Abstract
Myxococcus xanthus cells self-organize into periodic bands of traveling waves, termed ripples, during multicellular fruiting body development and predation on other bacteria. To investigate the mechanistic basis of rippling behavior and its physiological role during predation by this Gram-negative soil bacterium, we have used an approach that combines mathematical modeling with experimental observations. Specifically, we developed an agent-based model (ABM) to simulate rippling behavior that employs a new signaling mechanism to trigger cellular reversals. The ABM has demonstrated that three ingredients are sufficient to generate rippling behavior: (i) side-to-side signaling between two cells that causes one of the cells to reverse, (ii) a minimal refractory time period after each reversal during which cells cannot reverse again, and (iii) physical interactions that cause the cells to locally align. To explain why rippling behavior appears as a consequence of the presence of prey, we postulate that prey-associated macromolecules indirectly induce ripples by stimulating side-to-side contact-mediated signaling. In parallel to the simulations, M. xanthus predatory rippling behavior was experimentally observed and analyzed using time-lapse microscopy. A formalized relationship between the wavelength, reversal time, and cell velocity has been predicted by the simulations and confirmed by the experimental data. Furthermore, the results suggest that the physiological role of rippling behavior during M. xanthus predation is to increase the rate of spreading over prey cells due to increased side-to-side contact-mediated signaling and to allow predatory cells to remain on the prey longer as a result of more periodic cell motility.
Highlights
Spatial self-organization of developing cells, which results the formation of complex dynamic structures, remains one of the most intriguing phenomena in modern biology [1,2,3,4]
The dynamic self-organization in biofilms formed by the soil bacterium Myxococcus xanthus is dependent on the ability of the cells to move on solid surfaces [7,8], while sensing, integrating and responding to a variety of intercellular and environmental cues [9,10,11,12]
Individual cells are represented as agents that move and interact according to the rules and equations that correspond to experimental observations
Summary
Spatial self-organization of developing cells, which results the formation of complex dynamic structures, remains one of the most intriguing phenomena in modern biology [1,2,3,4]. At high density and under nutrient stress M. xanthus cells execute a complex multicellular developmental program by aggregating into multicellular mounds, termed fruiting bodies, and differentiating into dormant, environmentally resistant myxospores [11]. These bacteria exhibit complex behaviors when they cooperatively prey on other microorganisms by collectively spreading over the prey cells, producing antibiotics and lytic compounds that kill and decompose their prey [13,14]. These waves are distinct from the waves originating from Turing instability diffusion-reaction patterns, such as those in chemical systems or observed during development of the other well-studied model social microorganism, the amoeba Dictyostelium discoideum [22,23,24]
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