Chained Structure of Dimeric F<sub>1</sub>-like ATPase in <named-content content-type="genus-species">Mycoplasma mobile</named-content> Gliding Machinery

ABSTRACT Mycoplasma mobile, a fish pathogen, exhibits gliding motility using ATP hydrolysis on solid surfaces, including animal cells. The gliding machinery can be divided into surface and internal structures. The internal structure of the motor is composed of 28 so-called “chains” that are each com...

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Autores principales:	Takuma Toyonaga, Takayuki Kato, Akihiro Kawamoto, Noriyuki Kodera, Tasuku Hamaguchi, Yuhei O. Tahara, Toshio Ando, Keiichi Namba, Makoto Miyata
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	F1-ATPase rotary motor parasitic bacteria electron microscopy atomic force microscopy bacterial motility Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/4e6b806026b8428da032d3d5312a1509
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spelling	oai:doaj.org-article:4e6b806026b8428da032d3d5312a15092021-11-10T18:37:51ZChained Structure of Dimeric F<sub>1</sub>-like ATPase in <named-content content-type="genus-species">Mycoplasma mobile</named-content> Gliding Machinery10.1128/mBio.01414-212150-7511https://doaj.org/article/4e6b806026b8428da032d3d5312a15092021-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01414-21https://doaj.org/toc/2150-7511ABSTRACT Mycoplasma mobile, a fish pathogen, exhibits gliding motility using ATP hydrolysis on solid surfaces, including animal cells. The gliding machinery can be divided into surface and internal structures. The internal structure of the motor is composed of 28 so-called “chains” that are each composed of 17 repeating protein units called “particles.” These proteins include homologs of the catalytic α and β subunits of F1-ATPase. In this study, we isolated the particles and determined their structures using negative-staining electron microscopy and high-speed atomic force microscopy. The isolated particles were composed of five proteins, MMOB1660 (α-subunit homolog), -1670 (β-subunit homolog), -1630, -1620, and -4530, and showed ATP hydrolyzing activity. The two-dimensional (2D) structure, with dimensions of 35 and 26 nm, showed a dimer of hexameric ring approximately 12 nm in diameter, resembling F1-ATPase catalytic (αβ)3. We isolated the F1-like ATPase unit, which is composed of MMOB1660, -1670, and -1630. Furthermore, we isolated the chain and analyzed the three-dimensional (3D) structure, showing that dimers of mushroom-like structures resembling F1-ATPase were connected and aligned along the dimer axis at 31-nm intervals. An atomic model of F1-ATPase catalytic (αβ)3 from Bacillus PS3 was successfully fitted to each hexameric ring of the mushroom-like structure. These results suggest that the motor for M. mobile gliding shares an evolutionary origin with F1-ATPase. Based on the obtained structure, we propose possible force transmission processes in the gliding mechanism. IMPORTANCE F1Fo-ATPase, a rotary ATPase, is widespread in the membranes of mitochondria, chloroplasts, and bacteria and converts ATP energy with a proton motive force across the membrane by its physical rotation. Homologous protein complexes play roles in ion and protein transport. Mycoplasma mobile, a pathogenic bacterium, was recently suggested to have a special motility system evolutionarily derived from F1-ATPase. The present study isolated the protein complex from Mycoplasma cells and supported this conclusion by clarifying the detailed structures containing common and novel features as F1-ATPase relatives.Takuma ToyonagaTakayuki KatoAkihiro KawamotoNoriyuki KoderaTasuku HamaguchiYuhei O. TaharaToshio AndoKeiichi NambaMakoto MiyataAmerican Society for MicrobiologyarticleF1-ATPaserotary motorparasitic bacteriaelectron microscopyatomic force microscopybacterial motilityMicrobiologyQR1-502ENmBio, Vol 12, Iss 4 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	F1-ATPase rotary motor parasitic bacteria electron microscopy atomic force microscopy bacterial motility Microbiology QR1-502
spellingShingle	F1-ATPase rotary motor parasitic bacteria electron microscopy atomic force microscopy bacterial motility Microbiology QR1-502 Takuma Toyonaga Takayuki Kato Akihiro Kawamoto Noriyuki Kodera Tasuku Hamaguchi Yuhei O. Tahara Toshio Ando Keiichi Namba Makoto Miyata Chained Structure of Dimeric F<sub>1</sub>-like ATPase in <named-content content-type="genus-species">Mycoplasma mobile</named-content> Gliding Machinery
description	ABSTRACT Mycoplasma mobile, a fish pathogen, exhibits gliding motility using ATP hydrolysis on solid surfaces, including animal cells. The gliding machinery can be divided into surface and internal structures. The internal structure of the motor is composed of 28 so-called “chains” that are each composed of 17 repeating protein units called “particles.” These proteins include homologs of the catalytic α and β subunits of F1-ATPase. In this study, we isolated the particles and determined their structures using negative-staining electron microscopy and high-speed atomic force microscopy. The isolated particles were composed of five proteins, MMOB1660 (α-subunit homolog), -1670 (β-subunit homolog), -1630, -1620, and -4530, and showed ATP hydrolyzing activity. The two-dimensional (2D) structure, with dimensions of 35 and 26 nm, showed a dimer of hexameric ring approximately 12 nm in diameter, resembling F1-ATPase catalytic (αβ)3. We isolated the F1-like ATPase unit, which is composed of MMOB1660, -1670, and -1630. Furthermore, we isolated the chain and analyzed the three-dimensional (3D) structure, showing that dimers of mushroom-like structures resembling F1-ATPase were connected and aligned along the dimer axis at 31-nm intervals. An atomic model of F1-ATPase catalytic (αβ)3 from Bacillus PS3 was successfully fitted to each hexameric ring of the mushroom-like structure. These results suggest that the motor for M. mobile gliding shares an evolutionary origin with F1-ATPase. Based on the obtained structure, we propose possible force transmission processes in the gliding mechanism. IMPORTANCE F1Fo-ATPase, a rotary ATPase, is widespread in the membranes of mitochondria, chloroplasts, and bacteria and converts ATP energy with a proton motive force across the membrane by its physical rotation. Homologous protein complexes play roles in ion and protein transport. Mycoplasma mobile, a pathogenic bacterium, was recently suggested to have a special motility system evolutionarily derived from F1-ATPase. The present study isolated the protein complex from Mycoplasma cells and supported this conclusion by clarifying the detailed structures containing common and novel features as F1-ATPase relatives.
format	article
author	Takuma Toyonaga Takayuki Kato Akihiro Kawamoto Noriyuki Kodera Tasuku Hamaguchi Yuhei O. Tahara Toshio Ando Keiichi Namba Makoto Miyata
author_facet	Takuma Toyonaga Takayuki Kato Akihiro Kawamoto Noriyuki Kodera Tasuku Hamaguchi Yuhei O. Tahara Toshio Ando Keiichi Namba Makoto Miyata
author_sort	Takuma Toyonaga
title	Chained Structure of Dimeric F<sub>1</sub>-like ATPase in <named-content content-type="genus-species">Mycoplasma mobile</named-content> Gliding Machinery
title_short	Chained Structure of Dimeric F<sub>1</sub>-like ATPase in <named-content content-type="genus-species">Mycoplasma mobile</named-content> Gliding Machinery
title_full	Chained Structure of Dimeric F<sub>1</sub>-like ATPase in <named-content content-type="genus-species">Mycoplasma mobile</named-content> Gliding Machinery
title_fullStr	Chained Structure of Dimeric F<sub>1</sub>-like ATPase in <named-content content-type="genus-species">Mycoplasma mobile</named-content> Gliding Machinery
title_full_unstemmed	Chained Structure of Dimeric F<sub>1</sub>-like ATPase in <named-content content-type="genus-species">Mycoplasma mobile</named-content> Gliding Machinery
title_sort	chained structure of dimeric f<sub>1</sub>-like atpase in <named-content content-type="genus-species">mycoplasma mobile</named-content> gliding machinery
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/4e6b806026b8428da032d3d5312a1509
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Chained Structure of Dimeric F<sub>1</sub>-like ATPase in <named-content content-type="genus-species">Mycoplasma mobile</named-content> Gliding Machinery

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