The Vegetative Micronucleus has a Critical Role in Maintenance of Cortical Structure in Tetrahymena thermophila.

Haremaki, Tomomi; Sugai, Toshiro; Takahashi, Mihoko

doi:10.1247/csf.20.239

Cited by 15 publications

(6 citation statements)

References 18 publications

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“…We observed that some exconjugant cells of the arrest inducing strain (both doublets and singlets) become amicronucleate. These amicronucleate cells lost their oral structures and CVPs, which is consistent with the studies of Haremaki, Sugai and Takehashi (1995, 1996), who showed that the loss of oral structures in amicronucleate cells depends upon the transcriptional and translational activity of their macronuclei and suggested that this activity is negatively controlled by the micronucleus. So far, however, somatic micronuclear DNA transcription has never been found.…”

Section: Discussionsupporting

confidence: 91%

Isolation of a Tetrahymena thermophila Strain which Induced Metaphase I Meiotic Arrest: New Pathway of Abortive Conjugation

Kaczanowski

Kiersnowska

Kaczanowska

2004

J Eukaryotic Microbiology

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A hypodiploid strain of Tetrahymena thermophila has been obtained that shows arrest at the stage of condensed nuclei, corresponding to metaphase I of normal conjugants and induced arrest at meiotic metaphase I (i.e. at the stage of condensed, bivalent chromosomes) in its wt partner mate. The metaphase I arrested conjugants retained their old macronuclei and most of them underwent cell fusion, instead of separation of exconjugants. The doublets were viable and cortically integrated. When the arrest inducing strain was crossed to the haploid tester strain, the haploid micronuclei were arrested in the meiotic metaphase I as the diploid ones had been; the monovalent, chromosomes were condensed, the arms of sister chromatids were not separated, and they were not segregated. Separation of the arms of sister chromatids and disjunction of bivalent chromosomes were not prerequisite for the formation of microtubular spindles in those cells that were arrested in meiotic metaphase I. After re-feeding, the doublet cells resumed cell divisions, segregating two macronuclei and micronuclei at random. One macronucleus was derived from the arrest inducing strain and the other from the tester strain. Heterokaryon strains with macronuclei derived from the parental arrest inducing strain and with the micronucleus derived from the parental wt tester strain were obtained. Surprisingly, these heterokaryons did not induce meiotic arrest. Thus, the arrest in the melotic metaphase I was induced by the micronucleus and not by the macronucleus of the arrest inducing strain.

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Section: Discussionsupporting

confidence: 91%

Isolation of a Tetrahymena thermophila Strain which Induced Metaphase I Meiotic Arrest: New Pathway of Abortive Conjugation

Kaczanowski

Kiersnowska

Kaczanowska

2004

J Eukaryotic Microbiology

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“…In strains lacking SEP1, 44% of cells lacked a detectable Mic (Fig. 6I and K), which correlates with the high clonal mortality of this strain, as the presence of a Mic is needed for viability (31). In cells lacking SEP2, amicronucleate cells were not seen, but 15% of cells had more than one Mic.…”

Section: Resultsmentioning

confidence: 64%

Septins Stabilize Mitochondria in Tetrahymena thermophila

et al. 2008

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We describe phylogenetic and functional studies of three septins in the free-living ciliate Tetrahymena thermophila. Both deletion and overproduction of septins led to vacuolization of mitochondria, destabilization of the nuclear envelope, and increased autophagy. All three green fluorescent protein-tagged septins localized to mitochondria. Specific septins localized to the outer mitochondrial membrane, to septa formed during mitochondrial scission, or to the mitochondrion-associated endoplasmic reticulum. The only other septins known to localize to mitochondria are human ARTS and murine M-septin, both alternatively spliced forms of Sep4 (S. Larisch, Cell Cycle 3:1021-1023, 2004; S. Takahashi, R. Inatome, H. Yamamura, and S. Yanagi, Genes Cells 8: [81][82][83][84][85][86][87][88][89][90][91][92][93] 2003). It therefore appears that septins have been recruited to mitochondrial functions independently in at least two eukaryotic lineages and in both cases are involved in apoptotic events.Septins are conserved GTP-binding and filament-forming proteins (51). Septins were discovered in Saccharomyces cerevisiae and later found to be ubiquitous in metazoans (39,53). The cellular functions of septins are diverse and include participation in cytokinesis (22, 40), establishment of diffusion barriers for proteins and mRNAs during cell division (16, 75), vesicle trafficking, exocytosis (7,28,33,37), and apoptosis (29,49). Accordingly, cellular localizations of septins are diverse and include the bud neck (14), division furrow (1), presynaptic vesicles (86), dendritic spines (73, 85), and mitochondria (50, 74). Septins interact with microtubules (45, 71) and microfilaments (46, 56) as well as the endoplasmic reticulum (ER) and filaments emanating from the Golgi network (54, 71). Recently, the diverse patterns of septins were classified into types: projections, partitions, and dispersal over whole cells (52). The molecular functions of septins remain unclear (reviewed in reference 81). So far, septins have been studied only for fungi and metazoans. Since septins are known to be involved in cytoskeletal organization and membrane remodeling events, we anticipated that Tetrahymena thermophila septins are involved in partitions of distinct domains in the structurally elaborate cell cortex of ciliates, in particular during cytokinesis, when the cortex undergoes longitudinal segmentation. Surprisingly, we have found that septins of Tetrahymena thermophila localize to mitochondria and regulate mitochondrial dynamics. MATERIALS AND METHODSBioinformatics. Protein sequences of the known septins were obtained from the following databases: Saccharomyces cerevisiae, Schizosaccharomyces pombe, Nannochloris bacillaris, Strongylocentrotus purpuratus, Danio rerio, and human sequences from NCBI (National Center for Biotechnology Information, http: //www.ncbi.nlm.nih.gov/); Drosophila melanogaster sequences from FlyBase (http: //flybase.bio.indiana.edu/); Caenorhabditis elegans sequences from the Sanger Institute (http://www.sanger.ac.uk/Project...

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“…If “pig” and genomic exclusion pathways are shared among tetrahymenas, then new amicronucleates capable of conjugation either die or receive new micronuclei upon first mating, leaving only amicronucleates incapable of conjugation in the population. The hypothesis in Figure 5 suggests that one or more errors during macronuclear development (perhaps epigenetically driven) result both in transfer of essential somatic micronuclear function(s) [1,17] to the macronucleus and in the non-mating phenotype. Subsequently, as the micronucleus accumulates genetic damage [10], it is lost, resulting in an amicronucleate cell.…”

Section: Discussionmentioning

confidence: 99%

“…This includes spontaneous amicronucleates formed in hypodiploid cells [15] as well as those formed by experimental means [1,16]. In both cases oral abnormalities are present, suggesting that the micronucleus has an essential somatic function [1,16,17] even though micronuclear transcription is undetected except at conjugation. Wild Tetrahymena amicronucleates are unable to form conjugating pairs despite the fact that mating type expression is a macronuclear, not micronuclear, function.…”

Section: Introductionmentioning

confidence: 99%

Abandoning sex: multiple origins of asexuality in the ciliate Tetrahymena

Doerder

2014

BMC Evol Biol

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BackgroundBy segregating somatic and germinal functions into large, compound macronuclei and small diploid micronuclei, respectively, ciliates can explore sexuality in ways other eukaryotes cannot. Sex, for instance, is not for reproduction but for nuclear replacement in the two cells temporarily joined in conjugation. With equal contributions from both conjugants, there is no cost of sex which theory predicts should favor asexuality. Yet ciliate asexuality is rare. The exceptional Tetrahymena has abandoned sex through loss of the micronucleus; its amicronucleates are abundant in nature where they reproduce by binary fission but never form conjugating pairs. A possible reason for their abundance is that the Tetrahymena macronucleus does not accumulate mutations as proposed by Muller’s ratchet. As such, Tetrahymena amicronucleates have the potential to be very old. This study used cytochrome oxidase-1 barcodes to determine the phylogenetic origin and relative age of amicronucleates isolated from nature.ResultsAmicronucleates constituted 25% of Tetrahymena-like wild isolates. Of the 244 amicronucleates examined for cox1 barcodes, 237 belonged to Tetrahymena, seven to other genera. Sixty percent originated from 12 named species or barcoded strains, including the model Tetrahymena thermophila, while the remaining 40% represent 19 putative new species, eight of which have micronucleate counterparts and 11 of which are known only as amicronucleates. In some instances, cox1 haplotypes were shared among micronucleate and amicronucleates collected from the same source. Phylogenetic analysis showed that most amicronucleates belong to the “borealis” clade in which mating type is determined by gene rearrangement. Some amicronucleate species were clustered on the SSU phylogenetic tree and had longer branch lengths, indicating more ancient origin.ConclusionsNaturally occurring Tetrahymena amicronucleates have multiple origins, arising from numerous species. Likely many more new species remain to be discovered. Shared haplotypes indicate that some are of contemporary origin, while phylogeny indicates that others may be millions of years old. The apparent success of amicronucleate Tetrahymena may be because macronuclear assortment and recombination allow them to avoid Muller’s ratchet, incorporate beneficial mutations, and evolve independently of sex. The inability of amicronucleates to mate may be the result of error(s) in mating type gene rearrangement.

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The Vegetative Micronucleus has a Critical Role in Maintenance of Cortical Structure in Tetrahymena thermophila.

Cited by 15 publications

References 18 publications

Isolation of a Tetrahymena thermophila Strain which Induced Metaphase I Meiotic Arrest: New Pathway of Abortive Conjugation

Isolation of a Tetrahymena thermophila Strain which Induced Metaphase I Meiotic Arrest: New Pathway of Abortive Conjugation

Septins Stabilize Mitochondria in Tetrahymena thermophila

Abandoning sex: multiple origins of asexuality in the ciliate Tetrahymena

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