Tough love: accommodating intracellular bacteria through directed secretion of antimicrobial peptides during the nitrogen-fixing symbiosis

The symbiosis formed by nitrogen-fixing bacteria with plant hosts mainly in the legume family involves a very intimate interaction. Within the symbiotic organ (the nodule) the bacteria are fully internalized by the host cell to become an intracellular organelle surrounded by a host-derived membrane. This arrangement is probably necessary for the efficient provision of energy and the sequestration of free oxygen molecules, two conditions required for sustained nitrogen fixation. Recent advances made in model legume species, such as Medicago truncatula, are beginning to uncover the genetic components allowing rhizobia to access the host cytoplasm and establish chronic intracellular infections without overt detrimental effects. It is now known that the rhizobial compartment in M. truncatula cells, the symbiosome, retains some features of the extracellular space as the target for a redirected host protein secretory pathway. A set of vesicle trafficking proteins function specifically in symbiotic cells to ensure the faithful delivery of secretory proteins to the intracellular bacteria, or bacteroid. This system is co-opted from the more ancient association with arbuscular mycorrhizal fungi found in most land plants, highlighting the evolutionary origin of the legume-rhizobia symbiosis. In some legume lineages, this heightened capability to process secretory proteins is needed to deliver a large number of symbiosis-specific antimicrobial peptides to the bacteria. Known as NCR peptides, these molecules transform bacteroids into a state of terminal differentiation, where the microbe loses its ability to proliferate outside their host. Numbering in their hundreds, these peptides manipulate various aspects of rhizobial biology, and affect the outcome of this symbiosis in complex ways. The extreme size of the NCR peptide family seems to be the result of an evolutionary conflict between the two partners to extract maximum benefit from each other.