Alba shapes the archaeal genome using a delicate balance of bridging and stiffening the DNA

Abstract

Architectural proteins have an important role in shaping the genome and act as global regulators of gene expression. How these proteins jointly modulate genome plasticity is largely unknown. In archaea, one of the most abundant proteins, Alba, is considered to have a key role in organizing the genome. Here we characterize the multimodal architectural properties and interplay of the Alba1 and Alba2 proteins using single-molecule imaging and manipulation techniques. We demonstrate that the two paralogues can bridge and rigidify DNA and that the interplay between the two proteins influences the balance between these effects. Our data yield a structural model that explains the multimodal behaviour of Alba proteins and its impact on genome folding.

Transcriptional Repressor TrmBL2 from Thermococcus kodakarensis Forms Filamentous Nucleoprotein Structures and Competes with Histones for DNA Binding in a Salt- and DNA Supercoiling-dependent Manner

“…So far, three families of highly abundant DNA-architectural proteins have been identified in these cells: 1) archaeal histones A/B, 2) Alba, and 3) TrmBL2 (20). Previously, it was shown that archaeal histones wrap DNA and form nucleosome like-particles (14 -16), whereas Alba proteins mediate DNA bridging (17,18). Thus, both of these proteins can contribute to the genomic DNA packaging: histone, via the direct DNA condensation, and Alba, via DNA loops formation and stabilization of pleconemic DNA supercoils.…”

“…Measuring A DNA-TrmBL2 as a function of the protein concentration, c, and by using the worm-like chain model of DNA (30), it is easy to calculate the fraction of DNA binding sites occupied by TrmBL2 proteins, ␣(c), as (18,31) follows. …”

“…Until recently, only two abundant DNA-structuring protein families had been identified as widespread among euryarchaeon cells, one of the two main phyla of the archaeal domain. It is now well established that these families, histones and Alba proteins (13), contribute to DNA condensation (14 -16) and to DNA bridging (17,18), respectively. More recently, another abundant DNA-architectural protein, TrmBL2, a 30.8-kDa protein with a helix-turn-helix motif typical for transcription factor and regulator proteins (19), was found in model euryarchaeon Thermococcus kodakarensis (20).…”

Structural Insights into Nonspecific Binding of DNA by TrmBL2, an Archaeal Chromatin Protein

“…The study also demonstrates that nonspecific interactions of TrmBL2 with DNA backbone contribute significantly to the TrmBL2-DNA binding energy [9]. Together with archaeal histones [10] and Alba (acetylation lowers binding affinity) [10,11], TK0471/TrmBL2 is now considered to be a member of chromosome structuring proteins in archaea [12].…”

Transcription Regulation in Archaea

“…Crenarchaeonencoded nucleoid-associated proteins have been shown to influence transcription output through the acetylation/deaceytlation of Alba in vitro (76), although Alba has not yet been shown to influence transcription in vivo. It is possible that Alba regulates transcription, given that Alba proteins can loop, condense, bridge, and even saturate DNA in vitro, but the in vivo dynamics remain unknown (178)(179)(180)(181)(182). In the euryarchaeal organism Methanococcus voltae the deletion of the gene encoding Alba resulted in the upregulation of only a small number of genes, implying that Albabased regulation may be limited in scope (173).…”