Cell rejuvenation and social behaviors promoted by LPS exchange in myxobacteria

Abstract

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...

Regulation of Gene Expression in Shewanella oneidensis MR-1 during Electron Acceptor Limitation and Bacterial Nanowire Formation

“…For example, chains of vesicles in Myxococcus xanthus are important for cell-cell signaling; outer membrane exchange between cells facilitated by these structures can help manage stress at the population level (9,10). Cryo-electron microscopy (cryo-EM) images of the M. xanthus vesicle chains show characteristics similar to those we observed for S. oneidensis nanowires using atomic force microscopy and fluorescence microscopy (8,11,12).…”

Sibling Rivalry in Myxococcus xanthus Is Mediated by Kin Recognition and a Polyploid Prophage

“…Similarly, individual Dictyostelium discoideum amoebae coalesce into fruiting bodies in response to starvation, and those cells compete to become a spore or to terminally differentiate into a stalk cell (39). In M. xanthus, monocultures of traA mutants develop (2,13), indicating that under laboratory conditions, OME is not required. Future studies in M. xanthus will need to test whether developmental lysis is a result of a toxin-antitoxin system, cell competition, and/or OME function.…”

“…Likewise, OME appears to involve both cooperative and competitive interactions. Cooperative interactions are suggested by sharing of cellular resources and, in some cases, the ability of cells to repair their damaged sibling cells (13). In contrast, the swarming and developmental behaviors of some motile strains can be antagonized by OME with some nonmotile strains (2).…”

Multifaceted Interfaces of Bacterial Competition

“…OME is also intertwined with colony swarming and sporulation (126). Furthermore, a recent report implicates OME as a powerful defensive mechanism to dilute membrane damage over a population of cells (127). OME requires the production of an outer membrane protein complex, TraAB, in both the donor and recipient cell (126).…”