Evolutionary Dynamics of Nitrogen Fixation in the Legume–Rhizobia Symbiosis

Abstract

The stabilization of host–symbiont mutualism against the emergence of parasitic individuals is pivotal to the evolution of cooperation. One of the most famous symbioses occurs between legumes and their colonizing rhizobia, in which rhizobia extract nutrients (or benefits) from legume plants while supplying them with nitrogen resources produced by nitrogen fixation (or costs). Natural environments, however, are widely populated by ineffective rhizobia that extract benefits without paying costs and thus proliferate more efficiently than nitrogen-fixing cooperators. How and why this mutualism becomes stabilized and evolutionarily persists has been extensively discussed. To better understand the evolutionary dynamics of this symbiosis system, we construct a simple model based on the continuous snowdrift game with multiple interacting players. We investigate the model using adaptive dynamics and numerical simulations. We find that symbiotic evolution depends on the cost–benefit balance, and that cheaters widely emerge when the cost and benefit are similar in strength. In this scenario, the persistence of the symbiotic system is compatible with the presence of cheaters. This result suggests that the symbiotic relationship is robust to the emergence of cheaters, and may explain the prevalence of cheating rhizobia in nature. In addition, various stabilizing mechanisms, such as partner fidelity feedback, partner choice, and host sanction, can reinforce the symbiotic relationship by affecting the fitness of symbionts in various ways. This result suggests that the symbiotic relationship is cooperatively stabilized by various mechanisms. In addition, mixed nodule populations are thought to encourage cheater emergence, but our model predicts that, in certain situations, cheaters can disappear from such populations. These findings provide a theoretical basis of the evolutionary dynamics of legume–rhizobia symbioses, which is extendable to other single-host, multiple-colonizer systems.

Black Queen evolution: the role of leakiness in structuring microbial communities

“…Moreover, heterotrophic and phototrophic microorganisms readily coexist in culture in the absence of reciprocation from the heterotrophic organism, as evidenced by the longterm persistence of bacterial contaminants in non-axenic algal cultures (personal observation). Beneficiary mutants unable to fix N also commonly arise in root-associated rhizobial communities and are able to coexist with their N-fixing relatives [59].…”

Rhizobium smilacinae sp. nov., an endophytic bacterium isolated from the leaf of Smilacina japonica

“…In the cross-nodulation tests, strain PTYR-5 T did not form nodules on three different legumes, while R. alkalisoli CCBAU 01393 T formed effective nodules on V. radiata. All these results suggested that the novel strain PTYR-5 T is likely to be one of the ineffective rhizobia that colonize their host plants without undertaking nitrogen fixation (Fujita et al 2014). …”

Nitrogen Fixation and Transfer in Agricultural Production Systems

“…The strain of Rhizobia also determines the level of N 2 fixation [38]. Most of these Rhizobia strains are highly specialized and due to this specialization and the intricacy of interaction between N 2 -fixing plant species and bacteria involved in N 2 fixation, any disturbance or manipulation may be detrimental to the amount of N 2 fixed [39].…”