Replication-biased genome organisation in the crenarchaeon Sulfolobus

Abstract

Background: Species of the crenarchaeon Sulfolobus harbour three replication origins in their single circular chromosome that are synchronously initiated during replication.

Results: We demonstrate that global gene expression in two Sulfolobus species is highly biased, such that early replicating genome regions are more highly expressed at all three origins. The bias by far exceeds what would be anticipated by gene dosage effects alone. In addition, early replicating regions are denser in archaeal core genes (enriched in essential functions), display lower intergenic distances, and are devoid of mobile genetic elements.

Conclusion: The strong replication-biased structuring of the Sulfolobus chromosome implies that the multiple replication origins serve purposes other than simply shortening the time required for replication. The higher-level chromosomal organisation could be of importance for minimizing the impact of DNA damage, and may also be linked to transcriptional regulation.

Figure 1

Schematic representation of the S. acidocaldarius (A) and S. solfataricus (B) chromosomes. The ellipses indicate replication origins (positions from [26]).

Figure 2

Distribution of gene expression over the S. acidocaldarius chromosome in exponentially growing cultures. Each filled circle represents a single gene, with expression provided as log₂-transformed (cDNA/genomic DNA) ratio. Arrows indicate positions of replication origins.

Figure 3

Distribution of expression for genes within indicated intervals of distance to nearest replication origin in exponential phase cultures of S. acidocaldarius. Fifty percent of the data points reside within boxes, 75% within whiskers, and medians are indicated by horizontal lines within boxes (open circles indicate individual genes). Gene expression was significantly negatively correlated with distance to nearest origin (Spearman rank-order correlation, ρ = -0.41; P < 10^-15 calculated on individual genes).

Figure 4

Distance to nearest origin, average gene expression, proportion of archaeal core genes, protein-coding density, and transposable element density over the chromosome of S. acidocaldarius (left panel) and S. solfataricus (right panel) in 100 kb sliding windows, translocated in 1 kb steps. Chromosomal positions for window mid-points are shown on the x-axis.