Abstract
Histone proteins compact and organize DNA resulting in a dynamic chromatin architecture impacting DNA accessibility and ultimately gene expression. Eukaryotic chromatin landscapes are structured through histone protein variants, epigenetic marks, the activities of chromatin-remodeling complexes, and post-translational modification of histone proteins. In most Archaea, histone-based chromatin structure is dominated by the helical polymerization of histone proteins wrapping DNA into a repetitive and closely gyred configuration. The formation of the archaeal-histone chromatin-superhelix is a regulatory force of adaptive gene expression and is likely critical for regulation of gene expression in all histone-encoding Archaea. Single amino acid substitutions in archaeal histones that block formation of tightly packed chromatin structures have profound effects on cellular fitness, but the underlying gene expression changes resultant from an altered chromatin landscape have not been resolved. Using the model organism Thermococcus kodakarensis, we genetically alter the chromatin landscape and quantify the resultant changes in gene expression, including unanticipated and significant impacts on provirus transcription. Global transcriptome changes resultant from varying chromatin landscapes reveal the regulatory importance of higher-order histone-based chromatin architectures in regulating archaeal gene expression.
Highlights
IntroductionMost Archaea encode histone proteins to organize their DNA into a protein:DNA complex known as chromatin (Sandman and Reeve, 2000, 2001, 2006; Peeters et al, 2015; Mattiroli et al, 2017; Bhattacharyya et al, 2018; Henneman et al, 2018; Sanders et al, 2019b; Henneman et al, 2020; Stevens et al, 2020; Bowerman et al, 2021; Laursen et al, 2021)
We report here that retention of a single WT histone variant is sufficient to maintain extended archaeal histonebased chromatin polymers (AHCPs) in archaeal cells, but extended AHCPs are abolished in strains encoding only the mutated AGA motif, HTkAG17D
We demonstrate here, using comparative differential RNAseq analyses of strains with unique AHCP landscapes, that substantial and genome-wide variations in gene expression result from alternating archaeal histone-based chromatin structures, underscoring the importance of AHCPs in normal regulation of gene expression
Summary
Most Archaea encode histone proteins to organize their DNA into a protein:DNA complex known as chromatin (Sandman and Reeve, 2000, 2001, 2006; Peeters et al, 2015; Mattiroli et al, 2017; Bhattacharyya et al, 2018; Henneman et al, 2018; Sanders et al, 2019b; Henneman et al, 2020; Stevens et al, 2020; Bowerman et al, 2021; Laursen et al, 2021). Continued polymerization of archaeal histone proteins produces a symmetrical superstructure composed of increasing lengths of DNA wrapped around a core of polymerized histone dimers (Mattiroli et al, 2017) This extended histone-based chromatin structure, alternatively termed the hypernucleosome (Bhattacharyya et al, 2018; Henneman et al, 2018; Henneman et al, 2020), is the biological form of archaeal chromatin within which gene expression is regulated (Figure 1A)
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