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Chromosome organization and segregation in bacteria

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Abstract

In the recent years, considerable advances have been made towards understanding the structure and function of the bacterial chromosome. A number of different factors appear to cooperate in condensing DNA into a highly dynamic assembly of supercoiled loops. Despite this variability in the lower levels of chromatin structure, the global arrangement of chromosomal DNA within the cell is surprisingly conserved, with loci being arrayed along the cellular long axis in line with their order on the genomic map. This conserved pattern is propagated during the course of DNA segregation. First, after entry into S-phase, the newly synthesized origin regions are segregated in an active and directed process, involving the bacterial actin homolog MreB. Subsequent DNA segments then follow by different mechanisms. They are separated immediately after release from the replisome and move rapidly to their conserved positions in the incipient daughter cell compartments. Partitioning of the bacterial chromosome thus takes place while DNA replication is in progress.

Introduction

A central problem in biology is the faithful transmission of hereditary information from the mother to its daughter cells. This process not only involves precise replication of chromosomal DNA, but also proper partitioning of the newly synthesized sister chromosomes as well as tight synchronization of DNA segregation with cell division. Whereas the enzymology of DNA replication has been studied in great detail (Johnson and O’Donnell, 2005), our understanding of chromosome architecture and dynamics is still far from complete. This is especially true for bacteria, which due to their small size have long remained unamenable to cell biological analyses. Recently, however, methodological and technical advances have provided the means to resolve the minute structural features of prokaryotic cells and, as a consequence, led to a change of paradigms in the field of microbiology. Whereas formerly regarded as ‘bags of enzymes’, whose proliferation relies mostly on physical forces and self-organizational processes, bacteria have now emerged as complex systems that are organized by a sophisticated and tightly regulated molecular machinery. This new concept is, in particular, underscored by recent findings on bacterial chromosome structure and segregation, which will be discussed in the following sections.

Section snippets

Mechanisms of DNA condensation

Most bacteria possess a single, circular chromosome, which is not encased in a membrane-bounded compartment, but embedded in the cytoplasm. Nevertheless, it frequently occupies a distinct region within the cell, which is functionally equivalent to a eukaryotic nucleus and thus termed the nucleoid. With an average genome size of 4 Mbp, a bacterium faces the problem of packaging a DNA molecule with a contour length of ∼1.3 mm into a cell body that typically measures 1–2 μm. Whereas eukaryotic cells

Topological structure of bacterial DNA

Early biochemical studies showed that many knicks are necessary to completely relax a supercoiled E. coli chromosome, indicating the existence of barriers that separate chromosomal DNA into a number of topologically isolated domains (Sinden and Pettijohn, 1981, Worcel and Burgi, 1972). This modular design was supported by the finding that, on electron micrographs, E. coli nucleoids appeared as clusters of plectonemically wound loops that radially emanated from a central core (Delius and Worcel,

General scheme of chromosome segregation in bacteria

FISH and FROS analyses revealed that DNA segregation follows a common scheme in bacteria, even though clear species-specific differences in the details of the process have been established. In a first step, which occurs soon after the initiation of DNA replication, the newly duplicated origin regions are rapidly moved away from each other in direction of the cell poles (Fogel and Waldor, 2005, Jensen, 2006, Jensen and Shapiro, 1999, Lau et al., 2003, Li et al., 2002, Niki et al., 2000, Roos et

Conclusions

In the recent years, technical advances have allowed unprecedented insight into the architecture of bacterial chromatin and the mechanisms responsible for its organization. DNA supercoiling and the activities of multiple DNA-structuring proteins were found to condense the chromosome into a highly dynamic but conserved structure that is actively segregated by the combined action of cytoskeletal elements and the forces generated by DNA condensation. However, despite the significant progress made

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