Positioning of the Motility Machinery in Halophilic Archaea

ABSTRACT Bacteria and archaea exhibit tactical behavior and can move up and down chemical gradients. This tactical behavior relies on a motility structure, which is guided by a chemosensory system. Environmental signals are sensed by membrane-inserted chemosensory receptors that are organized in lar...

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Autores principales:	Zhengqun Li, Yoshiaki Kinosita, Marta Rodriguez-Franco, Phillip Nußbaum, Frank Braun, Floriane Delpech, Tessa E. F. Quax, Sonja-Verena Albers
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	archaea archaellum cell polarity chemotaxis motility Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/62e0d0b936eb405392c5d126842adc0a
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spelling	oai:doaj.org-article:62e0d0b936eb405392c5d126842adc0a2021-11-15T15:55:24ZPositioning of the Motility Machinery in Halophilic Archaea10.1128/mBio.00377-192150-7511https://doaj.org/article/62e0d0b936eb405392c5d126842adc0a2019-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00377-19https://doaj.org/toc/2150-7511ABSTRACT Bacteria and archaea exhibit tactical behavior and can move up and down chemical gradients. This tactical behavior relies on a motility structure, which is guided by a chemosensory system. Environmental signals are sensed by membrane-inserted chemosensory receptors that are organized in large ordered arrays. While the cellular positioning of the chemotaxis machinery and that of the flagellum have been studied in detail in bacteria, we have little knowledge about the localization of such macromolecular assemblies in archaea. Although the archaeal motility structure, the archaellum, is fundamentally different from the flagellum, archaea have received the chemosensory machinery from bacteria and have connected this system with the archaellum. Here, we applied a combination of time-lapse imaging and fluorescence and electron microscopy using the model euryarchaeon Haloferax volcanii and found that archaella were specifically present at the cell poles of actively dividing rod-shaped cells. The chemosensory arrays also had a polar preference, but in addition, several smaller arrays moved freely in the lateral membranes. In the stationary phase, rod-shaped cells became round and chemosensory arrays were disassembled. The positioning of archaella and that of chemosensory arrays are not interdependent and likely require an independent form of positioning machinery. This work showed that, in the rod-shaped haloarchaeal cells, the positioning of the archaellum and of the chemosensory arrays is regulated in time and in space. These insights into the cellular organization of H. volcanii suggest the presence of an active mechanism responsible for the positioning of macromolecular protein complexes in archaea. IMPORTANCE Archaea are ubiquitous single cellular microorganisms that play important ecological roles in nature. The intracellular organization of archaeal cells is among the unresolved mysteries of archaeal biology. With this work, we show that cells of haloarchaea are polarized. The cellular positioning of proteins involved in chemotaxis and motility is spatially and temporally organized in these cells. This suggests the presence of a specific mechanism responsible for the positioning of macromolecular protein complexes in archaea.Zhengqun LiYoshiaki KinositaMarta Rodriguez-FrancoPhillip NußbaumFrank BraunFloriane DelpechTessa E. F. QuaxSonja-Verena AlbersAmerican Society for Microbiologyarticlearchaeaarchaellumcell polaritychemotaxismotilityMicrobiologyQR1-502ENmBio, Vol 10, Iss 3 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	archaea archaellum cell polarity chemotaxis motility Microbiology QR1-502
spellingShingle	archaea archaellum cell polarity chemotaxis motility Microbiology QR1-502 Zhengqun Li Yoshiaki Kinosita Marta Rodriguez-Franco Phillip Nußbaum Frank Braun Floriane Delpech Tessa E. F. Quax Sonja-Verena Albers Positioning of the Motility Machinery in Halophilic Archaea
description	ABSTRACT Bacteria and archaea exhibit tactical behavior and can move up and down chemical gradients. This tactical behavior relies on a motility structure, which is guided by a chemosensory system. Environmental signals are sensed by membrane-inserted chemosensory receptors that are organized in large ordered arrays. While the cellular positioning of the chemotaxis machinery and that of the flagellum have been studied in detail in bacteria, we have little knowledge about the localization of such macromolecular assemblies in archaea. Although the archaeal motility structure, the archaellum, is fundamentally different from the flagellum, archaea have received the chemosensory machinery from bacteria and have connected this system with the archaellum. Here, we applied a combination of time-lapse imaging and fluorescence and electron microscopy using the model euryarchaeon Haloferax volcanii and found that archaella were specifically present at the cell poles of actively dividing rod-shaped cells. The chemosensory arrays also had a polar preference, but in addition, several smaller arrays moved freely in the lateral membranes. In the stationary phase, rod-shaped cells became round and chemosensory arrays were disassembled. The positioning of archaella and that of chemosensory arrays are not interdependent and likely require an independent form of positioning machinery. This work showed that, in the rod-shaped haloarchaeal cells, the positioning of the archaellum and of the chemosensory arrays is regulated in time and in space. These insights into the cellular organization of H. volcanii suggest the presence of an active mechanism responsible for the positioning of macromolecular protein complexes in archaea. IMPORTANCE Archaea are ubiquitous single cellular microorganisms that play important ecological roles in nature. The intracellular organization of archaeal cells is among the unresolved mysteries of archaeal biology. With this work, we show that cells of haloarchaea are polarized. The cellular positioning of proteins involved in chemotaxis and motility is spatially and temporally organized in these cells. This suggests the presence of a specific mechanism responsible for the positioning of macromolecular protein complexes in archaea.
format	article
author	Zhengqun Li Yoshiaki Kinosita Marta Rodriguez-Franco Phillip Nußbaum Frank Braun Floriane Delpech Tessa E. F. Quax Sonja-Verena Albers
author_facet	Zhengqun Li Yoshiaki Kinosita Marta Rodriguez-Franco Phillip Nußbaum Frank Braun Floriane Delpech Tessa E. F. Quax Sonja-Verena Albers
author_sort	Zhengqun Li
title	Positioning of the Motility Machinery in Halophilic Archaea
title_short	Positioning of the Motility Machinery in Halophilic Archaea
title_full	Positioning of the Motility Machinery in Halophilic Archaea
title_fullStr	Positioning of the Motility Machinery in Halophilic Archaea
title_full_unstemmed	Positioning of the Motility Machinery in Halophilic Archaea
title_sort	positioning of the motility machinery in halophilic archaea
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/62e0d0b936eb405392c5d126842adc0a
work_keys_str_mv	AT zhengqunli positioningofthemotilitymachineryinhalophilicarchaea AT yoshiakikinosita positioningofthemotilitymachineryinhalophilicarchaea AT martarodriguezfranco positioningofthemotilitymachineryinhalophilicarchaea AT phillipnußbaum positioningofthemotilitymachineryinhalophilicarchaea AT frankbraun positioningofthemotilitymachineryinhalophilicarchaea AT florianedelpech positioningofthemotilitymachineryinhalophilicarchaea AT tessaefquax positioningofthemotilitymachineryinhalophilicarchaea AT sonjaverenaalbers positioningofthemotilitymachineryinhalophilicarchaea
_version_	1718427220538556416

Positioning of the Motility Machinery in Halophilic Archaea

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