Modulation of DNA-Biding Properties of Euryarchaeal Architectural Proteins by MG2+ Ions Triggers Drastic Changes in the Global DNA Organization

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DNA-architectural proteins play a major role in the cell genome organization, packaging DNA into a highly ordered chromatin structure inside living cells. It has been previously shown that the conformation of this structure can be very sensitive to surrounding conditions. This way, DNA-architectural proteins not only help to preserve integrity of the chromosomal DNA but also actively participate in the regulation of the cells’ behaviour via modulation of the global gene expression profile in response to environmental cues. Recent experimental studies have provided a lot of useful insights into possible biological functions of individual architectural proteins. However, there is still a large gap in understanding of molecular mechanisms underlying the emergent collective behaviour of these proteins in DNA organization and gene transcription regulation, which is especially the case for archaea cells, whose genome organization remains much less understood comparing to eukaryotic and bacterial cells. Here we report a single-molecule study of the DNA-binding properties of the three major architectural proteins (Alba, histones and TrmBL2), which have been recently identified in model euryarchaeon T. kodakarensis. Using single-DNA manipulation assays, we show how the interplay between physicochemical characteristics of each of these architectural proteins and the global DNA topology lead to very intricate regulation of the DNA organization, explaining high plasticity of the nucleoid structure in archaeal cells. It was found that DNA-binding competition among Alba, TrmBL2 and histone proteins results in a delicate balance between the DNA open (extended) and closed (collapsed) conformations, which can be shifted to one or the other side via slight changes in the proteins stochiometry, Mg2+ concentration in solution or the DNA supercoiling level. These findings provide important insights into the potential molecular mechanisms accountable for the modulation of the nucleoid structure and the global gene expression profile in archaeal cells in response to environmental changes.