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  • Review Article
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Prokaryotic cytoskeletons: protein filaments organizing small cells

Nature Reviews Microbiology volume 16, pages 187–201 (2018)Cite this article

Subjects

Key Points

  • Bacteria and archaea use protein filament systems to organize cellular processes in time and space. Filaments can act as static scaffolds or as dynamic motors.

  • In some cases, these filament systems function analogously to components of the eukaryotic cytoskeleton, and the term 'prokaryotic cytoskeletons' has been adopted and broadened to include many different filament systems in small cells.

  • Many of the proteins that form these filaments fall into a small number of groups. The three largest and most-studied groups are the actin superfamily, the tubulin superfamily and filaments formed by coiled coil proteins.

  • Within a filament family, the structural basis of filament formation is typically conserved, whereas the biological functions of the related filaments are often divergent. This observation is important for our understanding of ancient evolutionary events and processes.

  • Remarkable progress has been made in understanding how filament systems function, although in most cases, the molecular mechanisms remain unclear. Structural biology, cryo-electron tomography of cells and advanced light microscopy methods are making important contributions to our mechanistic understanding.

  • An emerging theme is that although some filaments function by forming large filaments, in many cases, short filaments formed from tens of monomers function in a highly dynamic way to organize local processes.

Abstract

Most, if not all, bacterial and archaeal cells contain at least one protein filament system. Although these filament systems in some cases form structures that are very similar to eukaryotic cytoskeletons, the term 'prokaryotic cytoskeletons' is used to refer to many different kinds of protein filaments. Cytoskeletons achieve their functions through polymerization of protein monomers and the resulting ability to access length scales larger than the size of the monomer. Prokaryotic cytoskeletons are involved in many fundamental aspects of prokaryotic cell biology and have important roles in cell shape determination, cell division and nonchromosomal DNA segregation. Some of the filament-forming proteins have been classified into a small number of conserved protein families, for example, the almost ubiquitous tubulin and actin superfamilies. To understand what makes filaments special and how the cytoskeletons they form enable cells to perform essential functions, the structure and function of cytoskeletal molecules and their filaments have been investigated in diverse bacteria and archaea. In this Review, we bring these data together to highlight the diverse ways that linear protein polymers can be used to organize other molecules and structures in bacteria and archaea.

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Figure 1: Tubulin superfamily.
Figure 2: Actin superfamily.
Figure 3: Towards a structural understanding of diverse prokaryotic cytoskeletal filaments.

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Acknowledgements

The authors acknowledge support from the Medical Research Council (U105184326) and the Wellcome Trust (095514/Z/11/Z). J.W. acknowledges the Boehringer Ingelheim Fonds for his PhD fellowship.

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    James Wagstaff & Jan Löwe

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J.W. and J.L. contributed to researching data for the article. J.W. and J.L. substantially contributed to the discussion of content, wrote the article and reviewed and edited the manuscript before submission.

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Glossary

Endomembrane

Membrane binding internal compartments in eukaryotic cells.

Segregation

The active partitioning of a cellular component into daughter cells at division.

Superfamily

In proteins, the largest group that can be determined to have a common ancestor.

Protofilament

The one-subunit-thick filament formed by repeated linear interactions between monomers; also known as a strand.

Divisome

The set of proteins that divide a bacterial cell.

Peptidoglycan

The peptide-crosslinked sugar polymer that is the major component of bacterial cell walls.

Treadmilling

The situation in which a filament simultaneously grows and shrinks at opposite ends, leading to overall motion in the direction of growth without subunits moving.

Magnetotactic bacteria

Bacteria that are able to sense magnetic fields using tiny intracellular magnets.

Magnetosome

Inward bulges of the inner membrane in some bacteria that contain biomineralized iron compound crystals.

Horizontal gene transfer

A process in which genetic material is transferred between genomes by any means except whole genome reproduction.

Seam

The discontinuity in helical symmetry classically observed in 13 protofilament microtubules.

Dynamic instability

Rapid and stochastic switching between filament growth and depolymerization, an emergent property of some filaments, notably microtubules.

TACK superphylum

An archaeal clade that is a sister to the clade that includes the Asgard superphylum and the archaeal ancestor of eukaryotes. TACK: Thaumarchaeota, Aigarchaeota, Crenarchaeota and Korarchaeota.

Elongasome

The set of proteins that allow bacterial cells to grow longer.

Cytomotive filament

A filament that pushes or pulls other molecules in a dynamic way.

Gliding motility

A mode of bacterial self-propulsion that results in smooth motion over a surface. This is achieved by different mechanisms in different organisms.

Coiled coil

The structural motif formed by intertwined α-helices.

Forespores

Precursors of spores, a 'cell in a cell'.

Subtomogram averaging

The process of aligning subvolumes extracted from tomograms to improve signal:noise ratio and obtain high-resolution structural information.

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Wagstaff, J., Löwe, J. Prokaryotic cytoskeletons: protein filaments organizing small cells. Nat Rev Microbiol 16, 187–201 (2018). https://doi.org/10.1038/nrmicro.2017.153

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