Emerging views of genome organization in Archaea

Abstract

Over the past decade, advances in methodologies for the determination of chromosome conformation have provided remarkable insight into the local and higher-order organization of bacterial and eukaryotic chromosomes. Locally folded domains are found in both bacterial and eukaryotic genomes, although they vary in size. Importantly, genomes of metazoans also possess higher-order organization into A- and B-type compartments, regions of transcriptionally active and inactive chromatin, respectively. Until recently, nothing was known about the organization of genomes of organisms in the third domain of life - the archaea. However, despite archaea possessing simple circular genomes that are morphologically reminiscent of those seen in many bacteria, a recent study of archaea of the genus Sulfolobus has revealed that it organizes its genome into large-scale domains. These domains further interact to form defined A- and B-type compartments. The interplay of transcription and localization of a novel structural maintenance of chromosomes (SMC) superfamily protein, termed coalescin, defines compartment identity. In this Review, we discuss the mechanistic and evolutionary implications of these findings.

Keywords: Archaea; Chromatin; Chromosome architecture; Hi-C; Sulfolobus.

Fig. 1.

Overview of chromosome organization in the three domains of life. Eukaryotic chromosomes are organized into two types of self-interacting domains; TADs and larger compartmental domains. Transcriptionally active and inactive compartmental domains segregate from each other to form the A compartment and the B compartment, respectively. Bacterial chromosomes are folded into self-interacting domains called CIDs but lack A- or B-type compartment-like structure. Another feature of many bacterial chromosomes is that the two chromosomal arms that connect the origin and terminus of replication are aligned in parallel. This so-called ori-ter configuration is manifested as the secondary diagonal perpendicular to the main diagonal in the Hi-C heatmap. Chromosomes of the archaea Sulfolobus form compartmental domains like eukaryotic chromosomes but apparently do not possess TAD- or CID-like structure. Thus, to the best of our knowledge, the two organizational principles (formation of TADs, CIDs and of A and B compartments) have different phylogenetic distributions.

Fig. 2.

Schematic representations of SMC complexes. (A) SMC monomers form a rod-like structure with a dimerization domain on one end, an ATPase head domain on the other and a coiled-coil arm between them. In canonical SMC complexes (cohesin, condensin, etc.), SMC proteins dimerize via their hinge domains and associate with accessory subunits to form a ring-shaped structure. (B) Rad50, which possesses a zinc hook instead of a hinge domain, associates with the nuclease protein Mre11.

Fig. 3.

Genomic features of Sulfolobus A- and B-type compartments. The Sulfolobus A compartment is enriched for housekeeping genes that need to be expressed constitutively, whereas the B compartment is enriched for conditionally-required genes. (A,B) Enrichment of gene ontology (GO) terms and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways was analyzed using DAVID 6.8 for the A and B compartments in Sulfolobus acidocaldarius (Huang da et al., 2009a,b; Takemata et al., 2019). For the GO analysis, only non-redundant GO terms (GOTERM_BP_FAT, GOTERM_CC_FAT and GOTERM_MF_FAT) were considered. Shown are GO terms and KEGG pathways with a Benjamini–Hochberg adjusted P-value of <0.05. (C) The number of essential genes per Mb was calculated for the A and B compartments in S. acidocaldarius. Homologs of the essential genes in Sulfolobus islandicus M.16.4 (Zhang et al., 2018) were considered as essential in S. acidocaldarius.