The DNA-binding protein HTa from Thermoplasma acidophilum is an archaeal histone analog

Abstract
Data availability
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Abstract

Histones are a principal constituent of chromatin in eukaryotes and fundamental to our understanding of eukaryotic gene regulation. In archaea, histones are widespread but not universal: several lineages have lost histone genes. What prompted or facilitated these losses and how archaea without histones organize their chromatin remains largely unknown. Here, we elucidate primary chromatin architecture in an archaeon without histones, Thermoplasma acidophilum, which harbours a HU family protein (HTa) that protects part of the genome from micrococcal nuclease digestion. Charting HTa-based chromatin architecture in vitro, in vivo and in an HTa-expressing E. coli strain, we present evidence that HTa is an archaeal histone analog. HTa preferentially binds to GC-rich sequences, exhibits invariant positioning throughout the growth cycle, and shows archaeal histone-like oligomerization behaviour. Our results suggest that HTa, a DNA-binding protein of bacterial origin, has converged onto an architectural role filled by histones in other archaea.

Data availability

All sequencing data generated for this study have been deposited in GEO under accession code GSE127728.

The following data sets were generated

1. Hocher A
2. Warnecke T
(2019) The DNA-binding protein HTa from Thermoplasma acidophilum is an archaeal histone analog
NCBI Gene Expression Omnibus, GSE127728.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE127728

The following previously published data sets were used

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2. Harwood JC
3. Moore KM
4. Paszkiewicz K
5. Durley SC
6. Fukushima H
7. Atomi H
8. Takeyasu K
9. Kent NA
(2013) Thermococcus kodakarensis MNase-Seq
NCBI Sequence Read Archive, SRR495445.

https://www.ncbi.nlm.nih.gov/sra/?term=SRR495445
1. Ammar R
2. Torti D
3. Tsui K
4. Gebbia M
5. Durbic T
6. Bader GD
7. Giaever G
8. Nislow C
(2012) Haloferax volcanii nucleosome map
NCBI Sequence Read Archive, SRR574592.

https://www.ncbi.nlm.nih.gov/sra/?term=SRR574592
1. Rojec M
2. Warnecke T
(2019) The role of archaeal histones in gene expression - a synthetic biology perspective
NCBI Gene Expression Omnibus, GSE127678.

https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE127678

Article and author information

Author details

Antoine Hocher

MRC London Institute of Medical Sciences (LMS), London, United Kingdom

For correspondence
a.hocher@lms.mrc.ac.uk

Competing interests
The authors declare that no competing interests exist.
Maria Rojec

MRC London Institute of Medical Sciences (LMS), London, United Kingdom

Competing interests
The authors declare that no competing interests exist.
Jacob B Swadling

MRC London Institute of Medical Sciences (LMS), London, United Kingdom

Competing interests
The authors declare that no competing interests exist.
Alexander Esin

MRC London Institute of Medical Sciences (LMS), London, United Kingdom

Competing interests
The authors declare that no competing interests exist.
Tobias Warnecke

MRC London Institute of Medical Sciences (LMS), London, United Kingdom

For correspondence
tobias.warnecke@imperial.ac.uk

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-4936-5428

Funding

Medical Research Council (MC_A658_5TY40)

Tobias Warnecke

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.