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Archaeal histones: dynamic and versatile genome architects

  • Received: 09 October 2015 Accepted: 26 November 2015 Published: 01 December 2015
  • Genome organization and compaction in Archaea involves different chromatin proteins, among which homologues of eukaryotic histones. Archaeal histones are considered the ancestors of their eukaryotic counterparts, which isreflected in the way they position along the genome and wrap DNA. Evolution from the archaeal modes of action to the prototypical eukaryotic nucleosome may be attributed to altered histone-histone interactions and DNA sequence determinants cooperating to yield stable multimeric structures. The identification of a new candidate phylum, proposed to be a missing link between archaea and eukaryotes, Lokiarchaeaota, may be instrumental in addressing this hypothesis.

    Citation: Bram Henneman, Remus T. Dame. Archaeal histones: dynamic and versatile genome architects[J]. AIMS Microbiology, 2015, 1(1): 72-81. doi: 10.3934/microbiol.2015.1.72

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  • Genome organization and compaction in Archaea involves different chromatin proteins, among which homologues of eukaryotic histones. Archaeal histones are considered the ancestors of their eukaryotic counterparts, which isreflected in the way they position along the genome and wrap DNA. Evolution from the archaeal modes of action to the prototypical eukaryotic nucleosome may be attributed to altered histone-histone interactions and DNA sequence determinants cooperating to yield stable multimeric structures. The identification of a new candidate phylum, proposed to be a missing link between archaea and eukaryotes, Lokiarchaeaota, may be instrumental in addressing this hypothesis.


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    [1] Zillig W (1991) Comparative biochemistry of Archaea and Bacteria. Curr Opin Gen Dev 1: 544-551. doi: 10.1016/S0959-437X(05)80206-0
    [2] Williams TA, Foster PG, Cox CJ, et al. (2013) An archaeal origin of eukaryotes supports only two primary domains of life. Nature 504: 231-236. doi: 10.1038/nature12779
    [3] Pereira SL, Reeve JN (1998) Histones and nucleosomes in Archaea and Eukarya: a comparative analysis. Extremophiles 2: 141-148. doi: 10.1007/s007920050053
    [4] Cheung P, Allis CD, Sassone-Corsi P(2000) Signaling to chromatin through histone modifications. Cell 103: 263-271.
    [5] White MF, Bell SD (2002) Holding it together: chromatin in the Archaea. Trends Genetics 18: 621-626. doi: 10.1016/S0168-9525(02)02808-1
    [6] Jelinska C, Conroy MJ, Craven CJ, et al. (2005)Obligate Heterodimerization of the Archaeal Alba2 Protein with Alba1 Provides a Mechanism for Control of DNA Packaging. Structure 13: 963-971.
    [7] Dame RT (2005)The role of nucleoid-associated proteins in the organization and compaction of bacterial chromatin. Mol Microbiol 56: 858-870.
    [8] Dame RT, Kalmykowa OJ, Grainger DC (2011)Chromosomal macrodomains and associated proteins: implications for DNA organization and replication in gram negative bacteria. PLoS Genet 7: e1002123.
    [9] Dorman CJ (2013)Genome architecture and global gene regulation in bacteria: making progress towards a unified model? Nat Rev Microbiol 11: 349-355.
    [10] Spang A, Saw JH, Jørgensen SL, et al. (2015)Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521: 173-179.
    [11] Talbert PB, Henikoff S (2010)Histone variants —ancient wrap artists of the epigenome. Nat Rev Mol Cell Biol 11: 264-275.
    [12] Peeters E, Driessen RPC, Werner F, et al. (2015)The interplay between nucleoid organization and transcription in archaeal genomes. Nature Rev Microbiol 13: 333-341.
    [13] Bailey KA, Marc F, Sandman K, et al. (2002)Both DNA and histone fold sequences contribute to archaeal nucleosome stability. J Biol Chem 277: 9293-9301.
    [14] Luger K, Dechassa ML, Tremethick DJ (2012)New insights into nucleosome and chromatin structure: an ordered state or a disordered affair? Nat Rev Mol Cell Biol 13: 436-447.
    [15] Pereira SL, Grayling RA, Lurz R, et al. (1997)Archaeal nucleosomes. Proc Natl Acad Sci U S A 94: 12633-12637. doi: 10.1073/pnas.94.23.12633
    [16] Pereira SL, Reeve JN (1999)Archaeal nucleosome positioning sequence from Methanothermus fervidus. J Mol Biol 289: 675-681.
    [17] Bailey KA, Pereira SL, Widom J, et al. (2000)Archaeal histone selection of nucleosome positioning sequences and the procaryotic origin of histone-dependent genome evolution. J Mol Biol 303: 25-34.
    [18] Maruyama H, Harwood JC, Moore KM, et al. (2013)An alternative beads-on-a-string chromatin architecture in Thermococcus kodakarensis. EMBO Reports 14: 711-717.
    [19] Kornberg RD, Thomas JO (1974)Chromatin structure; oligomers of the histones. Science 184: 865-868.
    [20] Kalashnikova AA, Porter-Goff ME, Muthurajan UM, et al. (2013)The role of the nucleosome acidic patch in modulating higher order chromatin structure. J R Soc Interface 10: 20121022.
    [21] Xie Y, Reeve JN (2004)Transcription by an archaeal RNA polymerase is slowed but not blocked by an archaeal nucleosome. J Bact 186: 3492-3498.
    [22] Marc F, Sandman K, Lurz R, et al. (2002)Archaeal histone tetramerization determines DNA affinity and the direction of DNA supercoiling. J Biol Chem 277: 30879-30886.
    [23] Sandman K, Reeve JN (2006)Archaeal histones and the origin of the histone fold. Curr Op Microbiol 9: 520-525.
    [24] Decanniere K, Babu AM, Sandman K, et al. (2000)Crystal structures of recombinant histones HMfA and HMfB from the hyperthermophilic archaeon Methanothermus fervidus. J Mol Biol 303: 35-47.
    [25] Li WT, Sandman K, Pereira SL, et al. (2000)MJ1647, an open reading frame in the genome of the hyperthermophile Methanococcus jannaschii, encodes a very thermostable archaeal histone with a C-terminal extension. Extremophiles 4: 43-51.
    [26] Hartman AL, Norais C, Badger JH, et al. (2010)The complete genome sequence of Haloferax volcanii DS2, a model archaeon. PLoS One 5: e9605.
    [27] Fahrner RL, Cascio D, Lake JA, et al. (2001)An ancestral nuclear protein assembly: crystal structure of the Methanopyrus kandleri histone. Prot Science 10: 2002-2007.
    [28] Laurens N, Driessen RPC, Heller I, et al. (2012)Alba shapes the archaeal genome using a delicate balance of bridging and stiffening the DNA. Nature Communications 3: 1328-1328.
    [29] Wardleworth BN, Russell RJM, Bell SD, et al. (2002)Structure of Alba: An archaeal chromatin protein modulated by acetylation. EMBO J 21: 4654-4662.
    [30] Ammar R, Torti D, Tsui K, et al. (2012)Chromatin is an ancient innovation conserved between Archaea and Eukarya. eLife 2012: 1-11.
    [31] Warnecke T, Becker EA, Facciotti MT, et al. (2013)Conserved Substitution Patterns around Nucleosome Footprints in Eukaryotes and Archaea Derive from Frequent Nucleosome Repositioning through Evolution. PLoS Comp Biol 9: 9-14.
    [32] Das C, Tyler JK (2013)Histone exchange and histone modifications during transcription and aging. Biochim Biophys Acta 1819: 332-342.
    [33] Sandman K, Reeve JN (2005)Archaeal chromatin proteins: Different structures but common function? Curr Opin Microbiol 8: 656-661.
    [34] Sandman K, Krzycki JA, Dobrinski B, et al. (1990)HMf, a DNA-binding protein isolated from the hyperthermophilic archaeon Methanothermus fervidus, is most closely related to histones. Proc Natl Acad Sci USA 87: 5788-5791.
    [35] van der Valk RA, Vreede J, Cremazy F, et al. (2014)Genomic looping: a key principle of chromatin organization. J Mol Microbiol Biotechnol 24: 344-359.
    [36] Hofmann A, Heermann DW (2015)The role of loops on the order of eukaryotes and prokaryotes. FEBS Lett 589: 2958-2965.
    [37] Ueguchi C, Mizuno T (1993)The Escherichia coli nucleoid protein H-NS functions directly as a transcriptional repressor. EMBO J 12: 1039-1046.
    [38] Efremov AK, Qu Y, Maruyama H, et al. (2015)Transcriptional Repressor TrmBL2 from Thermococcus kodakarensis Forms Filamentous Nucleoprotein Structures and Competes with Histones for DNA Binding in a Salt- and DNA Supercoiling-dependent Manner. J Biol Chem 290: 15770-15784.
    [39] Dulmage KA, Todor H, Schmid K (2015)Growth-Phase-Specific Modulation of Cell Morphology and Gene Expression by an Archaeal Histone Protein. mBio 6: e00649-00615.
    [40] Heinicke I, Müller J, Pittelkow M, et al. (2004)Mutational analysis of genes encoding chromatin proteins in the archaeon Methanococcus voltae indicates their involvement in the regulation of gene expression. Mol Genet Genom 272: 76-87.
    [41] Weidenbach K, Glöer J, Ehlers C, et al. (2008)Deletion of the archaeal histone in Methanosarcina mazei Gö1 results in reduced growth and genomic transcription. Mol Microbiol 67: 662-671.
    [42] Čuboňová L, Katano M, Kanai T, et al. (2012)An archaeal histone is required for transformation of Thermococcus kodakarensis. J Bact 194: 6864-6874.
    [43] Nalabothula N, Xi L, Bhattacharyya S, et al. (2013)Archaeal nucleosome positioning in vivo and in vitro is directed by primary sequence motifs. BMC Genomics 14: 391-391.
    [44] Sandman K, Grayling RA, Dobrinskit B, et al. (1994)Growth-phase-dependent synthesis of histones in the archaeon Methanothermus fervidus. Biochemistry 91: 12624-12628.
    [45] Bailey KA, Reeve JN (1999)DNA repeats and archaeal nucleosome positioning. Res Microbiol 150: 701-709.
    [46] Maruyama H, Shin M, Oda T, et al.(2011)Histone and TK0471/TrmBL2 form a novel heterogeneous genome architecture in the hyperthermophilic archaeon Thermococcus kodakarensis. Mol Biol Cell 22: 386-398.
    [47] Hamiche A, Richard-Foy H (1998)The switch in the helical handedness of the histone (H3-H4)2 tetramer within a nucleoprotein particle requires a reorientation of the H3-H3 interface. J Biol Chem 273: 9261-9269.
    [48] Musgrave D, Forterre P, Slesarev A (2000)Negative constrained DNA supercoiling in archaeal nucleosomes. Mol Microbiol 35: 341-349.
    [49] Barbi M, Mozziconacci J, Victor JM(2012) On the topology of chromatin fibres. Interface Focus 2: 546-554.
    [50] Kouzine F, Levens D, Baranello L (2014)DNA topology and transcription. Nucleus 5: 195-202.
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