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Multiple ParA/MinD ATPases coordinate the positioning of disparate cargos in a bacterial cell

In eukaryotes, linear motor proteins govern intracellular transport and organization. In bacteria, where linear motors involved in spatial regulation are absent, the ParA/MinD family of ATPases organize an array of genetic- and protein-based cellular cargos. The positioning of these cargos has been...

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Autores principales: Pulianmackal, Lisa T., Limcaoco, Jose Miguel I., Ravi, Keerthikka, Yang, Sinyu, Zhang, Jeffrey, Tran, Mimi K., Ghalmi, Maria, O’Meara, Matthew J., Vecchiarelli, Anthony G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10241942/
https://www.ncbi.nlm.nih.gov/pubmed/37277398
http://dx.doi.org/10.1038/s41467-023-39019-x
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author Pulianmackal, Lisa T.
Limcaoco, Jose Miguel I.
Ravi, Keerthikka
Yang, Sinyu
Zhang, Jeffrey
Tran, Mimi K.
Ghalmi, Maria
O’Meara, Matthew J.
Vecchiarelli, Anthony G.
author_facet Pulianmackal, Lisa T.
Limcaoco, Jose Miguel I.
Ravi, Keerthikka
Yang, Sinyu
Zhang, Jeffrey
Tran, Mimi K.
Ghalmi, Maria
O’Meara, Matthew J.
Vecchiarelli, Anthony G.
author_sort Pulianmackal, Lisa T.
collection PubMed
description In eukaryotes, linear motor proteins govern intracellular transport and organization. In bacteria, where linear motors involved in spatial regulation are absent, the ParA/MinD family of ATPases organize an array of genetic- and protein-based cellular cargos. The positioning of these cargos has been independently investigated to varying degrees in several bacterial species. However, it remains unclear how multiple ParA/MinD ATPases can coordinate the positioning of diverse cargos in the same cell. Here, we find that over a third of sequenced bacterial genomes encode multiple ParA/MinD ATPases. We identify an organism (Halothiobacillus neapolitanus) with seven ParA/MinD ATPases, demonstrate that five of these are each dedicated to the spatial regulation of a single cellular cargo, and define potential specificity determinants for each system. Furthermore, we show how these positioning reactions can influence each other, stressing the importance of understanding how organelle trafficking, chromosome segregation, and cell division are coordinated in bacterial cells. Together, our data show how multiple ParA/MinD ATPases coexist and function to position a diverse set of fundamental cargos in the same bacterial cell.
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spelling pubmed-102419422023-06-07 Multiple ParA/MinD ATPases coordinate the positioning of disparate cargos in a bacterial cell Pulianmackal, Lisa T. Limcaoco, Jose Miguel I. Ravi, Keerthikka Yang, Sinyu Zhang, Jeffrey Tran, Mimi K. Ghalmi, Maria O’Meara, Matthew J. Vecchiarelli, Anthony G. Nat Commun Article In eukaryotes, linear motor proteins govern intracellular transport and organization. In bacteria, where linear motors involved in spatial regulation are absent, the ParA/MinD family of ATPases organize an array of genetic- and protein-based cellular cargos. The positioning of these cargos has been independently investigated to varying degrees in several bacterial species. However, it remains unclear how multiple ParA/MinD ATPases can coordinate the positioning of diverse cargos in the same cell. Here, we find that over a third of sequenced bacterial genomes encode multiple ParA/MinD ATPases. We identify an organism (Halothiobacillus neapolitanus) with seven ParA/MinD ATPases, demonstrate that five of these are each dedicated to the spatial regulation of a single cellular cargo, and define potential specificity determinants for each system. Furthermore, we show how these positioning reactions can influence each other, stressing the importance of understanding how organelle trafficking, chromosome segregation, and cell division are coordinated in bacterial cells. Together, our data show how multiple ParA/MinD ATPases coexist and function to position a diverse set of fundamental cargos in the same bacterial cell. Nature Publishing Group UK 2023-06-05 /pmc/articles/PMC10241942/ /pubmed/37277398 http://dx.doi.org/10.1038/s41467-023-39019-x Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Pulianmackal, Lisa T.
Limcaoco, Jose Miguel I.
Ravi, Keerthikka
Yang, Sinyu
Zhang, Jeffrey
Tran, Mimi K.
Ghalmi, Maria
O’Meara, Matthew J.
Vecchiarelli, Anthony G.
Multiple ParA/MinD ATPases coordinate the positioning of disparate cargos in a bacterial cell
title Multiple ParA/MinD ATPases coordinate the positioning of disparate cargos in a bacterial cell
title_full Multiple ParA/MinD ATPases coordinate the positioning of disparate cargos in a bacterial cell
title_fullStr Multiple ParA/MinD ATPases coordinate the positioning of disparate cargos in a bacterial cell
title_full_unstemmed Multiple ParA/MinD ATPases coordinate the positioning of disparate cargos in a bacterial cell
title_short Multiple ParA/MinD ATPases coordinate the positioning of disparate cargos in a bacterial cell
title_sort multiple para/mind atpases coordinate the positioning of disparate cargos in a bacterial cell
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10241942/
https://www.ncbi.nlm.nih.gov/pubmed/37277398
http://dx.doi.org/10.1038/s41467-023-39019-x
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