HupB Is a Bacterial Nucleoid-Associated Protein with an Indispensable Eukaryotic-Like Tail

ABSTRACT In bacteria, chromosomal DNA must be efficiently compacted to fit inside the small cell compartment while remaining available for the proteins involved in replication, segregation, and transcription. Among the nucleoid-associated proteins (NAPs) responsible for maintaining this highly organ...

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Autores principales:	Joanna Hołówka, Damian Trojanowski, Katarzyna Ginda, Bartosz Wojtaś, Bartłomiej Gielniewski, Dagmara Jakimowicz, Jolanta Zakrzewska-Czerwińska
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	HU HupB Mycobacterium chromosome dynamics chromosome organization nucleoid-associated proteins Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/3c89f1c0785342979323dd7115daa83f
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spelling	oai:doaj.org-article:3c89f1c0785342979323dd7115daa83f2021-11-15T15:51:56ZHupB Is a Bacterial Nucleoid-Associated Protein with an Indispensable Eukaryotic-Like Tail10.1128/mBio.01272-172150-7511https://doaj.org/article/3c89f1c0785342979323dd7115daa83f2017-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01272-17https://doaj.org/toc/2150-7511ABSTRACT In bacteria, chromosomal DNA must be efficiently compacted to fit inside the small cell compartment while remaining available for the proteins involved in replication, segregation, and transcription. Among the nucleoid-associated proteins (NAPs) responsible for maintaining this highly organized and yet dynamic chromosome structure, the HU protein is one of the most conserved and highly abundant. HupB, a homologue of HU, was recently identified in mycobacteria. This intriguing mycobacterial NAP is composed of two domains: an N-terminal domain that resembles bacterial HU, and a long and distinctive C-terminal domain that contains several PAKK/KAAK motifs, which are characteristic of the H1/H5 family of eukaryotic histones. In this study, we analyzed the in vivo binding of HupB on the chromosome scale. By using PALM (photoactivated localization microscopy) and ChIP-Seq (chromatin immunoprecipitation followed by deep sequencing), we observed that the C-terminal domain is indispensable for the association of HupB with the nucleoid. Strikingly, the in vivo binding of HupB displayed a bias from the origin (oriC) to the terminus (ter) of the mycobacterial chromosome (numbers of binding sites decreased toward ter). We hypothesized that this binding mode reflects a role for HupB in organizing newly replicated oriC regions. Thus, HupB may be involved in coordinating replication with chromosome segregation. IMPORTANCE We currently know little about the organization of the mycobacterial chromosome and its dynamics during the cell cycle. Among the mycobacterial nucleoid-associated proteins (NAPs) responsible for chromosome organization and dynamics, HupB is one of the most intriguing. It contains a long and distinctive C-terminal domain that harbors several PAKK/KAAK motifs, which are characteristic of the eukaryotic histone H1/H5 proteins. The HupB protein is also known to be crucial for the survival of tubercle bacilli during infection. Here, we provide in vivo experimental evidence showing that the C-terminal domain of HupB is crucial for its DNA binding. Our results suggest that HupB may be involved in organizing newly replicated regions and could help coordinate chromosome replication with segregation. Given that tuberculosis (TB) remains a serious worldwide health problem (10.4 million new TB cases were diagnosed in 2015, according to WHO) and new multidrug-resistant Mycobacterium tuberculosis strains are continually emerging, further studies of the biological function of HupB are needed to determine if this protein could be a prospect for novel antimicrobial drug development.Joanna HołówkaDamian TrojanowskiKatarzyna GindaBartosz WojtaśBartłomiej GielniewskiDagmara JakimowiczJolanta Zakrzewska-CzerwińskaAmerican Society for MicrobiologyarticleHUHupBMycobacteriumchromosome dynamicschromosome organizationnucleoid-associated proteinsMicrobiologyQR1-502ENmBio, Vol 8, Iss 6 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	HU HupB Mycobacterium chromosome dynamics chromosome organization nucleoid-associated proteins Microbiology QR1-502
spellingShingle	HU HupB Mycobacterium chromosome dynamics chromosome organization nucleoid-associated proteins Microbiology QR1-502 Joanna Hołówka Damian Trojanowski Katarzyna Ginda Bartosz Wojtaś Bartłomiej Gielniewski Dagmara Jakimowicz Jolanta Zakrzewska-Czerwińska HupB Is a Bacterial Nucleoid-Associated Protein with an Indispensable Eukaryotic-Like Tail
description	ABSTRACT In bacteria, chromosomal DNA must be efficiently compacted to fit inside the small cell compartment while remaining available for the proteins involved in replication, segregation, and transcription. Among the nucleoid-associated proteins (NAPs) responsible for maintaining this highly organized and yet dynamic chromosome structure, the HU protein is one of the most conserved and highly abundant. HupB, a homologue of HU, was recently identified in mycobacteria. This intriguing mycobacterial NAP is composed of two domains: an N-terminal domain that resembles bacterial HU, and a long and distinctive C-terminal domain that contains several PAKK/KAAK motifs, which are characteristic of the H1/H5 family of eukaryotic histones. In this study, we analyzed the in vivo binding of HupB on the chromosome scale. By using PALM (photoactivated localization microscopy) and ChIP-Seq (chromatin immunoprecipitation followed by deep sequencing), we observed that the C-terminal domain is indispensable for the association of HupB with the nucleoid. Strikingly, the in vivo binding of HupB displayed a bias from the origin (oriC) to the terminus (ter) of the mycobacterial chromosome (numbers of binding sites decreased toward ter). We hypothesized that this binding mode reflects a role for HupB in organizing newly replicated oriC regions. Thus, HupB may be involved in coordinating replication with chromosome segregation. IMPORTANCE We currently know little about the organization of the mycobacterial chromosome and its dynamics during the cell cycle. Among the mycobacterial nucleoid-associated proteins (NAPs) responsible for chromosome organization and dynamics, HupB is one of the most intriguing. It contains a long and distinctive C-terminal domain that harbors several PAKK/KAAK motifs, which are characteristic of the eukaryotic histone H1/H5 proteins. The HupB protein is also known to be crucial for the survival of tubercle bacilli during infection. Here, we provide in vivo experimental evidence showing that the C-terminal domain of HupB is crucial for its DNA binding. Our results suggest that HupB may be involved in organizing newly replicated regions and could help coordinate chromosome replication with segregation. Given that tuberculosis (TB) remains a serious worldwide health problem (10.4 million new TB cases were diagnosed in 2015, according to WHO) and new multidrug-resistant Mycobacterium tuberculosis strains are continually emerging, further studies of the biological function of HupB are needed to determine if this protein could be a prospect for novel antimicrobial drug development.
format	article
author	Joanna Hołówka Damian Trojanowski Katarzyna Ginda Bartosz Wojtaś Bartłomiej Gielniewski Dagmara Jakimowicz Jolanta Zakrzewska-Czerwińska
author_facet	Joanna Hołówka Damian Trojanowski Katarzyna Ginda Bartosz Wojtaś Bartłomiej Gielniewski Dagmara Jakimowicz Jolanta Zakrzewska-Czerwińska
author_sort	Joanna Hołówka
title	HupB Is a Bacterial Nucleoid-Associated Protein with an Indispensable Eukaryotic-Like Tail
title_short	HupB Is a Bacterial Nucleoid-Associated Protein with an Indispensable Eukaryotic-Like Tail
title_full	HupB Is a Bacterial Nucleoid-Associated Protein with an Indispensable Eukaryotic-Like Tail
title_fullStr	HupB Is a Bacterial Nucleoid-Associated Protein with an Indispensable Eukaryotic-Like Tail
title_full_unstemmed	HupB Is a Bacterial Nucleoid-Associated Protein with an Indispensable Eukaryotic-Like Tail
title_sort	hupb is a bacterial nucleoid-associated protein with an indispensable eukaryotic-like tail
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/3c89f1c0785342979323dd7115daa83f
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HupB Is a Bacterial Nucleoid-Associated Protein with an Indispensable Eukaryotic-Like Tail

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