Hosts winnow symbionts with multiple layers of absolute and conditional discrimination mechanisms

Abstract

In mutualism, hosts select symbionts via partner choice and preferentially direct more resources to symbionts that provide greater benefits via sanctions. At the initiation of symbiosis, prior to resource exchange, it is not known how the presence of multiple symbiont options (i.e. the symbiont social environment) impacts partner choice outcomes. Furthermore, little research addresses whether hosts primarily discriminate among symbionts via sanctions, partner choice or a combination. We inoculated the legume , Acmispon wrangelianus, with 28 pairs of fluorescently labelled Mesorhizobium strains that vary continuously in quality as nitrogen-fixing symbionts. We find that hosts exert robust partner choice, which enhances their fitness. This partner choice is conditional such that a strain's success in initiating nodules is impacted by other strains in the social environment. This social genetic effect is as important as a strain's own genotype in determining nodulation and has both transitive (consistent) and intransitive (idiosyncratic) effects on the probability that a symbiont will form a nodule. Furthermore, both absolute and conditional partner choice act in concert with sanctions, among and within nodules. Thus, multiple forms of host discrimination act as a series of sieves that optimize host benefits and select for costly symbiont cooperation in mixed symbiont populations.

Plant-Rhizobia Symbiosis and Nitrogen Fixation in Legumes

“…Although in nature strains that exhibit high competitiveness for nodulation often demonstrate high nitrogen fixation efficiency as well (Burghardt et al, 2018;Fields et al, 2023;Rahman et al, 2023), the capacity to fix atmospheric nitrogen itself does not contribute to nodulation competitiveness (Amarger, 1981;Hahn and Studer, 1986;Daubech et al, 2017;Westhoek et al, 2017;Bourion et al, 2018). Interestingly, co-inoculation of highly competitive and efficient nitrogen-fixing strains with another rhizobial strain can lead either to higher plant benefits than in single inoculation or, on the contrary, to a decrease in both nodulation and plant benefits, indicating the existence of positive and negative competitive interferences between the rhizobial strains (Heath and Tiffin, 2007;Montoya et al, 2023;Rahman et al, 2023). Other interactions negatively affecting nodulation initiation were described by Gano-Cohen et al (2016), who showed that the presence of non-nodulating Bradyrhizobium reduced the number of nodules formed by nodulating Bradyrhizobium on the legume Acmispon strigosus, probably by directly competing for attachment sites on the root.…”

The role of microbial interactions on rhizobial fitness

“…Although in nature strains that exhibit high competitiveness for nodulation often demonstrate high nitrogen fixation efficiency as well ( Burghardt et al., 2018 ; Fields et al., 2023 ; Rahman et al., 2023 ), the capacity to fix atmospheric nitrogen itself does not contribute to nodulation competitiveness ( Amarger, 1981 ; Hahn and Studer, 1986 ; Daubech et al., 2017 ; Westhoek et al., 2017 ; Bourion et al., 2018 ). Interestingly, co-inoculation of highly competitive and efficient nitrogen-fixing strains with another rhizobial strain can lead either to higher plant benefits than in single inoculation or, on the contrary, to a decrease in both nodulation and plant benefits, indicating the existence of positive and negative competitive interferences between the rhizobial strains ( Heath and Tiffin, 2007 ; Montoya et al., 2023 ; Rahman et al., 2023 ). Other interactions negatively affecting nodulation initiation were described by Gano-Cohen et al.…”