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  • Review Article
  • Published:

Getting organized — how bacterial cells move proteins and DNA

Nature Reviews Microbiology volume 6, pages 28–40 (2008)Cite this article

Key Points

  • In recent years, bacterial cells have been shown to be spatially organized by localized protein complexes and dynamic cytoskeletal filaments.

  • Localized protein complexes are frequently based on integral membrane proteins. Their specific subcellular localization occurs by diffusion and capture or targeted membrane insertion.

  • Dynamic cytoskeletal filaments serve as scaffolds that determine the localization of other proteins and provide directionality and force for macromolecular transport processes.

  • Actin homologues of the MreB family assemble into helical cables that line the inner face of the cytoplasmic membrane. They show dynamic subcellular localization patterns and function in the positioning of proteins that are involved in cell-wall biosynthesis.

  • Plasmid segregation is achieved by three-component partitioning systems. One of the components is an actin homologue, a tubulin homologue or a Walker-type ATPase that assembles into dynamic cytoskeletal filaments. The other two components establish centromere-like nucleoprotein complexes that mediate the attachment of plasmids to these filaments and regulate the partitioning process.

  • Bacterial chromosomes have a conserved circular arrangement within the cell, with the loci arrayed in a linear order that reflects their position on the chromosomal DNA. The subcellular location of each locus is determined during DNA segregation.

  • Unlike in eukaryotes, bacteria segregate their chromosomes while DNA replication is in progress. The chromosomal-origin regions are partitioned by an active mechanism that might involve cytoskeletal structures that are formed by the dynamic assembly of Walker-type ATPases.

  • Bacteria have evolved at least three independent mechanisms to define the site of cell division — the Min system, nucleoid occlusion, and the MipZ and ParB system. In all cases, an inhibitor of cell division is dynamically localized within the cell so that cytokinesis is restricted to a region at mid-cell between the two sister nucleoids.

Abstract

In recent years, the subcellular organization of prokaryotic cells has become a focal point of interest in microbiology. Bacteria have evolved several different mechanisms to target protein complexes, membrane vesicles and DNA to specific positions within the cell. This versatility allows bacteria to establish the complex temporal and spatial regulatory networks that couple morphological and physiological differentiation with cell-cycle progression. In addition to stationary localization factors, dynamic cytoskeletal structures also have a fundamental role in many of these processes. In this Review, we summarize the current knowledge on localization mechanisms in bacteria, with an emphasis on the role of polymeric protein assemblies in the directed movement and positioning of macromolecular complexes.

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Figure 1: Protein localization to the septal membrane during Bacillus subtilis sporulation.
Figure 2: Dynamics of actin-like filaments in bacteria.
Figure 3: Plasmid segregation by the actin homologue ParM.
Figure 4: The arrangement of chromosomal DNA in bacteria.
Figure 5: Positioning of the cell-division plane.

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Acknowledgements

This work was supported by funding from the Max Planck Society to M.T. and grants from the National Institutes of Health to L.S.

Author information

Authors and Affiliations

  1. Max Planck Institute for Terrestrial Microbiology, Karl-von-Frisch-Straße, Marburg, 35043, Germany

    Martin Thanbichler

  2. Department of Developmental Biology, Stanford University School of Medicine, Beckman Center B300, 279 Campus Drive, Stanford, 94305, California, USA

    Lucy Shapiro

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  1. Martin Thanbichler
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Correspondence to Martin Thanbichler.

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DATABASES

Entrez Genome Project

Bacillus subtilis

Caulobacter crescentus

Escherichia coli

Magnetospirillum gryphiswaldense

Magnetospirillum magneticum

Rhodobacter sphaeroides

Shigella flexneri

Thermotoga maritima

Vibrio cholerae

Entrez Protein

FtsY

IcsA

MreC

SpoIVFB

SpoIIQ

SpoIIIAH

TipN

FURTHER INFORMATION

Martin Thanbichler's homepage

Glossary

Forespore

Precursor of the spore; a resting cell that is highly resistant to a number of environmental stresses, such as heat, ultraviolet irradiation and desiccation.

Single-molecule tracking

Microscopic analysis of the movement of individual fluorescently labelled molecules within a cell.

Protofilament

The basic polymeric unit of a filamentous structure; consists of a linear row of monomers.

Fluorescence recovery after photobleaching

(FRAP). A method used to study the dynamics of polymeric structures. A region within a filament that has been assembled from fluorescently labelled monomers is bleached by illumination with a high-intensity laser. Subsequently, fluorescence microscopy is used to monitor the kinetics of fluorescence recovery that results from the substitution of bleached by unbleached subunits in the course of filament turnover.

Peptidoglycan

Meshwork of highly crosslinked glycan strands that constitutes the bacterial cell wall.

Penicillin-binding protein

A protein involved in peptidoglycan biosynthesis that is targeted and inactivated by the antibiotic penicillin and its derivatives.

Centromere

A region of a DNA molecule that is attached to the DNA-segregation apparatus.

Walker ATPase

This ATPase is characterized by the presence of two conserved sequence motifs (Walker A and Walker B motif), which form parts of the nucleotide-binding pocket.

Walker A cytoskeletal ATPases

(WACA). A group of Walker ATPases that possess a distinct version of the Walker A motif that deviates from the universal consensus. These proteins share structural similarity with P-loop GTPases and are recognized as members of the GTPase superfamily.

Nucleoid

A distinct region within the cytoplasm that harbours the chromosomal DNA.

Origin of replication

A chromosomal site that serves as the starting point of the bidirectional DNA-replication process.

Terminus

A chromosomal region in which the two replication forks meet towards the end of DNA replication.

Nucleoid occlusion

The inhibitory effect of the nucleoid on the formation of the septal FtsZ ring.

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Thanbichler, M., Shapiro, L. Getting organized — how bacterial cells move proteins and DNA. Nat Rev Microbiol 6, 28–40 (2008). https://doi.org/10.1038/nrmicro1795

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