Evolution of Germline-Limited Sequences in Two Populations of the Ciliate Chilodonella uncinata

Zufall, Rebecca A.; Sturm, Mariel; Mahon, Brian C.

doi:10.1007/s00239-012-9493-4

Cited by 6 publications

(7 citation statements)

References 33 publications

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“…The considerable heterogeneity in Oxytricha IES boundaries and “unscrambling” of a large subset of them [56], together with the observation of pronounced developmental upregulation of numerous additional MAC- and MIC-encoded transposases raises the possibility that additional transposases other than those of TBEs could also be involved in IES excision [39, 56]. Knowledge of IESs in other ciliates is sparse (primarily confined to the phyllopharyngean Chilodonella uncinata [80, 81]), and, as far as we are aware, no specific IES excisases have been proposed for them.…”

Section: Discussionmentioning

confidence: 99%

“…The considerable heterogeneity in Oxytricha IES boundaries and "unscrambling" of a large subset of them [56], together with the observation of pronounced developmental upregulation of numerous additional MAC-and MIC-encoded transposases raises the possibility that additional transposases other than those of TBEs could also be involved in IES excision [39,56]. Knowledge of IESs in other ciliates is sparse (primarily confined to the phyllopharyngean Chilodonella uncinata [80,81]), and, as far as we are aware, no specific IES excisases have been proposed for them. In Paramecium, since the discovery of multiple PiggyBac homologs (PiggyMac-likes), there have been questions about their role, since, aside from PiggyMac, they all have incomplete catalytic triads, and are thus likely catalytically inactive, but nevertheless their gene knockdowns lead to pronounced IES retention [55].…”

Section: Blepharismamentioning

confidence: 99%

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Genome editing excisase origins illuminated by somatic genome of Blepharisma

Singh

Seah

Emmerich

et al. 2021

Preprint

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The germ-soma distinction is a defining feature of multicellular eukaryotes. Analogous to this, ciliates, a ubiquitous microbial eukaryote lineage, have morphologically and functionally distinct nuclei, but within single cells: the germline micronucleus (MIC) and somatic macronucleus (MAC). The origins and mechanisms of the MIC to MAC transformation, especially the extensive elimination of abundant internally eliminated sequences (IESs) and transposons during genome reorganization, are great biological mysteries. Blepharisma represents one of the two earliest diverging ciliate classes, and has unique, dual pathways of MAC development, making it ideal for investigating the functioning, origins and evolution of these processes. Here, we report the MAC genome assembly of Blepharisma stoltei strain ATCC 30299 (41 Mb), arranged as numerous alternative telomere-capped minichromosomes, tens to hundreds of kilobases long. The B. stoltei MAC genome encodes eight PiggyBac transposase homologs liberated from transposons. All are subject to purifying selection, but just one, the putative Blepharisma IES excisase, has a complete catalytic amino acid triad. Numerous genes encoding other domesticated transposases are present in B. stoltei, and often are comparably strongly upregulated in a similar timeframe to model ciliate genome reorganization homologs. Our phylogenetic investigations suggest the PiggyBac homologs may have been ancestral ciliate IES excisases. The B. stoltei MAC genome, together with the upcoming MIC genome, highlights the evolution and complex interplay between transposons, domesticated transposases, and genome reorganization in the context of germline-soma differentiation within single cells.

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Section: Discussionmentioning

confidence: 99%

Section: Blepharismamentioning

confidence: 99%

Genome editing excisase origins illuminated by somatic genome of Blepharisma

Singh

Seah

Emmerich

et al. 2021

Preprint

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“…The macronucleus contains gene‐sized chromosomes and has similar function to somatic nuclei of animals (Riley & Katz ; Bellec & Katz ; Zufall et al . ). The macronucleus formation occurs through a comprehensive rearrangement, including genome fragmentation, amplification and elimination of micronuclear‐limited sequences (Prescott ; Juranek & Lipps ; Bellec & Katz ).…”

Section: Chilodonella Spp Morphology and Genetic Characteristicsmentioning

confidence: 97%

“…Most Chilodonella species have been characterized on potentially plastic morphological features. Recent genetic analyses of nuclear small subunit ribosomal DNA (rDNA) and mitochondrial SSU (mtSSU) rDNA of C. uncinata collected from the environment have shown that significant cryptic species diversity exists in North America (Riley & Katz ; Bellec & Katz ; Zufall, Sturm & Mahon ). This genetic variation appears to be a common feature within other Chilodonella species, suggesting there is significant cryptic diversity yet to be characterized (Katz et al .…”

Section: Chilodonella Spp Morphology and Genetic Characteristicsmentioning

confidence: 99%

“…Each chilodonellid cell contains an inactive micronucleus and a macronucleus responsible for gene expression (generative diploid micronuclei and vegetative polyploidy macronuclei) (Riley & Katz 2001;Bellec & Katz 2012). The macronucleus contains gene-sized chromosomes and has similar function to somatic nuclei of animals (Riley & Katz 2001;Bellec & Katz 2012;Zufall et al 2012). The macronucleus formation occurs through a comprehensive rearrangement, including genome fragmentation, amplifi cation and elimination of micronuclear-limited sequences (Prescott 1994;Juranek & Lipps 2007;Bellec & Katz 2012).…”

Section: Introductionmentioning

confidence: 99%

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Current status of parasitic ciliates Chilodonella spp. (Phyllopharyngea: Chilodonellidae) in freshwater fish aquaculture

Gomes

Jerry

Miller

et al. 2016

Journal of Fish Diseases

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Freshwater fish farming contributes to more than two-thirds of global aquaculture production. Parasitic ciliates are one of the largest causes of production loss in freshwater farmed fishes, with species from the genus Chilodonella being particularly problematic. While Chilodonella spp. include 'free-living' fauna, some species are involved in mortality events of fish, particularly in high-density aquaculture. Indeed, chilodonellosis causes major productivity losses in over 16 species of farmed freshwater fishes in more than 14 countries. Traditionally, Chilodonella species are identified based on morphological features; however, the genus comprises yet uncharacterized cryptic species, which indicates the necessity for molecular diagnostic methods. This review synthesizes current knowledge on the biology, ecology and geographic distribution of harmful Chilodonella spp. and examines pathological signs, diagnostic methods and treatments. Recent advances in molecular diagnostics and the ability to culture Chilodonella spp. in vitro will enable the development of preventative management practices and sustained freshwater fish aquaculture production.

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A paradox: rapid evolution rates of germline-limited sequences are associated with conserved patterns of rearrangements in cryptic species of Chilodonella uncinata (Protista, Ciliophora)

Zhang

Wang

Katz

et al. 2018

Sci. China Life Sci.

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Some of the most extreme genome wide rearrangements are found in ciliates, which are unique in possessing both germline micronucleus and somatic macronucleus in every cell/organism. A series of DNA rearrangement events, including DNA elimination, chromosomal fragmentation, gene unscrambling and alternative processing, happen during macronuclear development. To assess the molecular evolution of macronuclear and germline-limited sequences in different cryptic species of Chilodonella uncinata, we characterized the actin, α-tubulin and β-tubulin genes in the micronucleus and macronucleus genomes of USA-SC2 strain and compared them with other strains (i.e. cryptic species). Three main results are: (i) rearrangement patterns between germline and soma are conserved for each gene among the cryptic species of C. uncinata; (ii) in contrast, the germline-limited regions are highly divergent in sequence and length among the cryptic species; (iii) pointer shifting is frequent among the cryptic species. We speculate that pointer sequences may serve as the buffer between the conserved macronuclear destined sequences and rapidly-evolving internal eliminated sequences. The data combined with previous studies demonstrate the plasticity of gene rearrangement among different groups of ciliates and add to the growing data for the role of genome rearrangements in species differentiation.

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Evolution of Germline-Limited Sequences in Two Populations of the Ciliate Chilodonella uncinata

Cited by 6 publications

References 33 publications

Genome editing excisase origins illuminated by somatic genome of Blepharisma

Genome editing excisase origins illuminated by somatic genome of Blepharisma

Current status of parasitic ciliates Chilodonella spp. (Phyllopharyngea: Chilodonellidae) in freshwater fish aquaculture

A paradox: rapid evolution rates of germline-limited sequences are associated with conserved patterns of rearrangements in cryptic species of Chilodonella uncinata (Protista, Ciliophora)

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