The precarious prokaryotic chromosome

Abstract

Evolutionary selection for optimal genome preservation, replication, and expression should yield similar chromosome organizations in any type of cells. And yet, the chromosome organization is surprisingly different between eukaryotes and prokaryotes. The nuclear versus cytoplasmic accommodation of genetic material accounts for the distinct eukaryotic and prokaryotic modes of genome evolution, but it falls short of explaining the differences in the chromosome organization. I propose that the two distinct ways to organize chromosomes are driven by the differences between the global-consecutive chromosome cycle of eukaryotes and the local-concurrent chromosome cycle of prokaryotes. Specifically, progressive chromosome segregation in prokaryotes demands a single duplicon per chromosome, while other "precarious" features of the prokaryotic chromosomes can be viewed as compensations for this severe restriction.

FIG 1

The differences between eukaryotic and prokaryotic chromosomes in organization and regulation of DNA replication. (A) Replication origins. (B) Replication termini. (C) Replication rounds. (D) Timing of origin firing.

FIG 2

The differences between segregation of eukaryotic and prokaryotic chromosomes and the severity of the replication-transcription conflict. (A) Spindle-driven ensemble segregation in eukaryotes versus the unknown mechanism of progressive segregation in prokaryotes. (B) Schematic differences in rates of replication (red lines) versus transcription (green lines). (C) Gene coorientation with replication through the region. (D) The ratio of control regions to genes.

FIG 3

Chromosome transactions and cycles. (A) The five standard chromosome transactions, color coded to correspond to the data in the schemes in panels C and E. (B) The eukaryotic chromosome cycle. (C) Individual transactions of the eukaryotic chromosome cycle over the standard cell cycle grid. (D) The prokaryotic chromosome cycle. (E) Individual transactions of the prokaryotic chromosome cycle over the standard cell cycle grid.

FIG 4

Subdomain presorting and logistic negotiation during chromosome segregation. Red and blue lines designate daughter duplexes containing, correspondingly, “Watson” or “Crick” strands of the parental duplex. (A to D) Prokaryotic chromosome. (A) The theta-replicating chromosome with a single-duplication bubble. (B) A similar replicating chromosome with four duplication bubbles. (C) Progressive segregation from a single-duplication bubble by default yields two completely separate daughter nucleoids. (D) Progressive segregation without subnucleoid presorting yields two daughter nucleoids intertwined due to misclustering of the individual subnucleoids. As a result, the daughter DNA duplex containing, for example, the “Watson” strand of the parental duplex finds itself in both daughter nucleoids. (E to J) Eukaryotic chromosome. (E) Still-to-be-condensed sister chromatids after replication. (F) Gradual condensation sorts sister chromatids out at the level of subdomains. (G) Coordinated condensation results in “single-body” chromosomes ready for segregation. (H) Uncoordinated independent condensation centers produce entangled subdomains. (I) Monocentric chromosomes condensed as “one body” should be able to disentangle during segregation. (J) Holocentric chromosomes likely need logistic negotiation to help sort out all the Watson subdomains (one sister) from all the Crick subdomains (the other sister) before segregation can even take place.

FIG 5

Prokaryotic chromosome organization compensates for the single duplicon but also creates a strategic opportunity. (A) Various factors minimizing the chromosome duplication time. (B) Multiple relocation cycles in the same chromosome strategically solve the duplication problem.