Sequence-Dependent T:G Base Pair Opening in DNA Double Helix Bound by Cren7, a Chromatin Protein Conserved among Crenarchaea

Lei, Tian; Zhang, Zhenfeng; Wang, Hanqian; Zhao, Mengchen; Dong, Yuhui; Gong, Yong

doi:10.1371/journal.pone.0163361

Cited by 6 publications

(5 citation statements)

References 30 publications

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“…MC1, for example, protects against radiation damage 34 , a frequent insult for halophiles that live in shallow aquatic environments. Conversely, Cren7 binds to T:G mismatches produced by cytosine deamination events 35 , which become more common at higher temperature. We propose that while denaturation might shape total NAP abundance, NAP diversity is likely a product of both exchangeability and species-specific requirements for nucleoid function and maintenance.…”

Section: Discussionmentioning

confidence: 99%

Growth temperature and chromatinization in archaea

et al. 2022

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DNA in cells is associated with proteins that constrain its structure and affect DNA-templated processes including transcription and replication. HU and histones are the main constituents of chromatin in bacteria and eukaryotes, respectively, with few exceptions. Archaea, in contrast, have diverse repertoires of nucleoid-associated proteins (NAPs). To analyse the evolutionary and ecological drivers of this diversity, we combined a phylogenomic survey of known and predicted NAPs with quantitative proteomic data. We identify the Diaforarchaea as a hotbed of NAP gain and loss, and experimentally validate candidate NAPs in two members of this clade, Thermoplasma volcanium and Methanomassiliicoccus luminyensis. Proteomic analysis across a diverse sample of 19 archaea revealed that NAP investment varies from <0.03% to >5% of total protein. This variation is predicted by growth temperature. We propose that high levels of chromatinization have evolved as a mechanism to prevent uncontrolled helix denaturation at higher temperatures, with implications for the origin of chromatin in both archaea and eukaryotes.

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Section: Discussionmentioning

confidence: 99%

Growth temperature and chromatinization in archaea

et al. 2022

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“…In contrast to the head-to-head arrangement of Sso7d molecules along DNA (Agback et al, 1998;Turaga et al, 2016), Cren7 molecules bind DNA in a head-to-tail manner, without protein-protein interaction, in the two multiprotein-DNA complexes. Modeling studies reveal that flipping of mol A, mol B or both would not result in conflicts between the two monomers (data not shown).…”

Section: Dna Binding Mode Of Cren7mentioning

confidence: 98%

“…Surface plasmon resonance experiments were carried out at 25°C using the BIAcore 3000 instrument (BIAcore AB, Uppsala, Sweden) as described previously (Tian et al, 2016). The running buffer contained 50 mM Tris-Cl, pH 7.6, 100 mM NaCl and 0.005% (v/v) Tween 20.…”

Section: Spr Assaysmentioning

confidence: 99%

“…Sul7 exists as monomers in solution. However, it appears to form head-to-head dimers upon binding to DNA (Agback et al, 1998;Turaga et al, 2016). In addition, the solution structure of Sso7d, a Sul7 protein from Sulfolobus solfataricus, in complex with CTAGCGCGCTAG (GC3) revealed that the Sso7d dimer deformed DNA differently from the Sso7d monomer in the protein-DNA co-crystals (Agback et al, 1998;Gao et al, 1998).…”

Section: Introductionmentioning

confidence: 99%

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Architectural roles of Cren7 in folding crenarchaeal chromatin filament

Zhang

Zhao

Chen

et al. 2019

Molecular Microbiology

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Summary Archaea have evolved various strategies in chromosomal organization. While histone homologues exist in most archaeal phyla, Cren7 is a chromatin protein conserved in the Crenarchaeota. Here, we show that Cren7 preferentially binds DNA with AT‐rich sequences over that with GC‐rich sequences with a binding size of 6~7 bp. Structural studies of Cren7 in complex with either an 18‐bp or a 20‐bp double‐stranded DNA fragment reveal that Cren7 binds to the minor groove of DNA as monomers in a head‐to‐tail manner. The neighboring Cren7 monomers are located on the opposite sides of the DNA duplex, with each introducing a single‐step sharp kink by intercalation of the hydrophobic side chain of Leu28, bending the DNA into an S‐shape conformation. A structural model for the chromatin fiber folded by Cren7 was established and verified by the analysis of cross‐linked Cren7‐DNA complexes by atomic force microscopy. Our results suggest that Cren7 differs significantly from Sul7, another chromatin protein conserved among Sulfolobus species, in both DNA binding and deformation. These data shed significant light on the strategy of chromosomal DNA organization in crenarchaea.

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“…Sso7d was also found to stimulate the intramolecular ligation of a 129-bp fragment, indicating the ability of the protein to induce DNA bending in solution ( 14 ). Structural studies showed that both proteins adopt an SH3-like fold, binding DNA in the minor groove and inducing a single-step sharp kink into DNA (approximately 50° to 60°) ( 15 – 19 ). A single-molecule (SM) analysis performed using magnetic tweezers revealed that Cren7 and Sso7d compact DNA to similar extents by introducing rigid bends ( 20 ).…”

Section: Introductionmentioning

confidence: 99%

Archaeal Chromatin Proteins Cren7 and Sul7d Compact DNA by Bending and Bridging

Zhang

Zhan

Wang

et al. 2020

mBio

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Archaeal chromatin proteins Cren7 and Sul7d from Sulfolobus are DNA benders. To better understand their architectural roles in chromosomal DNA organization, we analyzed DNA compaction by Cren7 and Sis7d, a Sul7d family member, from Sulfolobus islandicus at the single-molecule (SM) level by total single-molecule internal reflection fluorescence microscopy (SM-TIRFM) and atomic force microscopy (AFM). We show that both Cren7 and Sis7d were able to compact singly tethered λ DNA into a highly condensed structure in a three-step process and that Cren7 was over an order of magnitude more efficient than Sis7d in DNA compaction. The two proteins were similar in DNA bending kinetics but different in DNA condensation patterns. At saturating concentrations, Sis7d formed randomly distributed clusters whereas Cren7 generated a single and highly condensed core on plasmid DNA. This observation is consistent with the greater ability of Cren7 than of Sis7d to bridge DNA. Our results offer significant insights into the mechanism and kinetics of chromosomal DNA organization in Crenarchaea. IMPORTANCE A long-standing question is how chromosomal DNA is packaged in Crenarchaeota, a major group of archaea, which synthesize large amounts of unique small DNA-binding proteins but in general contain no archaeal histones. In the present work, we tested our hypothesis that the two well-studied crenarchaeal chromatin proteins Cren7 and Sul7d compact DNA by both DNA bending and bridging. We show that the two proteins are capable of compacting DNA, albeit with different efficiencies and in different manners, at the single molecule level. We demonstrate for the first time that the two proteins, which have long been regarded as DNA binders and benders, are able to mediate DNA bridging, and this previously unknown property of the proteins allows DNA to be packaged into highly condensed structures. Therefore, our results provide significant insights into the mechanism and kinetics of chromosomal DNA organization in Crenarchaeota.

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Sequence-Dependent T:G Base Pair Opening in DNA Double Helix Bound by Cren7, a Chromatin Protein Conserved among Crenarchaea

Cited by 6 publications

References 30 publications

Growth temperature and chromatinization in archaea

Growth temperature and chromatinization in archaea

Architectural roles of Cren7 in folding crenarchaeal chromatin filament

Archaeal Chromatin Proteins Cren7 and Sul7d Compact DNA by Bending and Bridging

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