Legumes can preferentially select beneficial rhizobial symbionts and sanction ineffective strains that fail to fix nitrogen. Yet paradoxically, rhizobial populations vary from highly beneficial to ineffective in natural and agricultural soils. Classic models of symbiosis focus on the single dimension of symbiont cost-benefit to sympatric hosts, but fail to explain the widespread persistence of ineffective rhizobia. Here, we test a novel framework predicting that spatio-temporal and community dynamics can maintain ineffective strains in rhizobial populations. We used clonal and multistrain inoculations and quantitative culturing to investigate the relative fitness of four focal Bradyrhizobium strains varying from effective to ineffective on Acmispon strigosus. We found that an ineffective Bradyrhizobium strain can be sanctioned by its native A. strigosus host across the host's range, forming fewer and smaller nodules compared to beneficial strains. But the same ineffective Bradyrhizobium strain exhibits a nearly opposite pattern on the broadly sympatric host Acmispon wrangelianus, forming large nodules in both clonal and multistrain inoculations. These data suggest that community-level effects could favour the persistence of ineffective rhizobia and contribute to variation in symbiotic nitrogen fixation.
Rhizobia are best known for nodulating legume roots and fixing atmospheric nitrogen for the host in exchange for photosynthates. However, the majority of the diverse strains of rhizobia do not form nodules on legumes, often because they lack key loci that are needed to induce nodulation. Nonnodulating rhizobia are robust heterotrophs that can persist in bulk soil, thrive in the rhizosphere, or colonize roots as endophytes, but their role in the legume-rhizobium mutualism remains unclear. Here, we investigated the effects of nonnodulating strains on the native Acmispon-Bradyrhizobium mutualism. To examine the effects on both host performance and symbiont fitness, we performed clonal inoculations of diverse nonnodulating Bradyrhizobium strains on Acmispon strigosus hosts and also coinoculated hosts with mixtures of sympatric nodulating and nonnodulating strains. In isolation, nonnodulating Bradyrhizobium strains did not affect plant performance. In most cases, coinoculation of nodulating and nonnodulating strains reduced host performance compared to that of hosts inoculated with only a symbiotic strain. However, coinoculation increased host performance only under one extreme experimental treatment. Nearly all estimates of nodulating strain fitness were reduced in the presence of nonnodulating strains. We discovered that nonnodulating strains were consistently capable of coinfecting legume nodules in the presence of nodulating strains but that the fitness effects of coinfection for hosts and symbionts were negligible. Our data suggest that nonnodulating strains most often attenuate the Acmispon-Bradyrhizobium mutualism and that this occurs via competitive interactions at the root-soil interface as opposed to in planta. IMPORTANCERhizobia are soil bacteria best known for their capacity to form root nodules on legume plants and enhance plant growth through nitrogen fixation. Yet, most rhizobia in soil do not have this capacity, and their effects on this symbiosis are poorly understood. We investigated the effects of diverse nonnodulating rhizobia on a native legume-rhizobium symbiosis. Nonnodulating strains did not affect plant growth in isolation. However, compared to inoculations with symbiotic rhizobia, coinoculations of symbiotic and nonnodulating strains often reduced plant and symbiont fitness. Coinoculation increased host performance only under one extreme treatment. Nonnodulating strains also invaded nodule interiors in the presence of nodulating strains, but this did not affect the fitness of either partner. Our data suggest that nonnodulating strains may be important competitors at the root-soil interface and that their capacity to attenuate this symbiosis should be considered in efforts to use rhizobia as biofertilizers. Rhizobia are heterotrophic soil bacteria with diverse lifestyles. Some rhizobial lineages have acquired the capacity to form nodules on legume roots and fix atmospheric nitrogen for these hosts (1). Nodulating rhizobia are attracted to flavonoids released by legumes. In response, t...
SummarySoil bacteria can exhibit extensive antibiotic resistomes and act as reservoirs of important antibiotic resistance traits. However, the geographic sources and evolutionary drivers of resistance traits are poorly understood in these natural settings. We investigated the prevalence, spatial structure and evolutionary drivers of multidrug resistance in natural populations of Bradyrhizobium, a cosmopolitan bacterial lineage that thrives in soil and aquatic systems as well as in plant and human hosts. We genotyped > 400 isolates from plant roots and soils across California and assayed 98 of them for resistance traits against 17 clinically relevant antibiotics. We investigated the geographic and phylogenetic structure of resistance traits, and analysed correlations of resistance with strain abundance, host infection capacity and in vitro fitness. We found: (i) multidrug resistance at all sites, (ii) subsets of resistance traits that are spatially structured and (iii) significant associations between resistance traits and increased strain abundance or host infection capacity. Our results highlight multiple selective factors that can result in the spread of resistance traits in native Bradyrhizobium populations.
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