Nematocida displodere mechanosensitive ion channel of small conductance 2 assembles into a unique 6-channel super-structure in vitro

Mechanosensitive ion channels play an essential role in reacting to environmental signals and sustaining cell integrity by facilitating ion flux across membranes. For obligate intracellular pathogens like microsporidia, adapting to changes in the host environment is crucial for survival and propagat...

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Published inPloS one Vol. 19; no. 7; p. e0301951
Main Authors Berg, Alexandra, Berntsson, Ronnie P-A, Barandun, Jonas
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 22.07.2024
Public Library of Science (PLoS)
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Abstract Mechanosensitive ion channels play an essential role in reacting to environmental signals and sustaining cell integrity by facilitating ion flux across membranes. For obligate intracellular pathogens like microsporidia, adapting to changes in the host environment is crucial for survival and propagation. Despite representing a eukaryote of extreme genome reduction, microsporidia have expanded the gene family of mechanosensitive ion channels of small conductance (mscS) through repeated gene duplication and horizontal gene transfer. All microsporidian genomes characterized to date contain mscS genes of both eukaryotic and bacterial origin. Here, we investigated the cryo-electron microscopy structure of the bacterially derived mechanosensitive ion channel of small conductance 2 (MscS2) from Nematocida displodere, an intracellular pathogen of Caenorhabditis elegans. MscS2 is the most compact MscS-like channel known and assembles into a unique superstructure in vitro with six heptameric MscS2 channels. Individual MscS2 channels are oriented in a heterogeneous manner to one another, resembling an asymmetric, flexible six-way cross joint. Finally, we show that microsporidian MscS2 still forms a heptameric membrane channel, however the extreme compaction suggests a potential new function of this MscS-like protein.
AbstractList Mechanosensitive ion channels play an essential role in reacting to environmental signals and sustaining cell integrity by facilitating ion flux across membranes. For obligate intracellular pathogens like microsporidia, adapting to changes in the host environment is crucial for survival and propagation. Despite representing a eukaryote of extreme genome reduction, microsporidia have expanded the gene family of mechanosensitive ion channels of small conductance (mscS) through repeated gene duplication and horizontal gene transfer. All microsporidian genomes characterized to date contain mscS genes of both eukaryotic and bacterial origin. Here, we investigated the cryo-electron microscopy structure of the bacterially derived mechanosensitive ion channel of small conductance 2 (MscS2) from Nematocida displodere, an intracellular pathogen of Caenorhabditis elegans. MscS2 is the most compact MscS-like channel known and assembles into a unique superstructure in vitro with six heptameric MscS2 channels. Individual MscS2 channels are oriented in a heterogeneous manner to one another, resembling an asymmetric, flexible six-way cross joint. Finally, we show that microsporidian MscS2 still forms a heptameric membrane channel, however the extreme compaction suggests a potential new function of this MscS-like protein.
Mechanosensitive ion channels play an essential role in reacting to environmental signals and sustaining cell integrity by facilitating ion flux across membranes. For obligate intracellular pathogens like microsporidia, adapting to changes in the host environment is crucial for survival and propagation. Despite representing a eukaryote of extreme genome reduction, microsporidia have expanded the gene family of mechanosensitive ion channels of small conductance ( mscS ) through repeated gene duplication and horizontal gene transfer. All microsporidian genomes characterized to date contain mscS genes of both eukaryotic and bacterial origin. Here, we investigated the cryo-electron microscopy structure of the bacterially derived mechanosensitive ion channel of small conductance 2 (MscS2) from Nematocida displodere , an intracellular pathogen of Caenorhabditis elegans . MscS2 is the most compact MscS-like channel known and assembles into a unique superstructure in vitro with six heptameric MscS2 channels. Individual MscS2 channels are oriented in a heterogeneous manner to one another, resembling an asymmetric, flexible six-way cross joint. Finally, we show that microsporidian MscS2 still forms a heptameric membrane channel, however the extreme compaction suggests a potential new function of this MscS-like protein.
Mechanosensitive ion channels play an essential role in reacting to environmental signals and sustaining cell integrity by facilitating ion flux across membranes. For obligate intracellular pathogens like microsporidia, adapting to changes in the host environment is crucial for survival and propagation. Despite representing a eukaryote of extreme genome reduction, microsporidia have expanded the gene family of mechanosensitive ion channels of small conductance (mscS) through repeated gene duplication and horizontal gene transfer. All microsporidian genomes characterized to date contain mscS genes of both eukaryotic and bacterial origin. Here, we investigated the cryo-electron microscopy structure of the bacterially derived mechanosensitive ion channel of small conductance 2 (MscS2) from Nematocida displodere, an intracellular pathogen of Caenorhabditis elegans. MscS2 is the most compact MscS-like channel known and assembles into a unique superstructure in vitro with six heptameric MscS2 channels. Individual MscS2 channels are oriented in a heterogeneous manner to one another, resembling an asymmetric, flexible six-way cross joint. Finally, we show that microsporidian MscS2 still forms a heptameric membrane channel, however the extreme compaction suggests a potential new function of this MscS-like protein.Mechanosensitive ion channels play an essential role in reacting to environmental signals and sustaining cell integrity by facilitating ion flux across membranes. For obligate intracellular pathogens like microsporidia, adapting to changes in the host environment is crucial for survival and propagation. Despite representing a eukaryote of extreme genome reduction, microsporidia have expanded the gene family of mechanosensitive ion channels of small conductance (mscS) through repeated gene duplication and horizontal gene transfer. All microsporidian genomes characterized to date contain mscS genes of both eukaryotic and bacterial origin. Here, we investigated the cryo-electron microscopy structure of the bacterially derived mechanosensitive ion channel of small conductance 2 (MscS2) from Nematocida displodere, an intracellular pathogen of Caenorhabditis elegans. MscS2 is the most compact MscS-like channel known and assembles into a unique superstructure in vitro with six heptameric MscS2 channels. Individual MscS2 channels are oriented in a heterogeneous manner to one another, resembling an asymmetric, flexible six-way cross joint. Finally, we show that microsporidian MscS2 still forms a heptameric membrane channel, however the extreme compaction suggests a potential new function of this MscS-like protein.
Audience Academic
Author Berg, Alexandra
Barandun, Jonas
Berntsson, Ronnie P-A
AuthorAffiliation 1 Department of Molecular Biology, The Laboratory for Molecular Infection Medicine Sweden (MIMS), Umeå Centre for Microbial Research, Science for Life Laboratory, Umeå University, Umeå, Västerbotten, Sweden
Weizmann Institute of Science, ISRAEL
2 Department of Medical Biochemistry and Biophysics, Wallenberg Centre for Molecular Medicine, Umeå University, Umeå, Västerbotten, Sweden
3 Wallenberg Centre for Molecular Medicine & Umeå Centre for Microbial Research, Umeå University, Umeå, Sweden
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Snippet Mechanosensitive ion channels play an essential role in reacting to environmental signals and sustaining cell integrity by facilitating ion flux across...
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StartPage e0301951
SubjectTerms Animals
Biology and Life Sciences
Caenorhabditis elegans - genetics
Caenorhabditis elegans - metabolism
Conductance
Cryoelectron Microscopy
E coli
Electron microscopy
Gene duplication
Gene transfer
Genes
Genomes
Genomics
Horizontal transfer
Intracellular
Ion channels
Ion Channels - chemistry
Ion Channels - genetics
Ion Channels - metabolism
Ion flux
Ions
Mechanotransduction, Cellular
Medicine and Health Sciences
Membrane proteins
Membranes
Microsporidia
Microsporidia - genetics
Microsporidia - metabolism
Pathogens
Physical Sciences
Proteins
Research and Analysis Methods
Superstructures
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Title Nematocida displodere mechanosensitive ion channel of small conductance 2 assembles into a unique 6-channel super-structure in vitro
URI https://www.ncbi.nlm.nih.gov/pubmed/39038013
https://www.proquest.com/docview/3083636757
https://www.proquest.com/docview/3083670952/abstract/
https://pubmed.ncbi.nlm.nih.gov/PMC11262690
https://urn.kb.se/resolve?urn=urn:nbn:se:umu:diva-228127
https://doaj.org/article/d67c2fc067d049fba7636f6ef1f4b2c6
Volume 19
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