Structure of histone-based chromatin in Archaea

Origin of DNA compaction As a repeating unit in eukaryotic chromatin, a nucleosome wraps DNA in superhelical turns around a histone octamer. Mattiroli et al. present the crystal structure of an archaeal histone-DNA complex in which the histone-mediated DNA geometry is exactly the same as that in the nucleosome. Comparing features of archaeal and eukaryotic chromatin structures offers important insights into the evolution of eukaryotic nucleosomes. Science, this issue p. 609 Archaeal histone homodimers form a complex with DNA that is similar to the eukaryotic nucleosome. Small basic proteins present in most Archaea share a common ancestor with the eukaryotic core histones. We report the crystal structure of an archaeal histone-DNA complex. DNA wraps around an extended polymer, formed by archaeal histone homodimers, in a quasi-continuous superhelix with the same geometry as DNA in the eukaryotic nucleosome. Substitutions of a conserved glycine at the interface of adjacent protein layers destabilize archaeal chromatin, reduce growth rate, and impair transcription regulation, confirming the biological importance of the polymeric structure. Our data establish that the histone-based mechanism of DNA compaction predates the nucleosome, illuminating the origin of the nucleosome.

[1]  H. Kono,et al.  Crystal structure of the overlapping dinucleosome composed of hexasome and octasome , 2017, Science.

[2]  T. Oshima,et al.  Archaeal histone distribution is associated with archaeal genome base composition. , 2017, The Journal of general and applied microbiology.

[3]  Thijs J. G. Ettema,et al.  Asgard archaea illuminate the origin of eukaryotic cellular complexity , 2017, Nature.

[4]  Thijs J. G. Ettema,et al.  Complex archaea that bridge the gap between prokaryotes and eukaryotes , 2015, Nature.

[5]  Borries Demeler,et al.  Characterization of Size, Anisotropy, and Density Heterogeneity of Nanoparticles by Sedimentation Velocity , 2014, Analytical chemistry.

[6]  L. Aravind,et al.  Protein and DNA modifications: evolutionary imprints of bacterial biochemical diversification and geochemistry on the provenance of eukaryotic epigenetics. , 2014, Cold Spring Harbor perspectives in biology.

[7]  Mingzhu Wang,et al.  Cryo-EM Study of the Chromatin Fiber Reveals a Double Helix Twisted by Tetranucleosomal Units , 2014, Science.

[8]  Gary Gorbet,et al.  A parametrically constrained optimization method for fitting sedimentation velocity experiments. , 2014, Biophysical journal.

[9]  K. Moore,et al.  An alternative beads‐on‐a‐string chromatin architecture in Thermococcus kodakarensis , 2013, EMBO reports.

[10]  Yvonne N Fondufe-Mittendorf,et al.  Archaeal nucleosome positioning in vivo and in vitro is directed by primary sequence motifs , 2013, BMC Genomics.

[11]  Marc T. Facciotti,et al.  Sequencing of Seven Haloarchaeal Genomes Reveals Patterns of Genomic Flux , 2012, PloS one.

[12]  Travis H. Hileman,et al.  Genetics Techniques for Thermococcus kodakarensis , 2012, Front. Microbio..

[13]  J. Reeve,et al.  Deletion of alternative pathways for reductant recycling in Thermococcus kodakarensis increases hydrogen production , 2011, Molecular microbiology.

[14]  S. McNicholas,et al.  Presenting your structures: the CCP4mg molecular-graphics software , 2011, Acta crystallographica. Section D, Biological crystallography.

[15]  N. Pannu,et al.  REFMAC5 for the refinement of macromolecular crystal structures , 2011, Acta crystallographica. Section D, Biological crystallography.

[16]  Randy J. Read,et al.  Overview of the CCP4 suite and current developments , 2011, Acta crystallographica. Section D, Biological crystallography.

[17]  M. Mann,et al.  Andromeda: a peptide search engine integrated into the MaxQuant environment. , 2011, Journal of proteome research.

[18]  Song Tan,et al.  Nucleosome structural studies. , 2011, Current opinion in structural biology.

[19]  Steven Henikoff,et al.  Histone variants — ancient wrap artists of the epigenome , 2010, Nature Reviews Molecular Cell Biology.

[20]  Stefano Piccolo,et al.  MicroRNA control of signal transduction , 2010, Nature Reviews Molecular Cell Biology.

[21]  Randy J. Read,et al.  Acta Crystallographica Section D Biological , 2003 .

[22]  Vincent B. Chen,et al.  Correspondence e-mail: , 2000 .

[23]  J. Reeve,et al.  Thermococcus kodakarensis Genetics: TK1827-Encoded β-Glycosidase, New Positive-Selection Protocol, and Targeted and Repetitive Deletion Technology , 2009, Applied and Environmental Microbiology.

[24]  M. Mann,et al.  MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification , 2008, Nature Biotechnology.

[25]  J. Reeve,et al.  Archaeal chromatin proteins histone HMtB and Alba have lost DNA-binding ability in laboratory strains of Methanothermobacter thermautotrophicus , 2008, Extremophiles.

[26]  Randy J. Read,et al.  Phaser crystallographic software , 2007, Journal of applied crystallography.

[27]  M. Mann,et al.  In-gel digestion for mass spectrometric characterization of proteins and proteomes , 2006, Nature Protocols.

[28]  J. Reeve,et al.  Archaeal histones and the origin of the histone fold. , 2006, Current opinion in microbiology.

[29]  Kevin Cowtan,et al.  research papers Acta Crystallographica Section D Biological , 2005 .

[30]  Karolin Luger,et al.  Molecular recognition of the nucleosomal "supergroove". , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[31]  Steven Henikoff,et al.  Phylogenomics of the nucleosome , 2003, Nature Structural Biology.

[32]  J. Reeve,et al.  Conserved Eukaryotic Histone-Fold Residues Substituted into an Archaeal Histone Increase DNA Affinity but Reduce Complex Flexibility , 2003, Journal of bacteriology.

[33]  J. Zlatanova,et al.  The archaeal histone-fold protein HMf organizes DNA into bona fide chromatin fibers. , 2001, Structure.

[34]  J A Lake,et al.  An ancestral nuclear protein assembly: Crystal structure of the Methanopyrus kandleri histone , 2001, Protein science : a publication of the Protein Society.

[35]  J. Reeve,et al.  Molecular components of the archaeal nucleosome. , 2001, Biochimie.

[36]  K. Decanniere,et al.  Crystal structures of recombinant histones HMfA and HMfB from the hyperthermophilic archaeon Methanothermus fervidus. , 2000, Journal of molecular biology.

[37]  J. Widom,et al.  Archaeal histone selection of nucleosome positioning sequences and the procaryotic origin of histone-dependent genome evolution. , 2000, Journal of molecular biology.

[38]  J. Reeve,et al.  Mutational analysis of archaeal histone-DNA interactions. , 2000, Journal of molecular biology.

[39]  T. Richmond,et al.  The histone tails of the nucleosome. , 1998, Current opinion in genetics & development.

[40]  J. Widom,et al.  New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. , 1998, Journal of molecular biology.

[41]  T. Richmond,et al.  Crystal structure of the nucleosome core particle at 2.8 Å resolution , 1997, Nature.

[42]  M. Summers,et al.  NMR structure of HMfB from the hyperthermophile, Methanothermus fervidus, confirms that this archaeal protein is a histone. , 1996, Journal of molecular biology.

[43]  Wolfgang Kabsch,et al.  Automatic indexing of rotation diffraction patterns , 1988 .

[44]  Uma M. Muthurajan,et al.  In Vitro Chromatin Assembly: Strategies and Quality Control. , 2016, Methods in enzymology.

[45]  Alexei Vagin,et al.  Molecular replacement with MOLREP. , 2010, Acta crystallographica. Section D, Biological crystallography.

[46]  P. Evans,et al.  Scaling and assessment of data quality. , 2006, Acta crystallographica. Section D, Biological crystallography.

[47]  Uma M. Muthurajan,et al.  Reconstitution of nucleosome core particles from recombinant histones and DNA. , 2004, Methods in enzymology.

[48]  Roman A. Laskowski,et al.  PDBsum: summaries and analyses of PDB structures , 2001, Nucleic Acids Res..