Capturing chromosome conformation in Crenarchaea

Abstract

While there is a considerable body of knowledge regarding the molecular and structural biology and biochemistry of archaeal information processing machineries, far less is known about the nature of the substrate for these machineries-the archaeal nucleoid. In this article, we will describe recent advances in our understanding of the three-dimensional organization of the chromosomes of model organisms in the crenarchaeal phylum.

Keywords: Sulfolobus; Archaea; SMC; condensin; evolution; genome.

FIGURE 1

Schematic representation of the two‐domain of life tree with eukaryotes emerging from within the Asgard grouping. Major phyla or superphyla of Archaea are indicated in purple (acronyms are explained in the text) eukaryotes in blue and bacteria in gray.

FIGURE 2

Chromosome conformation capture contact maps of chromosomes of a range of Sulfolobales species (left column). Sis—Sulfolobus islandicus REY15A: Sto—Sulfurisphaera (formerly Sulfolobus) tokodaii: Sac—Sulfolobus acidocaldarius DSM639 Ste—Sulfuracidifex tepidarius. The scale (CS) indicated contact score × 10⁻3. Pearson correlation coefficient heat maps are also shown in the middle column, and the scale (PC) indicates the Pearson correlation coefficient and on the right are principal component plots indicating the localization of loci falling into A or B compartment. Figures are generated from previously published 3C experiments (Badel et al., ; Takemata et al., ; Takemata & Bell, 2021c). Data are available at the Gene Expression Omnibus (GEO) Accession code GSE128063 and GES159537 and NIH SRA Project numbers PRJNA814106 (Ste and Sto).

FIGURE 3

(a) Pearson correlation coefficient heat map of contacts within the Saccharolobus solfataricus P2 chromosome. (b) Principal component analysis of the data shown in part (a). Regions of the genome corresponding to A and B compartments are shown above and below the midline, respectively. (c) ChIP‐Seq analyses of the localization of ClsN on the Saccharolobus solfataricus chromosome. The positions of A and B compartments are shown with white and gray backgrounds, respectively. (d) Violin plot of the binding of ClsN to A and B compartment loci. Data were analyzed using a Wilcoxon test (two sided) and the p‐value indicated. Data will be deposited at the SRA. Note that these data are previously unpublished and have been deposited at the Sequence Read Archive, BioProject Accession PRJNA1074953.

FIGURE 4

Distribution of condensin and ClsN SMC superfamily proteins in the TACK superphylum. Black circles indicate the presence of orthologs, and gray circles indicate non‐ubiquitous presence of orthologs in a lineage. Rkd4 is a distant paralog of ClsN found in the Thermoproteales.

FIGURE 5

(a) Pearson correlation coefficient heat map arising from 3C analyses of the Aeropyrum pernix chromosome. The main region corresponding to the HEID domain is highlighted in a dashed yellow box. Additional constituent regions contributing to HEID are indicated with purple triangles. The principal component analysis is shown below with HEID domain in purple and the rest of the chromosome in blue. These figures were generated from data deposited in NCBI Sequence Read Archive (SRA). Submission ID: SUB13894161. BioProject ID: PRJNA1027590 (Badel & Bell, 2024). (b) Schematic proposing a pathway for the evolution of the compartmentalized organization of the Sulfolobales chromosomes. Orthologous DNA replication origins are color‐coded to overcome the rather unfortunate current nomenclature. We suggest that the integration of an extrachromosomal element that was replicated via the green replication origin and additionally encoded clsN led to the generation of a three‐replication origin, clsN‐encoding ancestral Sulfolobus chromosome. ClsN with its preference for the transcriptionally more‐quiescent regions of the chromosome would lead to coalescence of loci into a B compartment.