C-Signal Control of Aggregation and Sporulation

Dale Kaiser

doi:10.1128/9781555815578.ch4

Chapter 4 : C-Signal Control of Aggregation and Sporulation

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Affiliations: 1: Departments of Biochemistry and Developmental Biology, Stanford University School of Medicine, Stanford, California 94305

Content Type: Monograph

Publication Year: 2008

Category: Microbial Genetics and Molecular Biology; Bacterial Pathogenesis

Book DOI: 10.1128/9781555815578

Chapter DOI: 10.1128/9781555815578.ch4

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Abstract:

Since 1970, the author's research group has been trying to decipher the instructions used by Myxococcus xanthus to build its fruiting body. Fruiting body development requires a solid surface because the structure is built by cell movement. Two molecular motors, retractile type IV pili at their leading end (S motility), and nozzles for secreting a slime gel at the trailing end (A motility) provide the adhesion and thrust necessary for moving on surfaces. Outward spreading stops when M. xanthus senses that it has begun to starve; instead it moves inward to the swarm center to establish centers for fruiting body aggregation. By tradition, the aggregation of cells has been considered to arise from chemotaxis, and this view was encouraged by the discovery of many "chemotaxis genes" in M. xanthus. Aggregation by local cell contact signaling has been tested by mathematical simulation. At the beginning of sporulation the cell density in the center is about one-third the density in the outer region. Temporal changes in gene expression are necessary to adjust to starvation, to aggregate, and finally to sporulate. All the defects in aggregation and sporulation could be traced to a particular segment of the C-signal transduction pathway namely the branch from the C-signal receptor to FruA~P. All aspects of the phenotype of either deletion mutant were accounted for by the hypothesis that mutant MXAN4899 severely restricts the rise in the level of phosphorylated FruA.

Citation: Kaiser D. 2008. C-Signal Control of Aggregation and Sporulation, p 51-63. In Winans S, Bassler B (ed), Chemical Communication among Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815578.ch4

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C-Signal Control of Aggregation and Sporulation

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FIGURE 1

The life cycle of M. xanthus. A swarm (a group of moving and interacting cells) can have either of two fates, depending on their environment. The fruiting body (A) is a spherical structure of approximately 105 cells that have become stress-resistant spores (B). The fruiting body is small (1/10 mm high) and sticky, and its spores are tightly packed. When a fruiting body receives nutrients, the individual spores germinate (C) and thousands of M. xanthus cells emerge together as an “instant” swarm (D). When prey is available (micrococci in the figure), the swarm becomes a predatory collective that surrounds the prey. Swarm cells feed by contacting, lysing, and consuming the prey bacteria (E–F). Fruiting body development is advantageous given the collective hunting behavior. Nutrient-poor conditions elicit a unified starvation stress response. That response initiates a self-organized program that changes cell movement behavior, leading to aggregation. The movement behaviors include wave formation (G) and streaming into mounded aggregates (H), which become spherical (A). Spores differentiate within mounded and spherical aggregates. We use the term “swarming” in its general sense to denote a process “in which motile organisms actively spread on the surface of a suitably moist solid medium” ( 69 ). Reprinted from the Proceedings of the National Academy of Sciences USA ( 16 ) with permission of the publisher.

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FIGURE 1

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FIGURE 2

Cell movement is correlated with the secretion of slime from its back. Selected frames from a time-lapse movie taken by Lars Jelsbak. (A) Frame 1 of movie; the upper cell has moved down, leaving a slime trail above it. The bottom cell has not moved. (B) Frame 4 of movie; both cells have moved down and left a slime trail above them. (C) Frame 20 of movie; both cells have moved up and left a slime trail below them. (D) Frame 37 of movie; both cells have moved down and left a slime trail above them. (E) Frame 58 of movie; the upper cell has moved down, leaving a slime trail above it. (F) The lower cell has moved up, leaving a slime trail below it.

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FIGURE 2

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FIGURE 3

M. xanthus cells are polarized to glide in one direction. For the cell shown, it is polarized to glide to the left. The A engine is a “pusher” and the S engine is a “puller.” Slime-secretion nozzles are always visible at both ends of each cell, and yet only one end secretes slime.

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FIGURE 3

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FIGURE 4

When a cell divides, two new ends are created by the division septum. Each daughter receives only one of the two engines at its new pole, and always the correct one. The cell’s peptidoglycan and cytoskeleton appear to be recognized as a polarized template specifying different working engines at the two poles.

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FIGURE 4

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FIGURE 5

Regulatory C-signal circuit. C signal is a 17-kDa cell surface protein. Cells must make end-to-end contact to transmit the signal, as shown. Reception of C signal activates FruA by forming FruA~P. FruA~P drives the oscillation of MeFrzCD and FrzE~P. FrzE~P switches MglA•GDP to MglA•GTP, which in turn inactivates old engines. C signaling increases csgA transcription, directly or indirectly, via the proteins of the act operon. Rippling, aggregation, sporulation, and C signal-dependent gene expression are induced by increasing levels of FruA~P. MXAN4899 is proposed to be the branch from reception of C signal to FruA~P.

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FIGURE 5

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