Resource hoarding facilitates cheating in the legume-rhizobia symbiosis and bet-hedging in the soil.

Abstract

The carbon that rhizobia in root nodules receive from their host powers both reproduction and the synthesis of the storage polyester poly3-hydroxybutyrate (PHB), as well as N2 fixation, which mainly benefits the host. Rhizobia escaping nodules can use stored PHB to survive starvation and reproduce up to 3-fold, but PHB synthesis is energetically expensive and trades-off with N2 fixation. As a result, PHB synthesis is a central mechanism in the evolution of conflict between rhizobia and legumes, and should be included in estimates of rhizobial fitness. Some rhizobia have evolved sophisticated mechanisms to increase PHB accumulation, such as the production of rhizobitoxine, a chemical inhibitor of legume ethylene synthesis. Rhizobitoxine reduces host growth, decreasing rhizobia per nodule for all strains on a plant, but substantially increases PHB accumulation for rhizobitoxine-producing rhizobia. In addition to enhancing reproduction, PHB has a role in bet-hedging: when starved, free-living high-PHB rhizobia divide asymmetrically, forming dormant, high-PHB „persisters‟ that survive long-term starvation and antibiotic treatment, and low-PHB „growers‟ that are sensitive to these stresses. Sinorhizobium meliloti integrates bet hedging and phenotypic plasticity, forming fewer high-PHB persister cells when low competitor density predicts shorter-term starvation. Declining populations may select for delayed reproduction when there is a trade-off between reproduction and longevity, as there is with starving S. meliloti.