Growth-Phase-Specific Modulation of Cell Morphology and Gene Expression by an Archaeal Histone Protein

ABSTRACT In all three domains of life, organisms use nonspecific DNA-binding proteins to compact and organize the genome as well as to regulate transcription on a global scale. Histone is the primary eukaryotic nucleoprotein, and its evolutionary roots can be traced to the archaea. However, not all...

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Autores principales:	Keely A. Dulmage, Horia Todor, Amy K. Schmid
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2015
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/a64e3a417e944118ad53da84cdff51ca
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spelling	oai:doaj.org-article:a64e3a417e944118ad53da84cdff51ca2021-11-15T15:41:30ZGrowth-Phase-Specific Modulation of Cell Morphology and Gene Expression by an Archaeal Histone Protein10.1128/mBio.00649-152150-7511https://doaj.org/article/a64e3a417e944118ad53da84cdff51ca2015-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00649-15https://doaj.org/toc/2150-7511ABSTRACT In all three domains of life, organisms use nonspecific DNA-binding proteins to compact and organize the genome as well as to regulate transcription on a global scale. Histone is the primary eukaryotic nucleoprotein, and its evolutionary roots can be traced to the archaea. However, not all archaea use this protein as the primary DNA-packaging component, raising questions regarding the role of histones in archaeal chromatin function. Here, quantitative phenotyping, transcriptomic, and proteomic assays were performed on deletion and overexpression mutants of the sole histone protein of the hypersaline-adapted haloarchaeal model organism Halobacterium salinarum. This protein is highly conserved among all sequenced haloarchaeal species and maintains hallmark residues required for eukaryotic histone functions. Surprisingly, despite this conservation at the sequence level, unlike in other archaea or eukaryotes, H. salinarum histone is required to regulate cell shape but is not necessary for survival. Genome-wide expression changes in histone deletion strains were global, significant but subtle in terms of fold change, bidirectional, and growth phase dependent. Mass spectrometric proteomic identification of proteins from chromatin enrichments yielded levels of histone and putative nucleoid-associated proteins similar to those of transcription factors, consistent with an open and transcriptionally active genome. Taken together, these data suggest that histone in H. salinarum plays a minor role in DNA compaction but important roles in growth-phase-dependent gene expression and regulation of cell shape. Histone function in haloarchaea more closely resembles a regulator of gene expression than a chromatin-organizing protein like canonical eukaryotic histone. IMPORTANCE Histones comprise the major protein component of eukaryotic chromatin and are required for both genome packaging and global regulation of expression. The current paradigm maintains that archaea whose genes encode histone also use these proteins to package DNA. In contrast, here we demonstrate that the sole histone encoded in the genome of the salt-adapted archaeon Halobacterium salinarum is both unessential and unlikely to be involved in DNA compaction despite conservation of residues important for eukaryotic histones. Rather, H. salinarum histone is required for global regulation of gene expression and cell shape. These data are consistent with the hypothesis that H. salinarum histone, strongly conserved across all other known salt-adapted archaea, serves a novel role in gene regulation and cell shape maintenance. Given that archaea possess the ancestral form of eukaryotic histone, this study has important implications for understanding the evolution of histone function.Keely A. DulmageHoria TodorAmy K. SchmidAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 5 (2015)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Keely A. Dulmage Horia Todor Amy K. Schmid Growth-Phase-Specific Modulation of Cell Morphology and Gene Expression by an Archaeal Histone Protein
description	ABSTRACT In all three domains of life, organisms use nonspecific DNA-binding proteins to compact and organize the genome as well as to regulate transcription on a global scale. Histone is the primary eukaryotic nucleoprotein, and its evolutionary roots can be traced to the archaea. However, not all archaea use this protein as the primary DNA-packaging component, raising questions regarding the role of histones in archaeal chromatin function. Here, quantitative phenotyping, transcriptomic, and proteomic assays were performed on deletion and overexpression mutants of the sole histone protein of the hypersaline-adapted haloarchaeal model organism Halobacterium salinarum. This protein is highly conserved among all sequenced haloarchaeal species and maintains hallmark residues required for eukaryotic histone functions. Surprisingly, despite this conservation at the sequence level, unlike in other archaea or eukaryotes, H. salinarum histone is required to regulate cell shape but is not necessary for survival. Genome-wide expression changes in histone deletion strains were global, significant but subtle in terms of fold change, bidirectional, and growth phase dependent. Mass spectrometric proteomic identification of proteins from chromatin enrichments yielded levels of histone and putative nucleoid-associated proteins similar to those of transcription factors, consistent with an open and transcriptionally active genome. Taken together, these data suggest that histone in H. salinarum plays a minor role in DNA compaction but important roles in growth-phase-dependent gene expression and regulation of cell shape. Histone function in haloarchaea more closely resembles a regulator of gene expression than a chromatin-organizing protein like canonical eukaryotic histone. IMPORTANCE Histones comprise the major protein component of eukaryotic chromatin and are required for both genome packaging and global regulation of expression. The current paradigm maintains that archaea whose genes encode histone also use these proteins to package DNA. In contrast, here we demonstrate that the sole histone encoded in the genome of the salt-adapted archaeon Halobacterium salinarum is both unessential and unlikely to be involved in DNA compaction despite conservation of residues important for eukaryotic histones. Rather, H. salinarum histone is required for global regulation of gene expression and cell shape. These data are consistent with the hypothesis that H. salinarum histone, strongly conserved across all other known salt-adapted archaea, serves a novel role in gene regulation and cell shape maintenance. Given that archaea possess the ancestral form of eukaryotic histone, this study has important implications for understanding the evolution of histone function.
format	article
author	Keely A. Dulmage Horia Todor Amy K. Schmid
author_facet	Keely A. Dulmage Horia Todor Amy K. Schmid
author_sort	Keely A. Dulmage
title	Growth-Phase-Specific Modulation of Cell Morphology and Gene Expression by an Archaeal Histone Protein
title_short	Growth-Phase-Specific Modulation of Cell Morphology and Gene Expression by an Archaeal Histone Protein
title_full	Growth-Phase-Specific Modulation of Cell Morphology and Gene Expression by an Archaeal Histone Protein
title_fullStr	Growth-Phase-Specific Modulation of Cell Morphology and Gene Expression by an Archaeal Histone Protein
title_full_unstemmed	Growth-Phase-Specific Modulation of Cell Morphology and Gene Expression by an Archaeal Histone Protein
title_sort	growth-phase-specific modulation of cell morphology and gene expression by an archaeal histone protein
publisher	American Society for Microbiology
publishDate	2015
url	https://doaj.org/article/a64e3a417e944118ad53da84cdff51ca
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Growth-Phase-Specific Modulation of Cell Morphology and Gene Expression by an Archaeal Histone Protein

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