than five months. Thus, Chor. parasitica and P. bursaria can form an intimate and long-term interaction. This study provides new insights into the diversity of P. bursaria algal symbionts. Full article
(This article belongs to the Special Issue Biodiversity of Ciliates and their Symbionts)
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11 pages, 795 KiB  
Communication
Effectiveness of Photoprotective Strategies in Three Mixotrophic Planktonic Ciliate Species
by Bettina Sonntag and Ruben Sommaruga
Diversity 2020, 12(6), 252; https://doi.org/10.3390/d12060252 - 20 Jun 2020
Cited by 7 | Viewed by 5526
Abstract
Mixotrophic ciliate assemblages often prevail in summer in the surface layers of lakes. During this time, they are potentially exposed to damaging levels of incident solar ultraviolet radiation (UVR) and need efficient photoprotective mechanisms to minimize the damage. Herein, we tested the algal-bearing [...] Read more.
Mixotrophic ciliate assemblages often prevail in summer in the surface layers of lakes. During this time, they are potentially exposed to damaging levels of incident solar ultraviolet radiation (UVR) and need efficient photoprotective mechanisms to minimize the damage. Herein, we tested the algal-bearing species of Pelagodileptus trachelioides, Stokesia vernalis, and Vorticella chlorellata for how they handled stress under exposure to the artificial sunlight spectrum (i.e., UV treatment), just photosynthetically active radiation (PAR), or in the dark (i.e., control). In addition to measurements of their survival, changes in behavior, shape, and whether dark or photoenzymatic repair (PER) mechanisms are present, we measured the concentration of UV-absorbing compounds (i.e., mycosporine-like amino acids). In contrast to the response in the PAR and dark treatments, sublethal effects were observed in all species when exposed to UVR. A wavelength-specific test for P. trachelioides revealed that UV-B was especially lethal. These results suggest that the photoprotective mechanisms found in these ciliates are not sufficient to allow for their survival directly at the surface and that, accordingly, they need to shift their position further down in the water column. Full article
(This article belongs to the Special Issue Biodiversity of Ciliates and their Symbionts)
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16 pages, 7570 KiB  
Article
“Candidatus Mystax nordicus” Aggregates with Mitochondria of Its Host, the Ciliate Paramecium nephridiatum
by Aleksandr Korotaev, Konstantin Benken and Elena Sabaneyeva
Diversity 2020, 12(6), 251; https://doi.org/10.3390/d12060251 - 19 Jun 2020
Cited by 10 | Viewed by 3383
Abstract
Extensive search for new endosymbiotic systems in ciliates occasionally reverts us to the endosymbiotic bacteria described in the pre-molecular biology era and, hence, lacking molecular characterization. A pool of these endosymbionts has been referred to as a hidden bacterial biodiversity from the past. [...] Read more.
Extensive search for new endosymbiotic systems in ciliates occasionally reverts us to the endosymbiotic bacteria described in the pre-molecular biology era and, hence, lacking molecular characterization. A pool of these endosymbionts has been referred to as a hidden bacterial biodiversity from the past. Here, we provide a description of one of such endosymbionts, retrieved from the ciliate Paramecium nephridiatum. This curve-shaped endosymbiont (CS), which shared the host cytoplasm with recently described “Candidatus Megaira venefica”, was found in the same host and in the same geographic location as one of the formerly reported endosymbiotic bacteria and demonstrated similar morphology. Based on morphological data obtained with DIC, TEM and AFM and molecular characterization by means of sequencing 16S rRNA gene, we propose a novel genus, “Candidatus Mystax”, with a single species “Ca. Mystax nordicus”. Phylogenetic analysis placed this species in Holosporales, among Holospora-like bacteria. Contrary to all Holospora species and many other Holospora-like bacteria, such as “Candidatus Gortzia”, “Candidatus Paraholospora” or “Candidatus Hafkinia”, “Ca. Mystax nordicus” was never observed inside the host nucleus. “Ca. Mystax nordicus” lacked infectivity and killer effect. The striking peculiarity of this endosymbiont was its ability to form aggregates with the host mitochondria, which distinguishes it from Holospora and Holospora-like bacteria inhabiting paramecia. Full article
(This article belongs to the Special Issue Biodiversity of Ciliates and their Symbionts)
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11 pages, 8586 KiB  
Article
Endosymbiotic Green Algae in Paramecium bursaria: A New Isolation Method and a Simple Diagnostic PCR Approach for the Identification
by Christian Spanner, Tatyana Darienko, Tracy Biehler, Bettina Sonntag and Thomas Pröschold
Diversity 2020, 12(6), 240; https://doi.org/10.3390/d12060240 - 12 Jun 2020
Cited by 15 | Viewed by 5838
Abstract
Paramecium bursaria is a single-celled model organism for studying endosymbiosis among ciliates and green algae. Most strains of P. bursaria bear either Chlorella variabilis or Micractinium conductrix as endosymbionts. Both algal genera are unicellular green algae characterized by cup-shaped chloroplasts containing a single [...] Read more.
Paramecium bursaria is a single-celled model organism for studying endosymbiosis among ciliates and green algae. Most strains of P. bursaria bear either Chlorella variabilis or Micractinium conductrix as endosymbionts. Both algal genera are unicellular green algae characterized by cup-shaped chloroplasts containing a single pyrenoid and reproduction by autospores. Due to their size and only few morphological characteristics, these green algae are very difficult to discriminate by microscopy only. Their cultivation is laborious and often unsuccessful, but we developed a three-step isolation method, which provided axenic cultures of endosymbionts. In addition to the time-consuming isolation, we developed a simple diagnostic PCR identification method using specific primers for C. variabilis and M. conductrix that provided reliable results. One advantage of this approach was that the algae do not have to be isolated from their host. For a comparative study, we investigated 19 strains of P. bursaria from all over the world (new isolates and available laboratory strains) belonging to the five known syngens (R1–R5). Six European ciliate strains belonging to syngens R1 and R2 bore M. conductrix as endosymbiont whereas C. variabilis was discovered in syngens R1–R5 having worldwide origins. Our results reveal the first evidence of C. variabilis as endosymbiont in P. bursaria in Europe. Full article
(This article belongs to the Special Issue Biodiversity of Ciliates and their Symbionts)
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15 pages, 7899 KiB  
Article
Micractinium tetrahymenae (Trebouxiophyceae, Chlorophyta), a New Endosymbiont Isolated from Ciliates
by Thomas Pröschold, Gianna Pitsch and Tatyana Darienko
Diversity 2020, 12(5), 200; https://doi.org/10.3390/d12050200 - 15 May 2020
Cited by 14 | Viewed by 5575
Abstract
Endosymbiosis between coccoid green algae and ciliates are widely distributed and occur in various phylogenetic lineages among the Ciliophora. Most mixotrophic ciliates live in symbiosis with different species and genera of the so-called Chlorella clade (Trebouxiophyceae). The mixotrophic ciliates can be differentiated into [...] Read more.
Endosymbiosis between coccoid green algae and ciliates are widely distributed and occur in various phylogenetic lineages among the Ciliophora. Most mixotrophic ciliates live in symbiosis with different species and genera of the so-called Chlorella clade (Trebouxiophyceae). The mixotrophic ciliates can be differentiated into two groups: (i) obligate, which always live in symbiosis with such green algae and are rarely algae-free and (ii) facultative, which formed under certain circumstances such as in anoxic environments an association with algae. A case of the facultative endosymbiosis is found in the recently described species of Tetrahymena, T. utriculariae, which lives in the bladder traps of the carnivorous aquatic plant Utricularia reflexa. The green endosymbiont of this ciliate belonged to the genus Micractinium. We characterized the isolated algal strain using an integrative approach and compared it to all described species of this genus. The phylogenetic analyses using complex evolutionary secondary structure-based models revealed that this endosymbiont represents a new species of Micractinium, M. tetrahymenae sp. nov., which was further confirmed by the ITS2/CBC approach. Full article
(This article belongs to the Special Issue Biodiversity of Ciliates and their Symbionts)
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11 pages, 5549 KiB  
Article
New Intranuclear Symbiotic Bacteria from Macronucleus of Paramecium putrinum—“Candidatus Gortzia Yakutica”
by Alexandra Y. Beliavskaia, Alexander V. Predeus, Sofya K. Garushyants, Maria D. Logacheva, Jun Gong, Songbao Zou, Mikhail S. Gelfand and Maria S. Rautian
Diversity 2020, 12(5), 198; https://doi.org/10.3390/d12050198 - 15 May 2020
Cited by 14 | Viewed by 5488
Abstract
Holospora-like bacteria (HLB) are obligate intracellular Alphaproteobacteria, inhabiting nuclei of Paramecium and other ciliates such as “Candidatus Hafkinia” is in Frontonia. The HLB clade is comprised of four genera, Holospora, Preeria, “Candidatus Gortzia”, and “Candidatus [...] Read more.
Holospora-like bacteria (HLB) are obligate intracellular Alphaproteobacteria, inhabiting nuclei of Paramecium and other ciliates such as “Candidatus Hafkinia” is in Frontonia. The HLB clade is comprised of four genera, Holospora, Preeria, “Candidatus Gortzia”, and “Candidatus Hafkinia”. These bacteria have a peculiar life cycle with two morphological forms and some degree of specificity to the host species and the type of nucleus they inhabit. Here we describe a novel species of HLB—“Candidatus Gortzia yakutica” sp. nov.—a symbiont from the macronucleus of Paramecium putrinum, the first described HLB for this Paramecium species. The new endosymbiont shows morphological similarities with other HLB. The phylogenetic analysis of the SSU rRNA gene places it into the “Candidatus Gortzia” clade. Full article
(This article belongs to the Special Issue Biodiversity of Ciliates and their Symbionts)
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20 pages, 16654 KiB  
Article
Paramecium Diversity and a New Member of the Paramecium aurelia Species Complex Described from Mexico
by Alexey Potekhin and Rosaura Mayén-Estrada
Diversity 2020, 12(5), 197; https://doi.org/10.3390/d12050197 - 15 May 2020
Cited by 16 | Viewed by 7580
Abstract
Paramecium (Ciliophora) is an ideal model organism to study the biogeography of protists. However, many regions of the world, such as Central America, are still neglected in understanding Paramecium diversity. We combined morphological and molecular approaches to identify paramecia isolated from more than [...] Read more.
Paramecium (Ciliophora) is an ideal model organism to study the biogeography of protists. However, many regions of the world, such as Central America, are still neglected in understanding Paramecium diversity. We combined morphological and molecular approaches to identify paramecia isolated from more than 130 samples collected from different waterbodies in several states of Mexico. We found representatives of six Paramecium morphospecies, including the rare species Paramecium jenningsi, and Paramecium putrinum, which is the first report of this species in tropical regions. We also retrieved five species of the Paramecium aurelia complex, and describe one new member of the complex, Paramecium quindecaurelia n. sp., which appears to be a sister species of Paramecium biaurelia. We discuss criteria currently applied for differentiating between sibling species in Paramecium. Additionally, we detected diverse bacterial symbionts in some of the collected ciliates. Full article
(This article belongs to the Special Issue Biodiversity of Ciliates and their Symbionts)
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