An individual based model of rippling movement in a myxobacteria population

Anderson, Alexander R.A.; Vasiev, Bakhtier

doi:10.1016/j.jtbi.2004.11.028

Cited by 8 publications

(12 citation statements)

References 12 publications

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“…It is still unclear why this organism requires a signal transduction system that is so much more complex than Escherichia coli (E. coli). However, these two pathways work synergistically to regulate cell movement and behavior (9,(12)(13)(14)(15)(16)(17) and provide an intriguing example of how disparate signal transduction pathways integrate in vivo. The fascinating combination of Che-like and Ras-like molecular control of M. xanthus cell polarity, as well as the availability of quantitative data from numerous studies on the behavior of M. xanthus signaling mutants, make this organism an excellent candidate for mathematical modeling so as to better understand signal transduction and cell motility.…”

Section: Introductionmentioning

confidence: 99%

“…To date, there have been many models of M. xanthus behavior, which have been helpful for untangling the nature of rippling behavior (9,13,(15)(16)(17)(18)(19), fruiting body formation (2,19,20), sporulation (9,16,20,21), cell-cell contacts (8,16,(21)(22)(23)(24), and mechanical models for individual cell motility (9,(22)(23)(24). Igoshin et al first proposed the Frizilator model of cyclic protein activation controlling reversal behavior of individual cells (9).…”

Section: Introductionmentioning

confidence: 99%

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Dual Biochemical Oscillators May Control Cellular Reversals in Myxococcus xanthus

Eckhert

Rangamani

Davis

et al. 2014

Biophysical Journal

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Myxococcus xanthus is a Gram-negative, soil-dwelling bacterium that glides on surfaces, reversing direction approximately once every 6 min. Motility in M. xanthus is governed by the Che-like Frz pathway and the Ras-like Mgl pathway, which together cause the cell to oscillate back and forth. Previously, Igoshin et al. (2004) suggested that the cellular oscillations are caused by cyclic changes in concentration of active Frz proteins that govern motility. In this study, we present a computational model that integrates both the Frz and Mgl pathways, and whose downstream components can be read as motor activity governing cellular reversals. This model faithfully reproduces wildtype and mutant behaviors by simulating individual protein knockouts. In addition, the model can be used to examine the impact of contact stimuli on cellular reversals. The basic model construction relies on the presence of two nested feedback circuits, which prompted us to reexamine the behavior of M. xanthus cells. We performed experiments to test the model, and this cell analysis challenges previous assumptions of 30 to 60 min reversal periods in frzCD, frzF, frzE, and frzZ mutants. We demonstrate that this average reversal period is an artifact of the method employed to record reversal data, and that in the absence of signal from the Frz pathway, Mgl components can occasionally reverse the cell near wildtype periodicity, but frz- cells are otherwise in a long nonoscillating state.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Dual Biochemical Oscillators May Control Cellular Reversals in Myxococcus xanthus

Eckhert

Rangamani

Davis

et al. 2014

Biophysical Journal

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“…Developmental rippling has been observed to occur spontaneously and sporadically in starving cultures of M. xanthus prior to and concurrent with fruiting body formation (6). Recent experimental and theoretical study of this process indicates that the rippling pattern can be produced through a minimal requirement of cell-cell contacts and an internal biochemical oscillation system (1,9,10,26,31). Developmental rippling has been proposed to rely on the levels of the starvation-induced C-signal, a 17-kDa form of the CsgA protein (12,27).…”

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confidence: 99%

Rippling Is a Predatory Behavior in Myxococcus xanthus

et al. 2006

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Cells of Myxococcus xanthus will, at times, organize their movement such that macroscopic traveling waves, termed ripples, are formed as groups of cells glide together on a solid surface. The reason for this behavior has long been a mystery, but we demonstrate here that rippling is a feeding behavior which occurs when M. xanthus cells make direct contact with either prey or large macromolecules. Rippling has been observed during two fundamentally distinct environmental conditions: (i) starvation-induced fruiting body development and (ii) predation of other organisms. Our results indicate that case (i) does not occur in all wild-type strains and is dependent on the intrinsic level of autolysis. Analysis of predatory rippling indicates that rippling behavior is inducible during predation on proteobacteria, gram-positive bacteria, yeast (such as Saccharomyces cerevisiae), and phage. Predatory efficiency decreases under genetic and physiological conditions in which rippling is inhibited. Rippling will also occur in the presence of purified macromolecules such as peptidoglycan, protein, and nucleic acid but does not occur in the presence of the respective monomeric components and also does not occur when the macromolecules are physically separated from M. xanthus cells. We conclude that rippling behavior is a mechanism utilized to efficiently consume nondiffusing growth substrates and that developmental rippling is a result of scavenging lysed cell debris.

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“…The use of particular terms can also imply certain features, e.g., “multicellularity” suggests a beneficial regulated biological phenomenon, which may not always be the case. Rippling in myxobacteria may merely be an emergent behavior manifested at particular reversal frequencies, rather than an adaptively evolved characteristic …”

Section: A Variety Of Mechanisms Allow the Evolution Of Cooperativitymentioning

confidence: 99%

Is “Wolf‐Pack” Predation by Antimicrobial Bacteria Cooperative? Cell Behaviour and Predatory Mechanisms Indicate Profound Selfishness, Even when Working Alongside Kin

Marshall

Whitworth

2019

BioEssays

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For decades, myxobacteria have been spotlighted as exemplars of social “wolf‐pack” predation, communally secreting antimicrobial substances into the shared public milieu. This behavior has been described as cooperative, becoming more efficient if performed by more cells. However, laboratory evidence for cooperativity is limited and of little relevance to predation in a natural setting. In contrast, there is accumulating evidence for predatory mechanisms promoting “selfish” behavior during predation, which together with conflicting definitions of cooperativity, casts doubt on whether microbial “wolf‐pack” predation really is cooperative. Here, it is hypothesized that public‐goods‐mediated predation is not cooperative, and it is argued that a holistic model of microbial predation is needed, accounting for predator and prey relatedness, social phenotypes, spatial organization, activity/specificity/transport of secreted toxins, and prey resistance mechanisms. Filling such gaps in our knowledge is vital if the evolutionary benefits of potentially costly microbial behaviors mediated by public goods are to be properly understood.

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An individual based model of rippling movement in a myxobacteria population

Cited by 8 publications

References 12 publications

Dual Biochemical Oscillators May Control Cellular Reversals in Myxococcus xanthus

Dual Biochemical Oscillators May Control Cellular Reversals in Myxococcus xanthus

Rippling Is a Predatory Behavior in Myxococcus xanthus

Is “Wolf‐Pack” Predation by Antimicrobial Bacteria Cooperative? Cell Behaviour and Predatory Mechanisms Indicate Profound Selfishness, Even when Working Alongside Kin

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