The Lrs14 family of DNA‐binding proteins as nucleoid‐associated proteins in the Crenarchaeal order Sulfolobales

Abstract

AbstractOrganization of archaeal chromatin combines bacterial, eukaryotic, and unique characteristics. Many archaeal lineages harbor a wide diversity of small and highly expressed nucleoid‐associated proteins, which are involved in DNA structuring. In Sulfolobales, representing model organisms within the Crenarchaeota, Sul7d, Cren7, Sul10a, and Sul12a are well‐characterized nucleoid‐associated proteins. Here, we combine evidence that the Lrs14 family of DNA binders is part of the repertoire of nucleoid‐associated proteins in Sulfolobales. Lrs14‐encoding genes are widespread within genomes of different members of the Sulfolobales, typically encoded as four to nine homologs per genome. The Lrs14 proteins harbor a winged helix‐turn‐helix DNA‐binding domain and are typified by a coiled–coil dimerization. They are characterized by distinct sequence‐ and structure‐based features, including redox‐sensitive motifs and residues targeted for posttranslational modification, allowing a further classification of the family into five conserved clusters. Lrs14‐like proteins have unique DNA‐organizing properties. By binding to the DNA nonsequence specifically and in a highly cooperative manner, with a slight preference for AT‐rich promoter regions, they introduce DNA kinks and are able to affect transcription of adjacent transcription units either positively or negatively. Genes encoding Lrs14‐type proteins display considerable differential expression themselves in response to various stress conditions, with certain homologs being specific to a particular stressor. Taken together, we postulate that members of the Lrs14 family can be considered nucleoid‐associated proteins in Sulfolobales, combining a DNA‐structuring role with a global gene expression role in response to stress conditions.