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

Darshankumar T Pathak,Daniel Wall,Xueming Wei,Arup Dey,Christopher S Hayes

doi:10.1371/journal.pgen.1003891

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.

Highlights

Cell-cell recognition is critical for differentiating friend from foe and for allowing populations of cells to coordinate multicellular functions [1,2]
Multicellularity is a trait that is typically associated with eukaryotes, certain groups of bacteria exhibit complex multicellular behaviors, which are perhaps best exemplified by the myxobacteria
In response to starvation myxobacteria will assemble fruiting bodies, wherein thousands of cells function as a coherent unit in development and cell differentiation

Summary

Introduction

Cell-cell recognition is critical for differentiating friend from foe and for allowing populations of cells to coordinate multicellular functions [1,2]. Many eukaryotes simplify aspects of cellular selfrecognition by clonal expansion from a single fertilized cell, wherein a privileged environment excludes nonself cells. Some eukaryotes and bacteria build multicellular structures from heterogeneous free-living cells in the environment. In these cases, coalescing cells are not necessarily siblings or even the same species [1,3,4]. Mechanisms involved in cellcell recognition are required to ensure selective inclusion of cells into cooperative multicellular cohorts. In the case of bacteria, little is known about how cells physically recognize one another to coordinate multicellular functions

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Discussion

Conclusion