Special Issue "Ciliates as Model Organisms: From ‘omics’ to Genetics, Ecology and Signaling"

A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Environmental Microbiology".

Deadline for manuscript submissions: 30 September 2022 | Viewed by 8836

Special Issue Editors

Prof. Dr. Cristina Miceli
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Guest Editor
School of Biosciences and Veterinary Medicine, University of Camerino, Via Gentile III da Varano, 62032 Camerino, Italy
Interests: cell biology; protistology; genomics
Dr. Adriana Vallesi
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Guest Editor
School of Biosciences and Veterinary Medicine, University of Camerino, 62032 Camerino, Italy
Interests: cell-cell communication; signaling proteins; bioactive molecules; cold-adaptation; oxidative stress; symbiosis; eukaryotic microbiology; ciliates
Dr. Ronald Edward Pearlman
E-Mail Website
Guest Editor
Department of Biology, York University, 4700 Keele Street, Toronto, ON M3J 1P3, Canada
Interests: molecular biology; cell biology; genetics; biochemistry; genomics; proteomics; chromatin; epigenetics; gene expression; ciliates

Special Issue Information

Dear Colleagues,

Ciliates represent a group of unicellular eukaryotes widespread in nature, living in aquatic habitats, in soil, and as symbionts of animals. They are adapted to different conditions; from very cold to hot temperatures, and from clean to polluted environments, and possess complex molecular systems for many processes such as ciliary beating, for self-/non-self-recognition, sexual phenomena, and predator–prey interactions. To effect these processes, ciliates are able to manage different signals which can be classified in three categories: (i) intercellular signals produced by other cells/organisms; (ii) environmental signals not produced by other organisms; and (iii) intracellular signals produced inside the cell body.

Ciliates are nuclear dimorphic, with two types of genome in a common cytoplasm. The diploid small germline micronucleus (MIC) is mostly transcriptionally silent and the repository of genetic information. The polyploid large somatic macronucleus (MAC) is responsible for gene transcription during cell growth. In the last 15 years, MAC genomes of many species have been investigated and disclosed, and the MIC genomes of a selected group of species are also under investigation. Comparative genomics, together with the analysis of transcriptomic and proteomic data, provides essential information to understand genetics, cell biology, and ecology of ciliates. Unraveling signaling systems in ciliates can provide important knowledge for understanding similar systems in other eukaryotes, including multicellular organisms. For example, ciliates are very useful biological models to study processes such as the evolution of calcium signaling. In addition, the hippo-signaling pathway, known to control the size of organs in animals, has been demonstrated to control cell polarity in ciliates and to specify the relative dimensions of the anterior and posterior daughter cells during division. Protein pheromones, which control self-/non-self-recognition and mating in ciliates, are considered the evolutionary precursors of animal growth factors.

This Special Issue is open to reporting all studies on ciliates as model organisms, seeking to understand their genetics, cell biology, biochemistry, evolution, ecological adaptation, and the complex mechanisms of signaling systems, from the genes involved to the changes in gene expression during cell response, and from the structure and involved evolution of signal molecules to the membrane traffic in the cells.

We look forward to receiving your contributions.

Prof. Dr. Cristina Miceli
Prof. Dr. Adriana Vallesi
Dr. Ronald Edward Pearlman
Guest Editors

Manuscript Submission Information

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Published Papers (8 papers)

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Research

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Article
Primary Structure and Coding Genes of Two Pheromones from the Antarctic Psychrophilic Ciliate, Euplotes focardii
Microorganisms 2022, 10(6), 1089; https://doi.org/10.3390/microorganisms10061089 - 25 May 2022
Viewed by 317
Abstract
In ciliates, diffusible cell type-specific pheromones regulate cell growth and mating phenomena acting competitively in both autocrine and heterologous fashion. In Euplotes species, these signaling molecules are represented by species-specific families of structurally homologous small, disulfide-rich proteins, each specified by one of a [...] Read more.
In ciliates, diffusible cell type-specific pheromones regulate cell growth and mating phenomena acting competitively in both autocrine and heterologous fashion. In Euplotes species, these signaling molecules are represented by species-specific families of structurally homologous small, disulfide-rich proteins, each specified by one of a series of multiple alleles that are inherited without relationships of dominance at the mat-genetic locus of the germinal micronuclear genome, and expressed as individual gene-sized molecules in the somatic macronuclear genome. Here we report the 85-amino acid sequences and the full-length macronuclear nucleotide coding sequences of two pheromones, designated Ef-1 and Ef-2, isolated from the supernatant of a wild-type strain of a psychrophilic species of Euplotes, E. focardii, endemic to Antarctic coastal waters. An overall comparison of the determined E. focardii pheromone and pheromone-gene structures with their homologs from congeneric species provides an initial picture of how an evolutionary increase in the complexity of these structures accompanies Euplotes speciation. Full article
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Article
Cryptic Diversity in Paramecium multimicronucleatum Revealed with a Polyphasic Approach
Microorganisms 2022, 10(5), 974; https://doi.org/10.3390/microorganisms10050974 - 05 May 2022
Viewed by 408
Abstract
Paramecium (Ciliophora) systematics is well studied, and about twenty morphological species have been described. The morphological species may include several genetic species. However, molecular phylogenetic analyses revealed that the species diversity within Paramecium could be even higher and has raised a problem of [...] Read more.
Paramecium (Ciliophora) systematics is well studied, and about twenty morphological species have been described. The morphological species may include several genetic species. However, molecular phylogenetic analyses revealed that the species diversity within Paramecium could be even higher and has raised a problem of cryptic species whose statuses remain uncertain. In the present study, we provide the morphological and molecular characterization of two novel Paramecium species. While Paramecium lynni n. sp., although morphologically similar to P. multimicronucleatum, is phylogenetically well separated from all other Paramecium species, Paramecium fokini n. sp. appears to be a cryptic sister species to P. multimicronucleatum. The latter two species can be distinguished only by molecular methods. The number and structure of micronuclei, traditionally utilized to discriminate species in Paramecium, vary not only between but also within each of the three studied species and, thus, cannot be considered a reliable feature for species identification. The geographic distribution of the P. multimicronucleatum and P. fokini n. sp. strains do not show defined patterns, still leaving space for a role of the geographic factor in initial speciation in Paramecium. Future findings of new Paramecium species can be predicted from the molecular data, while morphological characteristics appear to be unstable and overlapping at least in some species. Full article
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Article
Intraspecies Variation in Tetrahymena rostrata
Microorganisms 2021, 9(10), 2100; https://doi.org/10.3390/microorganisms9102100 - 05 Oct 2021
Viewed by 534
Abstract
Two distinct isolates of the facultative parasite, Tetrahymena rostrata were compared, identifying and utilising markers that are useful for studying clonal variation within the species were identified and utilised. The sequences of mitochondrial genomes and several nuclear genes were determined using Illumina short [...] Read more.
Two distinct isolates of the facultative parasite, Tetrahymena rostrata were compared, identifying and utilising markers that are useful for studying clonal variation within the species were identified and utilised. The sequences of mitochondrial genomes and several nuclear genes were determined using Illumina short read sequencing. The two T. rostrata isolates had similar morphology. The linear mitogenomes had the gene content and organisation typical of the Tetrahymena genus, comprising 8 tRNA genes, 6 ribosomal RNA genes and 45 protein coding sequences (CDS), twenty-two of which had known function. The two isolates had nucleotide identity within common nuclear markers encoded within the histone H3 and H4 and small subunit ribosomal RNA genes and differed by only 2–4 nucleotides in a region of the characterised actin genes. Variation was observed in several mitochondrial genes and was used to determine intraspecies variation and may reflect the natural history of T. rostrata from different hosts or the geographic origins of the isolates. Full article
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Article
Characterization of Simple Sequence Repeats (SSRs) in Ciliated Protists Inferred by Comparative Genomics
Microorganisms 2020, 8(5), 662; https://doi.org/10.3390/microorganisms8050662 - 01 May 2020
Cited by 5 | Viewed by 1350
Abstract
Simple sequence repeats (SSRs) are prevalent in the genomes of all organisms. They are widely used as genetic markers, and are insertion/deletion mutation hotspots, which directly influence genome evolution. However, little is known about such important genomic components in ciliated protists, a large [...] Read more.
Simple sequence repeats (SSRs) are prevalent in the genomes of all organisms. They are widely used as genetic markers, and are insertion/deletion mutation hotspots, which directly influence genome evolution. However, little is known about such important genomic components in ciliated protists, a large group of unicellular eukaryotes with extremely long evolutionary history and genome diversity. With recent publications of multiple ciliate genomes, we start to get a chance to explore perfect SSRs with motif size 1–100 bp and at least three motif repeats in nine species of two ciliate classes, Oligohymenophorea and Spirotrichea. We found that homopolymers are the most prevalent SSRs in these A/T-rich species, with AAA (lysine, charged amino acid; also seen as an SSR with one-adenine motif repeated three times) being the codons repeated at the highest frequencies in coding SSR regions, consistent with the widespread alveolin proteins rich in lysine repeats as found in Tetrahymena. Micronuclear SSRs are universally more abundant than the macronuclear ones of the same motif-size, except for the 8-bp-motif SSRs in extensively fragmented chromosomes. Both the abundance and A/T content of SSRs decrease as motif-size increases, while the abundance is positively correlated with the A/T content of the genome. Also, smaller genomes have lower proportions of coding SSRs out of all SSRs in Paramecium species. This genome-wide and cross-species analysis reveals the high diversity of SSRs and reflects the rapid evolution of these simple repetitive elements in ciliate genomes. Full article
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Article
Comparative Transcriptomics Reveals Distinct Gene Expressions of a Model Ciliated Protozoan Feeding on Bacteria-Free Medium, Digestible, and Digestion-Resistant Bacteria
Microorganisms 2020, 8(4), 559; https://doi.org/10.3390/microorganisms8040559 - 13 Apr 2020
Cited by 2 | Viewed by 1781
Abstract
Bacterivory is an important ecological function of protists in natural ecosystems. However, there are diverse bacterial species resistant to protistan digestion, which reduces the carbon flow to higher trophic levels. So far, a molecular biological view of metabolic processes in heterotrophic protists during [...] Read more.
Bacterivory is an important ecological function of protists in natural ecosystems. However, there are diverse bacterial species resistant to protistan digestion, which reduces the carbon flow to higher trophic levels. So far, a molecular biological view of metabolic processes in heterotrophic protists during predation of bacterial preys of different digestibility is still lacking. In this study, we investigated the growth performance a ciliated protozoan Tetrahymena thermophila cultivated in a bacteria-free Super Proteose Peptone (SPP) medium (control), and in the media mixed with either a digestion-resistant bacterial species (DRB) or a digestible strain of E. coli (ECO). We found the protist population grew fastest in the SPP and slowest in the DRB treatment. Fluorescence in situ hybridization confirmed that there were indeed non-digested, viable bacteria in the ciliate cells fed with DRB, but none in other treatments. Comparative analysis of RNA-seq data showed that, relative to the control, 637 and 511 genes in T. thermophila were significantly and differentially expressed in the DRB and ECO treatments, respectively. The protistan expression of lysosomal proteases (especially papain-like cysteine proteinases), GH18 chitinases, and an isocitrate lyase were upregulated in both bacterial treatments. The genes encoding protease, glycosidase and involving glycolysis, TCA and glyoxylate cycles of carbon metabolic processes were higher expressed in the DRB treatment when compared with the ECO. Nevertheless, the genes for glutathione metabolism were more upregulated in the control than those in both bacterial treatments, regardless of the digestibility of the bacteria. The results of this study indicate that not only bacterial food but also digestibility of bacterial taxa modulate multiple metabolic processes in heterotrophic protists, which contribute to a better understanding of protistan bacterivory and bacteria-protists interactions on a molecular basis. Full article
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Article
Comparative Transcriptome Analyses during the Vegetative Cell Cycle in the Mono-Cellular Organism Pseudokeronopsis erythrina (Alveolata, Ciliophora)
Microorganisms 2020, 8(1), 108; https://doi.org/10.3390/microorganisms8010108 - 12 Jan 2020
Cited by 3 | Viewed by 1458
Abstract
Studies focusing on molecular mechanisms of cell cycles have been lagging in unicellular eukaryotes compared to other groups. Ciliates, a group of unicellular eukaryotes, have complex cell division cycles characterized by multiple events. During their vegetative cell cycle, ciliates undergo macronuclear amitosis, micronuclear [...] Read more.
Studies focusing on molecular mechanisms of cell cycles have been lagging in unicellular eukaryotes compared to other groups. Ciliates, a group of unicellular eukaryotes, have complex cell division cycles characterized by multiple events. During their vegetative cell cycle, ciliates undergo macronuclear amitosis, micronuclear mitosis, stomatogenesis and somatic cortex morphogenesis, and cytokinesis. Herein, we used the hypotrich ciliate Pseudokeronopsis erythrina, whose morphogenesis has been well studied, to examine molecular mechanisms of ciliate vegetative cell cycles. Single-cell transcriptomes of the growth (G) and cell division (D) stages were compared. The results showed that (i) More than 2051 significantly differentially expressed genes (DEGs) were detected, among which 1545 were up-regulated, while 256 were down-regulated at the D stage. Of these, 11 randomly picked DEGs were validated by reverse transcription quantitative polymerase chain reaction (RT-qPCR); (ii) Enriched DEGs during the D stage of the vegetative cell cycle of P. erythrina were involved in development, cortex modifications, and several organelle-related biological processes, showing correspondence of molecular evidence to morphogenetic changes for the first time; (iii) Several individual components of molecular mechanisms of ciliate vegetative division, the sexual cell cycle and cellular regeneration overlap; and (iv) The P. erythrina cell cycle and division have the same essential components as other eukaryotes, including cyclin-dependent kinases (CDKs), cyclins, and genes closely related to cell proliferation, indicating the conserved nature of this biological process. Further studies are needed focusing on detailed inventory and gene interactions that regulate specific ciliated cell-phase events. Full article
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Review

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Review
Experimental Evolution in Tetrahymena
Microorganisms 2022, 10(2), 414; https://doi.org/10.3390/microorganisms10020414 - 11 Feb 2022
Viewed by 495
Abstract
Experimental evolution has provided novel insight into a wide array of biological processes. Species in the genus Tetrahymena are proving to be a highly useful system for studying a range of questions using experimental evolution. Their unusual genomic architecture, diversity of life history [...] Read more.
Experimental evolution has provided novel insight into a wide array of biological processes. Species in the genus Tetrahymena are proving to be a highly useful system for studying a range of questions using experimental evolution. Their unusual genomic architecture, diversity of life history traits, importance as both predator and prey, and amenability to laboratory culture allow them to be studied in a variety of contexts. In this paper, we review what we are learning from experimental evolution with Tetrahymena about mutation, adaptation, and eco-evolutionary dynamics. We predict that future experimental evolution studies using Tetrahyemena will continue to shed new light on these processes. Full article
Review
Natural Function and Structural Modification of Climacostol, a Ciliate Secondary Metabolite
Microorganisms 2020, 8(6), 809; https://doi.org/10.3390/microorganisms8060809 - 27 May 2020
Cited by 1 | Viewed by 1087
Abstract
The review highlights the main results of two decades of research on climacostol (5-[(2Z)-non-2-en-1-yl]benzene-1,3-diol), the resorcinolic lipid produced and used by the ciliated protozoan Climacostomum virens for chemical defense against a wide range of predators, and to assist its carnivorous feeding. [...] Read more.
The review highlights the main results of two decades of research on climacostol (5-[(2Z)-non-2-en-1-yl]benzene-1,3-diol), the resorcinolic lipid produced and used by the ciliated protozoan Climacostomum virens for chemical defense against a wide range of predators, and to assist its carnivorous feeding. After the first studies on the physiological function of climacostol, the compound and some analogues were chemically synthesized, thus allowing us to explore both its effect on different prokaryotic and eukaryotic biological systems, and the role of its relevant structural traits. In particular, the results obtained in the last 10 years indicate climacostol is an effective antimicrobial and anticancer agent, bringing new clues to the attempt to design and synthesize additional novel analogues that can increase or optimize its pharmacological properties. Full article
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Planned Papers

The below list represents only planned manuscripts. Some of these manuscripts have not been received by the Editorial Office yet. Papers submitted to MDPI journals are subject to peer-review.

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