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: closed (30 November 2022) | Viewed by 42354

Special Issue Editors


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Guest Editor
School of Biosciences and Veterinary Medicine, University of Camerino, Via Gentile III da Varano, 62032 Camerino, Italy
Interests: cold-adaptation; transcriptomics; genomics of eukaryotic microorganisms; gut microbiota interactions; enzyme biotechnology

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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

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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

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Published Papers (17 papers)

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24 pages, 7547 KiB  
Article
Codon Usage Bias Analysis in Macronuclear Genomes of Ciliated Protozoa
by Yu Fu, Fasheng Liang, Congjun Li, Alan Warren, Mann Kyoon Shin and Lifang Li
Microorganisms 2023, 11(7), 1833; https://doi.org/10.3390/microorganisms11071833 - 18 Jul 2023
Cited by 2 | Viewed by 1364
Abstract
Ciliated protozoa (ciliates) are unicellular eukaryotes, several of which are important model organisms for molecular biology research. Analyses of codon usage bias (CUB) of the macronuclear (MAC) genome of ciliates can promote a better understanding of the genetic mode and evolutionary history of [...] Read more.
Ciliated protozoa (ciliates) are unicellular eukaryotes, several of which are important model organisms for molecular biology research. Analyses of codon usage bias (CUB) of the macronuclear (MAC) genome of ciliates can promote a better understanding of the genetic mode and evolutionary history of these organisms and help optimize codons to improve gene editing efficiency in model ciliates. In this study, the following indices were calculated: the guanine-cytosine (GC) content, the frequency of the nucleotides at the third position of codons (T3, C3, A3, G3), the effective number of codons (ENc), GC content at the 3rd position of synonymous codons (GC3s), and the relative synonymous codon usage (RSCU). Parity rule 2 plot analysis, Neutrality plot analysis, ENc plot analysis, and correlation analysis were employed to explore the main influencing factors of CUB. The results showed that the GC content in the MAC genomes of each of 21 ciliate species, the genomes of which were relatively complete, was lower than 50%, and the base compositions of GC and GC3s were markedly distinct. Synonymous codon analysis revealed that the codons in most of the 21 ciliates ended with A or T and four codons were the general putative optimal codons. Collectively, our results indicated that most of the ciliates investigated preferred using the codons with anof AT-ending and that codon usage bias was affected by gene mutation and natural selection. Full article
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18 pages, 2479 KiB  
Article
Developmentally Programmed Switches in DNA Replication: Gene Amplification and Genome-Wide Endoreplication in Tetrahymena
by Xiangzhou Meng, Hung Quang Dang and Geoffrey M. Kapler
Microorganisms 2023, 11(2), 491; https://doi.org/10.3390/microorganisms11020491 - 16 Feb 2023
Cited by 2 | Viewed by 1652
Abstract
Locus-specific gene amplification and genome-wide endoreplication generate the elevated copy number of ribosomal DNA (rDNA, 9000 C) and non-rDNA (90 C) chromosomes in the developing macronucleus of Tetrahymena thermophila. Subsequently, all macronuclear chromosomes replicate once per cell cycle during vegetative growth. Here, [...] Read more.
Locus-specific gene amplification and genome-wide endoreplication generate the elevated copy number of ribosomal DNA (rDNA, 9000 C) and non-rDNA (90 C) chromosomes in the developing macronucleus of Tetrahymena thermophila. Subsequently, all macronuclear chromosomes replicate once per cell cycle during vegetative growth. Here, we describe an unanticipated, programmed switch in the regulation of replication initiation in the rDNA minichromosome. Early in development, the 21 kb rDNA minichromosome is preferentially amplified from 2 C to ~800 C from well-defined origins, concurrent with genome-wide endoreplication (2 C to 8–16 C) in starved mating Tetrahymena (endoreplication (ER) Phase 1). Upon refeeding, rDNA and non-rDNA chromosomes achieve their final copy number through resumption of just the endoreplication program (ER Phase 2). Unconventional rDNA replication intermediates are generated primarily during ER phase 2, consistent with delocalized replication initiation and possible formation of persistent RNA-DNA hybrids. Origin usage and replication fork elongation are affected in non-rDNA chromosomes as well. Despite the developmentally programmed 10-fold reduction in the ubiquitous eukaryotic initiator, the Origin Recognition Complex (ORC), active initiation sites are more closely spaced in ER phases 1 and 2 compared to vegetative growing cells. We propose that initiation site selection is relaxed in endoreplicating macronuclear chromosomes and may be less dependent on ORC. Full article
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14 pages, 1608 KiB  
Article
The Conjusome—A Transient Organelle Linking Genome Rearrangements in the Parental and Developing Macronuclei
by Christopher Janetopoulos and Karl J. Aufderheide
Microorganisms 2023, 11(2), 418; https://doi.org/10.3390/microorganisms11020418 - 7 Feb 2023
Viewed by 1569
Abstract
The conjusome plays an important role in the conjugation events that occur in Tetrahymena thermophila. The conjusome appears in the anterior of conjugant pairs during the early stages of new macronuclei (anlagen) development. It lacks a membrane, and is composed of a [...] Read more.
The conjusome plays an important role in the conjugation events that occur in Tetrahymena thermophila. The conjusome appears in the anterior of conjugant pairs during the early stages of new macronuclei (anlagen) development. It lacks a membrane, and is composed of a network of fibrous, electron dense material, containing background cytoplasm and ribosomes. Several proteins localize to this organelle, including Pdd1p, a chromodomain protein that participates in the formation of chromatin-containing structures in developing macronuclear anlagen, and is associated with the elimination of specific germ-line sequences from developing macronuclei. Conjugants lacking the PDD1 allele in the parental macronucleus do not show Pdd1p antibody staining in conjusomes. Investigations were performed using mutant cell lines, uniparental cytogamy and drug treatment, and show that the conjusome appears to be dependent on parental macronuclei condensation, and is a transitory organelle that traffics nuclear determinants from the parental macronucleus to the developing anlagen. These data, taken together with Pdd1p knockout experiments, suggest the conjusome is involved in the epigenetic phenomena that occur during conjugation and sexual reorganization. This is likely a conserved organelle. Conjusome-like structures were also observed in another Ciliate, Stylonichia. In general, conjusomes have features that resemble germ line P-granules. Full article
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21 pages, 3262 KiB  
Article
Exploration of the Nuclear Proteomes in the Ciliate Oxytricha trifallax
by Michael W. Lu, Leslie Y. Beh, V. Talya Yerlici, Wenwen Fang, Katarzyna Kulej, Benjamin A. Garcia and Laura F. Landweber
Microorganisms 2023, 11(2), 343; https://doi.org/10.3390/microorganisms11020343 - 30 Jan 2023
Viewed by 1785
Abstract
Nuclear dimorphism is a fundamental feature of ciliated protozoa, which have separate somatic and germline genomes in two distinct organelles within a single cell. The transcriptionally active somatic genome, contained within the physically larger macronucleus, is both structurally and functionally different from the [...] Read more.
Nuclear dimorphism is a fundamental feature of ciliated protozoa, which have separate somatic and germline genomes in two distinct organelles within a single cell. The transcriptionally active somatic genome, contained within the physically larger macronucleus, is both structurally and functionally different from the silent germline genome housed in the smaller micronucleus. This difference in genome architecture is particularly exaggerated in Oxytricha trifallax, in which the somatic genome comprises tens of thousands of gene-sized nanochromosomes maintained at a high and variable ploidy, while the germline has a diploid set of megabase-scale chromosomes. To examine the compositional differences between the nuclear structures housing the genomes, we performed a proteomic survey of both types of nuclei and of macronuclear histones using quantitative mass spectrometry. We note distinct differences between the somatic and germline nuclei, with many functional proteins being highly enriched in one of the two nuclei. To validate our conclusions and the efficacy of nuclear separation, we used protein localization through a combination of transformations and immunofluorescence. We also note that the macronuclear histones strikingly display only activating marks, consistent with the conclusion that the macronucleus is the hub of transcription. These observations suggest that the compartmentalization of different genome features into separate structures has been accompanied by a similar specialization of nuclear components that maintain and facilitate the functions of the genomes specific to each nucleus. Full article
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12 pages, 2225 KiB  
Article
Possible Third Step Preventing Conjugation between Different Species of Blepharisma
by Ayu Sugino, Mayumi Kobayashi, Mayumi Sugiura and Terue Harumoto
Microorganisms 2023, 11(1), 188; https://doi.org/10.3390/microorganisms11010188 - 12 Jan 2023
Cited by 1 | Viewed by 1456
Abstract
In the genus Blepharisma, reproductive isolation between different species appears to be established at least by two barriers: (1) a mating pheromone, i.e., gamone 1, and (2) a factor involved in pair formation. Using four species, we experimentally investigated other potential barriers [...] Read more.
In the genus Blepharisma, reproductive isolation between different species appears to be established at least by two barriers: (1) a mating pheromone, i.e., gamone 1, and (2) a factor involved in pair formation. Using four species, we experimentally investigated other potential barriers to interspecific conjugation in Blepharisma, as well as the first and second barriers. Cell-free fluid from type I cells (CFF1) of B. americanum had no effect on B. undulans, B. japonicum, or B. stoltei. Type II cells of B. americanum responded to CFF1 from B. americanum but not to CFF1 from B. undulans, B. japonicum, or B. stoltei. Gamone 1, therefore, seems to be the first reproductive barrier (with the inclusion of B. americanum species [megakaryotype 3]) as reported previously. In pretreated cells with complementary gamones in B. undulans and B. americanum, inter-species pair formation was rare, but pair formation between B. americanum and B. japonicum and between B. americanum and B. stoltei occurred at relatively high frequency. Most of the inter-species B. americanumB. stoltei pairs underwent nuclear changes specific to conjugation. No significant difference was observed between the intra- and inter-species pairs over the time course of the nuclear changes, but the percentage of abnormal cells was higher in inter-species pairs than in intra-species pairs, and no progenies were produced by inter-species pairs. These results suggest a third barrier or step, in addition to the first and second ones, in nuclear changes after pair formation that prevents interspecific conjugation in Blepharisma. Full article
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15 pages, 2791 KiB  
Article
Changes in Phylogenetic and Functional Diversity of Ciliates along the Course of a Mediterranean Karstic River
by Vesna Gulin Beljak, Antonija Kulaš, Guillaume Lentendu, Barbara Vlaičević, Marija Gligora Udovič, Mirela Sertić Perić, Fran Rebrina, Petar Žutinić, Sandi Orlić and Renata Matoničkin Kepčija
Microorganisms 2022, 10(12), 2493; https://doi.org/10.3390/microorganisms10122493 - 16 Dec 2022
Cited by 1 | Viewed by 1928
Abstract
Ciliates are a group of phagotrophic protists found in a wide variety of ecosystems. This study builds on recent studies of ciliates in the Krka river and investigates changes in the phylogenetic and functional diversity of ciliates in biofilm to predict the phylogenetic [...] Read more.
Ciliates are a group of phagotrophic protists found in a wide variety of ecosystems. This study builds on recent studies of ciliates in the Krka river and investigates changes in the phylogenetic and functional diversity of ciliates in biofilm to predict the phylogenetic and functional structure of ciliates in other karstic rivers. Biofilm samples were collected from four representative locations: upstream (Krka spring), midstream (Marasovine), and downstream (Roški slap, Skradinski buk) of the Krka river to test for differences in phylogenetic and functional diversity of ciliates in relation to location and positioning on tufa stones (light/dark-exposed side of tufa stone). Our results showed that Krka spring had higher phylogenetic species variability, lower phylogenetic diversity, and lower functional richness than Skradinski buk, suggesting phylogenetic overdispersal at Krka spring. This could be due to environmental filtering, competitive exclusion, or a combination of these factors. As the first study of its kind in the Mediterranean, our results shed light on the phylogenetic and functional diversity of ciliates in karst ecosystems and provide a basis for future ecological and conservation efforts. Full article
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18 pages, 4294 KiB  
Article
Snf2 Proteins Are Required to Generate Gamete Pronuclei in Tetrahymena thermophila
by Yasuhiro Fukuda, Takahiko Akematsu, Hironori Bando and Kentaro Kato
Microorganisms 2022, 10(12), 2426; https://doi.org/10.3390/microorganisms10122426 - 7 Dec 2022
Viewed by 2504
Abstract
During sexual reproduction/conjugation of the ciliate Tetrahymena thermophila, the germinal micronucleus undergoes meiosis resulting in four haploid micronuclei (hMICs). All hMICs undergo post-meiotic DNA double-strand break (PM-DSB) formation, cleaving their genome. DNA lesions are subsequently repaired in only one ‘selected’ hMIC, which eventually [...] Read more.
During sexual reproduction/conjugation of the ciliate Tetrahymena thermophila, the germinal micronucleus undergoes meiosis resulting in four haploid micronuclei (hMICs). All hMICs undergo post-meiotic DNA double-strand break (PM-DSB) formation, cleaving their genome. DNA lesions are subsequently repaired in only one ‘selected’ hMIC, which eventually produces gametic pronuclei. DNA repair in the selected hMIC involves chromatin remodeling by switching from the heterochromatic to the euchromatic state of its genome. Here, we demonstrate that, among the 15 Tetrahymena Snf2 family proteins, a core of the ATP-dependent chromatin remodeling complex in Tetrahymena, the germline nucleus specific Iswi in Tetrahymena IswiGTt and Rad5Tt is crucial for the generation of gametic pronuclei. In either gene knockout, the selected hMIC which shows euchromatin markers such as lysine-acetylated histone H3 does not appear, but all hMICs in which markers for DNA lesions persist are degraded, indicating that both IswiGTt and Rad5Tt have important roles in repairing PM-DSB DNA lesions and remodeling chromatin for the euchromatic state in the selected hMIC. Full article
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13 pages, 1593 KiB  
Article
Ciliate Microtubule Diversities: Insights from the EFBTU3 Tubulin in the Antarctic Ciliate Euplotes focardii
by Sandra Pucciarelli, Daniela Sparvoli, Patrizia Ballarini, Angela Piersanti, Matteo Mozzicafreddo, Lucia Arregui and Cristina Miceli
Microorganisms 2022, 10(12), 2415; https://doi.org/10.3390/microorganisms10122415 - 6 Dec 2022
Viewed by 2047
Abstract
Protozoans of the Phylum Ciliophora (ciliates) assemble many diverse microtubular structures in a single cell throughout the life cycle, a feature that made them useful models to study microtubule complexity and the role of tubulin isotypes. In the Antarctic ciliate Euplotes focardii we identified [...] Read more.
Protozoans of the Phylum Ciliophora (ciliates) assemble many diverse microtubular structures in a single cell throughout the life cycle, a feature that made them useful models to study microtubule complexity and the role of tubulin isotypes. In the Antarctic ciliate Euplotes focardii we identified five β-tubulin isotypes by genome sequencing, named EFBTU1, EFBTU2, EFBTU3, EFBTU4 and EFBTU5. By using polyclonal antibodies directed against EFBTU2/EFBTU1 and EFBTU3, we show that the former isotypes appear to be involved in the formation of all microtubular structures and are particularly abundant in cilia, whereas the latter specifically localizes at the bases of cilia. By RNA interference (RNAi) technology, we silenced the EFBTU3 gene and provided evidence that this isotype has a relevant role in cilia regeneration upon deciliation and in cell division. These results support the long-standing concept that tubulin isotypes possess functional specificity in building diverse microtubular structures. Full article
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11 pages, 2300 KiB  
Article
Primary Structure and Coding Genes of Two Pheromones from the Antarctic Psychrophilic Ciliate, Euplotes focardii
by Claudio Alimenti, Annalisa Candelori, Yaohan Jiang, Pierangelo Luporini and Adriana Vallesi
Microorganisms 2022, 10(6), 1089; https://doi.org/10.3390/microorganisms10061089 - 25 May 2022
Cited by 1 | Viewed by 1727
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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25 pages, 7944 KiB  
Article
Cryptic Diversity in Paramecium multimicronucleatum Revealed with a Polyphasic Approach
by Maksim Melekhin, Yulia Yakovleva, Natalia Lebedeva, Irina Nekrasova, Liubov Nikitashina, Michele Castelli, Rosaura Mayén-Estrada, Anna E. Romanovich, Giulio Petroni and Alexey Potekhin
Microorganisms 2022, 10(5), 974; https://doi.org/10.3390/microorganisms10050974 - 5 May 2022
Cited by 9 | Viewed by 2810
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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12 pages, 1772 KiB  
Article
Intraspecies Variation in Tetrahymena rostrata
by Anne Watt, Neil Young, Ruth Haites, Kerry Dunse, Derek Russell and Helen Billman-Jacobe
Microorganisms 2021, 9(10), 2100; https://doi.org/10.3390/microorganisms9102100 - 5 Oct 2021
Cited by 2 | Viewed by 1768
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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13 pages, 2202 KiB  
Article
Characterization of Simple Sequence Repeats (SSRs) in Ciliated Protists Inferred by Comparative Genomics
by Yuan Li, Xiao Chen, Kun Wu, Jiao Pan, Hongan Long and Ying Yan
Microorganisms 2020, 8(5), 662; https://doi.org/10.3390/microorganisms8050662 - 1 May 2020
Cited by 8 | Viewed by 3038
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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21 pages, 5546 KiB  
Article
Comparative Transcriptomics Reveals Distinct Gene Expressions of a Model Ciliated Protozoan Feeding on Bacteria-Free Medium, Digestible, and Digestion-Resistant Bacteria
by Songbao Zou, Qianqian Zhang and Jun Gong
Microorganisms 2020, 8(4), 559; https://doi.org/10.3390/microorganisms8040559 - 13 Apr 2020
Cited by 8 | Viewed by 4362
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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17 pages, 4879 KiB  
Article
Comparative Transcriptome Analyses during the Vegetative Cell Cycle in the Mono-Cellular Organism Pseudokeronopsis erythrina (Alveolata, Ciliophora)
by Yiwei Xu, Zhuo Shen, Eleni Gentekaki, Jiahui Xu and Zhenzhen Yi
Microorganisms 2020, 8(1), 108; https://doi.org/10.3390/microorganisms8010108 - 12 Jan 2020
Cited by 8 | Viewed by 3213
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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14 pages, 1236 KiB  
Review
Ciliate Morpho-Taxonomy and Practical Considerations before Deploying Metabarcoding to Ciliate Community Diversity Surveys in Urban Receiving Waters
by Yan Zhao and Gaytha A. Langlois
Microorganisms 2022, 10(12), 2512; https://doi.org/10.3390/microorganisms10122512 - 19 Dec 2022
Cited by 1 | Viewed by 1987
Abstract
Disentangling biodiversity and community assembly effects on ecosystem function has always been an important topic in ecological research. The development and application of a DNA metabarcoding method has fundamentally changed the way we describe prokaryotic communities and estimate biodiversity. Compared to prokaryotes (bacteria [...] Read more.
Disentangling biodiversity and community assembly effects on ecosystem function has always been an important topic in ecological research. The development and application of a DNA metabarcoding method has fundamentally changed the way we describe prokaryotic communities and estimate biodiversity. Compared to prokaryotes (bacteria and archaea), the eukaryotic microbes (unicellular eukaryotes) also fulfill extremely important ecological functions in different ecosystems regarding their intermediate trophic positions. For instance, ciliated microbes (accounting for a substantial portion of the diversity of unicellular eukaryotes) perform pivotal roles in microbial loops and are essential components in different ecosystems, especially in water purification processes. Therefore, the community composition of ciliated species has been widely utilized as a proxy for water quality and biological assessment in urban river ecosystems and WWTPs (wastewater treatment plants). Unfortunately, investigating the dynamic changes and compositions in ciliate communities relies heavily on existing morpho-taxonomical descriptions, which is limited by traditional microscopic approaches. To deal with this dilemma, we discuss the DNA-based taxonomy of ciliates, the relative merits and challenges of deploying its application using DNA metabarcoding for surveys of ciliate community diversity in urban waterbodies, and provide suggestions for minimizing relevant sources of biases in its implementation. We expect that DNA metabarcoding could untangle relationships between community assembly and environmental changes affecting ciliate communities. These analyses and discussions could offer a replicable method in support of the application of evaluating communities of ciliated protozoa as indicators of urban freshwater ecosystems. Full article
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11 pages, 271 KiB  
Review
Experimental Evolution in Tetrahymena
by Karissa Plum, Jason Tarkington and Rebecca A. Zufall
Microorganisms 2022, 10(2), 414; https://doi.org/10.3390/microorganisms10020414 - 11 Feb 2022
Cited by 2 | Viewed by 2163
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
13 pages, 3835 KiB  
Review
Natural Function and Structural Modification of Climacostol, a Ciliate Secondary Metabolite
by Federico Buonanno, Elisabetta Catalani, Davide Cervia, Cristina Cimarelli, Enrico Marcantoni and Claudio Ortenzi
Microorganisms 2020, 8(6), 809; https://doi.org/10.3390/microorganisms8060809 - 27 May 2020
Cited by 4 | Viewed by 2800
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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