How Myxobacteria Cooperate

Abstract

Prokaryotes often reside in groups where a high degree of relatedness has allowed the evolution of cooperative behaviors. However, very few bacteria or archaea have made the successful transition from unicellular to obligate multicellular life. A notable exception is the myxobacteria, in which cells cooperate to perform group functions highlighted by fruiting body development, an obligate multicellular function. Like all multicellular organisms, myxobacteria face challenges in how to organize and maintain multicellularity. These challenges include maintaining population homeostasis, carrying out tissue repair and regulating the behavior of non-cooperators. Here, we describe the major cooperative behaviors that myxobacteria use: motility, predation and development. In addition, this review emphasizes recent discoveries in the social behavior of outer membrane exchange, wherein kin share outer membrane contents. Finally, we review evidence that outer membrane exchange may be involved in regulating population homeostasis, thus serving as a social tool for myxobacteria to make the cyclic transitions from unicellular to multicellular states.

Keywords: Myxococcus xanthus; cell–cell communication; cooperation; outer membrane exchange.

Fig. 1

Cell recognition and fruiting body development in myxobacteria. A) A schematic model of fruiting body formation by M. xanthus cells (yellow). The natural soil environment of myxobacteria contains diverse microbial communities (depicted by cells of different shapes and colors, left). Upon starvation, M. xanthus cells recognize kin and migrate into aggregates. The aggregates increase in size and form a haystack-shaped fruiting body, within which cells sporulate (depicted by circles). B) Micrograph of Chondromyces crocatus fruiting body [20] (courtesy of Hans Reichenbach).

Fig. 2

Model for outer membrane exchange (OME) in myxobacteria. A) 1) TraA-TraA recognition occurs between neighboring cells. Green and red symbolize different fluorescent markers in the OM. 2) Cells are brought into close proximity upon recognition and motility. 3) ‘Prefusion junctions’ form and cells continue to move. 4) Motility helps trigger fusion to facilitate OM exchange. 5) Cells separate after OME. B) TraAB overexpression leads to cell-cell ‘prefusion junctions’ (arrows) as seen by cryo-electron microscopy. Cross-section shows center cell interacting with three neighboring cells. Bar, 100 nm [85]. C) Schematic model of OM fusion dynamics (based on eukaryotic models) during OME. Upon TraA-TraA interaction, the OMs of two aligned cells come into close contact and form a prefusion junction. The outer leaflets of the two OMs then fuse creating a hemifusion complex. Subsequently, full fusion of the OM (both outer and inner leaflets) is presumed to occur, though soluble periplasmic proteins have not been found to transfer. Dashed arrows indicate lateral diffusion of OM components between cells.

Fig. 3

A model for the utility of OME in a bacterial community. Two distinct but compatible populations meet (green and red, left), OME catalyzes OM mixing (yellow cells contain components from red and green cells). The mixed population then transitions towards membrane homeostasis (middle right), in which membrane content from both populations is equally distributed among cells. This integrated population is now larger, more homogenous and better equipped for cooperative behaviors (fruiting body, right). Damage that has occurred to some cells can be repaired by dilution followed by active repair (yellow to light green transition).