Polyhydroxyalkanoate synthesis by Sinorhizobium meliloti drives a host-specific collapse in symbiosis with Medicago sativa

Naturally occurring root-nodule bacteria (rhizobia) vary substantially in their effectiveness at promoting growth of different plant hosts via symbiotic nitrogen fixation. These variations in rhizobial partner quality have important implications for the productivity of nitrogen-fixing symbioses in natural and agricultural ecosystems, yet we have a limited understanding of the genetic basis for this variation. In a case of host-specific reduction in symbiotic effectiveness (N₂-fixation) with Medicago sativa, we identified the causative genetic elements from the pSymA replicon of Sinorhizobum meliloti HM006 and show them to be involved in polyhydroxyalkanoate (PHA) production in nitrogen-fixing bacteroids. Transfer of this gene region to a strain that forms an effective symbiosis with Medicago sativa resulted in a complete loss of symbiotic N₂-fixation. We showed the mechanism for symbiotic collapse is the diversion of succinate semialdehyde pools in the bacteroid to gamma-hydroxybutyrate (GHB) by an iron-containing dehydrogenase, GhbD. These findings reveal unexpected impacts of carbon metabolism changes in nodules on symbiont performance and provide a rare example of mechanism for variation in rhizobium partner quality, suggesting that host-specific metabolic incompatibility may be a key player in the variations in partner quality observed in nature.