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Coupling cell movement to multicellular development in myxobacteria

Nature Reviews Microbiology volume 1, pages 45–54 (2003)Cite this article

Key Points

  • Myxobacteria are Gram-negatives commonly found in the top soil that exhibit social, multicellular behaviour.

  • In the presence of nutrients, myxobacteria feed by forming cooperative swarms of cells, and can prey on other bacteria. In the absence of nutrients, at high cell density on a solid surface they undergo a complex developmental programme, which culminates in the formation of a multicellular fruiting body.

  • Myxobacteria move by gliding motility, which is controlled by two different gliding engines: the S-engine and the A-engine. The S-engine acts as the 'puller' and comprises pili that pull the cells forward by retraction. The A-engine acts as the 'pusher' and pushes cells forward by secreting ribbons of polysaccharide-rich slime.

  • The multicellular development programme of myxobacteria is controlled by a cell-contact-dependent signal, the C-signal.

  • The following development scheme for fruiting-body formation is proposed. The first form of organized movement in a myxobacterial culture is the formation of a wave pattern. The collision of travelling waves of cells in an area of high-cell density creates stationary aggregates of cells, which can become motile and fuse with adjacent aggregates by an as-yet-unknown mechanism. Within the motile aggregates, the myxobacterial cells are streaming in cycles. Travelling waves of cells continue to wash over the aggregates, which accumulate in size to form fruiting bodies comprising up to 105 individual cells. Cell-to-cell contact by motile cells within the aggregates transmits the C-signal between cells, and through a positive-feedback mechanism, the level of C-signal reaches the threshold required for sporulation.

  • The 40 different species of myxobacteria can form fruiting bodies in a variety of shapes and sizes, with both depending on multicellular communication through a cell-contact-dependent system. Understanding this fascinating process could have implications for eukaryotic developmental biology.

Abstract

The myxobacteria are Gram-negative organisms that are capable of multicellular, social behaviour. In the presence of nutrients, swarms of myxobacteria feed cooperatively by sharing extracellular digestive enzymes, and can prey on other bacteria. When the food supply runs low, they initiate a complex developmental programme that culminates in the production of a fruiting body. Myxobacteria move by gliding and have two, polarly positioned engines to control their motility. The two engines undergo coordinated reversals, and changes in the reversal frequency and speed are responsible for the different patterns of movement that are seen during development. The myxobacteria communicate with each other and coordinate their movements through a cell-contact-dependent signal. Here, the cell movements that culminate in the development of the multicellular fruiting body are reviewed.

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Figure 1: The swarm edges of an A−S+ strain and an A+S− strain.
Figure 2: The two engines of myxobacteria.
Figure 3: Slime trails at the edge of a Myxococcus xanthus A+S− swarm.
Figure 4: Electron micrograph of the sacculus of a Myxococcus xanthus cell.
Figure 5: The directing effect of elasticotaxis on a Myxoccocus swarm towards a colony of prey cells.
Figure 6: The C-signal transduction circuit.
Figure 7: Fruiting-body aggregation in submerged agar culture.
Figure 8: A traffic jam and streaming in the construction of fruiting bodies in submerged agar culture.

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Acknowledgements

I thank L. Jelsbak, O. Igoshin, G. Oster and M. Alber for their suggestions. D. K. is supported by a grant from the National Institute of General Medical Sciences.

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  1. Departments of Biochemistry and Developmental Biology, Stanford University, Stanford, 94305, California, USA

    Dale Kaiser

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FURTHER INFORMATION

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TIGR

Glossary

SPORANGIUM

A specialized structure that contains myxobacterial spores.

TRANSDUCTION

The virus-mediated transfer of host DNA (plasmid or chromosomal) from a donor cell to a recipient cell.

TRANSFECTION

The transformation of prokaryotic cells with viral DNA or RNA.

TYPE IV PILI

Elongated hair-like structures extending from the surface of Gram-negative cells that are independent of flagella, and which can retract and pull the cell forward.

AAA MOTOR PROTEIN

An ATPase that is associated with various cellular activities. AAA proteins are essential in all organisms.

FIBRILS

Filamentous extracellular matrix material comprising polysaccharides and protein.

O-ANTIGEN

A heat-stable antigen that is associated with Gram-negative bacteria and which comprises chains of identical oligosaccharide units that can vary in length.

QUORUM SENSOR

An extracellular signal molecule, the concentration of which is proportional to the cell concentration, and which is used by many bacteria to detect cell density

FOURIER ANALYSIS

Mathematical decomposition of a complex periodic function into a sum of simple sine waves.

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Kaiser, D. Coupling cell movement to multicellular development in myxobacteria. Nat Rev Microbiol 1, 45–54 (2003). https://doi.org/10.1038/nrmicro733

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