Environmental dependence of species interactions: Plant-rhizobium interactions shift from mutualism to parasitism depending on resource availability

Background/Question/Methods: In mutualisms, the relative abundance of traded resources can shift the interaction between mutually-beneficial and detrimental to one or both partners. For example, in the mutualism between plants and rhizobia, in which plants exchange carbon for the nitrogen fixed by their rhizobium symbionts, one might expect the benefit to plants to be reduced under high nitrogen conditions. Similarly, one might expect the cost to plants to be increased under light-limited conditions, where photosynthesis is reduced and excess carbon might be less available. We conducted parallel experiments to investigate how the fitness costs and benefits of the legume-rhizobium symbiosis shift across environments that differ in the availability of the traded resources. The first experiment employed isogenic soybean lines that differed in their ability to form associations with rhizobia; the second used experimental manipulations of the presence of rhizobia.

Results/Conclusions: Similar results were observed across both experiments. In low nitrogen, high light environments, rhizobia significantly increased plant biomass by over 62%. In contrast, when plants were light-limited, the costs of mutualism increased: rhizobia did not increase above-ground biomass and significantly reduced belowground biomass by 46%. Similarly, fertilization reduced the fitness benefits of association with rhizobia, and rhizobia only significantly increased plant biomass under low nitrogen conditions. Thus, consistent with theoretical predications, the legume-rhizobium symbiosis ranges from mutualism to comensalism to parasitism depending on the availability and costs of synthesizing the traded resources. Rhizobium fitness also differs across plants grown in different abiotic conditions, however, and these impacts on rhizobia may limit how far this symbiosis shifts towards parasitism--plants produced fewer nodules when grown in conditions where the benefits conferred by rhizobia to their plant hosts were reduced. In this situation, plants may reduce investment in mutualists in parallel with the decrease in benefits of mutualism, thereby minimizing costs and limiting the extent of negative fitness effects for plant hosts.