The Polar Organizing Protein PopZ Is Fundamental for Proper Cell Division and Segregation of Cellular Content in <italic toggle="yes">Magnetospirillum gryphiswaldense</italic>

ABSTRACT Magnetotactic bacteria (MTB) are of special scientific interest due to the formation of magnetosomes, intracellular membrane-enveloped magnetite crystals arranged into a linear chain by a dedicated cytoskeleton. Magnetotaxis relies on the formation and proper inheritance of these unique mag...

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Autores principales:	Daniel Pfeiffer, Mauricio Toro-Nahuelpan, Marc Bramkamp, Jürgen M. Plitzko, Dirk Schüler
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	magnetosome Magnetospirillum magnetotaxis PopZ polarity Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/fb4799db11154c3094550412705d35e3
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spelling	oai:doaj.org-article:fb4799db11154c3094550412705d35e32021-11-15T15:55:25ZThe Polar Organizing Protein PopZ Is Fundamental for Proper Cell Division and Segregation of Cellular Content in <italic toggle="yes">Magnetospirillum gryphiswaldense</italic>10.1128/mBio.02716-182150-7511https://doaj.org/article/fb4799db11154c3094550412705d35e32019-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02716-18https://doaj.org/toc/2150-7511ABSTRACT Magnetotactic bacteria (MTB) are of special scientific interest due to the formation of magnetosomes, intracellular membrane-enveloped magnetite crystals arranged into a linear chain by a dedicated cytoskeleton. Magnetotaxis relies on the formation and proper inheritance of these unique magnetic organelles, both of which need to be coordinated with the segregation of other cellular content such as chromosomes or motility and chemotaxis related structures. Thus, elaborated mechanisms are required in MTB to coordinate and maintain a high level of spatial and temporal subcellular organization during cytokinesis. However, thus far, underlying mechanisms and polarity determinants such as landmark proteins remained obscure in MTB. Here, we analyzed an ortholog of the polar organizing protein Z in the alphaproteobacterium Magnetospirillum gryphiswaldense termed PopZMgr. We show that deletion of the popZMgr gene causes abnormal cell elongation, minicell formation, DNA missegregation, and impairs motility. Overproduction of PopZMgr results in PopZ-rich regions near the poles, which are devoid of larger macromolecules, such as ribosomes, chromosomal DNA, and polyhydroxybutyrate (PHB) granules. Using superresolution microscopy, we show that PopZMgr exhibits a bipolar localization pattern throughout the cell cycle, indicating that the definition of new poles in M. gryphiswaldense occurs immediately upon completion of cytokinesis. Moreover, substitution of PopZ orthologs between M. gryphiswaldense and the related alphaproteobacterium Caulobacter crescentus indicated that PopZ localization depends on host-specific cues and that both orthologs have diverged to an extent that allows only partial reciprocal functional complementation. Altogether, our results indicate that in M. gryphiswaldense, PopZ plays a critical role during cell division and segregation of cellular content. IMPORTANCE Magnetotactic bacteria (MTB) share the unique capability of magnetic navigation, one of the most complex behavioral responses found in prokaryotes, by means of magnetosomes, which act as an internal compass. Due to formation of these unique nanoparticles, MTB have emerged as a model to study prokaryotic organelle formation and cytoskeletal organization in conjunction with complex motility systems. Despite the high degree of subcellular organization required in MTB, less is known about cell-cycle-related factors or proteins responsible for spatiotemporal polarity control. Here, we investigate the function of the polar organizer PopZ in the magnetotactic alphaproteobacterium Magnetospirillum gryphiswaldense. Although PopZ is widely distributed among the alphaproteobacteria, its function in MTB belonging to this class has remained unexplored. Our results suggest that in M. gryphiswaldense, PopZ has a key role during cell division and subcellular organization. Furthermore, we show that PopZ localization and function differ from other nonmagnetotactic alphaproteobacterial model organisms.Daniel PfeifferMauricio Toro-NahuelpanMarc BramkampJürgen M. PlitzkoDirk SchülerAmerican Society for MicrobiologyarticlemagnetosomeMagnetospirillummagnetotaxisPopZpolarityMicrobiologyQR1-502ENmBio, Vol 10, Iss 2 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	magnetosome Magnetospirillum magnetotaxis PopZ polarity Microbiology QR1-502
spellingShingle	magnetosome Magnetospirillum magnetotaxis PopZ polarity Microbiology QR1-502 Daniel Pfeiffer Mauricio Toro-Nahuelpan Marc Bramkamp Jürgen M. Plitzko Dirk Schüler The Polar Organizing Protein PopZ Is Fundamental for Proper Cell Division and Segregation of Cellular Content in <italic toggle="yes">Magnetospirillum gryphiswaldense</italic>
description	ABSTRACT Magnetotactic bacteria (MTB) are of special scientific interest due to the formation of magnetosomes, intracellular membrane-enveloped magnetite crystals arranged into a linear chain by a dedicated cytoskeleton. Magnetotaxis relies on the formation and proper inheritance of these unique magnetic organelles, both of which need to be coordinated with the segregation of other cellular content such as chromosomes or motility and chemotaxis related structures. Thus, elaborated mechanisms are required in MTB to coordinate and maintain a high level of spatial and temporal subcellular organization during cytokinesis. However, thus far, underlying mechanisms and polarity determinants such as landmark proteins remained obscure in MTB. Here, we analyzed an ortholog of the polar organizing protein Z in the alphaproteobacterium Magnetospirillum gryphiswaldense termed PopZMgr. We show that deletion of the popZMgr gene causes abnormal cell elongation, minicell formation, DNA missegregation, and impairs motility. Overproduction of PopZMgr results in PopZ-rich regions near the poles, which are devoid of larger macromolecules, such as ribosomes, chromosomal DNA, and polyhydroxybutyrate (PHB) granules. Using superresolution microscopy, we show that PopZMgr exhibits a bipolar localization pattern throughout the cell cycle, indicating that the definition of new poles in M. gryphiswaldense occurs immediately upon completion of cytokinesis. Moreover, substitution of PopZ orthologs between M. gryphiswaldense and the related alphaproteobacterium Caulobacter crescentus indicated that PopZ localization depends on host-specific cues and that both orthologs have diverged to an extent that allows only partial reciprocal functional complementation. Altogether, our results indicate that in M. gryphiswaldense, PopZ plays a critical role during cell division and segregation of cellular content. IMPORTANCE Magnetotactic bacteria (MTB) share the unique capability of magnetic navigation, one of the most complex behavioral responses found in prokaryotes, by means of magnetosomes, which act as an internal compass. Due to formation of these unique nanoparticles, MTB have emerged as a model to study prokaryotic organelle formation and cytoskeletal organization in conjunction with complex motility systems. Despite the high degree of subcellular organization required in MTB, less is known about cell-cycle-related factors or proteins responsible for spatiotemporal polarity control. Here, we investigate the function of the polar organizer PopZ in the magnetotactic alphaproteobacterium Magnetospirillum gryphiswaldense. Although PopZ is widely distributed among the alphaproteobacteria, its function in MTB belonging to this class has remained unexplored. Our results suggest that in M. gryphiswaldense, PopZ has a key role during cell division and subcellular organization. Furthermore, we show that PopZ localization and function differ from other nonmagnetotactic alphaproteobacterial model organisms.
format	article
author	Daniel Pfeiffer Mauricio Toro-Nahuelpan Marc Bramkamp Jürgen M. Plitzko Dirk Schüler
author_facet	Daniel Pfeiffer Mauricio Toro-Nahuelpan Marc Bramkamp Jürgen M. Plitzko Dirk Schüler
author_sort	Daniel Pfeiffer
title	The Polar Organizing Protein PopZ Is Fundamental for Proper Cell Division and Segregation of Cellular Content in <italic toggle="yes">Magnetospirillum gryphiswaldense</italic>
title_short	The Polar Organizing Protein PopZ Is Fundamental for Proper Cell Division and Segregation of Cellular Content in <italic toggle="yes">Magnetospirillum gryphiswaldense</italic>
title_full	The Polar Organizing Protein PopZ Is Fundamental for Proper Cell Division and Segregation of Cellular Content in <italic toggle="yes">Magnetospirillum gryphiswaldense</italic>
title_fullStr	The Polar Organizing Protein PopZ Is Fundamental for Proper Cell Division and Segregation of Cellular Content in <italic toggle="yes">Magnetospirillum gryphiswaldense</italic>
title_full_unstemmed	The Polar Organizing Protein PopZ Is Fundamental for Proper Cell Division and Segregation of Cellular Content in <italic toggle="yes">Magnetospirillum gryphiswaldense</italic>
title_sort	polar organizing protein popz is fundamental for proper cell division and segregation of cellular content in <italic toggle="yes">magnetospirillum gryphiswaldense</italic>
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/fb4799db11154c3094550412705d35e3
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The Polar Organizing Protein PopZ Is Fundamental for Proper Cell Division and Segregation of Cellular Content in <italic toggle="yes">Magnetospirillum gryphiswaldense</italic>

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