Archaeal histones: structures, stability and DNA binding

Jn, Reeve; Bailey, Kent R.; Wt, Li; Frederic, Marc; Sandman, Kathleen; Dj, Soares

doi:10.1042/bst0320227

Cited by 53 publications

(31 citation statements)

References 23 publications

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“…In bacteria, whereas nucleoid proteins play architectural roles in processes such as DNA replication and transcription (25), there is, to the best of our knowledge, no evidence of regulatory covalent modification of these proteins. Although histones are present in a significant subset of Archaea, they lack the N-and C-terminal tails that are the principal sites of modification in eukaryotic histones (26) and are not covalently modified (5). Even in very early diverging eukaryotes such as trypanosomes, histones possess tails and are covalently modified (27).…”

Section: Discussionmentioning

confidence: 99%

Sir2 and the Acetyltransferase, Pat, Regulate the Archaeal Chromatin Protein, Alba

Marsh

Peak‐Chew

Bell

2005

Journal of Biological Chemistry

105

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The DNA binding affinity of Alba, a chromatin protein of the archaeon Sulfolobus solfataricus P2, is regulated by acetylation of lysine 16. Here we identify an acetyltransferase that specifically acetylates Alba on this residue. The effect of acetylation is to lower the affinity of Alba for DNA. Remarkably, the acetyltransferase is conserved not only in archaea but also in bacteria where it appears to play a role in metabolic regulation. Therefore, our data suggest that S. solfataricus has co-opted this bacterial regulatory system to generate a rudimentary form of chromatin regulation.

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Section: Discussionmentioning

confidence: 99%

Sir2 and the Acetyltransferase, Pat, Regulate the Archaeal Chromatin Protein, Alba

Marsh

Peak‐Chew

Bell

2005

Journal of Biological Chemistry

105

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“…Eubacteria do not as a rule have proteins with histonefolds [137]. An exception are the homologs of the nonhistone-fold protein histone H1 in Chlamydiae [64,119] likely acquired by lateral transfer from a eukaryotic host.…”

Section: The Architecture Of Chromatinmentioning

confidence: 99%

“…Dinoflagellates have secondarily lost their histones and do not form nucleosomes [115]. Their major ChAP, HCC, is most closely related to bacterial HU proteins [188].Eubacteria do not as a rule have proteins with histonefolds [137]. An exception are the homologs of the nonhistone-fold protein histone H1 in Chlamydiae [64,119] likely acquired by lateral transfer from a eukaryotic host.…”

mentioning

confidence: 99%

Innovation in gene regulation: The case of chromatin computation

Prohaska

Stadler

Krakauer

2010

Journal of Theoretical Biology

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Chromatin regulation is understood to be one of the fundamental modes of gene regulation in eukaryotic cells. We argue that the basic proteins that determine the chromatin architecture constitute an evolutionary ancient layer of transcriptional regulation common to all three domains of life. We explore phylogenetically, sources of innovation in chromatin regulation, focusing on protein domains related to chromatin structure and function, demonstrating a step-wise increase of complexity in chromatin regulation. Building upon the highly conserved use of variants of chromosomal architectural proteins to distinguish chromosomal states, Eukarya secondarily acquired mechanisms for "writing" chemical modifications onto chromatin that constitute persistent signals. The acquisition of reader domains enabled decoding of these complex, signal combinations and a decoupling of the signal from immediate biochemical effects. We show how the coupling of reading and writing, which is most prevalent in crown-group Eukarya, could have converted chromatin into a powerful computational device capable of storing and processing more information than pure cis-regulatory networks.Key words: Chromatin, gene regulation, evolution Summary of Findings and Evolutionary HypothesisGene regulation in extant organisms is a complex adaptive system making use of a diversity of mechanisms to ensure that proteins and complementary macromolecular components are produced and maintained at functional levels in variable environments.In this contribution we focus on one key regulatory subsystem of the cell: chromatin regulation. We argue that chromatin functioned as general regulator of transcription in the primordial nucleus, and that a series of key molecular innovations has significantly expanded the regulatory scope of the cell. In this section we summarize the key empirical results of the paper. Sections 2 through 6 provide the empirical support for these claims. In section 7, we formulate an evolutionary Email addresses: sonja@bioinf.uni-leipzig.de (Sonja J. Prohaska), studla@bioinf.uni-leipzig.de (Peter F. Stadler), krakauer@santafe.edu (David C. Krakauer) hypothesis that seeks to explain our findings in terms of the evolution of proto-genetic regulation. We then interpret this evolutionary sequence in terms of increasing computational power by locating key stages of the evolutionary sequence within a formal model of computation. Since sections 2-6 are primarily concerned with presenting evidence, those interested in the conceptual development of the argument can focus on sections 7 and 8.Two variants of Chromosomal Architectural Proteins (ChAPs) are sufficient to define binary genomic, and potentially phenotypic, states. We show how extensions to this binary system lead to potential distinctions among an increasing number of genomic states, culminating in forms of control localized to specific sites in the genome, as illustrated for example by extant mammalian histone variants capable of differential expression and/or localization to r...

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“…Many trees suggest archaebacterial holophyly (Yutin et al 2008), but despite incontrovertible evidence for multiple losses within Filarchaeota, some investigators ignore the possibility of eurybacterial actin/ESCRT loss and suppose that eukaryotes evolved from filarchaeotes. Contradictorily, others assumed that eukaryotes evolved from euryarchaeotes (where eukaryotic-like glycosyltransferase is more widespread than in crenarchaeotes) because of histone similarities (Reeve et al 2004;Cubonova et al 2005) or the phylogenetically refuted and mechanistically implausible hypothesis that eukaryotes evolved from a methanogenic euryarchaeote (Martin and Müller 1998).…”

Section: Diverse Cell Biology Of Filarchaeota Clarifies Neomuran Earlmentioning

confidence: 99%

The Neomuran Revolution and Phagotrophic Origin of Eukaryotes and Cilia in the Light of Intracellular Coevolution and a Revised Tree of Life

Cavalier‐Smith

2014

Cold Spring Harbor Perspectives in Biology

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Three kinds of cells exist with increasingly complex membrane-protein targeting: Unibacteria (Archaebacteria, Posibacteria) with one cytoplasmic membrane (CM); Negibacteria with a two-membrane envelope (inner CM; outer membrane [OM]); eukaryotes with a plasma membrane and topologically distinct endomembranes and peroxisomes. I combine evidence from multigene trees, palaeontology, and cell biology to show that eukaryotes and archaebacteria are sisters, forming the clade neomura that evolved 1.2 Gy ago from a posibacterium, whose DNA segregation and cell division were destabilized by murein wall loss and rescued by the evolving novel neomuran endoskeleton, histones, cytokinesis, and glycoproteins. Phagotrophy then induced coevolving serial major changes making eukaryote cells, culminating in two dissimilar cilia via a novel gliding-fishing -swimming scenario. I transfer Chloroflexi to Posibacteria, root the universal tree between them and Heliobacteria, and argue that Negibacteria are a clade whose OM, evolving in a green posibacterium, was never lost. THE FIVE KINDS OF CELLST he eukaryotic cell originated by the most complex set of evolutionary changes since life began: eukaryogenesis. Their complexity and mechanistic difficulty explain why eukaryotes evolved 2 billion years or more after prokaryotes (Cavalier-Smith 2006a). To understand these changes, we must consider the cell biology of all five major kinds of cells (Fig. 1); determine their correct phylogenetic relationships; and explain the causes, steps, and detailed mechanisms of the radical transitions between them. Figure 1 highlights three fundamentally different kinds of prokaryote differing greatly in membrane topology and membrane and wall chemistry. In all cells, the major membrane lipids are glycerophospholipids having two hydrophobic hydrocarbon tails attached to a hydrophilic phosphorylated glycerol head, but glycerol-phosphate stereochemistry differs in archaebacteria (sn-glycerol-1-phosphate) from that in all other cells (sn-glycerol-3-phosphate). Negibacteria and posibacteria (collectively called

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Archaeal histones: structures, stability and DNA binding

Cited by 53 publications

References 23 publications

Sir2 and the Acetyltransferase, Pat, Regulate the Archaeal Chromatin Protein, Alba

Sir2 and the Acetyltransferase, Pat, Regulate the Archaeal Chromatin Protein, Alba

Innovation in gene regulation: The case of chromatin computation

The Neomuran Revolution and Phagotrophic Origin of Eukaryotes and Cilia in the Light of Intracellular Coevolution and a Revised Tree of Life

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