Morphogenesis and Developmental Interactions in Myxobacteria

Wireman, John W.; Dworkin, Martin

doi:10.1126/science.806967

Cited by 154 publications

(126 citation statements)

References 62 publications

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“…Although a direct fitness benefit for the recipient cells was clear, we hypothesized that when damaged and healthy populations merge and exchange OMs the subsequent increase in population density could help offset the cost to the donor. In this regard, myxobacteria require a threshold cell density to develop (34,35). During starvation, M. xanthus monitors population density and will continue development if the density exceeds a threshold of ∼3 × 10 8 cells/mL (36).…”

Section: Content Mixing Bestows a Fitness Advantage To Heterogeneousmentioning

confidence: 99%

Cell rejuvenation and social behaviors promoted by LPS exchange in myxobacteria

Vassallo

Pathak

Cao

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Bacterial cells in their native environments must cope with factors that compromise the integrity of the cell. The mechanisms of coping with damage in a social or multicellular context are poorly understood. Here we investigated how a model social bacterium, Myxococcus xanthus, approaches this problem. We focused on the social behavior of outer membrane exchange (OME), in which cells transiently fuse and exchange their outer membrane (OM) contents. This behavior requires TraA, a homophilic cell surface receptor that identifies kin based on similarities in a polymorphic region, and the TraB cohort protein. As observed by electron microscopy, TraAB overexpression catalyzed a prefusion OM junction between cells. We then showed that damage sustained by the OM of one population was repaired by OME with a healthy population. Specifically, LPS mutants that were defective in motility and sporulation were rescued by OME with healthy donors. In addition, a mutant with a conditional lethal mutation in lpxC, an essential gene required for lipid A biosynthesis, was rescued by Tradependent interactions with a healthy population. Furthermore, lpxC cells with damaged OMs, which were more susceptible to antibiotics, had resistance conferred to them by OME with healthy donors. We also show that OME has beneficial fitness consequences to all cells. Here, in merged populations of damaged and healthy cells, OME catalyzed a dilution of OM damage, increasing developmental sporulation outcomes of the combined population by allowing it to reach a threshold density. We propose that OME is a mechanism that myxobacteria use to overcome cell damage and to transition to a multicellular organism.Myxococcus xanthus | outer membrane | lipopolysaccharide | lpxC | fusion A fundamental question in biology is how cells cope with damage. Microbes occupy diverse habitats fraught with physical, biological, and chemical insults (1, 2). UV radiation, desiccation, predation, extracellular enzymes, antimicrobial compounds, pH, temperature, and osmolarity changes are all stresses to the individual cell. In addition, when cells are in nutrient-poor environments, cell division can be rare, taking days to months to complete (3). In a slow-growing state, cell-surface components that may not be undergoing active repair can accumulate damage through natural aging processes such as oxidation (4, 5) and protein denaturation. Although internal cell stress response pathways are known (6), mechanisms to cope with cell surface damage are less well understood.Although cell damage threatens the fitness of the individual, social organisms have strength in numbers. The strategy of kin selection allows evolutionarily viable cooperation between individuals in a closely related population (7). Communication between individuals and sharing of resources establishes the potential for assistance between individual population members. Social support can be beneficial when the fitness of individuals in a group depends on collaborative behaviors such as prey hunting or the developm...

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Section: Content Mixing Bestows a Fitness Advantage To Heterogeneousmentioning

confidence: 99%

Cell rejuvenation and social behaviors promoted by LPS exchange in myxobacteria

Vassallo

Pathak

Cao

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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“…Wireman & Dworkin (1975& Dworkin ( , 1977 have reported that a large part of the cell population lyses during fruiting body formation and that the remainder form myxospores. To show that the loss of rneso-diaminopimelic acid shown in Fig.…”

Section: Results a N D Discussionmentioning

confidence: 99%

“…To estimate the radioactivity in myxospores alone, fruiting bodies were prepared by spreading 0.1 ml of a washed suspension of pre-labelled organisms on fruiting medium. After 6 d myxospores were recovered by the method of Wireman & Dworkin (1975). Vegetative cells and myxospore numbers were determined by counting in a Thoma chamber.…”

Section: Methodsmentioning

confidence: 99%

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Use of Membrane Filters to Study the Development of Fruiting Bodies of Myxococcus xanthus

Dawson¹,

Jones

1979

Journal of General Microbiology

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“…During growth in the presence of nutrients, vegetative cells swarm in groups by gliding motility [23] and cooperatively prey upon other microbial species [24]. Under starvation conditions, the developmental cycle is initiated and fruiting bodies filled with stress-resistant spores are formed [24,25]. Group movement, fruiting body development and predation are all considered to be social behaviours, as they involve coordinated action among cells [26,27].…”

Section: Introductionmentioning

confidence: 99%

Chimaeric load among sympatric social bacteria increases with genotype richness

et al. 2014

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The total productivity of social groups can be determined by interactions among their constituents. Chimaeric load—the reduction of group productivity caused by antagonistic within-group heterogeneity—may be common in heterogeneous microbial groups due to dysfunctional behavioural interactions between distinct individuals. However, some instances of chimaerism in social microbes can increase group productivity, thus making a general relationship between chimaerism and group-level performance non-obvious. Using genetically similar strains of the soil bacterium Myxococcus xanthus that were isolated from a single centimetre-scale patch of soil, we tested for a relationship between degree of chimaerism (genotype richness) and total group performance at social behaviours displayed by this species. Within-group genotype richness was found to correlate negatively with total group performance at most traits examined, including swarming in both predatory and prey-free environments and spore production during development. These results suggest that interactions between such neighbouring strains in the wild will tend to be mutually antagonistic. Negative correlations between group performance and average genetic distance among group constituents at three known social genes were not found, suggesting that divergence at other loci that govern social interaction phenotypes is responsible for the observed chimaeric load. The potential for chimaeric load to result from co-aggregation among even closely related neighbours may promote the maintenance and strengthening of kin discrimination mechanisms, such as colony-merger incompatibilities observed in M. xanthus . The findings reported here may thus have implications for understanding the evolution and maintenance of diversity in structured populations of soil microbes.

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Morphogenesis and Developmental Interactions in Myxobacteria

Cited by 154 publications

References 62 publications

Cell rejuvenation and social behaviors promoted by LPS exchange in myxobacteria

Cell rejuvenation and social behaviors promoted by LPS exchange in myxobacteria

Use of Membrane Filters to Study the Development of Fruiting Bodies of Myxococcus xanthus

Chimaeric load among sympatric social bacteria increases with genotype richness

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