Mechanical and structural properties of archaeal hypernucleosomes

Author:

Henneman Bram1,Brouwer Thomas B2,Erkelens Amanda M1,Kuijntjes Gert-Jan2,van Emmerik Clara3,van der Valk Ramon A1,Timmer Monika1,Kirolos Nancy C S1,van Ingen Hugo3ORCID,van Noort John2ORCID,Dame Remus T14ORCID

Affiliation:

1. Leiden Institute of Chemistry, Leiden University, Einsteinweg 55, 2333CC Leiden, The Netherlands

2. Biological and Soft Matter Physics, Huygens-Kamerlingh Onnes Laboratory, Leiden University, Niels Bohrweg 2, 2333CA Leiden, The Netherlands

3. Bijvoet Center for Biomolecular Research, Utrecht University, Padualaan 8, 3584CH Utrecht, The Netherlands

4. Centre for Microbial Cell Biology, Leiden University, Einsteinweg 55, 2333CC Leiden, The Netherlands

Abstract

Abstract Many archaea express histones, which organize the genome and play a key role in gene regulation. The structure and function of archaeal histone–DNA complexes remain however largely unclear. Recent studies show formation of hypernucleosomes consisting of DNA wrapped around an ‘endless’ histone-protein core. However, if and how such a hypernucleosome structure assembles on a long DNA substrate and which interactions provide for its stability, remains unclear. Here, we describe micromanipulation studies of complexes of the histones HMfA and HMfB with DNA. Our experiments show hypernucleosome assembly which results from cooperative binding of histones to DNA, facilitated by weak stacking interactions between neighboring histone dimers. Furthermore, rotational force spectroscopy demonstrates that the HMfB–DNA complex has a left-handed chirality, but that torque can drive it in a right-handed conformation. The structure of the hypernucleosome thus depends on stacking interactions, torque, and force. In vivo, such modulation of the archaeal hypernucleosome structure may play an important role in transcription regulation in response to environmental changes.

Funder

Netherlands Organization for Scientific Research

FOM Foundation

Human Frontiers Science

Publisher

Oxford University Press (OUP)

Subject

Genetics

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