Left-right cortical interactions drive intracellular pattern formation in the ciliate Tetrahymena
Chinkyu Lee, Ewa Joachimiak, Wolfgang Maier, Yu-Yang Jiang, Mireya Parra, Karl F. Lechtreck, Eric S. Cole, Jacek Gaertig
Abstract
In ciliates, cortical organelles, including ciliary arrays, are positioned at precise locations along two polarity axes: anterior-posterior and circumferential (lateral). We explored the poorly understood mechanism of circumferential patterning, which generates left-right asymmetry. The model ciliate Tetrahymena has a single anteriorly-located oral apparatus. During cell division, a single new oral apparatus forms near the equator of the parental cell and along the longitude of the parental organelle.
Introduction
Eukaryotic cells typically have a prominent anterior-posterior (also called front-to-rear or apical-basal) polarity. In addition, some cell types, including cells that move while adhering to a substrate or single-cell metazoan embryos, also have a distinguishable dorsal-ventral polarity axis. Moreover, some cells display chiral asymmetries in reference to the anterior-posterior axis. Ciliated protists have features that are favorable for exploring how multiple polarities and chiral asymmetries are generated in the cell.
Materials and method
Strains and culture
All strains used were obtained from the Tetrahymena Stock Center (Cornell University, Ithaca NY, currently housed at Washington University, St Louis, MO USA; https://sites.wustl.edu/tetrahymena/). Cultures were grown in the SPPA medium (1% proteose-peptone, 0.2% dextrose, 0.1% yeast extract and 0.003% EDTA:ferric sodium salt) supplemented with antibiotics (SPPA medium) [59,60].
Results
Hpo1 is an ARMC9-like protein, TTHERM_001276421
Tetrahymena cells have two permanent polarity axes: anterior-posterior (AP) and circumferential (C). AP polarity is reflected by an asymmetric placement of major cortical organelles: the oral apparatus (OA) near the anterior cell end, the contractile vacuole pores (CVPs) and the cytoproct near the posterior cell end (Fig 1A-1).
Discussion
Ciliates are well suited for studies on intracellular pattern formation but remain relatively unexplored. In Tetrahymena, mutations in several loci selectively affect organelle positioning along either the AP or C axes (reviewed in [2,14]), suggesting that the pathways operating on each of the two orthogonal polarity axes have a degree of independence. Several highly conserved kinases and kinase-binding proteins, including components of conserved Hippo signaling, mediate organelle positioning along the AP axis [29–34].
Acknowledgments
J.G. gratefully acknowledges Joseph Frankel (University of Iowa) for providing the inspiration and encouragement to investigate the hypoangular 1 mutant. The SR-SIM imaging was done at the Biomedical Microscopy Core, University of Georgia.
Citation: Lee C, Joachimiak E, Maier W, Jiang Y-Y, Parra M, Lechtreck KF, et al. (2025) Left-right cortical interactions drive intracellular pattern formation in the ciliate Tetrahymena. PLoS Genet 21(6): e1011735. https://doi.org/10.1371/journal.pgen.1011735
Editor: Gregory J. Pazour, University of Massachusetts Chan Medical School, UNITED STATES OF AMERICA
Received: January 27, 2025; Accepted: May 19, 2025; Published: June 2, 2025
Copyright: © 2025 Lee et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All relevant data are within the paper and its Supporting Information files. The raw NGS data were deposited at the public SRA database (Bioproject PRJNA1216161).
Funding: This work was supported by the National Institutes of Health (grant R01GM135444 to J.G., R01GM110413 to K.F.L.), National Science Foundation (grant 1947608 to E.C.) and the German Federal Ministry of Education and Research (Bundesministerium für Bildung und Forschung) (grant 031L0101C de.NBI-epi to W.M.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
