Molecular Recognition by a Polymorphic Cell Surface Receptor Governs Cooperative Behaviors in Bacteria

Abstract

Cell-cell recognition is a fundamental process that allows cells to coordinate multicellular behaviors. Some microbes, such as myxobacteria, build multicellular fruiting bodies from free-living cells. However, how bacterial cells recognize each other by contact is poorly understood. Here we show that myxobacteria engage in recognition through interactions between TraA cell surface receptors, which leads to the fusion and exchange of outer membrane (OM) components. OM exchange is shown to be selective among 17 environmental isolates, as exchange partners parsed into five major recognition groups. TraA is the determinant of molecular specificity because: (i) exchange partners correlated with sequence conservation within its polymorphic PA14-like domain and (ii) traA allele replacements predictably changed partner specificity. Swapping traA alleles also reprogrammed social interactions among strains, including the regulation of motility and conferred immunity from inter-strain killing. We suggest that TraA helps guide the transition of single cells into a coherent bacterial community, by a proposed mechanism that is analogous to mitochondrial fusion and fission cycling that mixes contents to establish a homogenous population. In evolutionary terms, traA functions as a rare greenbeard gene that recognizes others that bear the same allele to confer beneficial treatment.

Cell rejuvenation and social behaviors promoted by LPS exchange in myxobacteria

“…1C). This cell-chaining pattern correlates with TraA cell-surface localization patterns (15), suggesting that TraA foci function as adhesion patches for cellcell binding. The cellular junctions were investigated further by cryo-EM.…”

“…This process is dependent on the cellsurface receptor TraA and the TraB cohort protein (14). Exchange between cells is highly selective, because TraA has evolved a polymorphic region that enables kin recognition (15,16). Although TraA is conserved across myxobacteria, only strains within the same compatibility group, determined by the traA allele they express, exchange OM components.…”

“…social "greenbeard" gene, because it can identify and confer preferential treatment to others that display the same allele (15,16).…”

Multifaceted Interfaces of Bacterial Competition

“…The net result is a population with shared functions in competitive fitness through defense and through close-quarters exclusion of competitors. Perhaps contact-mediated mechanisms, like CDI, T6SS, or OME, are needed to selectively inhibit closely related competitors with the capacity to pass unharmed across a chemical defensive barrier (91,129,145).…”

“…OME requires the production of an outer membrane protein complex, TraAB, in both the donor and recipient cell (126). TraAB appears to be the only component necessary to mediate OME (128) and, similarly to the BamA receptor in CDI systems, TraAB contains a polymorphic domain that limits OME to a narrow range of related targets (129). Given the functional similarities to CDI systems and the potential of OME to directly deliver toxic effectors into the envelope of target bacteria, it is not surprising that Myxobacteria use OME to mediate competition and engage in kin recognition.…”