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. 2007 Aug;189(15):5675-82.
doi: 10.1128/JB.00544-07. Epub 2007 May 18.

Multicellular development in Myxococcus xanthus is stimulated by predator-prey interactions

James E Berleman  1 , John R Kirby
Affiliations

Multicellular development in Myxococcus xanthus is stimulated by predator-prey interactions

James E Berleman et al. J Bacteriol. 2007 Aug.

Abstract

Myxococcus xanthus is a predatory bacterium that exhibits complex social behavior. The most pronounced behavior is the aggregation of cells into raised fruiting body structures in which cells differentiate into stress-resistant spores. In the laboratory, monocultures of M. xanthus at a very high density will reproducibly induce hundreds of randomly localized fruiting bodies when exposed to low nutrient availability and a solid surface. In this report, we analyze how M. xanthus fruiting body development proceeds in a coculture with suitable prey. Our analysis indicates that when prey bacteria are provided as a nutrient source, fruiting body aggregation is more organized, such that fruiting bodies form specifically after a step-down or loss of prey availability, whereas a step-up in prey availability inhibits fruiting body formation. This localization of aggregates occurs independently of the basal nutrient levels tested, indicating that starvation is not required for this process. Analysis of early developmental signaling relA and asgD mutants indicates that they are capable of forming fruiting body aggregates in the presence of prey, demonstrating that the stringent response and A-signal production are surprisingly not required for the initiation of fruiting behavior. However, these strains are still defective in differentiating to spores. We conclude that fruiting body formation does not occur exclusively in response to starvation and propose an alternative model in which multicellular development is driven by the interactions between M. xanthus cells and their cognate prey.

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Figures

FIG. 1.
FIG. 1.
Prey-directed fruiting body formation. Twenty microliters of E. coli β2155 cells was pipetted and allowed to dry on CFL agar medium as prey for 1 μl of M. xanthus DZ2 cells mixed with India ink, which were pipetted onto the E. coli prey. As the M. xanthus swarm expands, the E. coli cells are lysed, and fruiting body formation is induced along the perimeter of the original prey colony. Photographs were captured at ×8 magnification at 0 h (A, D, and G), 48 h (B, E, and H), and 72 h (C, F, and I). J shows a control experiment with no E. coli prey at 120 h.
FIG. 2.
FIG. 2.
Effect of basal nutrient level on prey-directed fruiting body formation. M. xanthus DZ2 cells were pipetted adjacent to prey colonies (first two columns) and alone (third column) on CFL plates containing (A to C) 0.0 g/liter, (D to F) 0.1 g/liter, and (G to I) 1.0 g/liter Casitone. In the presence of prey, fruiting aggregates were observed at 72 h under conditions ranging from 0.0 to 1.0 g/liter Casitone. In the absence of prey, fruiting aggregates were observed only at 0.1 g/liter Casitone.
FIG. 3.
FIG. 3.
Prey effect on sporulation levels. M. xanthus DZ2 cells were incubated in either the presence or the absence of prey for 4 days on CFL plates with various levels of Casitone. Cells were harvested, and the viable M. xanthus cell count was determined through plating serial dilutions before and after a 2-h 50°C heat stress. Closed bars, 107 M. xanthus cells; open bars, 107 M. xanthus cells with 109 E. coli cells; hatched bars, 108 M. xanthus cells. The presence of prey increases the sporulation percentage of the population at 0 g/liter Casitone but not at 1.0 g/liter Casitone.
FIG. 4.
FIG. 4.
Analysis of early signaling mutants. In a monoculture starvation assay, (A) DZ2 forms fruiting bodies in 48 h, whereas (B) asgD mutant and (C) relA mutant strains are defective at aggregation. In a coculture predation assay, (D to G) DZ2, (H to K) asgD mutant, and (L to O) relA mutant strains are all proficient at inducing fruiting aggregation, particularly at the edges of the predation zone. Pictures were captured at 0, 40, 64, and 74 h (left to right) during predation. Analysis of wet mounts indicated that phase-bright spores are present in the predation-induced aggregates of (P) DZ2 but not (Q) asgD mutant or (R) relA mutant cells.
FIG. 5.
FIG. 5.
Response to stepped changes in prey cell density. E. coli β2155 cell suspensions were pipetted in a series of small drops and allowed to dry to generate relatively straight lines of prey at 4 × 107 cells/mm2 and 1 × 107 cells/mm2. M. xanthus cells were mixed with India ink and added to the edge of the dried prey colonies in a 1-μl aliquot. Prey cells were provided at (A to D) a constant low cell density, (E to H) a constant high cell density, (I to L) a step change down from a high cell density to a low cell density, or (M to P) a step change up from a low cell density to a high cell density. The left column portrays a conceptual diagram of the assay followed by images captured at 0 h and 72 h showing the pattern of fruiting bodies formed. For each assay, the field of view was sliced into 11 equivalent horizontal sections, and quantification of the fruiting body localization pattern is provided in the right column. The arrows highlight the location at which a step-up or a step-down in prey availability occurs.
FIG. 6.
FIG. 6.
Model for the initiation of multicellular development. Although a combination of high cell density and starvation will induce fruiting body formation in monoculture, it is important to consider that M. xanthus is a predatory bacterium and that prey availability alters the timing and localization of fruiting body aggregation as well. The early signals for this process are therefore dependent on interspecies signals, and self-generated signals from the relA and asg loci are not required for cellular differentiation until later in development.
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References

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