Archaeal chromatin ‘slinkies’ are inherently dynamic complexes with deflected DNA wrapping pathways

Eukaryotes and many archaea package their DNA with histones. While the four eukaryotic histones wrap ~147 DNA base pairs into nucleosomes, archaeal histones form ‘nucleosome-like’ complexes that continuously wind between 60 and 500 base pairs of DNA (‘archaeasomes’), suggested by crystal contacts an...

Full description

Bibliographic Details
Main Authors: Samuel Bowerman, Jeff Wereszczynski, Karolin Luger
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2021-03-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/65587
_version_ 1818019825059889152
author Samuel Bowerman
Jeff Wereszczynski
Karolin Luger
author_facet Samuel Bowerman
Jeff Wereszczynski
Karolin Luger
author_sort Samuel Bowerman
collection DOAJ
description Eukaryotes and many archaea package their DNA with histones. While the four eukaryotic histones wrap ~147 DNA base pairs into nucleosomes, archaeal histones form ‘nucleosome-like’ complexes that continuously wind between 60 and 500 base pairs of DNA (‘archaeasomes’), suggested by crystal contacts and analysis of cellular chromatin. Solution structures of large archaeasomes (>90 DNA base pairs) have never been directly observed. Here, we utilize molecular dynamics simulations, analytical ultracentrifugation, and cryoEM to structurally characterize the solution state of archaeasomes on longer DNA. Simulations reveal dynamics of increased accessibility without disruption of DNA-binding or tetramerization interfaces. Mg2+ concentration influences compaction, and cryoEM densities illustrate that DNA is wrapped in consecutive substates arranged 90o out-of-plane with one another. Without ATP-dependent remodelers, archaea may leverage these inherent dynamics to balance chromatin packing and accessibility.
first_indexed 2024-04-14T07:57:26Z
format Article
id doaj.art-5f0dd6e1756d42e1b8f1d2bda0cd1a7d
institution Directory Open Access Journal
issn 2050-084X
language English
last_indexed 2024-04-14T07:57:26Z
publishDate 2021-03-01
publisher eLife Sciences Publications Ltd
record_format Article
series eLife
spelling doaj.art-5f0dd6e1756d42e1b8f1d2bda0cd1a7d2022-12-22T02:05:00ZengeLife Sciences Publications LtdeLife2050-084X2021-03-011010.7554/eLife.65587Archaeal chromatin ‘slinkies’ are inherently dynamic complexes with deflected DNA wrapping pathwaysSamuel Bowerman0https://orcid.org/0000-0003-0753-4294Jeff Wereszczynski1https://orcid.org/0000-0002-2218-3827Karolin Luger2https://orcid.org/0000-0001-5136-5331Department of Biochemistry and Howard Hughes Medical Institute, University of Colorado Boulder, Boulder, United StatesDepartment of Physics and Center for the Molecular Study of Condensed Soft Matter, Illinois Institute of Technology, Chicago, United StatesDepartment of Biochemistry and Howard Hughes Medical Institute, University of Colorado Boulder, Boulder, United StatesEukaryotes and many archaea package their DNA with histones. While the four eukaryotic histones wrap ~147 DNA base pairs into nucleosomes, archaeal histones form ‘nucleosome-like’ complexes that continuously wind between 60 and 500 base pairs of DNA (‘archaeasomes’), suggested by crystal contacts and analysis of cellular chromatin. Solution structures of large archaeasomes (>90 DNA base pairs) have never been directly observed. Here, we utilize molecular dynamics simulations, analytical ultracentrifugation, and cryoEM to structurally characterize the solution state of archaeasomes on longer DNA. Simulations reveal dynamics of increased accessibility without disruption of DNA-binding or tetramerization interfaces. Mg2+ concentration influences compaction, and cryoEM densities illustrate that DNA is wrapped in consecutive substates arranged 90o out-of-plane with one another. Without ATP-dependent remodelers, archaea may leverage these inherent dynamics to balance chromatin packing and accessibility.https://elifesciences.org/articles/65587nucleosomehistonearchaeamolecular dynamicscryo-EMAUC
spellingShingle Samuel Bowerman
Jeff Wereszczynski
Karolin Luger
Archaeal chromatin ‘slinkies’ are inherently dynamic complexes with deflected DNA wrapping pathways
eLife
nucleosome
histone
archaea
molecular dynamics
cryo-EM
AUC
title Archaeal chromatin ‘slinkies’ are inherently dynamic complexes with deflected DNA wrapping pathways
title_full Archaeal chromatin ‘slinkies’ are inherently dynamic complexes with deflected DNA wrapping pathways
title_fullStr Archaeal chromatin ‘slinkies’ are inherently dynamic complexes with deflected DNA wrapping pathways
title_full_unstemmed Archaeal chromatin ‘slinkies’ are inherently dynamic complexes with deflected DNA wrapping pathways
title_short Archaeal chromatin ‘slinkies’ are inherently dynamic complexes with deflected DNA wrapping pathways
title_sort archaeal chromatin slinkies are inherently dynamic complexes with deflected dna wrapping pathways
topic nucleosome
histone
archaea
molecular dynamics
cryo-EM
AUC
url https://elifesciences.org/articles/65587
work_keys_str_mv AT samuelbowerman archaealchromatinslinkiesareinherentlydynamiccomplexeswithdeflecteddnawrappingpathways
AT jeffwereszczynski archaealchromatinslinkiesareinherentlydynamiccomplexeswithdeflecteddnawrappingpathways
AT karolinluger archaealchromatinslinkiesareinherentlydynamiccomplexeswithdeflecteddnawrappingpathways