The evolutionary genomics of novel endosymbiosis in wild rhizobia bacteria.

The advent of endosymbiosis underlies evolutionary innovation and ecosystem function. However, whether free-living partners tend to benefit or exploit each other during the early stages of novel endosymbiosis remains a dilemma. Rhizobia soil bacteria can initiate root nodules and fix nitrogen for host plants as endosymbionts due to genes carried on mobile genetic elements such as the symbiosis island (SI). We conjugated marked SIs into the genomes of non-nodulating strains, which was sufficient to generate de novo root nodule-forming endosymbionts. Most novel endosymbionts originated as commensals that incurred no detectable costs to host plants, in contrast to predictions of exploitation. In fact, a third of novel endosymbionts originated as nitrogen-fixing mutualists. Consistent with phylogenetic limits to transfer of mobile genetic element function, novel endosymbionts derived from more closely related SI donor and recipient strains showed greater nitrogen fixation. However, consistent with selection on the SI for broad horizontal transfer, we did not detect phylogenetic limits to SI transmission, and the SI was able to displace other genomic elements residing at its characteristic tRNA gene insertion site. We thus provide genetic, genomic, and functional evidence of how mobile genetic elements can potentiate and constrain major evolutionary transitions to expand bacterial niches, with cascading impacts on the fitness of host organisms.