Cargando…

Genus-Specific Interactions of Bacterial Chromosome Segregation Machinery Are Critical for Their Function

Most bacteria use the ParABS system to segregate their newly replicated chromosomes. The two protein components of this system from various bacterial species share their biochemical properties: ParB is a CTPase that binds specific centromere-like parS sequences to assemble a nucleoprotein complex, w...

Descripción completa

Detalles Bibliográficos
Autores principales: Pióro, Monika, Matusiak, Izabela, Gawek, Adam, Łebkowski, Tomasz, Jaroszek, Patrycja, Bergé, Matthieu, Böhm, Kati, Armitage, Judith, Viollier, Patrick H., Bramkamp, Marc, Jakimowicz, Dagmara
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9298525/
https://www.ncbi.nlm.nih.gov/pubmed/35875543
http://dx.doi.org/10.3389/fmicb.2022.928139
_version_ 1784750725996216320
author Pióro, Monika
Matusiak, Izabela
Gawek, Adam
Łebkowski, Tomasz
Jaroszek, Patrycja
Bergé, Matthieu
Böhm, Kati
Armitage, Judith
Viollier, Patrick H.
Bramkamp, Marc
Jakimowicz, Dagmara
author_facet Pióro, Monika
Matusiak, Izabela
Gawek, Adam
Łebkowski, Tomasz
Jaroszek, Patrycja
Bergé, Matthieu
Böhm, Kati
Armitage, Judith
Viollier, Patrick H.
Bramkamp, Marc
Jakimowicz, Dagmara
author_sort Pióro, Monika
collection PubMed
description Most bacteria use the ParABS system to segregate their newly replicated chromosomes. The two protein components of this system from various bacterial species share their biochemical properties: ParB is a CTPase that binds specific centromere-like parS sequences to assemble a nucleoprotein complex, while the ParA ATPase forms a dimer that binds DNA non-specifically and interacts with ParB complexes. The ParA-ParB interaction incites the movement of ParB complexes toward the opposite cell poles. However, apart from their function in chromosome segregation, both ParAB may engage in genus-specific interactions with other protein partners. One such example is the polar-growth controlling protein DivIVA in Actinomycetota, which binds ParA in Mycobacteria while interacts with ParB in Corynebacteria. Here, we used heterologous hosts to investigate whether the interactions between DivIVA and ParA or ParB are maintained across phylogenic classes. Specifically, we examined interactions of proteins from four bacterial species, two belonging to the Gram positive Actinomycetota phylum and two belonging to the Gram-negative Pseudomonadota. We show that while the interactions between ParA and ParB are preserved for closely related orthologs, the interactions with polarly localised protein partners are not conferred by orthologous ParABs. Moreover, we demonstrate that heterologous ParA cannot substitute for endogenous ParA, despite their high sequence similarity. Therefore, we conclude that ParA orthologs are fine-tuned to interact with their partners, especially their interactions with polarly localised proteins are adjusted to particular bacterial species demands.
format Online
Article
Text
id pubmed-9298525
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-92985252022-07-21 Genus-Specific Interactions of Bacterial Chromosome Segregation Machinery Are Critical for Their Function Pióro, Monika Matusiak, Izabela Gawek, Adam Łebkowski, Tomasz Jaroszek, Patrycja Bergé, Matthieu Böhm, Kati Armitage, Judith Viollier, Patrick H. Bramkamp, Marc Jakimowicz, Dagmara Front Microbiol Microbiology Most bacteria use the ParABS system to segregate their newly replicated chromosomes. The two protein components of this system from various bacterial species share their biochemical properties: ParB is a CTPase that binds specific centromere-like parS sequences to assemble a nucleoprotein complex, while the ParA ATPase forms a dimer that binds DNA non-specifically and interacts with ParB complexes. The ParA-ParB interaction incites the movement of ParB complexes toward the opposite cell poles. However, apart from their function in chromosome segregation, both ParAB may engage in genus-specific interactions with other protein partners. One such example is the polar-growth controlling protein DivIVA in Actinomycetota, which binds ParA in Mycobacteria while interacts with ParB in Corynebacteria. Here, we used heterologous hosts to investigate whether the interactions between DivIVA and ParA or ParB are maintained across phylogenic classes. Specifically, we examined interactions of proteins from four bacterial species, two belonging to the Gram positive Actinomycetota phylum and two belonging to the Gram-negative Pseudomonadota. We show that while the interactions between ParA and ParB are preserved for closely related orthologs, the interactions with polarly localised protein partners are not conferred by orthologous ParABs. Moreover, we demonstrate that heterologous ParA cannot substitute for endogenous ParA, despite their high sequence similarity. Therefore, we conclude that ParA orthologs are fine-tuned to interact with their partners, especially their interactions with polarly localised proteins are adjusted to particular bacterial species demands. Frontiers Media S.A. 2022-07-06 /pmc/articles/PMC9298525/ /pubmed/35875543 http://dx.doi.org/10.3389/fmicb.2022.928139 Text en Copyright © 2022 Pióro, Matusiak, Gawek, Łebkowski, Jaroszek, Bergé, Böhm, Armitage, Viollier, Bramkamp and Jakimowicz. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Pióro, Monika
Matusiak, Izabela
Gawek, Adam
Łebkowski, Tomasz
Jaroszek, Patrycja
Bergé, Matthieu
Böhm, Kati
Armitage, Judith
Viollier, Patrick H.
Bramkamp, Marc
Jakimowicz, Dagmara
Genus-Specific Interactions of Bacterial Chromosome Segregation Machinery Are Critical for Their Function
title Genus-Specific Interactions of Bacterial Chromosome Segregation Machinery Are Critical for Their Function
title_full Genus-Specific Interactions of Bacterial Chromosome Segregation Machinery Are Critical for Their Function
title_fullStr Genus-Specific Interactions of Bacterial Chromosome Segregation Machinery Are Critical for Their Function
title_full_unstemmed Genus-Specific Interactions of Bacterial Chromosome Segregation Machinery Are Critical for Their Function
title_short Genus-Specific Interactions of Bacterial Chromosome Segregation Machinery Are Critical for Their Function
title_sort genus-specific interactions of bacterial chromosome segregation machinery are critical for their function
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9298525/
https://www.ncbi.nlm.nih.gov/pubmed/35875543
http://dx.doi.org/10.3389/fmicb.2022.928139
work_keys_str_mv AT pioromonika genusspecificinteractionsofbacterialchromosomesegregationmachineryarecriticalfortheirfunction
AT matusiakizabela genusspecificinteractionsofbacterialchromosomesegregationmachineryarecriticalfortheirfunction
AT gawekadam genusspecificinteractionsofbacterialchromosomesegregationmachineryarecriticalfortheirfunction
AT łebkowskitomasz genusspecificinteractionsofbacterialchromosomesegregationmachineryarecriticalfortheirfunction
AT jaroszekpatrycja genusspecificinteractionsofbacterialchromosomesegregationmachineryarecriticalfortheirfunction
AT bergematthieu genusspecificinteractionsofbacterialchromosomesegregationmachineryarecriticalfortheirfunction
AT bohmkati genusspecificinteractionsofbacterialchromosomesegregationmachineryarecriticalfortheirfunction
AT armitagejudith genusspecificinteractionsofbacterialchromosomesegregationmachineryarecriticalfortheirfunction
AT viollierpatrickh genusspecificinteractionsofbacterialchromosomesegregationmachineryarecriticalfortheirfunction
AT bramkampmarc genusspecificinteractionsofbacterialchromosomesegregationmachineryarecriticalfortheirfunction
AT jakimowiczdagmara genusspecificinteractionsofbacterialchromosomesegregationmachineryarecriticalfortheirfunction