Key Points
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Myxococcus xanthus is a Gram-negative bacterium that grows by microbial predation or by degradation of complex macromolecules. When starved, M. xanthus cells aggregate and form spore-filled fruiting bodies.
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M. xanthus cells have two very different gliding motility systems. Social (S-) motility, powered by type IV pili, moves cells in groups, whereas adventurous (A-) motility, powered by uncharacterized motors that use adhesion complexes, moves isolated cells.
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M. xanthus contains an extremely large genome that encodes eight clusters of chemotaxis-like genes that define eight two-component chemosensory pathways, most of which have dedicated functions.
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The Frz (Che1) chemosensory pathway was the first to be characterized. It controls the reversal frequency of cells, which is important for cellular reorientation, and is required for directed movements during colony swarming and fruiting-body formation. During fruiting-body formation, FrzCD, a cytoplasmic receptor, becomes highly methylated, which might indicate that it responds to a developmental signal.
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Extracellular polysaccharide serves as a receptor for pilus adhesion and stimulates pilus retraction. The Dif (Che2) chemosensory pathway controls the production of extracellular polysaccharide and also functions in cellular recognition and chemotaxis towards lipids.
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The Che3 chemosensory system does not control motility, but instead controls gene expression during development. Mutants in the che3 system express developmental genes inappropriately and form fruiting bodies on rich media.
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The Che4–8 chemosensory systems control varied and complex functions, many of which remain uncharacterized.
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Multiple chemosensory systems are found in many other bacterial species and are not unique to the myxobacteria. The key advantage that is provided by chemosensory systems is temporal regulation of a given output in response to a persistent stimulus, as these systems show adaptation. One interesting question is: how do these multiple chemosensory systems remain insulated from each other so that crosstalk is controlled?
Abstract
The complex life cycle of Myxococcus xanthus includes predation, swarming, fruiting-body formation and sporulation. The genome of M. xanthus is large and comprises an estimated 7,400 open reading frames, of which approximately 605 code for regulatory genes. These include eight clusters of chemotaxis-like genes that define eight chemosensory pathways, most of which have dedicated functions. Although many of these chemosensory pathways have a role in controlling motility, at least two of these pathways control gene expression during development.
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Acknowledgements
We are grateful to members of the Zusman laboratory, past and present, for many helpful discussions. Our research is supported by grants from the National Institutes of Health GM20509 and GM64463 to D.R.Z., GM071601 to Z.Y. and AI59682 to J.R.K. A.E.S was supported by a predoctoral fellowship from the National Science Foundation.
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FURTHER INFORMATION
Glossary
- Development
-
A programmed change in gene expression and morphology. In Myxococcus xanthus, this process is triggered by starvation and results in cellular aggregation, fruiting-body formation and sporulation.
- Rippling
-
Coordinated rhythmic movement of cells.
- Cell reversal
-
When a cell changes its direction along its long axis so that the leading cell pole becomes the lagging cell pole.
- Mound
-
An early stage of development during which cells aggregate before sporulation.
- Fruiting body
-
The final stage of Myxococcus xanthus development during which cells form a large aggregate and develop into environmentally resistant spores.
- Peripheral rod
-
A cell that maintains its rod shape and does not form a spore during development.
- DZ2
-
A wild-type laboratory strain of Myxococcus xanthus. It was obtained from the Berkeley microbiology laboratory culture collection in 1973. It is thought to be the parent strain of FB, DK101, DZF1 and DK1622.
- FB
-
A strain of Myxococcus xanthus that has been selected for its ability to form single colonies.
- DK1622
-
A 'wild-type' laboratory strain of Myxococcus xanthus. It was derived by restoring full social motility to strain FB, which is thought to have originated by mutagenesis from strain DZ2. Strain DK1622 contains a ∼250-kb deletion of unknown function.
- S-motility
-
Movement of cells in groups that involves extension and retraction of the type IV pili.
- CheW
-
An adaptor protein that links CheA to methyl-accepting chemotaxis protein receptors in bacterial chemotaxis.
- CheA
-
A histidine kinase that is involved in bacterial chemotaxis and that phosphorylates a cognate response regulator such as CheY. Chemosensory pathways can usually be identified by a specific CheA.
- Frz pathway
-
A Myxococcus xanthus chemotaxis pathway that controls cellular reversal frequency.
- Chemotaxis
-
Directed movement towards attractants or away from repellents.
- Adaptation
-
A process whereby cells can adjust to the levels of an attractant or repellent. In bacteria this involves the methylation and/or demethylation of receptors or the dephosphorylation of response regulators. Adaptation allows bacteria to sense small changes in stimuli.
- Methyl-accepting chemotaxis protein
-
A protein that is involved in bacterial chemotaxis and that senses attractants and repellents.
- Slime
-
Polysaccharide that contains material secreted by Myxococcus xanthus.
- Extracellular polysaccharides
-
Extracellular polysaccharides that stimulate the retraction of the type IV pili of Myxococcus xanthus.
- Dif pathway
-
A Myxococcus xanthus chemosensory pathway that controls the production of extracellular polysaccharide and lipid chemotaxis. This pathway is essential for social motility.
- CheY
-
A receiver-domain protein that is phosphorylated by CheA on an Asp residue. Phosphorylated CheY interacts with the output functions of the chemosensory system, which signals stimulation. In Escherichia coli, this results in reversal of the flagellar motor rotation.
- CheR
-
A methyltransferase that methylates methyl-accepting chemotaxis protein receptors in response to stimuli. It is involved in adaptation in bacterial chemotaxis.
- CheB
-
A methylesterase that removes methyl groups from receptors and is involved in adaptation. In Escherichia coli, CheB is phosphorylated, and thereby activated, by phosphorylated CheA.
- Che3 pathway
-
A Myxococcus xanthus chemosensory pathway that controls the expression of many developmental genes.
- Che4 pathway
-
A Myxococcus xanthus chemosensory pathway that regulates social motility.
- Type IV pili
-
Long flexible appendages that are found at the poles of cells and can power motility.
- Myxospore
-
A spherical, environmentally resistant and metabolically inactive Myxococcus xanthus cell.
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Zusman, D., Scott, A., Yang, Z. et al. Chemosensory pathways, motility and development in Myxococcus xanthus. Nat Rev Microbiol 5, 862–872 (2007). https://doi.org/10.1038/nrmicro1770
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DOI: https://doi.org/10.1038/nrmicro1770
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