The Role of Membrane-Bound Extracellular Vesicles During Co-Stimulation and Conjugation in the Ciliate <i>Tetrahymena thermophila</i>

During sexual reproduction, the freshwater ciliate <i>Tetrahymena thermophila</i> sheds membrane-bound vesicles into the extracellular environment (cEMVs: ciliary extracellular micro-vesicles). We provide evidence that 100 nm vesicles shed from the cilia of starved cells promote mating b...

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Main Authors: Eric S. Cole, Oleksandr Dmytrenko, Mark Li, Neetij Krishnan, Josh Thorp, LeeAnn Higgins, Todd Markowski, Garry Morgan, Eileen O’Toole
Format: Article
Language:English
Published: MDPI AG 2025-04-01
Series:Microorganisms
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Online Access:https://www.mdpi.com/2076-2607/13/4/803
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author Eric S. Cole
Oleksandr Dmytrenko
Mark Li
Neetij Krishnan
Josh Thorp
LeeAnn Higgins
Todd Markowski
Garry Morgan
Eileen O’Toole
author_facet Eric S. Cole
Oleksandr Dmytrenko
Mark Li
Neetij Krishnan
Josh Thorp
LeeAnn Higgins
Todd Markowski
Garry Morgan
Eileen O’Toole
author_sort Eric S. Cole
collection DOAJ
description During sexual reproduction, the freshwater ciliate <i>Tetrahymena thermophila</i> sheds membrane-bound vesicles into the extracellular environment (cEMVs: ciliary extracellular micro-vesicles). We provide evidence that 100 nm vesicles shed from the cilia of starved cells promote mating between cells of complementary mating types. A proteomic analysis revealed that these EMVs are decorated with mating-type proteins expressed from the MAT locus, proteins that define a cell’s sex (one of seven). Once the mating junction is established between cells, smaller 60 nm vesicles (junction vesicles) appear within the extracellular gap that separates mating partners. Junction vesicles (jEMVs) may play a role in remodeling the mating junction through which gametic pronuclei are exchanged. Evidence is presented demonstrating that cells must be able to internalize extracellular signals via some form of endocytosis in order to trigger conjugation. Finally, an evolutionarily conserved fusogen (Hap2) implicated in pore formation also appears necessary for jEMV processing. This system offers an excellent opportunity for studies on ectosome shedding, intercellular signaling and shed vesicle uptake by macro-pinocytosis, as they relate to sexual reproduction in the ciliate <i>Tetrahymena thermophila</i>.
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spelling doaj-art-84bb5bd2712e45de94de59e0e5ce49c82025-08-20T03:13:58ZengMDPI AGMicroorganisms2076-26072025-04-0113480310.3390/microorganisms13040803The Role of Membrane-Bound Extracellular Vesicles During Co-Stimulation and Conjugation in the Ciliate <i>Tetrahymena thermophila</i>Eric S. Cole0Oleksandr Dmytrenko1Mark Li2Neetij Krishnan3Josh Thorp4LeeAnn Higgins5Todd Markowski6Garry Morgan7Eileen O’Toole8Biology Department, St. Olaf College, Northfield, MN 55057, USACenter for Cardiovascular Research, Departmental of Medicine, Cardiovascular Division, Washington University School of Medicine, 660 South Euclid Campus Box 8086, St. Louis, MO 63110, USADivision of Endocrinology, Diabetes and Metabolism, Beth Israel Deaconess Medical Center and Harvard, Medical School, Howard Hughes Medical Institute, Boston, MA 02115, USADepartment of Pediatrics, Division of Hematology/Oncology, Washington University School of Medicine, St. Louis, MO 63110, USABiology Department, St. Olaf College, Northfield, MN 55057, USACenter for Metabolomics and Proteomics, Department of BMBB, University of Minnesota, Minneapolis, MN 55455, USACenter for Metabolomics and Proteomics, Department of BMBB, University of Minnesota, Minneapolis, MN 55455, USABoulder Electron Microcopy Facility, Department of Molecular, Cellular and Developmental Biology, University of Colorado, Boulder, CO 80309, USABoulder Electron Microcopy Facility, Department of Molecular, Cellular and Developmental Biology, University of Colorado, Boulder, CO 80309, USADuring sexual reproduction, the freshwater ciliate <i>Tetrahymena thermophila</i> sheds membrane-bound vesicles into the extracellular environment (cEMVs: ciliary extracellular micro-vesicles). We provide evidence that 100 nm vesicles shed from the cilia of starved cells promote mating between cells of complementary mating types. A proteomic analysis revealed that these EMVs are decorated with mating-type proteins expressed from the MAT locus, proteins that define a cell’s sex (one of seven). Once the mating junction is established between cells, smaller 60 nm vesicles (junction vesicles) appear within the extracellular gap that separates mating partners. Junction vesicles (jEMVs) may play a role in remodeling the mating junction through which gametic pronuclei are exchanged. Evidence is presented demonstrating that cells must be able to internalize extracellular signals via some form of endocytosis in order to trigger conjugation. Finally, an evolutionarily conserved fusogen (Hap2) implicated in pore formation also appears necessary for jEMV processing. This system offers an excellent opportunity for studies on ectosome shedding, intercellular signaling and shed vesicle uptake by macro-pinocytosis, as they relate to sexual reproduction in the ciliate <i>Tetrahymena thermophila</i>.https://www.mdpi.com/2076-2607/13/4/803ciliates<i>Tetrahymena</i>conjugationco-stimulationectosomesEMVs
spellingShingle Eric S. Cole
Oleksandr Dmytrenko
Mark Li
Neetij Krishnan
Josh Thorp
LeeAnn Higgins
Todd Markowski
Garry Morgan
Eileen O’Toole
The Role of Membrane-Bound Extracellular Vesicles During Co-Stimulation and Conjugation in the Ciliate <i>Tetrahymena thermophila</i>
Microorganisms
ciliates
<i>Tetrahymena</i>
conjugation
co-stimulation
ectosomes
EMVs
title The Role of Membrane-Bound Extracellular Vesicles During Co-Stimulation and Conjugation in the Ciliate <i>Tetrahymena thermophila</i>
title_full The Role of Membrane-Bound Extracellular Vesicles During Co-Stimulation and Conjugation in the Ciliate <i>Tetrahymena thermophila</i>
title_fullStr The Role of Membrane-Bound Extracellular Vesicles During Co-Stimulation and Conjugation in the Ciliate <i>Tetrahymena thermophila</i>
title_full_unstemmed The Role of Membrane-Bound Extracellular Vesicles During Co-Stimulation and Conjugation in the Ciliate <i>Tetrahymena thermophila</i>
title_short The Role of Membrane-Bound Extracellular Vesicles During Co-Stimulation and Conjugation in the Ciliate <i>Tetrahymena thermophila</i>
title_sort role of membrane bound extracellular vesicles during co stimulation and conjugation in the ciliate i tetrahymena thermophila i
topic ciliates
<i>Tetrahymena</i>
conjugation
co-stimulation
ectosomes
EMVs
url https://www.mdpi.com/2076-2607/13/4/803
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