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Review
. 2010 Aug;2(8):a000380.
doi: 10.1101/cshperspect.a000380. Epub 2010 Jul 7.

Myxobacteria, polarity, and multicellular morphogenesis

Dale Kaiser  1 , Mark Robinson, Lee Kroos
Affiliations
Review

Myxobacteria, polarity, and multicellular morphogenesis

Dale Kaiser et al. Cold Spring Harb Perspect Biol. 2010 Aug.

Abstract

Myxobacteria are renowned for the ability to sporulate within fruiting bodies whose shapes are species-specific. The capacity to build those multicellular structures arises from the ability of M. xanthus to organize high cell-density swarms, in which the cells tend to be aligned with each other while constantly in motion. The intrinsic polarity of rod-shaped cells lays the foundation, and each cell uses two polar engines for gliding on surfaces. It sprouts retractile type IV pili from the leading cell pole and secretes capsular polysaccharide through nozzles from the trailing pole. Regularly periodic reversal of the gliding direction was found to be required for swarming. Those reversals are generated by a G-protein switch which is driven by a sharply tuned oscillator. Starvation induces fruiting body development, and systematic reductions in the reversal frequency are necessary for the cells to aggregate rather than continue to swarm. Developmental gene expression is regulated by a network that is connected to the suppression of reversals.

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Figures

Figure 1.
Figure 1.
Fruiting bodies of five different species of myxobacteria are shown, illustrating differences in morphology. From left to right: Myxococcus xanthus, Chondromyces crocatus, Stigmatella aurantiaca, Chondromyces apiculatus, Myxococcus stipitatus. (Reprinted, with permission, from Kaiser 2008b [Annual Reviews].)
Figure 2.
Figure 2.
The lifecycle of Myxococcus xanthus. A group of swarming and interacting cells can have either of two fates depending on the swarm’s environment. A Myxococcus fruiting body (A) is a spherical structure of approximately 1 × 105 cells that contains stress-resistant spores. The fruiting body is small (1/10 mm), sticky, and its spores are tightly packed. When a fruiting body receives nutrients, the individual spores germinate and thousands of M. xanthus cells emerge together as an “instant” swarm (B–D). When prey or other nutrient is available, the swarm becomes a predatory collective that moves and feeds cooperatively, pooling extracellular enzymes to lyse and consume prey bacteria (E–F). Multicellular fruiting body development is advantageous given the collective hunting behavior of swarms. Nutrient-poor conditions elicit a unified starvation stress-response that leads to the formation of fruiting bodies. Other multicellular behaviors include wave formation (G), streaming into aggregates (H), and mound building (I). (Adapted from Goldman et al. 2006.)
Figure 3.
Figure 3.
Type IV pilus engine. Tgl is an outer membrane lipoprotein. PilQ is the secretin protein. Once the pilus tip has attached to polysaccharide fibrils on cells ahead, PilT, a AAA ATPase causes the pilus fiber to retract. (Reprinted, with permission, from Kaiser 2008b [Annual Reviews].)
Figure 4.
Figure 4.
A swarm of Myxococcus xanthus, strain DK1622, on agar. Photo taken by Dr. Lotte Jelsbak after incubation at 32 °C. The center of the swarm has several layers of cells. At the edge of the swarm, a single layer of single cells and lateral clusters of cells are spreading outward. Slightly higher cell densities over their surroundings are indicated by the rings and spokes. (Reprinted, with permission, from Jelsbak and Kaiser 2005 [© ASM].)
Figure 5.
Figure 5.
Distribution of cells and multicellular structures at the swarm edge. In addition to some individual cells and slime trails, multicellular rafts and multicellular mounds are labeled. The swarm is expanding in the radial direction, which is to the right in this image. (Scale bar, 50 µ). (Reprinted, with permission, from Wu et al. 2009 [National Academy of Sciences].)
Figure 6.
Figure 6.
The Frizilator and the reversal generator are shown to the right of the dashed vertical line. That circuit is always active and it regulates swarming. The C-signal, which appears shortly after starvation induces fruiting body development, is a 17 kDa cell surface protein. Cells must make end-to-end contact with each other to transmit the signal. The C-signal transduction pathway is shown to the left of the dashed vertical line. FruA, a response regulator, that has been activated by C-signaling is symbolized FruA*. It may include FruA∼P.
Figure 7.
Figure 7.
Network diagram of regulation during M. xanthus development. Arrows indicate positive regulation and lines with barred ends indicate negative regulation. Several lines are colored for emphasis. Background colors distinguish three regulatory modules.
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