Cell Contact–Dependent Outer Membrane Exchange in Myxobacteria: Genetic Determinants and Mechanism

Pathak, Darshankumar T.; Wei, Xueming; Bucuvalas, Alex; Haft, Daniel H.; Gerloff, Dietlind L.; Wall, Daniel

doi:10.1371/journal.pgen.1002626

Cited by 99 publications

(245 citation statements)

References 60 publications

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“…As a consequence, physical mixing of cells was required to increase the chance of a given recipient to encounter and attach to suitable donor cells. This is in contrast to previous reports on B. subtilis 18 or M. xanthus 27,41 in which cell-cell interactions required a solid surface. In our experiments, nanotubes did not establish on (agarose) surfaces.…”

Section: Greencontrasting

confidence: 99%

Metabolic cross-feeding via intercellular nanotubes among bacteria

et al. 2015

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Bacteria frequently exchange metabolites by diffusion through the extracellular environment, yet it remains generally unclear whether bacteria can also use cell-cell connections to directly exchange nutrients. Here we address this question by engineering cross-feeding interactions within and between Acinetobacter baylyi and Escherichia coli, in which two distant bacterial species reciprocally exchange essential amino acids. We establish that in a well-mixed environment E. coli, but likely not A. baylyi, can connect to other bacterial cells via membranederived nanotubes and use these to exchange cytoplasmic constituents. Intercellular connections are induced by auxotrophy-causing mutations and cease to establish when amino acids are externally supplied. Electron and fluorescence microscopy reveal a network of nanotubular structures that connects bacterial cells and enables an intercellular transfer of cytoplasmic materials. Together, our results demonstrate that bacteria can use nanotubes to exchange nutrients among connected cells and thus help to distribute metabolic functions within microbial communities.

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Section: Greencontrasting

confidence: 99%

Metabolic cross-feeding via intercellular nanotubes among bacteria

et al. 2015

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“…3), suggesting that OME can rescue development in cells that otherwise would be incapable of carrying out this process. As a control, under these conditions the ΔtraA mutant sporulates at WT levels (14). These results suggest that OME confers a strong fitness advantage when OM damage impairs the developmental program.…”

Section: Ome Rescues the Motility And Development Of O-antigen Mutantsmentioning

confidence: 77%

“…Because myxobacteria exchange large amounts of OM proteins and fluorescent lipid dyes and can transiently rescue phenotypic defects caused by missing proteins (13,14,24), we asked if OME could rescue motility defects of O-antigen LPS mutants. To this end, we introduced mutations to the previously identified wzm locus, which is required for O-antigen production and S-motility (17), and to two additional loci (rfbB and wzy) that were predicted from bioinformatic analysis to be required for LPS biosynthesis (Fig.…”

Section: Ome Rescues the Motility And Development Of O-antigen Mutantsmentioning

confidence: 99%

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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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“…OME has been demonstrated to extracellularly complement mutants deficient in the production of particular outer membrane products. For example, via OME, the gliding motility of nonmotile M. xanthus mutants is stimulated when mutant cells are mixed with wild-type cells (126). OME is also intertwined with colony swarming and sporulation (126).…”

Section: Contact-mediated Competitionmentioning

confidence: 99%

Multifaceted Interfaces of Bacterial Competition

2016

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bMicrobial communities span many orders of magnitude, ranging in scale from hundreds of cells on a single particle of soil to billions of cells within the lumen of the gastrointestinal tract. Bacterial cells in all habitats are members of densely populated local environments that facilitate competition between neighboring cells. Accordingly, bacteria require dynamic systems to respond to the competitive challenges and the fluctuations in environmental circumstances that tax their fitness. The assemblage of bacteria into communities provides an environment where competitive mechanisms are developed into new strategies for survival. In this minireview, we highlight a number of mechanisms used by bacteria to compete between species. We focus on recent discoveries that illustrate the dynamic and multifaceted functions used in bacterial competition and discuss how specific mechanisms provide a foundation for understanding bacterial community development and function.

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Cell Contact–Dependent Outer Membrane Exchange in Myxobacteria: Genetic Determinants and Mechanism

Cited by 99 publications

References 60 publications

Metabolic cross-feeding via intercellular nanotubes among bacteria

Metabolic cross-feeding via intercellular nanotubes among bacteria

Cell rejuvenation and social behaviors promoted by LPS exchange in myxobacteria

Multifaceted Interfaces of Bacterial Competition

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