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...

Descripción completa

Guardado en:
Detalles Bibliográficos
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:
Acceso en línea:https://doaj.org/article/fb4799db11154c3094550412705d35e3
Etiquetas: Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
id oai:doaj.org-article:fb4799db11154c3094550412705d35e3
record_format dspace
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
work_keys_str_mv AT danielpfeiffer thepolarorganizingproteinpopzisfundamentalforpropercelldivisionandsegregationofcellularcontentinitalictoggleyesmagnetospirillumgryphiswaldenseitalic
AT mauriciotoronahuelpan thepolarorganizingproteinpopzisfundamentalforpropercelldivisionandsegregationofcellularcontentinitalictoggleyesmagnetospirillumgryphiswaldenseitalic
AT marcbramkamp thepolarorganizingproteinpopzisfundamentalforpropercelldivisionandsegregationofcellularcontentinitalictoggleyesmagnetospirillumgryphiswaldenseitalic
AT jurgenmplitzko thepolarorganizingproteinpopzisfundamentalforpropercelldivisionandsegregationofcellularcontentinitalictoggleyesmagnetospirillumgryphiswaldenseitalic
AT dirkschuler thepolarorganizingproteinpopzisfundamentalforpropercelldivisionandsegregationofcellularcontentinitalictoggleyesmagnetospirillumgryphiswaldenseitalic
AT danielpfeiffer polarorganizingproteinpopzisfundamentalforpropercelldivisionandsegregationofcellularcontentinitalictoggleyesmagnetospirillumgryphiswaldenseitalic
AT mauriciotoronahuelpan polarorganizingproteinpopzisfundamentalforpropercelldivisionandsegregationofcellularcontentinitalictoggleyesmagnetospirillumgryphiswaldenseitalic
AT marcbramkamp polarorganizingproteinpopzisfundamentalforpropercelldivisionandsegregationofcellularcontentinitalictoggleyesmagnetospirillumgryphiswaldenseitalic
AT jurgenmplitzko polarorganizingproteinpopzisfundamentalforpropercelldivisionandsegregationofcellularcontentinitalictoggleyesmagnetospirillumgryphiswaldenseitalic
AT dirkschuler polarorganizingproteinpopzisfundamentalforpropercelldivisionandsegregationofcellularcontentinitalictoggleyesmagnetospirillumgryphiswaldenseitalic
_version_ 1718427192450351104