Symbiosis within Symbiosis: Evolving Nitrogen-Fixing Legume Symbionts

Bacterial accessory genes are genomic symbionts with an evolutionary history and future that is different from that of their hosts. Packages of accessory genes move from strain to strain and confer important adaptations, such as interaction with eukaryotes. The ability to fix nitrogen with legumes is a remarkable example of a complex trait spread by horizontal transfer of a few key symbiotic genes, converting soil bacteria into legume symbionts. Rhizobia belong to hundreds of species restricted to a dozen genera of the Alphaproteobacteria and Betaproteobacteria, suggesting infrequent successful transfer between genera but frequent successful transfer within genera. Here we review the genetic and environmental conditions and selective forces that have shaped evolution of this complex symbiotic trait.

TrendsNitrogen fixation in symbiosis with legumes involves hundreds of genes, yet rhizobia arose through horizontal transfer of a few essential genes. These nod–nif genes have spread in many taxons during evolution so that rhizobia currently belong to a dozen genera of the Alphaproteobacteria and Betaproteobacteria.Recent data suggest a two-scale dispersion of key symbiotic genes: colonizing a new genus is rare and requires recipient genome modifications, whereas expanding within rhizobial genera is frequent and allows symbiovar emergence.The ecological success of the transfer is enhanced by the strong selection the plant exerts towards efficient nodulation and infection, and the action of error-prone DNA polymerases that accelerate adaptation to symbiosis after horizontal gene transfer (HGT).Rhizobia can behave as parasites (not nitrogen-fixing), and emergence and maintenance of mutualism may rely on antagonistic co-evolution.