 The Mechanistic Basis of Myxococcus xanthus Rippling Behavior and Its Physiological Role during PredationHaiyang Zhang, Zalman Vaksman, Douglas B Litwin, Peng Shi, Heidi B Kaplan and Oleg A Igoshin PLOS Computational Biology, 2012, vol. 8, issue 9, 1-13 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. Author Summary: Myxococcus xanthus cells collectively move on solid surfaces and reorganize their colonies in response to environmental cues. Under some conditions, cells exhibit an intriguing form of collective motility by self-organizing into bands of travelling alternating-density waves termed ripples. These waves are distinct from the waves originating from Turing instability in diffusion-reaction systems, as these counter-traveling waves do not annihilate but appear to pass through each other. Here we developed a new mathematical model of rippling behavior based on a recently observed contact signaling mechanism – cells that make side-to-side contacts can signal one another to reverse. We hypothesize that this signaling is enhanced by the presence of prey-associated macromolecules and compare modeling predictions with experimentally observed waves generated on E. coli prey cells. The model predicts a modified relationship between the wavelength and individual predatory cell motility parameters and provides a physiological role for rippling during predation. We show that ripples allow predatory cells to increase the rate of their spreading to quickly envelope the prey, and subsequently to decrease their random drift to remain in the prey region for longer. These and other predictions are confirmed by the experimental observations. Date: 2012 Downloads: (external link) Related works: Export reference: BibTeX RIS (EndNote, ProCite, RefMan) HTML/Text Persistent link: https://EconPapers.repec.org/RePEc:plo:pcbi00:1002715 DOI: 10.1371/journal.pcbi.1002715 Access Statistics for this article More articles in PLOS Computational Biology from Public Library of Science |
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