The surprisingly diverse ways that prokaryotes move

Key Points

  • Prokaryotic cells have evolved numerous machineries to swim through liquid or crawl over surfaces. Perhaps the most common of these are the well-studied bacterial flagella and the unrelated archaeal flagella, which both function as rotary propellers. Extension and retraction of type IV pili allow movement over surfaces, as do a range of apparently unrelated gliding motors. In addition, prokaryotes can move passively by floating and sliding.

  • The bacterial flagellum is the best understood prokaryotic motility structure. It consists of a motor and a basal body that are embedded in the cell envelope and a long filament that usually extends from the cell. Rotation of the flagellum is driven by gradients of protons or sodium ions across the cytoplasmic membrane.

  • Bacterial flagella assemble by an unusual process that involves transport of many of the component proteins via a type III secretion system through the core of the basal body and filament before they are added to the tip of the growing structure. Expression of the genes that encode flagellar proteins is highly regulated in a hierarchical manner.

  • The flagellar filaments of spirochaetes are present entirely within the periplasm of the cell. Rotation of these periplasmic flagella is thought to result in movement of the cytoplasmic and outer membranes and attached structures in opposite directions, and results in cell movements.

  • Although bacterial flagella are usually involved in swimming in liquid, some bacteria express numerous flagella and use these to swim or crawl over moist surfaces in a process that is known as swarming.

  • Flagella are the motility structures that are responsible for swimming in the Archaea. Although these structures rotate, in common with bacterial flagella, the archaeal flagella lack a central channel, which means that they must assemble differently from bacterial flagella. Instead, archaeal flagella seem to share similarities in structure and assembly to bacterial type IV pili.

  • Some bacteria swim without using flagella. The wall-less spiroplasmas seem to use their well-developed cytoskeletons to alter their cell shape, which results in cell movement. Although some unicellular marine cyanobacteria swim, the mechanism (or mechanisms) that underlies this movement remains undefined.

  • Bacteria have various non-flagellar mechanisms that are used for crawling over surfaces. Type IV pilus extension and retraction pulls cells over moist surfaces by twitching motility. Flavobacterium spp. gliding motility involves a motor embedded in the cell envelope that moves adhesins along the cell surface. Two models have recently been proposed for Myxococcus spp. adventurous gliding: first, extrusion of polysaccharides, and second, a focal adhesion model that involves movement of cell surface adhesins by cytoplasmic motor proteins that interact with the cytoskeleton. Mycoplasma spp. might glide by 'inchworm' movements that involve the cytoskeleton or by 'centipede' movements of multiple leg-like structures on the cell surface.

Abstract

Prokaryotic cells move through liquids or over moist surfaces by swimming, swarming, gliding, twitching or floating. An impressive diversity of motility mechanisms has evolved in prokaryotes. Movement can involve surface appendages, such as flagella that spin, pili that pull and Mycoplasma 'legs' that walk. Internal structures, such as the cytoskeleton and gas vesicles, are involved in some types of motility, whereas the mechanisms of some other types of movement remain mysterious. Regardless of the type of motility machinery that is employed, most motile microorganisms use complex sensory systems to control their movements in response to stimuli, which allows them to migrate to optimal environments.

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Figure 1: Model of the bacterial flagellum — structure and assembly.
Figure 2: Model of the archaeal flagellum — structure and assembly.
Figure 3: Model to explain Flavobacterium johnsoniae gliding motility.
Figure 4: Models to explain Myxococcus xanthus adventurous motility.
Figure 5: Two models to explain the gliding of different mycoplasmas.

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Acknowledgements

The authors thank the members of their laboratories for helpful discussions and the researchers who generously supplied videos. Research in the authors laboratories is supported by grants from the National Science Foundation (MCB-0641366) to M.J.M. and from the Natural Sciences and Engineering Research Council of Canada to K.F.J.

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Correspondence to Ken F. Jarrell.

Supplementary information

Supplementary information S1 (movie)

Movement of SprB protein on cell surface of gliding cells of Flavobacterium johnsoniae. Protein G coated 0.5 μm polystyrene spheres with anti-SprB antibodies were added to cells of Flavobacterium johnsoniae on a glass slide and images were recorded using a phase-contrast microscope. Bar indicates 10 μm. (MOV 4932 kb)

Supplementary information S2 (movie)

Preparation and reactivation of Mycoplasma mobile ghosts. The cells gliding on a glass coverslip were treated with 0.01% Triton X 100, 1 mg/ml each of DNase and RNase, and ATP at the times indicated in the video. Reproduced with permission from: Uenoyama, A. & Miyata, M. Gliding ghosts of Mycoplasma mobile. Proc. Natl. Acad. Sci. USA 102, 12754–12758 (2005) © (2005) National Academy of Sciences. Video courtesy of Makoto Miyata. (MOV 8084 kb)

Supplementary information S3 (movie)

Digital microcinematography of cell-independent gliding of detached mutant MPN311 terminal organelles of Mycoplasma pnuemoniae. Reproduced with permission from: Hasselbring, B. M. & Krause, D. C. Cytoskeletal protein P41 is required to anchor the terminal organelle of the wall-less prokaryote Mycoplasma pneumoniae. Mol. Microbiol. 63, 44 53 (2007) © (2007) Blackwell Publishing. Video courtesy of Duncan Krause. (AVI 8406 kb)

Supplementary information S4 (movie)

Digital microcinematography of Mycoplasma pnuemoniae mutant MPN311 terminal organelle detachment after cell intersection. Reproduced with permission from: Hasselbring, B. M. & Krause, D. C. Cytoskeletal protein P41 is required to anchor the terminal organelle of the wall-less prokaryote Mycoplasma pneumoniae. Mol. Microbiol. 63, 44–53 (2007) © (2007) Blackwell Publishing. Video courtesy of Duncan Krause. (AVI 6431 kb)

Related links

Related links

DATABASES

Entrez Genome Project

Bdellovibrio bacteriovorus

Borrelia burgdorferi

Caulobacter crescentus

Clostridium perfringens

Escherichia coli

Flavobacterium johnsoniae

Halobacterium salinarum

Helicobacter pylori

Listeria monocytogenes

Methanococcus maripaludis

Methanococcus voltae

Mycoplasma mobile

Mycoplasma pneumoniae

Myxococcus xanthus

Neisseria gonorrhoeae

Nostoc punctiforme

Proteus mirabilis

Pseudomonas aeruginosa

Salmonella typhimurium

Shigella flexneri

Vibrio parahaemolyticus

Entrez Protein

BfpE

FlgN

FliA

FliG

FliI

FliJ

FliM

FliN

FliS

FliT

MotA

MotB

P42

PilA

PilB

PilD

TolB

TolQ

TolR

FURTHER INFORMATION

Ken F. Jarrell's homepage

Mark J. McBride's homepage

Howard Berg's laboratory website (movies: bacteria swarming; type IV pili 1 and type IV pili 2)

Howard Berg's laboratory website (movies: bacteria swarming; type IV pili 1 and type IV pili 2)

Howard Berg's laboratory website (movies: bacteria swarming; type IV pili 1 and type IV pili 2)

Howard Berg's laboratory website (movies: bacteria swarming; type IV pili 1 and type IV pili 2)

Joshua Shaevitz's laboratory website (movie: Spiroplasma kinking)

Keiichi Namba's laboratory website (movie: flagella assembly)

Nyles Charon's laboratory website (movie: Borrelia swimming)

Glossary

Proton motive force

A special case of an electrochemical potential. Proton motive force is the force that is created by the accumulation of protons on one side of a cell membrane. This concentration gradient is generated using energy sources, such as redox potential or ATP. Once established, the proton motive force can be used to carry out work, for example, to synthesize ATP or pump compounds across the membrane.

Chemotaxis

Directed movement towards attractants or away from repellents.

Halophile

A bacterium or archaeon that can grow in environments that contain high concentrations of salt (at least 2 M).

Signal peptide

A short (3–60 amino acid long) peptide chain that directs the post-translational transport of a protein. Signal peptides are also known as targeting signals, signal sequences, transit peptides or localization signals.

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Jarrell, K., McBride, M. The surprisingly diverse ways that prokaryotes move. Nat Rev Microbiol 6, 466–476 (2008). https://doi.org/10.1038/nrmicro1900

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