Dimensions: Collaborative Research: Elucidating the drivers of mutualism variation in host-symbiont metapopulations

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Symbiotic bacteria transform how plants and animals interact with their environment. These bacteria are well known for their ability to enhance host growth and tolerance to stress, but symbioses vary greatly in their effects on host health and fitness. Little is understood about the forces that shape this variation and drive the spread of symbionts that interact, but fail to benefit the host. Here, researchers use the relationship between native California legumes and nitrogen-fixing Bradyrhizobium bacteria to study the drivers of variation in symbioses. The project will employ environmental sampling of interacting plants, bacteria, and soil, genetic approaches, and greenhouse experiments. The research will determine the magnitude of benefits the bacteria provide to the host, what bacterial genes facilitate benefit or exploitation of the host, and how the host responds and defends itself against ineffective symbionts. The project will train undergraduate and graduate students as well as two postdoctoral fellows. The researchers will educate local farmers on plant-microbe interactions, and they will generate and curate a collection of plant and bacterial variants that will be made freely available to other researchers. The project is important because it will provide information on the parameters that influence symbiosis and help guide how microbes can be better deployed to increase productivity of agricultural systems and promote health of humans and the planet. The maintenance of diversity in microbial symbioses is paradoxical. Conventional theory predicts a lack of variation in symbiont function because host species reward beneficial symbionts and intensely select against ineffective partners. Here, a novel framework is tested to explain the maintenance of symbiont variation. The planned work transcends the dominant theoretical paradigm by investigating ecological, spatiotemporal, and genomic drivers in a metapopulation of rhizobial bacteria and their native legume hosts. Like other hosts, legumes exhibit host control traits: legumes can discriminate against ineffective rhizobia during nodule formation, and can reduce within-nodule growth rates of ineffective rhizobia. Despite the apparent efficiency of host control, ineffective rhizobia are commonly uncovered in natural and agricultural soils. Four aims are proposed to explain the maintenance of symbiont variation in this key model system. Experimental inoculations coupled with genetic and selection analysis are used to investigate i) variation among legume host populations in their capacity to sanction ineffective rhizobia, ii) the spatial and phylogenetic origins of invasions by ineffective rhizobia, and iii) the genomic basis for the evolution of ineffective rhizobia. iv) Inferred invasions of ineffective rhizobia will be recapitulated using experiments that test fitness predictions under realistic conditions. This work challenges conventional mutualism theory and highlights the importance of genetic variation, spatio-temporal dynamics, and fitness tradeoffs.