Transcriptional activation in the context of repression mediated by archaeal histones

Wilkinson, Steven; Ouhammouch, Mohamed; Geiduschek, E. Peter

doi:10.1073/pnas.1002360107

Cited by 30 publications

(31 citation statements)

References 40 publications

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“…For most ORFs for which an increase in the transcription level occurred, it occurred in the absence of either HTkA or HTkB, consistent with both histones normally negatively regulating the transcriptions of these genes. Based on in vitro studies, promoter binding by HTkA and HTkB most likely limits access of the transcription apparatus and thus limits the initiation of the transcription of these genes (7,43,44). By using high-resolution nucleosome position technology (1), and with the availability of T. kodakarensis LC124 and LC125, this prediction can now be tested.…”

Section: Discussionmentioning

confidence: 99%

“…All transactions in these species that involve chromosomal DNA must therefore be considered in terms of histone-bound chromatin. The presence of histones in Archaea, but not in Bacteria, was a major distinction first recognized ϳ20 years ago (26), and research since then has established the detailed structure of archaeal histones (3, 19); the composition and architecture of the archaeal nucleosome (11,20,22,24,30); and the consequences of archaeal histone binding on DNA topology, replication, and transcription in vitro (7,37,43,44). Archaeal nucleosomes resemble the eukaryotic tetrasome, the structure at the center of the eukaryotic nucleosome formed by ϳ90 bp of DNA wrapped around a histone (H3ϩH4) 2 tetramer (20,28,30).…”

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confidence: 99%

“…It is therefore intriguing and important to determine if archaeal histones nevertheless participate in regulating genome functions. In this regard, in species with more than one archaeal histone, differences in their expression levels do correlate with differences in laboratory growth rates (4, 25), but how this regulation is achieved and its physiological consequences are unknown.Archaeal histone binding to DNA in vitro introduces DNA topology constraints, prevents transcription initiation, and impedes transcript extension (7,20,43,44). However, only with the development of genetic approaches has it become possible to investigate how these in vitro observations relate to in vivo functions.…”

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confidence: 99%

“…Archaeal histone binding to DNA in vitro introduces DNA topology constraints, prevents transcription initiation, and impedes transcript extension (7,20,43,44). However, only with the development of genetic approaches has it become possible to investigate how these in vitro observations relate to in vivo functions.…”

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An Archaeal Histone Is Required for Transformation of Thermococcus kodakarensis

et al. 2012

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dArchaeal histones wrap DNA into complexes, designated archaeal nucleosomes, that resemble the tetrasome core of a eukaryotic nucleosome. Therefore, all DNA interactions in vivo in Thermococcus kodakarensis, the most genetically versatile model species for archaeal research, must occur in the context of a histone-bound genome. Here we report the construction and properties of T. kodakarensis strains that have TK1413 or TK2289 deleted, the genes that encode HTkA and HTkB, respectively, the two archaeal histones present in this archaeon. All attempts to generate a strain with both TK1413 and TK2289 deleted were unsuccessful, arguing that a histone-mediated event(s) in T. kodakarensis is essential. The HTkA and HTkB amino acid sequences are 84% identical (56 of 67 residues) and 94% similar (63 of 67 residues), but despite this homology and their apparent redundancy in terms of supporting viability, the absence of HTkA and HTkB resulted in differences in growth and in quantitative and qualitative differences in genome transcription. A most surprising result was that the deletion of TK1413 (⌬htkA) resulted in a T. kodakarensis strain that was no longer amenable to transformation, whereas the deletion of TK2289 (⌬htkB) had no detrimental effects on transformation. Potential roles for the archaeal histones in regulating gene expression and for HTkA in DNA uptake and recombination are discussed.T he histone fold apparently evolved before the archaeal and eukaryotic lineages diverged ϳ1.5 to 1.9 billion years ago, and now almost all eukaryotes, Euryarchaea, Nanoarchaea, Thaumarchaea, and some Crenarchaea employ histone fold-based DNA binding to wrap and compact their genomic DNA (2,9,14,21,28,30,38). All transactions in these species that involve chromosomal DNA must therefore be considered in terms of histone-bound chromatin. The presence of histones in Archaea, but not in Bacteria, was a major distinction first recognized ϳ20 years ago (26), and research since then has established the detailed structure of archaeal histones (3, 19); the composition and architecture of the archaeal nucleosome (11,20,22,24,30); and the consequences of archaeal histone binding on DNA topology, replication, and transcription in vitro (7,37,43,44). Archaeal nucleosomes resemble the eukaryotic tetrasome, the structure at the center of the eukaryotic nucleosome formed by ϳ90 bp of DNA wrapped around a histone (H3ϩH4) 2 tetramer (20,28,30). Archaeal histones do not, however, have homologues of the N-and C-terminal amino acid extensions (21) that contain the targets for eukaryotic histone acetylation and methylation and thus provide the basis for epigenetic regulation. Consistent with this, scrutiny of archaeal genome sequences has failed to detect recognizable homologues of the eukaryotic histone modification systems, and to date, no archaeal histone modification has been described (5). It is therefore intriguing and important to determine if archaeal histones nevertheless participate in regulating genome functions. In this regard, in species ...

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

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confidence: 99%

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An Archaeal Histone Is Required for Transformation of Thermococcus kodakarensis

et al. 2012

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“…This appears to be a general mechanism of histone-based regulation in some halophiles and a more specialized mechanism of regulation in other species. The transcriptional activator Ptr2 from Methanocaldococcus jannaschii must outcompete histones for binding to the promoter to activate transcription of select genes (183).…”

Section: Nucleosome Occupancy At the Promotermentioning

confidence: 99%

Transcription Regulation in Archaea

2016

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The known diversity of metabolic strategies and physiological adaptations of archaeal species to extreme environments is extraordinary. Accurate and responsive mechanisms to ensure that gene expression patterns match the needs of the cell necessitate regulatory strategies that control the activities and output of the archaeal transcription apparatus. Archaea are reliant on a single RNA polymerase for all transcription, and many of the known regulatory mechanisms employed for archaeal transcription mimic strategies also employed for eukaryotic and bacterial species. Novel mechanisms of transcription regulation have become apparent by increasingly sophisticated in vivo and in vitro investigations of archaeal species. This review emphasizes recent progress in understanding archaeal transcription regulatory mechanisms and highlights insights gained from studies of the influence of archaeal chromatin on transcription. RNA polymerase (RNAP) is a well-conserved, multisubunit essential enzyme that transcribes DNA to generate RNA in all cells. Although RNA synthesis is carried out by RNAP, the activities of RNAP during each phase of transcription are subject to basal and regulatory transcription factors. Substantial differences in transcription regulatory strategies exist in the three domains (Bacteria, Archaea, and Eukarya). Only a single transcription factor (NusG or Spt5) is universally conserved (1, 2), and the roles of many archaeon-encoded factors have not been evaluated using in vivo and in vitro techniques. Archaea are reliant on a transcription apparatus that is homologous to the eukaryotic transcription machinery; similarities include additional RNAP subunits that form a discrete subdomain of RNAP (3, 4) as well as basal transcription factors that direct transcription initiation and elongation (5-8).The shared homology of archaeal-eukaryotic transcription components aligns with the shared ancestry of Archaea and Eukarya, and this homology often is exclusive of Bacteria. Archaea are prokaryotic, but the transcription apparatus of Bacteria differs significantly from that of Archaea and Eukarya.The archaeal transcription apparatus is most commonly summarized as a simplified version of the eukaryotic machinery. In some respects this is true, as homologs of only a few eukaryotic transcription factors are encoded in archaeal genomes, and archaeal transcription in vitro can be supported by just a few transcription factors. However, much regulatory activity in eukaryotes is devoted to posttranslational modifications of chromatin, RNAP, and transcription factors, and this complexity seemingly does not transfer to the Archaea, where few posttranslational modifications or chromatin-imposed regulation events are currently known. The ostensible simplicity of archaeal transcription is under constant revision, as more detailed examinations of archaeon-encoded factors become possible through increasingly sophisticated in vivo and in vitro techniques. This review will highlight the current understanding of archaeal transcriptio...

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