Tethered Magnets Are the Key to Magnetotaxis: Direct Observations of <italic toggle="yes">Magnetospirillum magneticum</italic> AMB-1 Show that MamK Distributes Magnetosome Organelles Equally to Daughter Cells

ABSTRACT Magnetotactic bacteria are a unique group of bacteria that synthesize a magnetic organelle termed the magnetosome, which they use to assist with their magnetic navigation in a specific type of bacterial motility called magneto-aerotaxis. Cytoskeletal filaments consisting of the actin-like p...

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Autores principales:	Azuma Taoka, Ayako Kiyokawa, Chika Uesugi, Yousuke Kikuchi, Zachery Oestreicher, Kaori Morii, Yukako Eguchi, Yoshihiro Fukumori
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	actin-like protein bacterial organelle cytoskeleton live-cell imaging magneto-reception magnetosome Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/74aa97f87c6247a49ef1aa48dd506d0e
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spelling	oai:doaj.org-article:74aa97f87c6247a49ef1aa48dd506d0e2021-11-15T15:51:44ZTethered Magnets Are the Key to Magnetotaxis: Direct Observations of <italic toggle="yes">Magnetospirillum magneticum</italic> AMB-1 Show that MamK Distributes Magnetosome Organelles Equally to Daughter Cells10.1128/mBio.00679-172150-7511https://doaj.org/article/74aa97f87c6247a49ef1aa48dd506d0e2017-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00679-17https://doaj.org/toc/2150-7511ABSTRACT Magnetotactic bacteria are a unique group of bacteria that synthesize a magnetic organelle termed the magnetosome, which they use to assist with their magnetic navigation in a specific type of bacterial motility called magneto-aerotaxis. Cytoskeletal filaments consisting of the actin-like protein MamK are associated with the magnetosome chain. Previously, the function of MamK was thought to be in positioning magnetosome organelles; this was proposed based on observations via electron microscopy still images. Here, we conducted live-cell time-lapse fluorescence imaging analyses employing highly inclined and laminated optical sheet microscopy, and these methods enabled us to visualize detailed dynamic movement of magnetosomes in growing cells during the entire cell cycle with high-temporal resolution and a high signal/noise ratio. We found that the MamK cytoskeleton anchors magnetosomes through a mechanism that requires MamK-ATPase activity throughout the cell cycle to prevent simple diffusion of magnetosomes within the cell. We concluded that the static chain-like arrangement of the magnetosomes is required to precisely and consistently segregate the magnetosomes to daughter cells. Thus, the daughter cells inherit a functional magnetic sensor that mediates magneto-reception. IMPORTANCE Half a century ago, bacterial cells were considered a simple “bag of enzymes”; only recently have they been shown to comprise ordered complexes of macromolecular structures, such as bacterial organelles and cytoskeletons, similar to their eukaryotic counterparts. In eukaryotic cells, the positioning of organelles is regulated by cytoskeletal elements. However, the role of cytoskeletal elements in the positioning of bacterial organelles, such as magnetosomes, remains unclear. Magnetosomes are associated with cytoskeletal filaments that consist of the actin-like protein MamK. In this study, we focused on how the MamK cytoskeleton regulates the dynamic movement of magnetosome organelles in living magnetotactic bacterial cells. Here, we used fluorescence imaging to visualize the dynamics of magnetosomes throughout the cell cycle in living magnetotactic bacterial cells to understand how they use the actin-like cytoskeleton to maintain and to make functional their nano-sized magnetic organelles.Azuma TaokaAyako KiyokawaChika UesugiYousuke KikuchiZachery OestreicherKaori MoriiYukako EguchiYoshihiro FukumoriAmerican Society for Microbiologyarticleactin-like proteinbacterial organellecytoskeletonlive-cell imagingmagneto-receptionmagnetosomeMicrobiologyQR1-502ENmBio, Vol 8, Iss 4 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	actin-like protein bacterial organelle cytoskeleton live-cell imaging magneto-reception magnetosome Microbiology QR1-502
spellingShingle	actin-like protein bacterial organelle cytoskeleton live-cell imaging magneto-reception magnetosome Microbiology QR1-502 Azuma Taoka Ayako Kiyokawa Chika Uesugi Yousuke Kikuchi Zachery Oestreicher Kaori Morii Yukako Eguchi Yoshihiro Fukumori Tethered Magnets Are the Key to Magnetotaxis: Direct Observations of <italic toggle="yes">Magnetospirillum magneticum</italic> AMB-1 Show that MamK Distributes Magnetosome Organelles Equally to Daughter Cells
description	ABSTRACT Magnetotactic bacteria are a unique group of bacteria that synthesize a magnetic organelle termed the magnetosome, which they use to assist with their magnetic navigation in a specific type of bacterial motility called magneto-aerotaxis. Cytoskeletal filaments consisting of the actin-like protein MamK are associated with the magnetosome chain. Previously, the function of MamK was thought to be in positioning magnetosome organelles; this was proposed based on observations via electron microscopy still images. Here, we conducted live-cell time-lapse fluorescence imaging analyses employing highly inclined and laminated optical sheet microscopy, and these methods enabled us to visualize detailed dynamic movement of magnetosomes in growing cells during the entire cell cycle with high-temporal resolution and a high signal/noise ratio. We found that the MamK cytoskeleton anchors magnetosomes through a mechanism that requires MamK-ATPase activity throughout the cell cycle to prevent simple diffusion of magnetosomes within the cell. We concluded that the static chain-like arrangement of the magnetosomes is required to precisely and consistently segregate the magnetosomes to daughter cells. Thus, the daughter cells inherit a functional magnetic sensor that mediates magneto-reception. IMPORTANCE Half a century ago, bacterial cells were considered a simple “bag of enzymes”; only recently have they been shown to comprise ordered complexes of macromolecular structures, such as bacterial organelles and cytoskeletons, similar to their eukaryotic counterparts. In eukaryotic cells, the positioning of organelles is regulated by cytoskeletal elements. However, the role of cytoskeletal elements in the positioning of bacterial organelles, such as magnetosomes, remains unclear. Magnetosomes are associated with cytoskeletal filaments that consist of the actin-like protein MamK. In this study, we focused on how the MamK cytoskeleton regulates the dynamic movement of magnetosome organelles in living magnetotactic bacterial cells. Here, we used fluorescence imaging to visualize the dynamics of magnetosomes throughout the cell cycle in living magnetotactic bacterial cells to understand how they use the actin-like cytoskeleton to maintain and to make functional their nano-sized magnetic organelles.
format	article
author	Azuma Taoka Ayako Kiyokawa Chika Uesugi Yousuke Kikuchi Zachery Oestreicher Kaori Morii Yukako Eguchi Yoshihiro Fukumori
author_facet	Azuma Taoka Ayako Kiyokawa Chika Uesugi Yousuke Kikuchi Zachery Oestreicher Kaori Morii Yukako Eguchi Yoshihiro Fukumori
author_sort	Azuma Taoka
title	Tethered Magnets Are the Key to Magnetotaxis: Direct Observations of <italic toggle="yes">Magnetospirillum magneticum</italic> AMB-1 Show that MamK Distributes Magnetosome Organelles Equally to Daughter Cells
title_short	Tethered Magnets Are the Key to Magnetotaxis: Direct Observations of <italic toggle="yes">Magnetospirillum magneticum</italic> AMB-1 Show that MamK Distributes Magnetosome Organelles Equally to Daughter Cells
title_full	Tethered Magnets Are the Key to Magnetotaxis: Direct Observations of <italic toggle="yes">Magnetospirillum magneticum</italic> AMB-1 Show that MamK Distributes Magnetosome Organelles Equally to Daughter Cells
title_fullStr	Tethered Magnets Are the Key to Magnetotaxis: Direct Observations of <italic toggle="yes">Magnetospirillum magneticum</italic> AMB-1 Show that MamK Distributes Magnetosome Organelles Equally to Daughter Cells
title_full_unstemmed	Tethered Magnets Are the Key to Magnetotaxis: Direct Observations of <italic toggle="yes">Magnetospirillum magneticum</italic> AMB-1 Show that MamK Distributes Magnetosome Organelles Equally to Daughter Cells
title_sort	tethered magnets are the key to magnetotaxis: direct observations of <italic toggle="yes">magnetospirillum magneticum</italic> amb-1 show that mamk distributes magnetosome organelles equally to daughter cells
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/74aa97f87c6247a49ef1aa48dd506d0e
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Tethered Magnets Are the Key to Magnetotaxis: Direct Observations of <italic toggle="yes">Magnetospirillum magneticum</italic> AMB-1 Show that MamK Distributes Magnetosome Organelles Equally to Daughter Cells

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