Cytokinesis in prokaryotes and eukaryotes: common principles and different solutions

Abstract

Cytokinesis requires duplication of cellular structures followed by bipolarization of the predivisional cell. As a common principle, this applies to prokaryotes as well as eukaryotes. With respect to eukaryotes, the discussion has focused mainly on Saccharomyces cerevisiae and on Schizosaccharomyces pombe. Escherichia coli and to a lesser extent Bacillus subtilis have been used as prokaryotic examples. To establish a bipolar cell, duplication of a eukaryotic origin of DNA replication as well as its genome is not sufficient. Duplication of the microtubule-organizing center is required as a prelude to mitosis, and it is here that the dynamic cytoskeleton with all its associated proteins comes to the fore. In prokaryotes, a cytoskeleton that pervades the cytoplasm appears to be absent. DNA replication and the concomitant DNA segregation seem to occur without help from extensive cytosolic supramacromolecular assemblies but with help from the elongating cellular envelope. Prokaryotic cytokinesis proceeds through a contracting ring, which has a roughly 100-fold-smaller circumference than its eukaryotic counterpart. Although the ring contains proteins that can be considered as predecessors of actin, tubulin, and microtubule-associated proteins, its macromolecular composition is essentially different.

FIG. 1

Position of the BSA relative to the site of cytokinesis. (a) Animal cell. In the right-hand cell, the BSA has been shifted to the periphery by pressing a glass bead onto the mitotic cell. (b) S. cerevisiae. The elongating nucleus positions itself relative to the neck of the growing bud (thick double arrows). (c) S. pombe. Medial ring positioning follows the predetermined site of the nucleus. MT, microtubules.

FIG. 2

Cell cycle phases in a prokaryote and in a eukaryote. In a prokaryote, the bacterial chromosome does not condense prior to segregation. The chromosome separates during its replication. Therefore, the S phase coincides with the M phase. G₁, cell cycle phase prior to DNA replication. In E. coli, this phase is denoted B. Its occurrence depends on the strain and on growth conditions. G₂, phase between termination of DNA replication and mitosis. This phase is not present in E. coli. S, DNA replication phase.

FIG. 3

Cytokinetic rings in a eukaryote and a prokaryote. In the highly schematized eukaryote, the cytokinetic ring is represented by a vertical white bar. In the prokaryote, E. coli, a cell division protein, FtsQ, has been labeled by its fusion to green fluorescent protein (GFP). Note the difference in the sizes of the two cells. (Copyright T. den Blaauwen and J. Chen.)

FIG. 4

Interaction between microtubules and growing poles in S. cerevisiae and S. pombe. (a) In S. cerevisiae, astral microtubles explore the poles while the nucleus moves into the bud. The motor protein dynein travels along microtubules and pulls at the dynactin molecules at the cell cortex. Reprinted from reference with permission of the publisher. (b) Growing microtubules deposit Tea1p at the poles. Adapted from reference , with permission of the publisher, MT, microtubules.

FIG. 5

The Rho-GTPase molecular switch. The conformation of the GTPase depends on whether GTP or GDP is bound. The GTP-bound form functions through an effector. This interaction is abolished when GTP is hydrolyzed with the aid of GAP. A guanine nucleotide exchange factor (GEF) catalyzes the production of active Rho-GTP. Adapted from reference .

FIG. 6

Domain composition and homology of IQGAP-related proteins from various organisms. The percentages refer to the conservation of domain composition compared to mammalian IQGAP1. CH, calponin homology domain; IR, internal repeats; WW, SH3-mimicking domain; IQ, calmodulin binding motifs; GRD, RasGAP-homology domain. For further details, see reference . Adapted from reference with permission of the publisher.

FIG. 7

Topology of E. coli cell division proteins relative to the plasma membrane. The numbers in the molecules reflect the molecular masses in kilodaltons. With the exception of FtsK and FtsW, the membrane-bound proteins contain a single membrane anchor. The way in which the various proteins interact with each other is not known. pm, plasma membrane; pg, peptidoglycan. Reprinted from reference with permission of the publisher.

FIG. 8

Schematic representation of the FtsZ ring and its associated subassemblies. The subassemblies are supposed to contain proteins involved in peptidoglycan synthesis in addition to the cell division proteins depicted in Fig. 7. Reprinted from reference with permission of the publisher.

FIG. 9

Replicating eukaryotic and prokaryotic (E. coli) chromosomes. A eukaryotic chromosome contains numerous bidirectional replicating units, each containing its own origin of replication. E. coli replication starts at a defined origin and proceeds bidirectionally. An E. coli chromosome does not contain a centromere or telomeres.

FIG. 10

Time-lapse images in seconds (numbers) of GFP-MinD oscillations in living E. coli cells. Fluorescent GFP-MinD appears as bright polar regions. The cells to the right were imaged with differential interference contrast. For details, see reference (reprinted with permission of the publisher).

FIG. 11

Comparison of cell wall extension in S. pombe and in E. coli. S. pombe extends at the poles, presumably aided by the polarized microtubular framework. In E. coli, the poles are inert with respect to cell wall extension and cell elongation takes place between the poles. Here the poles are not connected through a cytoskeletal structure in the cytoplasm. A diffusible component oscillates between the poles instead. MT, microtuble. For further details, see the text.

FIG. 12

Cotranslational insertion of membrane proteins in the plasma membrane of E. coli. OM, outer membrane; PM, plasma membrane. (Copyright C. L. Woldringh.)

FIG. 13

Schematic model of E. coli nucleoid segregation. The nucleoid is transiently connected to the plasma membrane through transcription loops. The model refers to slowly growing cells, where segregation takes place in the long axis of the cell. Reprinted from reference with permission of the publisher.

FIG. 14

Bipolarization in a eukaryote and in a prokaryote. In a eukaryotic cell, the compacted chromosomes are arranged in the metaphase plate, which is symmetrically located between the MTOCs. In a prokaryote like E. coli, the replisome is symmetrically located between the duplicated origins (oriC). In this representation, the oriC region of the chromosome and associated proteins are analogues of the MTOC. However, in E. coli, no distinction can be made between the centromere and MTOC functions. Note also that the chromosomes have completed replication in the metaphase plate whereas it is the replisome, active in DNA replication, that is centrally located.