A novel mechanosensitive channel controls osmoregulation, differentiation, and infectivity in Trypanosoma cruzi

The causative agent of Chagas disease undergoes drastic morphological and biochemical modifications as it passes between hosts and transitions from extracellular to intracellular stages. The osmotic and mechanical aspects of these cellular transformations are not understood. Here we identify and cha...

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Main Authors: Noopur Dave, Ugur Cetiner, Daniel Arroyo, Joshua Fonbuena, Megna Tiwari, Patricia Barrera, Noelia Lander, Andriy Anishkin, Sergei Sukharev, Veronica Jimenez
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2021-07-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/67449
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author Noopur Dave
Ugur Cetiner
Daniel Arroyo
Joshua Fonbuena
Megna Tiwari
Patricia Barrera
Noelia Lander
Andriy Anishkin
Sergei Sukharev
Veronica Jimenez
author_facet Noopur Dave
Ugur Cetiner
Daniel Arroyo
Joshua Fonbuena
Megna Tiwari
Patricia Barrera
Noelia Lander
Andriy Anishkin
Sergei Sukharev
Veronica Jimenez
author_sort Noopur Dave
collection DOAJ
description The causative agent of Chagas disease undergoes drastic morphological and biochemical modifications as it passes between hosts and transitions from extracellular to intracellular stages. The osmotic and mechanical aspects of these cellular transformations are not understood. Here we identify and characterize a novel mechanosensitive channel in Trypanosoma cruzi (TcMscS) belonging to the superfamily of small-conductance mechanosensitive channels (MscS). TcMscS is activated by membrane tension and forms a large pore permeable to anions, cations, and small osmolytes. The channel changes its location from the contractile vacuole complex in epimastigotes to the plasma membrane as the parasites develop into intracellular amastigotes. TcMscS knockout parasites show significant fitness defects, including increased cell volume, calcium dysregulation, impaired differentiation, and a dramatic decrease in infectivity. Our work provides mechanistic insights into components supporting pathogen adaptation inside the host, thus opening the exploration of mechanosensation as a prerequisite for protozoan infectivity.
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spelling doaj.art-be362ba0d1914056ba1128e801a858f52022-12-22T03:24:29ZengeLife Sciences Publications LtdeLife2050-084X2021-07-011010.7554/eLife.67449A novel mechanosensitive channel controls osmoregulation, differentiation, and infectivity in Trypanosoma cruziNoopur Dave0https://orcid.org/0000-0002-1798-1824Ugur Cetiner1https://orcid.org/0000-0002-5267-0749Daniel Arroyo2Joshua Fonbuena3Megna Tiwari4Patricia Barrera5Noelia Lander6Andriy Anishkin7Sergei Sukharev8Veronica Jimenez9https://orcid.org/0000-0002-0744-8137Department of Biological Science, College of Natural Sciences and Mathematics, California State University Fullerton, Fullerton, United StatesDepartment of Biology, University of Maryland, College Park, United StatesDepartment of Biological Science, College of Natural Sciences and Mathematics, California State University Fullerton, Fullerton, United StatesDepartment of Biological Science, College of Natural Sciences and Mathematics, California State University Fullerton, Fullerton, United StatesDepartment of Biological Science, College of Natural Sciences and Mathematics, California State University Fullerton, Fullerton, United StatesDepartmento de Biología, Facultad de Ciencias Exactas y Naturales, Instituto de Histologia y Embriologia IHEM-CONICET, Facultad de Medicina, Universidad Nacional de Cuyo, Mendoza, ArgentinaDepartment of Biological Sciences, University of Cincinnati, Cincinnati, United StatesDepartment of Biology, University of Maryland, College Park, United StatesDepartment of Biology, University of Maryland, College Park, United StatesDepartment of Biological Science, College of Natural Sciences and Mathematics, California State University Fullerton, Fullerton, United StatesThe causative agent of Chagas disease undergoes drastic morphological and biochemical modifications as it passes between hosts and transitions from extracellular to intracellular stages. The osmotic and mechanical aspects of these cellular transformations are not understood. Here we identify and characterize a novel mechanosensitive channel in Trypanosoma cruzi (TcMscS) belonging to the superfamily of small-conductance mechanosensitive channels (MscS). TcMscS is activated by membrane tension and forms a large pore permeable to anions, cations, and small osmolytes. The channel changes its location from the contractile vacuole complex in epimastigotes to the plasma membrane as the parasites develop into intracellular amastigotes. TcMscS knockout parasites show significant fitness defects, including increased cell volume, calcium dysregulation, impaired differentiation, and a dramatic decrease in infectivity. Our work provides mechanistic insights into components supporting pathogen adaptation inside the host, thus opening the exploration of mechanosensation as a prerequisite for protozoan infectivity.https://elifesciences.org/articles/67449mechanosensationcalciumosmoregulationTrypanosoma cruziCRISPR-Cas9electrophysiology
spellingShingle Noopur Dave
Ugur Cetiner
Daniel Arroyo
Joshua Fonbuena
Megna Tiwari
Patricia Barrera
Noelia Lander
Andriy Anishkin
Sergei Sukharev
Veronica Jimenez
A novel mechanosensitive channel controls osmoregulation, differentiation, and infectivity in Trypanosoma cruzi
eLife
mechanosensation
calcium
osmoregulation
Trypanosoma cruzi
CRISPR-Cas9
electrophysiology
title A novel mechanosensitive channel controls osmoregulation, differentiation, and infectivity in Trypanosoma cruzi
title_full A novel mechanosensitive channel controls osmoregulation, differentiation, and infectivity in Trypanosoma cruzi
title_fullStr A novel mechanosensitive channel controls osmoregulation, differentiation, and infectivity in Trypanosoma cruzi
title_full_unstemmed A novel mechanosensitive channel controls osmoregulation, differentiation, and infectivity in Trypanosoma cruzi
title_short A novel mechanosensitive channel controls osmoregulation, differentiation, and infectivity in Trypanosoma cruzi
title_sort novel mechanosensitive channel controls osmoregulation differentiation and infectivity in trypanosoma cruzi
topic mechanosensation
calcium
osmoregulation
Trypanosoma cruzi
CRISPR-Cas9
electrophysiology
url https://elifesciences.org/articles/67449
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