Negotiating mutualism: A locus for exploitation by rhizobia has a broad effect size distribution and context‐dependent effects on legume hosts

Abstract

In mutualisms, variation at genes determining partner fitness provides the raw material upon which coevolutionary selection acts, setting the dynamics and pace of coevolution. However, we know little about variation in the effects of genes that underlie symbiotic fitness in natural mutualist populations. In some species of legumes that form root nodule symbioses with nitrogen‐fixing rhizobial bacteria, hosts secrete nodule‐specific cysteine‐rich (NCR) peptides that cause rhizobia to differentiate in the nodule environment. However, rhizobia can cleave NCR peptides through the expression of genes like the plasmid‐borne Host range restriction peptidase (hrrP), whose product degrades specific NCR peptides. Although hrrP activity can confer host exploitation by depressing host fitness and enhancing symbiont fitness, the effects of hrrP on symbiosis phenotypes depend strongly on the genotypes of the interacting partners. However, the effects of hrrP have yet to be characterised in a natural population context, so its contribution to variation in wild mutualist populations is unknown. To understand the distribution of effects of hrrP in wild rhizobia, we measured mutualism phenotypes conferred by hrrP in 12 wild Ensifer medicae strains. To evaluate context dependency of hrrP effects, we compared hrrP effects across two Medicago polymorpha host genotypes and across two experimental years for five E. medicae strains. We show for the first time in a natural population context that hrrP has a wide distribution of effect sizes for many mutualism traits, ranging from strongly positive to strongly negative. Furthermore, we show that hrrP effect size varies across host genotypes and experiment years, suggesting that researchers should be cautious about extrapolating the role of genes in natural populations from controlled laboratory studies of single genetic variants.

Phenotypic and genomic signatures of interspecies cooperation and conflict in naturally occurring isolates of a model plant symbiont

“…In addition to controlling the total number of nodules formed, legumes can also allocate more carbon to nodules that fix more nitrogen [ 35 , 66 , 67 ], which acts to couple rhizobium quality and fitness even when multiple strains are present. Such fitness-coupling mechanisms can be disrupted by mismatches among legume and rhizobium genotypes, allowing strains that fix little to no N to proliferate within nodules [ 19 , 68 , 69 ]. Our observations of abundant alignment between host fitness proxies, nodule size, and rhizobium relative fitness would predict that such mismatches may be rare in nature, although we only included two host lines and neither was likely to naturally co-occur with our rhizobia strains.…”

Phenotypic and genomic signatures of interspecies cooperation and conflict in naturally-occurring isolates of a model plant symbiont

“…In addition to controlling the total number of nodules formed, legumes can also allocate more carbon to nodules that fix more nitrogen (35, 66, 67), which acts to couple rhizobium quality and fitness even when multiple strains are present. Such fitness coupling mechanisms can be disrupted by mismatches between legume and rhizobium genotypes, allowing strains that fix little to no N to proliferate within nodules (19, 68, 69). Our observations of abundant alignment between host fitness proxies, nodule size, and rhizobium relative fitness suggest that such mismatches may be rare in nature, although in our study, neither host line was collected from the same sites as the rhizobia strains, and thus, are unlikely to naturally co-occur.…”

The role of microbial interactions on rhizobial fitness

“…Plants can even discriminate fixing versus non-fixing strains in mixed nodules, and only target non-fixing bacteria for premature degeneration ( Daubech et al., 2017 ; Regus et al., 2017 ). However, there are exceptions, where non-fixing rhizobia show higher fitness than fixing ones [( Crook et al., 2012 ; Porter and Simms, 2014 ; Gano‐Cohen et al., 2019 ) but see ( Frederickson, 2020 ; Wendlandt et al., 2022 ) to ponder two of these examples]. Nodule size or weight are sometimes used as convenient proxies for bacterial fitness, but in certain cases, these values should be interpreted with caution.…”