Chromatin is an ancient innovation conserved between Archaea and Eukarya

Ammar, Ron; Torti, Dax; Tsui, Kyle; Gebbia, Marinella; Durbic, Tanja; Bader, Gary D.; Giaever, Guri; Nislow, Corey

doi:10.7554/elife.00078

Cited by 90 publications

(119 citation statements)

References 39 publications

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“…Interestingly, it was well known that Archaea contain histone-like proteins and form nucleosomelike structures but without tails or chromatin remodeling complex (56)(57)(58). It seems that RNA polymerases alone in Archaea could overcome tailless nucleosomes during transcription since there is no known chromatin remodeling complex in Archaea (58).…”

Section: Discussionmentioning

confidence: 99%

Clipping of arginine-methylated histone tails by JMJD5 and JMJD7

Liu

Wang

Lee

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Two of the unsolved, important questions about epigenetics are: do histone arginine demethylases exist, and is the removal of histone tails by proteolysis a major epigenetic modification process? Here, we report that two orphan Jumonji C domain (JmjC)-containing proteins, JMJD5 and JMJD7, have divalent cationdependent protease activities that preferentially cleave the tails of histones 2, 3, or 4 containing methylated arginines. After the initial specific cleavage, JMJD5 and JMJD7, acting as aminopeptidases, progressively digest the C-terminal products. JMJD5-deficient fibroblasts exhibit dramatically increased levels of methylated arginines and histones. Furthermore, depletion of JMJD7 in breast cancer cells greatly decreases cell proliferation. The protease activities of JMJD5 and JMJD7 represent a mechanism for removal of histone tails bearing methylated arginine residues and define a potential mechanism of transcription regulation.histone tail | arginine methylation | clipping | JMJD5/7

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Section: Discussionmentioning

confidence: 99%

Clipping of arginine-methylated histone tails by JMJD5 and JMJD7

Liu

Wang

Lee

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…The topology of naked DNA templates does influence the positions and efficiencies of intrinsic terminators, suggesting that chromatin templates may also influence termination patterns. Nucleosomes are depleted not only from promoter regions but also from predicted termination regions, suggesting a potential regulatory role for chromatin architecture on termination of transcription (164).…”

Section: Chromatin Architecture Affects the Transcription Cyclementioning

confidence: 99%

“…The best-described complexes are homo-or hetero-histone tetramers, homologous to the H3/H4 tetramer in eukaryotes, that associate with ϳ60 bp of double-stranded DNA. Archaeal histones share similar biases with eukaryotic nucleosomes for flexible DNA sequences and are, in general, absent from the core promoters of archaeal genes (164,165). Archaeal histone proteins share the same core fold as eukaryotic histones but lack the extensions from this fold (i.e., tails) that are highly modified and essential for proper nucleosome dynamics in eukaryotes (166).…”

Section: Chromatin Architecture Affects the Transcription Cyclementioning

confidence: 99%

“…Chromatin architecture at a promoter could influence or prevent transcription initiation by occluding transcription factor binding or inhibiting DNA melting (164,167,168,177). Crenarchaeonencoded nucleoid-associated proteins have been shown to influence transcription output through the acetylation/deaceytlation of Alba in vitro (76), although Alba has not yet been shown to influence transcription in vivo.…”

Section: Nucleosome Occupancy At the Promotermentioning

confidence: 99%

“…These studies contrast the view of histone proteins as general organizational factors with the global influence on gene expression and minimally suggest that the archaeal chromatin of some species is dependent on the activities of many nucleoid-associated proteins. When histone-encoding genes have been deleted, or have been attempted to be deleted from other species, more global disruption of gene expression has been noted (161,164,165,167,(171)(172)(173)(174)(175)(176). Some species are reliant on at least one histone protein, and it is unclear at this point whether the noted global changes in gene expression seen in deletion strains stem from reorganization or disorganization of the archaeal genomes or the primary, secondary, and tertiary effects of localized disruptions that lead to additional differences in regulation at remote sites.…”

Section: Histone-based Regulation Of Transcriptionmentioning

confidence: 99%

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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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Birth of the eukaryotes by a set of reactive innovations: New insights force us to relinquish gradual models

Speijer

2015

BioEssays

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Of two contending models for eukaryotic evolution the "archezoan" has an amitochondriate eukaryote take up an endosymbiont, while "symbiogenesis" states that an Archaeon became a eukaryote as the result of this uptake. If so, organelle formation resulting from new engulfments is simplified by the primordial symbiogenesis, and less informative regarding the bacterium-to-mitochondrion conversion. Gradualist archezoan visions still permeate evolutionary thinking, but are much less likely than symbiogenesis. Genuine amitochondriate eukaryotes have never been found and rapid, explosive adaptive periods characteristic of symbiogenetic models explain this. Mitochondrial proteomes, encoded by genes of "eukaryotic origin" not easily linked to host or endosymbiont, can be understood in light of rapid adjustments to new evolutionary pressures. Symbiogenesis allows "expensive" eukaryotic inventions via efficient ATP generation by nascent mitochondria. However, efficient ATP production equals enhanced toxic internal ROS formation. The synergistic combination of these two driving forces gave rise to the rapid evolution of eukaryotes. Also watch the Video Abstract.

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Chromatin is an ancient innovation conserved between Archaea and Eukarya

Cited by 90 publications

References 39 publications

Clipping of arginine-methylated histone tails by JMJD5 and JMJD7

Clipping of arginine-methylated histone tails by JMJD5 and JMJD7

Transcription Regulation in Archaea

Birth of the eukaryotes by a set of reactive innovations: New insights force us to relinquish gradual models

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