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.

Static and Dynamic Factors Limit Chromosomal Replication Complexity inEscherichia coli, Avoiding Dangers of Runaway Overreplication

“…The bacterial chromosome cycle (Kuzminov 2013(Kuzminov , 2014) is distinct from the eukaryotic one in that segregation shortly follows replication, separated from it by a 5-to 10-min-long period of sister-chromatid cohesion (Viollier et al 2004;Nielsen et al 2007;Vallet-Gely and Boccard 2013). Stalling of replication forks or accumulation of single-strand interruptions behind the forks in bacteria, therefore, leads to catastrophic chromosomal consequences, reflected in such phenomena as thymineless death (Kuong and Kuzminov 2012), ligase-deficient death (Kouzminova and Kuzminov 2012), or sensitivity of seqA mutants to DNA damage (Sutera and Lovett 2006) and to rapid growth .…”

“…Indeed, in a chromosome with CRC = 2 ( Figure 6A), the only available duplex to reattach the double-strand end to after replication fork disintegration is the sister duplex, while in a chromosome with CRC = 4 ( Figure 6B), this intact sister (theoretically) has to compete with two cousin duplexes of identical DNA sequence. Normally, sister-chromatid cohesion, although extremely short in bacteria (Kuzminov 2013(Kuzminov , 2014, would still guide the repaired double-strand end toward the sister, while the concurrent segregation (Viollier et al 2004;Nielsen et al 2007; Vallet-Gely and Boccard 2013) will physically separate cousins, making them even less available. However, in conditions of CRC soaring beyond the control of the eclipse system, the now unregulated distance between replication forks may become too short, reducing sister-chromatid cohesion to a minimum.…”

“…Whereas recombinational repair is beneficial for cells at the natural and functional CRC limits, we show that it becomes detrimental at the tolerance CRC limit, suggesting recombinational misrepair during the runaway overreplication and giving a rationale for avoidance of the latter. KEYWORDS overinitiation; hydroxyurea; seqA; rep; recA E UKARYOTIC and prokaryotic chromosomes differ in many important aspects (Kuzminov 2014), and one key difference lies in the spatio-temporal organization of chromosomal replication. In contrast to eukaryotes, which perform multibubble replication (Masai et al 2010), most bacteria replicate their singular chromosome in the unibubble format by initiating bidirectional replication from a designated replication origin (oriC) (Sernova and Gelfand 2008;Leonard and Méchali 2013) and finishing replication within a broad termination zone (ter) (Mirkin and Mirkin 2007;Duggin et al 2008).…”

Dynamic Organization: Chromosome Domains in <b><i>Escherichia coli</i></b>

“…But this information would be in great danger of being lost, destroyed or unusable if cells did not have efficient systems to repair, duplicate, segregate and organize their chromosomes. These processes are implemented very differently in bacteria as compared to eukaryotic systems [Kuzminov, 2014]. The most striking features of bacteria are the lack of a nucleus and the temporal co-occurrence of DNA replication and chromosome segregation.…”

Fifty Years after the Replicon Hypothesis: Cell-Specific Master Regulators as New Players in Chromosome Replication Control

“…In contrast to Eukaryota, bacterial chromosomes possess a single, unique replication origin, in which the DNA synthesis starts generating a single replication eye per chromosome (2,3). Replication of the bacterial chromosome is initiated by the binding of the initiator protein called DnaA to specific 9-mer sequences (called DnaA boxes) within the oriC region (origin of chromosomal replication-the replicator) (originally described by the Kornberg group; see, e.g., references 4 and 5).…”