Transformation in Tetrahymena thermophila: Development of an inducible phenotype

doi:10.1016/0012-1606(78)90270-1

Developmental Biology

Volume 66, Issue 1, September 1978, Pages 17-31

https://doi.org/10.1016/0012-1606(78)90270-1 Get rights and content

Abstract

Tetrahymena thermophila transforms from a pyriform-shaped trophic form to an elongate rapidly swimming, dispersal form under the appropriate conditions of starvation [Nelsen, E. M., and DeBault, L. E. (1978). J. Protozool. 25, 113–119]. The development and control of the dispersal phenotype are examined. After an initial starvation period, the cell replaces its oral structures. During oral replacement, a caudal cilium emerges at the posterior end of the cell. As oral replacement is completed, the cell becomes spindle shaped and the newly-formed oral membranelles are positioned beneath the surface of the cell with somatic ciliary rows exterior to them. The spindle-shaped cell then elongates to become the dispersal form. While the cell is developing the new oral structures, it is also drastically increasing its numbers of somatic basal bodies and cilia. The events in the transformation pathway may be arrested or reversed by feeding the cell, except that once oral replacement has begun, it is completed along with an associated streamlining of the cell. Refed cells revert to the normal vegetative phenotype, except that some shape changes persist for several hours, suggesting that they are compatible with, but independent of, growth. Blockage of protein synthesis with cycloheximide prevents all changes associated with transformation, including the shape changes and elongation of the caudal cilium. The relation between transformation and conjugation has also been examined. Less transformation takes place when mating is possible, but transformed cells may also mate.

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Plastic cell morphology changes during dispersal
2021, iScience
Citation Excerpt :
This is a distinct example of a transiently emerging morphology that is not present before dispersal behavior is initiated. Caudal cilia do not appear to beat and may serve as a rudder for steering rapid cell motility (Video S1 (Nelsen, 1978)). Caudal cilia have also been detected on other Tetrahymena species and ciliates including Ichthyophthirius, Uronema, Paramecium, and Coleps/Levicoleps (Corliss, 1957; Foissner et al., 2008; Holz and Corliss, 1956; Lu et al., 2016; Nelsen and Debault, 1978; Tamm, 1978; Kozel, 1986).
Dispersal is the movement of organisms from one habitat to another that potentially results in gene flow. It is often plastic, allowing organisms to adjust dispersal movements depending on environmental conditions. A fundamental aim in ecology is to understand the determinants underlying dispersal and its plasticity. We utilized 22 strains of the ciliate Tetrahymena thermophila to determine if different phenotypic dispersal strategies co-exist within a species and which mechanisms underlie this variability. We quantified the cell morphologies impacting cell motility and dispersal. Distinct differences in innate cellular morphology and dispersal rates were detected, but no universally utilized combinations of morphological parameters correlate with dispersal. Rather, multiple distinct and plastic morphological changes impact cilia-dependent motility during dispersal, especially in proficient dispersing strains facing challenging environmental conditions. Combining ecology and cell biology experiments, we show that dispersal can be promoted through plastic motility-associated changes to cell morphology and motile cilia.
From Molecules to Morphology: Cellular Organization of Tetrahymena thermophila
2012, Methods in Cell Biology
Citation Excerpt :
Cells starved for several hours in inorganic medium assemble cilia on generally unciliated somatic BBs, including anterior BBs of the apical crown (Nelsen and Debault, 1978). Moreover, such cells form an exceptionally long cilium (15–20 μm) at the posterior pole of the cell (caudal cilium) as a part of their transformation into the “rapid swimmer” phenotype (Nelsen, 1978; Nelsen and Debault, 1978). Tetrahymena assembles motile cilia with highly conserved 9 + 2 axonemes (Allen, 1968) (Fig. 2C).
Tetrahymena thermophila is both a cell and an organism, which combines great intracellular complexity with a remarkable accessibility to investigation using many different approaches. In this review, we start with a description of the elaborate cortical organization of the Tetrahymena cell, and then proceed inward to consider the mitochondria and then the nuclei. For each of these cellular organelles and organelle-systems, first we familiarize the reader with its location in the cell and its structure and ultrastructure, and then we analyze the molecular mechanisms associated with organelle assembly, function, and subdivision. This analysis includes a molecular inventory of the organelle or organelle system, as well as a review of the consequences of modification, disruption or overexpression of important molecular components of each structure or system. Relevant comparisons to results obtained with other well-studied organisms, from Paramecium to Homo sapiens, are also included. Our goal is to provide investigators, in particular those who are new to this organism, both the background and the motivation to work with this model system and achieve further insight into its organization and dynamics.
Starvation-induced cleavage of the tRNA anticodon loop in Tetrahymena thermophila
2005, Journal of Biological Chemistry
Amino acid deprivation triggers dramatic physiological responses in all organisms, altering both the synthesis and destruction of RNA and protein. Here we describe, using the ciliate Tetrahymena thermophila, a previously unidentified response to amino acid deprivation in which mature transfer RNA (tRNA) is cleaved in the anticodon loop. We observed that anticodon loop cleavage affects a small fraction of most or all tRNA sequences. Accumulation of cleaved tRNA is temporally coordinated with the morphological and metabolic changes of adaptation to starvation. The starvation-induced endonucleolytic cleavage activity targets tRNAs that have undergone maturation by 5′ and 3′ end processing and base modification. Curiously, the majority of cleaved tRNAs lack the 3′ terminal CCA nucleotides required for aminoacylation. Starvation-induced tRNA cleavage is inhibited in the presence of essential amino acids, independent of the persistence of other starvation-induced responses. Our findings suggest that anticodon loop cleavage may reduce the accumulation of uncharged tRNAs as part of a specific response induced by amino acid starvation.
Hypoangular: A gene potentially involved in specifying positional information in a ciliate, Tetrahymena thermophila
1993, Developmental Biology
In Tetrahymena, two unique cell-surface structures, the oral apparatus and the cytoproct, are formed at opposite ends of one ciliary row, the reference meridian, which is propagated longitudinally during clonal growth. A third set of unique structures, the contractile vacuole pore(s) (CVP), is located at a nearly constant proportion of the cell circumference to the cell's right of the reference meridian. Three allelic recessive temperature-sensitive mutations, collectively named hypoangular (hpo), alter both the geometry of propagation of the reference meridian and the location of the CVPs. In mutant cells, the reference meridian typically undergoes a steady rightward shift in successive cell generations ("cortical slippage"); concomitantly, CVP sets come to lie closer to the reference meridian. Although CVP location is still proportional to the cell circumference, the constant of proportionality (the "CVP angle") is reduced. Another effect is an alteration in the widths of morphogenetic domains within the cortex. As the temperature is raised (made more restrictive), these effects are accentuated and the CVP angle becomes reduced further. At the extreme, the CVP angle collapses to zero and less, i.e., there is a topological switch such that CVPs come to lie to the left of the reference meridian, and the direction of cortical slippage reverses from rightward to leftward. These observations are hard to reconcile with existing formal models of pattern specification in this system and suggest that the hpo locus might specify a key component of the intracellular positional system.
Conjugal blocks in Tetrahymena pattern mutants and their cytoplasmic rescue. II. janus A
1991, Developmental Biology
A conjugal block phenotype is described for the Tetrahymena pattern mutant, janA. janA exhibits a characteristic “janus” phenotype in which cells develop with a global mirror-image duplication of the ventral pattern of cortical organelles. janA cells are competent to form mating pairs, but later become irreversibly fused as heteropolar doublets. The few pairs that successfully dissociate fail to undergo postconjugal oral replacement and perish. The janA conjugal block is 100% penetrant, is under prezygotic macronuclear control, and is lethal. Here we characterize this conjugal block genetically and cytologically and demonstrate that it can be rescued by a transferable, wild-type product. New insights into late conjugal events, especially the replacement of the oral apparatus, are reported for wild-type cells as well.
The energy budget of Tetrahymena and the material fluxes into and out of the adenylate pool
1986, Experimental Cell Research
The material budget of the adenylate pool deals with all processes which physically establish and maintain this pool, while the energy budget is concerned with the intracompartmental ATP recycling. Both budgets were analysed in Tetrahymena thermophila exposed to various energy and material demands. Some of the general conclusions are: at a maximum growth rate the overall ATP consumption during one cell cycle is 10⁻¹⁰ mol ATP; the contribution of osmoregulation and ciliary motion to the budget is about 1% each; at zero net growth, energy is consumed because of a continuous recycling of matter between the monomer and the polymer compartment. The rate of ATP production is about 1000-fold greater than the rate of adenylate monomere influx. The residence time of adenylate monomers within the pool is about 30 min, but for ATP molecules it is only 2 sec.

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^☆: This research was supported in part by National Institutes of Health Grant No. HD 08485 to Dr. Joseph Frankel.

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Full paperTransformation in Tetrahymena thermophila: Development of an inducible phenotype☆

Abstract

Develop. Biol

Develop. Biol

Develop. Biol

Exp. Cell Res

Develop. Biol

Exp. Cell Res

Develop. Biol

Genetics of Tetrahymena

Pair formation in Tetrahymena pyriformis, an inducible developmental system

J. Exp. Zool

Oral morphogenesis during transformation from microstome to macrostome and macrostome to microstome in Tetrahymena vorax strain V2 type S

Trans. Amer. Microsc. Soc

History, taxonomy, ecology and evolution of species of Tetrahymena

Flagellar elongation and shortening in Chlamydomonas

J. Cell Biol

Cell differentiation in Naegleria

Cytofluorimetric analysis of nuclear DNA during meiosis, fertilization and macronuclear development in the ciliate Tetrahymena pyriformis, syngen 1

J. Cell Sci

Form and pattern in ciliated protozoa: Analysis of a genic mutant with altered cell shape in Tetrahymena pyriformis, syngen 1

J. Exp. Zool

Participation of the undulating membrane in the formation of oral replacement primordia in Tetrahymena pyriformis

J. Protozool

The synchronization of oral development without cell division in Tetrahymena pyriformis GL-C

J. Exp. Zool

A simplified Chatton-Lwoff silver impregnation procedure for use in experimental studies with ciliates

Trans. Amer. Microsc. Soc

Cortical development in Tetrahymena

Full paper
Transformation in Tetrahymena thermophila: Development of an inducible phenotype☆

Oral morphogenesis during transformation from microstome to macrostome and macrostome to microstome in Tetrahymena vorax strain V₂ type S