The chromosome cycle of prokaryotes

Abstract

In both eukaryotes and prokaryotes, chromosomal DNA undergoes replication, condensation-decondensation and segregation, sequentially, in some fixed order. Other conditions, like sister-chromatid cohesion (SCC), may span several chromosomal events. One set of these chromosomal transactions within a single cell cycle constitutes the 'chromosome cycle'. For many years it was generally assumed that the prokaryotic chromosome cycle follows major phases of the eukaryotic one: -replication-condensation-segregation-(cell division)-decondensation-, with SCC of unspecified length. Eventually it became evident that, in contrast to the strictly consecutive chromosome cycle of eukaryotes, all stages of the prokaryotic chromosome cycle run concurrently. Thus, prokaryotes practice 'progressive' chromosome segregation separated from replication by a brief SCC, and all three transactions move along the chromosome at the same fast rate. In other words, in addition to replication forks, there are 'segregation forks' in prokaryotic chromosomes. Moreover, the bulk of prokaryotic DNA outside the replication-segregation transition stays compacted. I consider possible origins of this concurrent replication-segregation and outline the 'nucleoid administration' system that organizes the dynamic part of the prokaryotic chromosome cycle.

Fig. 1. The eukaryotic chromosome cycle

A–C: Timing of events of the eukaryotic chromosomal cycle in the overall cell cycle. The cell cycle is presented in the linear form and is plotted along the X axis. A. Chromosomal DNA replication. B. Condensation-decondensation. C. Sisiter-chromatid cohesion (SCC) and chromosome segregation. In “B” and “C”, the plot of chromosomal DNA replication is shown on the background. D–F: The three major chromosomal transactions. These three panels represent mechanisms behind the read-outs in panels A–C. In this and subsequent diagrams, DNA duplex is shown as a single line. D. Replication and sister-chromatid cohesion. There are two types of SCC: the physical cohesion due to sister chromatid catenation on the left and the “biochemical” cohesion due to encircling by cohesin protein on the right. E. Condensation-decondensation. F. Segregation. G. The eukaryotic chromosome cycle. The colored triangle covering the top right part of the diagram shows duration of sister-chromatid cohesion. It also coincides with the area of the cell cycle under the control of CDK.

Fig. 2. The prokaryotic nucleoid

In this and subsequent diagrams, the cylinders represent condensed chromosomal DNA, small light blue circles represent the replication origins, and small orange circles represent replication forks. A. A scheme of a circular prokaryotic chromosome with a unique replication origin. B. In fact, the chromosomal DNA is an extremely long molecule, roughly 1,000 times longer than the nucleoid structure in which it is packed. A chloramphenicol-condensed nucleoid of a non-replicating monomer chromosome is a toroid with a rosette-like DNA packing at the cross-section (several of these rosettes are shown). C. A scheme of bacterial chromosome undergoing theta-replication (the Cairns structure). D. The same theta-structure represented in its segregation-oriented “butterfly” form (Peter et al., 1998). E. Replication of the packed chromosome followed by immediate segregation leads to the formation of two packed daughter nucleoids. In this and some subsequent diagrams, replicating nucleoids are shown as cylinders, instead of partial toroids, for simplicity. F. Same as in “E”, but the period of sister-chromatid cohesion (SCC) is shown right behind the replication forks.

Fig. 3. Chromosome replication and segregation in prokaryotes

A–C: General formats of eukaryotic versus prokaryotic replication. A. Multi-bubble single round replication of eukaryotes. B. Unibubble single round replication of slowly-growing prokaryotes. C. Unibubble multiround replication of fast-growing prokaryotes. D and E: Bacterial DNA compaction. D. The general pattern of DNA compaction: “continuous-feed printer paper”. Green circles here and in “E”, DNA-compacting proteins. E. The radial loop model of a compacted bacterial chromosome. Orange ovals, condensins MukBEF. F–I: The first model of chromosomal segregation in prokaryotes by Jacob, Brenner and Cuzin (1963). Letters in the nucleoid: O, origin; T, terminus; L, the left replichore; R, the right replichore. F. An unreplicated nucleoid. G. A nucleoid in the process of replication. H. Fully replicated but unsegregated nucleoid. Small red or magenta rectangles designate nucleoid attachment to the cell envelope. I. Preferential growth of the envelope between the sites of attachment of the sister nucleoids not only elongates the cell, but also moves the sister nucleoids apart, effecting segregation.

Fig. 4. “Everything progressive”: SCC, segregation and controlled compaction/decompaction

A. The “sliding zipper” segregation scheme. Brown box, mother nucleoid; green boxes, daughter nucleoids. Dark blue, parental DNA duplex; medium blue, unsegregated daughter duplexes; light blue, segregated daughter duplexes. Orange arrow, the replisome; yellow arrow (the slider of the zipper), the “segresome”. B. The main events of the prokaryotic chromosomal cycle: mother nucleoid decompaction, replication of the decompacted DNA, SCC due to precatenanes, segregation of uncompacted DNA, daughter nucleoid organization (DNA recompaction). Yellow triangles designate “segresomes”. Rudner and colleagues (Wang et al., 2013) present essentially the same collection and order of events in their Fig. 2C.

Fig. 5. The prokaryotic chromosome cycle

A–C: Timing of events of the prokaryotic chromosomal cycle in the overall cell cycle. See the legend of Fig. 1A–C for description. D. A scheme of the prokaryotic chromosomal cycle. The percentages on the right show approximately how much of the total chromosomal DNA falls into these categories. E. A snapshot of the prokaryotic chromosomal cycle within the cell. The “replication station” shows the two replisomes together, like in Bacillus subtilis (Lemon & Grossman, 1998), but they may also be physically unlinked, as in Escherichia coli (Reyes-Lamothe et al., 2008a).

Fig. 6. The proposed steps of nucleoid administration

Red cones: activities that clean the template DNAs entering the replisomes of the bound proteins; yellow cones, the DNA segregation activities.